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Geranium and Pelargonium

2002 Edited by Taylor & Francis

Medicinal and Aromatic Plants Industrial Profiles


Individual volumes in this series provide both industry and academia with in-depth coverage of
one major medicinal or aromatic plant of industrial importance.

Edited by Dr Roland Hardman


Volume 1
Valerian, edited by Peter J. Houghton

Volume 15
Ginseng, edited by W.E. Court

Volume 2
Perilla, edited by He-ci Yu,
Kenichi Kosuna and Megumi Haga

Volume 16
Mistletoe, edited by Arndt Bssing

Volume 3
Poppy, edited by Jen Bernth
Volume 4
Cannabis, edited by David T. Brown
Volume 5
Neem, edited by H.S. Puri
Volume 6
Ergot, edited by Vladimr Kren and
Ladislav Cvak
Volume 7
Caraway, edited by va Nmeth
Volume 8
Saffron, edited by Moshe Negbi
Volume 9
Tea Tree, edited by Ian Southwell and
Robert Lowe
Volume 10
Basil, edited by Raimo Hiltunen and
Yvonne Holm

Volume 17
Tea, edited by Yong-su Zhen
Volume 18
Artemisia, edited by Colin W. Wright
Volume 19
Stevia, edited by A. Douglas Kinghorn
Volume 20
Vetiveria, edited by Massimo Maffei
Volume 21
Narcissus and Daffodil, edited by
Gordon R. Hanks
Volume 22
Eucalyptus, edited by John J.W. Coppen
Volume 23
Pueraria, edited by Wing Ming Keung
Volume 24
Thyme, edited by E. Stahl-Biskup and
F. Sez
Volume 25
Oregano, edited by Spiridon E. Kintzios

Volume 11
Fenugreek, edited by
Georgios Petropoulos

Volume 26
Citrus, edited by Giovanni Dugo and
Angelo Di Giacomo

Volume 12
Gingko biloba, edited by Teris A. Van Beek

Volume 27
Geranium and Pelargonium, edited by
Maria Lis-Balchin

Volume 13
Black Pepper, edited by P.N. Ravindran
Volume 14
Sage, edited by Spiridon E. Kintzios

2002 Edited by Taylor & Francis

Volume 28
Magnolia, edited by Satyajit D. Sarker
and Yuji Maruyama

Geranium and Pelargonium


The genera Geranium and Pelargonium

Edited by

Maria Lis-Balchin
South Bank University, London, UK

2002 Edited by Taylor & Francis

First published 2002


by Taylor & Francis
11 New Fetter Lane, London EC4P 4EE
Simultaneously published in the USA and Canada
by Taylor & Francis Inc,
29 West 35th Street, New York, NY 10001
Taylor & Francis is an imprint of the Taylor & Francis Group
This edition published in the Taylor & Francis e-Library, 2004.
2002 Edited by Taylor & Francis
All rights reserved. No part of this book may be reprinted or reproduced
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this book is true and accurate at the time of going to press. However,
neither the publisher nor the authors can accept any legal responsibility
or liability for any errors or omissions that may be made. In the case of
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consult the manufacturers guidelines.
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ISBN 0-203-21653-9 Master e-book ISBN

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ISBN 0415284872 (Print Edition)

2002 Edited by Taylor & Francis

Contents

List of contributors
Preface to the series
1 General introduction

viii
x
1

MARIA LIS-BALCHIN

PART 1

Geranium
2 History of nomenclature, usage and cultivation of Geranium and
Pelargonium species

3
5

MARIA LIS-BALCHIN

3 The taxonomy of Geranium species and cultivars, their origins


and growth in the wild

11

DIANA M. MILLER

4 Phytochemistry of the genus Geranium

20

JEFFREY B. HARBORNE AND CHRISTINE A. WILLIAMS

Cultivation and harvesting of Geranium macrorrhizum and


Geranium sanguineum for medicinal use in Bulgaria

30

TATYANA STOEVA

6 Essential oil of Geranium macrorrhizum L. production, extraction,


distillation and use

36

TATYANA STOEVA

7 Use of Geranium species extracts as herbal medicines

40

ELIZABETH M. WILLIAMSON

PART 2

Pelargonium

47

8 The taxonomy of Pelargonium species and cultivars, their


origins and growth in the wild

49

DIANA M. MILLER

2002 Edited by Taylor & Francis

vi

Contents

9 Cultivation and sales of Pelargonium plants for ornamental


use in the UK and worldwide

80

JANET JAMES

10 Growing pelargoniums in the garden, conservatory


and for shows

92

MARIA LIS-BALCHIN

11 Phytochemistry of the genus Pelargonium

99

CHRISTINE A. WILLIAMS AND JEFFREY B. HARBORNE

12 Pharmacology of Pelargonium essential oils and


extracts in vitro and in vivo

116

STEPHEN HART AND MARIA LIS-BALCHIN

13 Antimicrobial properties of Pelargonium extracts


contrasted with that of Geranium

132

STANLEY G. DEANS

14 Essential oils from different Pelargonium species and cultivars:


their chemical composition (using GC, GC/MS) and appearance
of trichomes (under EM)

147

MARIA LIS-BALCHIN

15 Chemotaxonomy of Pelargonium based on alkaloids and


essential oils

166

PETER HOUGHTON AND MARIA LIS-BALCHIN

16 Phylogenetical relationship within the genus Pelargonium


based on the RAPD-PCR method of DNA analysis correlated
with the essential oil composition

174

J. RENATA OCHOCKA, ADAM BOGDAN, ARKADIUSZ PIOTROWSKI


AND MARIA LIS-BALCHIN

17 Geranium essential oil: standardisation, ISO; adulteration and its


detection using GC, enantiomeric columns, toxicity and bioactivity

184

MARIA LIS-BALCHIN

18 Rose-scented geranium a Pelargonium grown for


the perfume industry

193

FRDRIC-EMMANUEL DEMARNE

19 Cultivation and distillation of Geranium oil from


Pelargonium species in India

212

B.R. RAJESWARA RAO

20 Micropropagation and biotechnological approaches to tissue


culture of Pelargonium species and production of essential
oils of scenteds
BARRY V. CHARLWOOD AND MARIA LIS-BALCHIN

2002 Edited by Taylor & Francis

218

Contents

21 Geranium oil and its use in aromatherapy

vii

234

MARIA LIS-BALCHIN

22 Perfumery and cosmetic products utilising Geranium oil

247

RHONA WELLS AND MARIA LIS-BALCHIN

23 New research: possible uses of various Pelargonium leaf


oils and extracts as food preservatives

251

MARIA LIS-BALCHIN

24

Pelargonium reniforme and Pelargonium sidoides: their botany,


chemistry and medicinal use

262

HERBERT KOLODZIEJ

25 Interactions between arthropod pests and pelargoniums

291

MONIQUE S.J. SIMMONDS

26 Correlation of the chemical profiles of the essential oil of


Pelargonium (Geranium oil) and others separately and
in mixes, with their relaxant or stimulant properties in
man and smooth muscle preparations in vitro
MARIA LIS-BALCHIN AND STEPHEN HART

2002 Edited by Taylor & Francis

299

Contributors

Maria Lis-Balchin
School of Applied Science
South Bank University
Borough Road
London
SE1 OAA
UK
Adam Bogdan
Department of Biology and
Pharmaceutical Botany
Medical University of Gdansk
ul. Hallera 107
60-416 Gdansk
Poland

Jeffrey B. Harborne
Department of Botany
School of Plant Sciences
The University of Reading
Whiteknights
Reading, RG6 6AS
Stephen Hart
Messenger & Signalling Research Group
School of Biomedical Sciences
Kings College London
Guys Campus
London
SE1 9RT
UK

Barry V. Charlwood
Division of Life Sciences
Kings College London
150 Stamford Street
London
SE1 8WA
UK

Peter Houghton
Pharmacy Department
Kings College London
The Franklin-Watkins Building
150 Stamford Street
London
SE1 8WA
UK

Stanley G. Deans
Aromatic and Medicinal Plant Group
Food Systems Division
SAC Auchincruive
Ayr, KA6 5HW
UK

Janet James
The Vernon Geranium Nursery
Cuddington Way
Cheam
Sutton SM2 7JB

Frdric-Emmanuel Demarne
ADRIAN S.A.
15, Rue de Cassis
F-13008 Marseille
France
2002 Edited by Taylor & Francis

Herbert Kolodziej
Institut fr Pharmazie
Pharmazeutische Biologie
Freie Universitt Berlin
Knigin-Luise-Str. 2  4, D-14195
Berlin, Germany

Contributors

Diana M. Miller
Royal Horticultural Society
Wisley
Woking Surrey GU23 6QB
UK
J. Renata Ochocka
Department of Biology and
Pharmaceutical Botany
Medical University of Gdansk
ul. Hallera 107
60-416 Gdansk, Poland
Arkadiusz Piotrowski
Department of Biology and
Pharmaceutical Botany
Medical University of Gdansk
ul. Hallera 107
60-416 Gdansk, Poland
B.R. Rajeswara Rao
Central Institute of Medicinal and
Aromatic Plants
Field Station
Boduppal
Uppal (PO)
Hyderabad 500 039, India
Monique S.J. Simmonds
Jodrell Laboratories
Royal Botanic Gardens
Kew, Surrey, TW9 3AB

2002 Edited by Taylor & Francis

ix

Tatyana Stoeva
Laboratory of Biology and Chemistry of
Medicinal and Aromatic Plants
Institute of Botany
Bulgarian Academy of Sciences
23, Acad. G. Bonchev Str.
1113, Sofia
Bulgaria
Rhona Wells
Charabot et Cie
Mill Hill
London
Christine A. Williams
Department of Botany
School of Plant Sciences
The University of Reading
Whiteknights
Reading
RG6 6AS
Elizabeth M. Williamson
Centre for Pharmacognosy and
Phytotherapy
The School of Pharmacy
University of London
Brunswick Square
London
WC1N 1AX

Preface to the series

There is increasing interest in industry, academia and the health sciences in medicinal and
aromatic plants. In passing from plant production to the eventual product used by the
public, many sciences are involved. This series brings together information which is
currently scattered through an ever increasing number of journals. Each volume gives an
in-depth look at one plant genus, about which an area specialist has assembled information
ranging from the production of the plant to market trends and quality control.
Many industries are involved such as forestry, agriculture, chemical, food, flavour,
beverage, pharmaceutical, cosmetic and fragrance. The plant raw materials are roots,
rhizomes, bulbs, leaves, stems, barks, wood, flowers, fruits and seeds. These yield
gums, resins, essential (volatile) oils, fixed oils, waxes, juices, extracts and spices for
medicinal and aromatic purposes. All these commodities are traded worldwide. A
dealers market report for an item may say Drought in the country of origin has forced
up prices.
Natural products do not mean safe products and account of this has to be taken by
the above industries, which are subject to regulation. For example, a number of plants
which are approved for use in medicine must not be used in cosmetic products.
The assessment of safe to use starts with the harvested plant material which has to
comply with an official monograph. This may require absence of, or prescribed limits
of, radioactive material, heavy metals, aflatoxin, pesticide residue, as well as the
required level of active principle. This analytical control is costly and tends to exclude
small batches of plant material. Large scale contracted mechanised cultivation with designated seed or plantlets is now preferable.
Today, plant selection is not only for the yield of active principle, but for the plants
ability to overcome disease, climatic stress and the hazards caused by mankind. Such
methods as in vitro fertilization, meristem cultures and somatic embryogenesis are used.
The transfer of sections of DNA is giving rise to controversy in the case of some enduses of the plant material.
Some suppliers of plant raw material are now able to certify that they are supplying
organically-farmed medicinal plants, herbs and spices. The Economic Union directive
(CVO/EU No. 2092/91) details the specifications for the obligatory quality controls to
be carried out at all stages of production and processing of organic products.
Fascinating plant folklore and ethnopharmacology leads to medicinal potential.
Examples are the muscle relaxants based on the arrow poison, curare, from species of
Chondrodendron, and the anti-malarials derived from species of Cinchona and Artemisia.
The methods of detection of pharmacological activity have become increasingly reliable
and specific, frequently involving enzymes in bioassays and avoiding the use of laboratory animals. By using bioassay linked fractionation of crude plant juices or extracts,

2002 Edited by Taylor & Francis

Preface to the series

xi

compounds can be specifically targeted which, for example, inhibit blood platelet
aggregation, or have anti-tumour, or anti-viral, or any other required activity. With the
assistance of robotic devices, all the members of a genus may be readily screened.
However, the plant material must be fully authenticated by a specialist.
The medicinal traditions of ancient civilisations such as those of China and India have
a large armamentaria of plants in their pharmacopoeias which are used throughout
South-East Asia. A similar situation exists in Africa and South America. Thus, a very
high percentage of the Worlds population relies on medicinal and aromatic plants for
their medicine. Western medicine is also responding. Already in Germany all medical
practitioners have to pass an examination in phytotherapy before being allowed to practise. It is noticeable that throughout Europe and the USA, medical, pharmacy and
health related schools are increasingly offering training in phytotherapy.
Multinational pharmaceutical companies have become less enamoured of the single
compound magic bullet cure. The high costs of such ventures and the endless competition from me too compounds from rival companies often discourage the attempt.
Independent phytomedicine companies have been very strong in Germany. However,
by the end of 1995, eleven (almost all) had been acquired by the multinational pharmaceutical firms, acknowledging the lay publics growing demand for phytomedicines
in the Western World.
The business of dietary supplements in the Western World has expanded from the
health store to the pharmacy. Alternative medicine includes plant-based products.
Appropriate measures to ensure the quality, safety and efficacy of these either already
exist or are being answered by greater legislative control by such bodies as the Food and
Drug Administration of the USA and the recently created European Agency for the
Evaluation of Medicinal Products, based in London.
In the USA, the Dietary Supplement and Health Education Act of 1994 recognised
the class of phytotherapeutic agents derived from medicinal and aromatic plants.
Furthermore, under public pressure, the US Congress set up an Office of Alternative
Medicine and this office in 1994 assisted the filing of several Investigational New Drug
(IND) applications, required for clinical trials of some Chinese herbal preparations. The
significance of these applications was that each Chinese preparation involved several
plants and yet was handled as a single IND. A demonstration of the contribution to efficacy, of each ingredient of each plant, was not required. This was a major step forward
towards more sensible regulations in regard to phytomedicines.
My thanks are due to the staffs of Harwood Academic Publishers and Taylor &
Francis who have made this series possible and especially to the volume editors and
their chapter contributors for the authoritative information.
Roland Hardman

2002 Edited by Taylor & Francis

General introduction
Maria Lis-Balchin

The genera Geranium and Pelargonium are invariably confused by the general public and
also plant sales personnel, health food shop workers and alternative medicine practitioners, especially aromatherapists. This confusion has existed before Linnaeus (1753)
and his binomial system of classification, where both genera were put under the genus
Geranium, and although Sweet (1820) and other botanists reclassified them under two
genera, acceptance by the majority of laymen as well as nurserymen is still low. The
flowers of typical Geranium and Pelargonium species are shown in Figure 1.1.
Geranium oil is extracted from the leaves of some Pelargonium species and cultivars,
but its paramedical effects are often equated with those of the genus Geranium
e.g. G. robertianum and G. maculatum. The latter are native to Europe and were used as
herbal medicines for hundreds of years; they were written up by Gerard (1633),
Culpeper (1652) and even Grieve (1937). The Pelargonium species, native to southern
Africa, although introduced to European Botanic Gardens for example in Leiden as
early as 1600, was used only as ornamental plants; their medicinal properties were
known only to Hottentots, Zulus and the local Boers in South Africa till the early
1900s when there was some mention in the literature. The medicinal properties of the
fat-soluble Geranium oil (from Pelargonium) are therefore largely unsubstantiated as

(a)

(b)

Figure 1.1 Flowers of typical Geranium (a) and Pelargonium (b) species.

2002 Edited by Taylor & Francis

Maria Lis-Balchin

they are based solely on the properties attributed to the mainly water-soluble extracts
(teas) of Geranium species. A further confusion arises with the Geranium oil derived
from G. macrorrhizum in Bulgaria, which is entirely different to the commercial
Geranium oil from Pelargonium species in both chemical composition and also medicinal
properties etc.
The main usage of Geranium species is in herbal medicine, whilst that of the
Pelargonium-derived Geranium oil is in perfumery, cosmetics and aromatherapy products. The production of commercial Geranium oil, from several Pelargonium cultivars,
is now mainly in Reunion, Egypt and China; however the true sales of Geranium oil are
greatly in excess of that derived from plants, due to the ever-increasing production of
synthetic and nature-identical Geranium oil.
Geranium oil contains mainly citronellol and geraniol and their esters, therefore can
be easily concocted from cheaper essential oils (EOs) and adjusted to the recommended
ISO standards. The antimicrobial activity of such EOs is much greater than that of
some authentic oils but has a similar pharmacological effect on smooth muscle (spasmolytic) and the actual odour can be even more appreciated by perfumers than the real
EO. It remains to be seen whether aromatherapy has any actual medicinal benefits,
other than stress-alleviating, and whether these are attributable only to the true EOs,
especially as there is a wide difference in the actual percentage chemical composition of
EOs obtained from different geographical sources and also different samples from plants
grown in various countries where differences in hybridization has occurred and even the
same plants grown under different climatic conditions etc.
The pharmacological activity of the water-soluble extracts of the two genera are not
very different: they both have a high proportion of tannins and have an antidiarrhoeal
function. The lipophylic EOs of Pelargonium species have mainly a spasmolytic effect
on smooth muscle, except for P. grossularioides, which was used as an abortifacient
in Southern African folk medicine and has been shown to have a spasmogenic action
on smooth and uterine muscle.
Pelargonium EOs from leaves of the many different species and cultivars (other than
those grown to produce commercial Geranium oil) have very different odours and
chemical compositions, but most of the floral-smelling ones act through cyclic AMP
(cAMP) as the secondary messenger; others with odours which are more pine or
menthol-like have a different mode of action. There is therefore some correlation
between their mode of action and their odour and chemical composition. The numerous aromatherapeutic uses for Geranium oil are yet to be scientifically validated,
although there is every reason to accept the scientific evidence that inhalation of the
aroma and its action through the limbic system has a relaxing effect; theoretically, this
could lead to the acceptance that many stress-related conditions like dermatitis,
asthma, intestinal problems and headaches could be alleviated.

2002 Edited by Taylor & Francis

Part 1

Geranium

2002 Edited by Taylor & Francis

History of nomenclature, usage


and cultivation of Geranium
and Pelargonium species
Maria Lis-Balchin

The genera Geranium and Pelargonium have remained confused for over 200 years, even
after Linnaeus (1753) and his binomial system of classification. Both genera were
then placed under the genus Geranium and although Sweet (1820) re-classified them
under two genera, acceptance by the general public as well as nurserymen is still
minimal.
The majority of plants sold as geraniums in garden centres, shops and supermarkets
are Pelargonium species and cultivars. There are however some Pelargonium cultivars sold
as Pelargoniums at garden centres: these are the large-flowered Regal Pelargoniums.
All the scented-leaf Pelargoniums, on the other hand, even those with large flowers, are
almost invariably sold as geraniums.
Most of the books about Pelargonium are mis-headed e.g. Geraniums (Delamain and
Kendall, 1987); Miniature and Dwarf Geraniums (Bagust, 1988); Geraniums for
home and garden (Shellard, 1981). The only difference between genera is seen when
books are entitled Hardy Geraniums (Bath and Jones, 1994; Yeo, 1985), which signifies that the true Geranium genus alone will be involved. This is because Pelargonium
species are not hardy plants and are not able to survive the weather in Europe, unlike
the hardy Geranium species found everywhere in hedgerows, wastelands and rockeries.
Pelargonium species originate from South Africa and different species are found in
distinct habitats. The Pelargonium species related to the Geranium oil-producing
cultivars are mainly located in the Cape area. The first Pelargonium species, Pelargonium
triste was brought over from the Cape to Leiden before 1600, then John Tradescant
obtained the species in 1631 (Miller, 1996), following this, other species were brought
over by various botanists for the next 300 years and hybridization became very
rampant. This occurred especially during Victorian times, where almost every rich
landowner had conservatories and glasshouses dedicated to the tender and rare plants,
which included the novelty Pelargonium species.
There are numerous misnomers given for the origin of Geranium oil in the dozens
of Aromatherapy books appearing during the last few decades, as well as some
scientific reference books (Fenaroli, 1997). The worst misnomer shows the total
misconception of the genus as in many aromatherapy books and journals, Geranium
maculatum, Geranium robertianum and other Geranium species are implicated either
directly or indirectly. This arose due to the unfortunate original mistake by aromatherapy
book authors, who read up the medicinal properties of true geranium from the many
Herbals (Culpeper, 1653, 1835; Gezard, 1597; Grieve, 1937) and thought that those
were attributable to the Pelargonium species.

2002 Edited by Taylor & Francis

Maria Lis-Balchin

For example, we have an amazing botanical concoction in this quote: The oil is
extracted not from the familiar brightly coloured geranium but from the species
Pelargonium Geranium Robert or lemon plant which is very often displayed in
abundance in Greek restaurants (Worwood, 1991).
Tisserand (1985) informs us that: Pelargonium odorantissimum graveolens grows about
2 ft. in height, has serrated, pointed leaves, and small, pink, flowers. The whole plant
is aromatic. It is found on wastelands, in hedgerows, and on the outskirts of woods. It
was used by the ancients as a remedy for wounds and tumours. He is undoubtedly
referring to G. robertianum (Culpeper, 1835), as the quote is partly extracted from this
source, and it continues: all geraniums are vulneraries but this herb more particularly
so, only rather more detersive and diuretic, which quality is discovered by its strong,
soapy smell.
Another quote taken from Lawless (1992) again shows a lack of understanding of the
origins of Geranium oil: The British plant herb Robert (G. robertianum) and the
American cranesbill, (G. maculatum) are the most widely-used types in herbal medicine
today, having been used since antiquity, as this has nothing to do with Pelargonium. In
fact this statement is partly true, as the main usage of Geranium species is in herbal
medicine, whilst that of the Pelargonium-derived geranium oil is in perfumery,
cosmetics and aromatherapy products. Furthermore, Geranium species are usually used
as a tea or alcoholic extract which is taken orally; comparatively few external applications are mentioned and these again use the water-soluble or alcoholic extracts and not
essential oils (EOs) (Culpeper, 1835; Grieve, 1937).
One of the misnomers most frequently used is Pelargonium odoratissimum or
P. odorantissimum (Lawless, 1992; Valnet, 1984) and Pelargonium odorantissium
(Westwood, 1991). Pelargonium odoratissimum is an actual species, with very small,
white, apple-scented leaves (van der Walt, 1977), and not used for Geranium
oil production. The name Pelargonium odoratissimum probably came from a particular P. graveolens variety as odoratissimum i.e. it was not a true species but a very
odoriferous variety. The name P. odoratissimum was then misquoted by Knuth (1912).
The early writers about (EOs) (Guenther, 1950) as well as the trade distributors used
the wrong name and it has been perpetuated by aromatherapists, who after all, are
not botanists.
Another misnomer used is P. asperum: which is described as a cross between unknown
parents (Knuth, 1912) and by Harvey (1860) as a garden variety of P. quercifolium
(which has a camphoraceus smell). On the other hand, almost identical drawings are
shown by Mastalerz (1982) for P. graveolens (LHeritier, 1792) and P.  asperum adapted
from G. radula Roth, but to confuse the issue further, P. asperum Ehrhart ex Willd is in
fact a hybrid between P. graveolens  P. radens.
Yet another name often used is P. roseum Willd. The problem is that Willdenovs
Herbarium (1800) shows two identical plants: one is labelled as P. radula var. roseum and
the other as P. graveolens var. roseum, but the description matches that of the hybrid
P. radula  P. graveolens which shows once more that it is not a species.
A fourth misnomer is P. graveolens. This may be partly true for some Geranium oil
originating in Africa (Ducellier, 1933), but this is doubtful as the species has a more
distinctive peppermint aroma (Demarne and van der Walt, 1989; Lis-Balchin, 1991).
However, the main source of the oil is from a cultivar known as P. cv. Ros which gives
rise to the commercial Geranium oil, Bourbon and originated from hybridization in
England, probably in the eighteenth century, and the cultivar was then exported to the

2002 Edited by Taylor & Francis

History of nomenclature, usage and cultivation of Geranium and Pelargonium 7

South of France and Reunion and also lately to China. The Ros cultivar has been
found to be, most probably, a hybrid between P. capitatum  P. radens (Demarne and van
der Walt, 1989). The cultivars used for the production of Geranium oil in many parts
of the world remain confused; in some papers originating in India, the cultivar is stated
to be that obtained as a cutting from the cultivar Ros from Reunion, however, many
papers state that their Geranium oil source is from P. graveolens.
The main usage of Geranium species is in herbal medicine, whilst that of the
Pelargonium-derived Geranium oil is in perfumery, cosmetics and aromatherapy
products. The production of commercial Geranium oil, from several Pelargonium
cultivars, is now mainly in Reunion, Egypt and China; however the true sales of
Geranium oil are greatly in excess of that derived from plants, due to the ever-increasing
production of synthetic and nature-identical Geranium oil. Geranium oil contains
mainly citronellol and geraniol and their esters, therefore can be easily concocted from
cheaper EOs and adjusted to the recommended ISO standards. The actual odour can be
even more appreciated by perfumers than the real essential oil. Synthetic Geranium oil
also has a more potent antimicrobial activity (Lis-Balchin et al., 1996).
The pharmacological activity of the water-soluble extracts of the two genera are not
very different: they both have a high proportion of tannins and have an antidiarrhoeal
function (Watt and Breyer-Brandwijk, 1962). The lipophylic EOs of Pelargonium
species have mainly a spasmolytic effect on smooth muscle, except for P. grossularioides,
which was used as an abortifacient in southern African folk medicine (Watt and BreyerBrandwijk, 1962) and has been shown to have a spasmogenic action on smooth and
uterine muscle in vitro (Lis-Balchin and Hart, 1994).
Many Pelargonium species were used as folk medicines: herbal teas and extracts of
leaves, tubers and roots were used (Watt and Breyer-Brandwijk, 1962) and one of these,
Umckaloabo, from P. sidoides or P. reniforme, is now commercially produced for use in
respiratory ailments (Kolodziej and Kaiser, 1997; Kolodziej et al., 1995).
Pelargonium EOs from leaves of the many different species and cultivars (other than
those grown to produce commercial Geranium oil) have very different odours and
chemical compositions, but most of the floral-smelling ones act through cyclicAMP as
the secondary messenger; others with odours which are more pine or menthol-like
have a different mode of action (Lis-Balchin and Hart, 1998). There is therefore
some correlation between their mode of action and their chemical composition. The
antimicrobial effects have also been studied in vitro on a number of bacteria and in vivo
as food preservatives, with promising results (Lis-Balchin et al., 1998a). The antimicrobial effect could not be directly correlated with the chemical composition so far
(Lis-Balchin and Roth, 2000), although an inverse relationship was found between the
amount of 1,8-cineole and antifungal activity (Lis-Balchin et al., 1998b). The DNA
relationship with chemical composition has also been studied in a number of scented
Pelargonium species and some correlation has become apparent (Piotrowski et al., 1999).
This has alsoprovided another aspect of chemotaxonomy to add to the alkaloid
chemotaxomy (Lis-Balchin, 1996, 1997; Lis-Balchin et al., 1996a).
The numerous aromatherapeutic uses for Geranium oil, both through massage and
inhalation, are yet to be scientifically validated (Lis-Balchin, 1997a), although there is
every reason to accept the scientific evidence that massage in itself can relax and that
inhalation of a pleasant aroma and its action through the limbic system also has a relaxing
effect (Buchbauer et al., 1991; Jellinek, 1954, 1956; Kubota et al., 1992; Manley, 1993;
Stoddart, 1990; Torii et al., 1988; Vickers, 1996). Theoretically, this could lead to the

2002 Edited by Taylor & Francis

Maria Lis-Balchin

acceptance that many stress-related conditions like dermatitis, asthma, intestinal


problems and headaches could be alleviated by the use of Geranium oil.
True Geranium species were used in the past all over the world. G. maculatum or
American cranesbill root was used as styptic, astringent, tonic, for piles and internal
bleeding; excellent as an injection for flooding and leucorrhoea; taken internally for
diarrhoea, childhood cholera, chronic dysentery and for gargling (Grieve, 1937). It
contains tannins and is said to be effective against stomach ulcers and inflammation of
the uterus and has possibilities in treating cancer (Chevallier, 1996).
Geranium species are used nowadays mainly in Japan, USA and also in eastern Europe.
Geranium thunbergii, which is one of the most important medicinal plants in Japan
(gen-noshouko) is used as an antidiarrhoeal folk medicine (Ishimaru and Shimomura,
1995). The use is the same therefore as that for many Pelargonium species in South
African folk medicine (Watt and Breyer-Brandwijk, 1962). It contains a large concentration of phenolic constituents in the form of hydrolyzable tannins such as corilagin,
geraniin and elaeocarpsin. Although elaeocarpsin has a high potential for tannin
activity, as measured in combination with proteins e.g. collagen, gelatin, casein,
haemoglobin, it shows little astringency. Due to this characteristic, which only slightly
stimulates the alimentary canal, it is used for treating digestive diseases. It is also used
for various other diseases (Nishioka, 1983) including psychotropic diseases (Ueki et al.,
1985). Geranium has also shown antiviral action (Courtout et al., 1991).
Both Geranium and Pelargonium species have been reproduced using micropropagation and some success has been made in producing active components by tissue culture
(Charlwood and Charlwood, 1991; Ishimaru and Shimomura, 1995). The means are
there therefore for producing plants as well as new active components when they are
discovered.

REFERENCES
Bagust, H. (1988) Miniature and Dwarf Geraniums, Christopher Helm, London.
Bath, T. and Jones, J. (1994) Hardy geraniums, A gardeners guide to growing, David & Charles,
Devon.
Buchbauer, G., Jirovetz, L., Jager, W., Dietrich, H., Plank, C. and Karamat, E. (1991).
Aromatherapy: evidence for the sedative effects of the essential oils of lavender after inhalation. Z. Naturforsch., 46, 10671072.
Charlwood, B.V. and Charlwood, K.A. (1991) Pelargonium spp. (Geranium): In vitro culture and
the production of aromatic compounds. In Y.P.S. Bajaj (ed.), Biotechnology in Agriculture and
Forestry vol. 15, Medicinal and Aromatic Plants III, Springer-Verlag, Berlin, pp. 339352.
Chevallier, A. (1996) Encyclopedia of Medicinal Plants, Dorling Kindersley, London.
Courtout, J., Pieters, L.A., Claeys, M., Berghe, D.A.V. and Vlietinck, A.J. (1991) Antiviral
ellagitanins from Spondias mombin. Phytochemistry, 30, 11291130.
Culpeper, N. (1653) The English physitian Enlarged, George Sawbridge, London.
Culpeper, N. (1835) The Complete Herbal. Reprinted, Th. Kelly, London.
Delamain, B. and Kendall, D. (1987) Geraniums., Christopher Helm, London.
Demarne, F. and van der Walt, J.J.A. (1989) Origin of the rose-scented Pelargonium grown on
Reunion Island. S. Afr. J. Bot., 55, 184191.
Ducellier, L. (1933) Bull. Soc. Hist. Nat. Afrique du Nord, 24, 142148.
Fenaroli, G. (1997) Handbook of flavour ingredients, 3rd ed. CRC Press, London. Vol. 1.
Gezard, J. (1597) The Herball or General History of Plants, John North, London.
Grieve, M. (1937) A Modern Herbal. Reprinted 1992, Tiger Books International, London.

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History of nomenclature, usage and cultivation of Geranium and Pelargonium 9


Guenther, E. (1950) The Essential Oils, Vol. 4. Van Nostrand Co., New York.
Harvey, W.H. (1860) Flora capensis, Hedges, Smith & Co., Dublin.
Ishimaru, K. and Shimomura, K. (1995) Geranium thunbergii: In vitro culture and the production
of geraniin and other tannins. In: Biotechnology in Agriculture and Forestry, Vol. 33. Medicinal
and Aromatic Plants VIII ed. Bajaj, Y.P.S. Springer-Verlag, Berlin, pp. 232247.
Jellinek, P. (1954) The Practice of Modern Perfumery, Leonard Hill, London.
Jellinek, P. (1956) Die Psychologischen Grundlagen der Parfumerie. Alfred Hutig Verlag, Heidelberg.
Kolodziej, H. and Kaiser, O. (1997) Pelargonium sidoides D.C. Neuste Erkenntnisse zum
Verstndnis des Phytotherapeutikums Umckaloabo. Z. Phytother., 19, 141151.
Kolodziej, H., Kaiser, O. and Gutman, M. (1995) Arzneilich verwendete Pelargonien aus
Sudfrika. Disch. Apotheker Ztg., 135, 853864.
Knuth, R. (1912) Das Pflanzenreich, 4, 129, Berlin.
Kubota, M., Ikemoto, T., Komaki, R. and Inui, M. (1992) Odor and emotion-effects of essential oils on contingent negative variation. Proc. 12th Int. Congress on Flavours, Fragrances and
Essential oils, Vienna, Austria, Oct. 48. pp. 456461.
L Heritier, C.L. (1792) Geraniologia. Paris.
Lawless, J. (1992) The Encyclopaedia of Essential Oils., Element, Dorset.
Linnaeus, C. (1753) Species Plantarum, Stockholm.
Lis-Balchin, M. (1991) Essential oil profiles and their possible use in hybridization of some common scented Geraniums. J. Essent. Oil Res., 3, 99105.
Lis-Balchin, M. and Hart, S. (1994) A pharmacological appraisal of the folk medicinal usage of
Pelargonium grossularioides and Erodium cicutarium (Geraniaceae). Herbs, Spices Med. Plants,
2, 4148.
Lis-Balchin, M. (1996) A chemotaxonomic reappraisal of the Section Ciconium, Pelargonium
(Geraniaceae). S. Afr. J. Bot., 62, 277279.
Lis-Balchin, M., Deans, S.G. and Hart, S. (1996) Bioactivity of commercial Geranium oil from
different sources. J. Essent. Oil Res., 8, 281290.
Lis-Balchin, M., Houghton, P. and Woldermariam, T. (1996a) Eleocarpidine alkaloids from
Pelargonium species (Geraniaceae). Nat. Prod. Letts., 8, 105112.
Lis-Balchin, M. (1997) A chemotaxonomic study of Pelargonium (Geraniaceae) species and their
modern cultivars. J. Hort. Sci., 72, 791795.
Lis-Balchin, M. (1997a) Essential oils and Aromatherapy: their modern role in healing. J. Roy.
Soc. Health, 117, 324329.
Lis-Balchin, M. and Hart, S. (1998) Studies on the mode of action of scented-leaf Pelargonium
(Geraniaceae). Phytother. Res., 12, 215217.
Lis-Balchin, M., Buchbauer, G., Hirtenlehner, T. and Resch, M. (1998a) Antimicrobial activity
of novel Pelargonium essential oils added to a quiche filling as a model food system. Lett.
Microbiol., 27, 207210.
Lis-Balchin, M., Deans, S.G. and Eaglesham, E. (1998b) Relationship between the bioactivity
and chemical composition of commercial plant essential oils. Flav. Fragr. J., 13, 98104.
Lis-Balchin, M. and Roth, G. (2000) Composition of the essential oils of P. odoratissimum,
P. exstipulatum and P. fragrans (Geraniaceae). Flavor & Fragr. J., 15(6), 391394.
Manley, C.H. (1993) Psychophysiological effect of odor. Crit. Rev. Food Sci. Nutr., 33, 5762.
Mastalerz, J.W. (1982) Geranium A Penn State Manual, 3rd ed. Pennsylvania Flower Growers.
Miller, D. (1996) Pelargoniums B.T. Batsford Ltd, London.
Nishioka, I. (1983) Chemistry and biological activities of tannins, Yakugaku Zasshi, 103,
125142.
Piotrowski, A., Bogdan, A., Lis-Balchin, M. and Ochocka, J.R. (1999) Genetic relationships
among Pelargonium genus assessed by RAPD-PCR method. 2000 years of Natural Products
Research: Past, Present and Future. Amsterdam, 2630 July 1999, Poster.
Shellard, A. (1981) Geraniums for Home and Garden, David & Charles, Devon.
Stoddart, M. (1990) The Scented Ape, University Press, Cambridge.
Sweet, R. (18201830) Geraniaceae, London.

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Tisserand, R. (1985) The Art of Aromatherapy, Revised ed. C.W. Daniel Co. Ltd, Saffron Walden,
p. 231.
Torii, S., Fukuda, H., Kanemoto, H., Miyanchio, R., Hamauzu, Y. and Kawasaki, M. (1988)
Contingent negative variation and the psychological effects of odor. In: Perfumery: The psychology and Biology of Fragrance. S. Toller and G.H. Dodds (eds), Chapman & Hall, New York.
Ueki, S., Nonaka, G., Nishioka, I. and Fujiwara, M. (1985) Psychotropic activity of GAO and
its active substances. J. Med. Pharm. Soc., Wakan-Yaku, 2, 502503.
Valnet, J. (1984) Aromatherapie, Maloine, S.A., Paris.
van der Walt, J.J.A. (1977) Pelargoniums of Southern Africa, Vol. 1. Purnell and Sons, Cape Town.
Vickers, A. (1996) Massage and Aromatherapy. A Guide for Health Professionals, Chapman & Hall,
London.
Watt, J.M. and Breyer-Brandwijk (1962) The Medicinal Plants of Southern Africa, Livingstone
Ltd, Edinburgh.
Westwood, C. (1991) Aromatherapy. A Guide for Home Use, Amberwood Publishing Ltd, Dorset.
Willdenov, C.L. (1800) Species Plantarum, Berlin.
Worwood, V.A. (1991) The Fragrant Pharmacy, Bantam Books, London.
Yeo, P.F. (1985) Hardy Geraniums, Croom Helm, London.

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The taxonomy of Geranium species


and cultivars, their origins
and growth in the wild
Diana M. Miller

HISTORY OF DISCOVERY

A number of species are native to Europe and there are records of geraniums in old
herbals since the late sixteenth and early seventeenth centuries. A few have been used
in herbal remedies in the past but may not have been cultivated. Species such as
Geranium robertianum are common wild plants in many parts of the country. More
recently, species have been introduced into cultivation such as G. maculatum from North
America which was used as a medicinal plant in the eighteenth century. Other species
were introduced from further afield mainly for their ornamental features from countries
around the Mediterranean, the Himalayas and the Far East and even towards the end of
the twentieth century, new species were still being introduced.
GENERAL CHARACTERISTICS OF THE GENUS GERANIUM

In habit, the species are herbaceous, annual, biennial or perennial and sometimes woody
at the base; a few have tubers. All have petiolate, usually glandular or aglandular hairy,
palmate to deeply palmately divided leaves; the divisions toothed or lobed, with stipules. The stem leaves are normally opposite but the lower leaves may be alternate. The
flowers of Geranium often pink or purplish or bluish-pink, are arranged in pairs or solitary or in small umbels subtended by bracteoles. Each radially symmetrical flower has
five, usually hairy sepals with mucronate apex, usually increasing in size as the fruit
develops. The five equal, free petals with a nectary at their base, may be clawed and are
sometimes notched at the apex. The ten free stamens, about as long as the sepals, are in
two whorls, the anthers of the outer dehiscing before those of the inner whorl. The style
divides into five stigmas, which open after the anthers have dehisced, thus avoiding self
pollination. Once the flower is fertilised, the five mericarps each containing a single
seed develop. The method by which the awned mericarps is separated is important in
division of the genus into three subgenera.
NATIVE HABITATS

The genus Geranium contains about 300 distinct species, the majority of which are to be
found in the Northern Hemisphere, mainly in temperate climates. Some may be found
in the tropics but at high altitudes in montane conditions. Many of those in cultivation
are from Eurasia and North America but species also grow wild in North and South
Africa, Australia, New Guinea and islands in the Atlantic and Pacific Oceans. Most of

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Diana Miller

those found in cultivation are hardy but some are slightly less such as G. maderense from
Madeira. In the warmer areas, many of the species are annual, passing the hottest part of
the year as seed or, if perennial, may have a tuber and die down in the summer. Species
native to alpine regions are frequently low growing. The perennial species, some
reaching well over 1 m in height, tend to be found in grasslands or wood margins.
CLASSIFICATION HISTORY

The earliest references to the genus, included so few species that no attempts were made
to classify them. However by 1912, Knuth produced his monograph, which included
over 250 species and a means of separating groups became important. He used the characteristics of the rootstock to make basic separations between the perennial plants and
kept the annuals in a separate group. More recently, Yeo (1984) recognised different
methods of seed discharge as an important characteristic. The fruit can break in three
different ways and this is used to create three subgenera within the genus, each subdivided into a number of smaller sections. However, this method results in the very large
section Geranium within the subgenus, Geranium, which contained the majority of the
known species. This has therefore been subdivided informally using other morphological features into groups (Yeo, 1985, 1992).
Subgenus Geranium
This subgenus includes over 250 annuals and perennials. The fruit breaks apart using
a method described as seed ejection because as the fruit splits, the seed is thrown upwards
out of the mericarps as the awn curves backwards. The awn may or may not remain
attached to the remaining part of the fruit. The mericarps are smooth.
Section Geranium

This very large section is recognised by the method of discharge of seeds in which the
awn remains attached to the central column of the fruit after the seeds are released.
Immediately before the seeds are discharged, they are retained within the mericarp by
bristles at the lower end of the mericarp. The section is divided into groups.
Endressii group

These are perennials with erect funnel-shaped flowers, petals usually notched and leaves
with diamond-shaped divisions.
G. endressii Gay: This is an evergreen perennial measuring up to about 45 cm with rhizomes near or on the surface. Flowers are bright pink about 3.5 cm across with barely
notched petals. Leaves are light green, somewhat wrinkled, 510 cm wide deeply
divided into five.
This is a summer flowering species native to the western Pyrenees with a number of
cultivars such as Wargrave Pink with numerous salmon pink flowers.
G. versicolor Linnaeus: Similar to G. endressii, this species has less divided leaves and
flowers, which are white, conspicuously veined, reddish-purple and distinctly notched
petals. It is native to southern Europe from Italy to Greece.
G.  oxonianum Yeo: This is a vigorous fertile hybrid between G. endressii and G. versicolor reaching 80 cm in height with pink-veined flowers to 4 cm diameter and notched
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The taxonomy of Geranium species and cultivars

13

petals. A large number of garden plants are cultivars of this hybrid such as
A.T. Johnson with silvery pink flowers. In f. thurstonianum the flowers have very
narrow strap-shaped purple flowers.
G. nodosum Linnaeus: This is a deciduous perennial, up to 50 cm, with leaves divided
into 35 toothed but not lobed divisions, 25 cm wide. Flowers are up to 3 cm diameter and are bright purple-pink with darker veins.
It is a native of southern Europe from central France to Yugoslavia, flowering in the
summer.
Sylvaticum group

These are perennial plants, leaves with broad much lobed divisions and relatively small
sepals.
G. sylvaticum Linnaeus: The plant is up to about 70 cm tall with glandular hairs and
leaves to over 20 cm wide deeply divided into seven or nine deeply cut divisions.
Flowers are usually purplish-blue, but sometimes pink or white, with a white centre
23 cm across, produced in early summer.
This plant grows wild in most parts of Europe to Turkey. A number of cultivars
include Album with white flowers and Mayflower with a bright violet-purple flower
but a smaller white centre.
G. psilostemon Ledebour: This is a tall erect perennial measuring to well over 1 m. Leaves
are up to 30 cm across, deeply divided into 7 divisions and lobes are divided and
toothed. Flowers are shallow cupped, up to 3.5 cm diameter and petals very bright
purplish-red, black at the base and with black veins.
This is a summer flowering species native to North Turkey and the southern Caucasus.
Pratense group

This includes perennials with large blue or pink flowers, petals not notched and usually
with glandular hairs at least on inflorescence.
G. himalayense Klotzsch: This is a deciduous spreading perennial to about 50 cm with
leaves up to 12 cm across, divided into seven sections, each more or less three-lobed and
toothed. Flowers are large, saucer shaped, up to 6 cm wide, blue or deep blue, with
a calyx which is not inflating after flowering.
Long flowering through the summer, this species is found wild in the Himalayas.
G. pratense Linnaeus: This is a deciduous perennial which may reach well over 1 m in
height. Leaves are divided almost to the base into seven or nine divisions, each deeply
pinnately divided, 1025 cm wide. Flowers are 3.54.5 cm, saucer-shaped, blue to
violet-blue or sometimes white, with a calyx which is inflated after flowering.
Flowering in summer, this species is native from Europe to western China and many
well known garden plants are cultivars of this species such as Mrs Kendall Clark
a light pearl gray-blue and the double flowered Plenum Caeruleum. This plant has
been used to produce a dye and the roots used in tanning.
Erianthum group

This includes perennials with few stem leaves but dense inflorescence of rather flat
flowers with petals unnotched, native to north-east Asia.
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Diana Miller

G. erianthum De Candolle: This is a deciduous perennial up to about 50 cm with leaves


520 cm wide divided nearly to base into seven or nine-lobed, overlapping divisions.
Flowers are 3 cm or more in diameter, light to dark purplish-blue and conspicuously
veined. Native to Japan, this is a very hardy species flowering in early summer, also
found in Siberia and north-western North America.
Wallichianum group

Plants with scrambling or trailing stems and leaves divided to 75 per cent or less. The
species are native to the Himalayas.
G. wallichianum D. Don: This is a deciduous, trailing perennial plant without a basal rosette
of leaves. Stem leaves are divided into five. The flower is saucer-shaped or more or less flat
up to 3.5 cm across, purple or pinkish-purple, veined and sometimes white at the base.
This is a variable species from western Himalayas from which a number of cultivars
have been selected such as the dense creeping, Buxtons Variety with smaller marbled
leaves and blue flowers. The roots of this plant have been used for dying and tanning.
G. procurrens Yeo: This is a perennial plant with long trailing red stems to 1 m, rooting
at the nodes. Leaves are 510 cm, divided into five, each division being shallow-lobed.
Flowers are 2.53.5 cm across, pinkish-purple with a distinct black v-shaped mark at
the base and veined with black.
This species is found in the Himalayas in Sikkim and Nepal.
Palustre group

These are bushy perennial plants with main leaves deeply divided, hairy but not glandular and flowers are pink to purple.
G. wlassovianum Link: This is a deciduous, perennial, densely hairy plant up to about
40 cm in height with softly hairy, gray-green leaves normally divided into seven
sharply toothed divisions. Flowers are 34 cm across, saucer-shaped, pale pink to pale
reddish-purple with conspicuous darker veins.
This is a very hardy mid-summer flowering plant from eastern Russia, Siberia and
northern China.
Pylzowianum Group

These are low growing alpines from western China with small underground tubers.
Flowers are few.
G. orientalitibeticum Knuth: This is a dwarf plant reaching 35 cm in height with distinct
strongly marbled, almost round leaves to about 7 cm across, deeply divided into 5-lobed segments. Flowers are more or less flat about 2.5 cm diameter, purplish-pink, white in centre.
This is a summer flowering species native to western China.
G. pylzowianum Maximowicz: This is a low growing perennial up to 25 cm tall and
individual leaves raising directly from the tubers, up to 6 cm across, divided into five
or seven narrow divisions, each further divided into narrow segments. Flowers are few,
about 3 cm in diameter, trumpet-shaped, deep pink fading to white at the base.
This is a species flowering in early summer from western China.

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Sanguineum group

This is made up of perennial plants with rhizomes and few basal leaves but leafy
flowering stems. Leaves are deeply divided into narrow segments, and flowers are large
and petals usually notched.
G. sanguineum Linnaeus: This is a low growing deciduous, perennial to about 30 cm in
height, with leaves 28 cm across, deeply cut almost to the base into narrow segments.
Flowers are saucer-shaped on one-flowered peduncles, to over 4 cm across, petals being
notched and white to deep purplish-red.
This is a summer flowering species native to Europe and Turkey. A large number of
cultivars are available such as the white flowered Album, the rose pink Glenluce and
Elspeth with large bright purple flowers. In var. striatum the flowers are white with
pale pink veins giving the impression of flesh pink flowers.
Sibiricum group

This includes perennial plants with leaves variously divided and small flowers.
G. thunbergii Lindley & Paxton: This is a spreading perennial, hairy plant with trailing
stems up to about 25 cm, sometimes rooting at the nodes, with leaves of light green,
510 cm wide, often blotched purple between the leaf divisions in winter. Flowers are
small to 5 cm across white to dark purple-pink.
This species is native to northern China and Japan and flowers in summer.
Sessiliflorum group

This includes perennial plants with a rosette of leaves but trailing inflorescence stems.
Flowers are in one-flowered clusters with the pedicel exceeding the peduncle.
G. sessiliflorum Cavanilles: This is an evergreen perennial plant with leaves 1.54.5 cm
across and small white flowers barely 1 cm in diameter.
It is a species from Australasia and is represented in gardens by ssp. novae-zelandiae
and more frequently by the cultivar Nigricans with dark bronze-leaves, which turn
orange as they fade.
Incanum group

This is a group of perennial species from South Africa with divided stipules, finely and
deeply divided leaves and notched petals.
G. incanum N.L. Burman: This is an evergreen perennial up to over 50 cm tall with
aromatic leaves which are finely divided into linear segments rarely exceeding
1 mm in width, with long white hairs on underside. It flowers in early summer to
early autumn and these are white or very pale pink in var. incanum but deep pink
and larger 2.53.5 cm in diameter in var. multifidum.
Maculatum group

This includes annual or perennial plants from North America with glandular hairs and
sepals with long mucronate points.
G. maculatum Linnaeus: This is a deciduous perennial plant, up to about 70 cm tall with
leaves up to 20 cm across, divided almost to the base into normally five sections, sharply

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Diana Miller

toothed in the upper part. Flowers are up to 3 cm in diameter, shallow-cupped, pale to deep
pink with a white centre, sometimes white sepals, with mucronate apex of 23.5 mm long.
This species grows wild in eastern North America and flowers in summer.
Section Dissecta

This includes annual, biennial or perennial plants. The seeds are retained within the
mericarp until the moment of release by a part of the wall which extends like a prong
and the awn remains attached to the central fruiting column after the seeds are released.
G. aspholdeloides N.L. Burman: This is a perennial species with leaves up to 8 cm across,
deeply divided into five or seven lobes. Flowers are up to 3.5 cm diameter, light to dark
pink with deeper coloured veins. This species is native to Europe and the Middle East.
Section Tuberosa

This includes annual, biennial or perennial plants with notched petals. The awn of the mericarp does not remain attached to the central fruiting column after the seeds are released.
Tuberosum group

This includes perennial plants with underground tubers, becoming dormant in


summer after flowering; leaves are deeply divided. Flowers are usually pinkish to
purplish-pink.
G. tuberosum Linnaeus: This is an erect plant up to about 40 cm with leaves up to
10 cm across, deeply divided into seven notched petals.
It is native to the Mediterranean region, eastwards to Iran. The tubers have been used
for food.
G. malviflorum Boissier: This is a large perennial, leaves usually over 10 cm wide less
finely divided than those of G. tuberosum, and the flower is large, bluish-purple with
darker veins up to 4.5 cm across, notched at the apex.
It is native to North Africa and southern Spain, flowering in spring.
Platypetalum group

This includes annual, biennial or perennial plants with leaves rarely divided to the base.
Flowers are usually bluish-purple.
G. platypetalum Fischer and Meyer: This is a perennial up to about 40 cm, conspicuously
hairy with leaves up to about 1520 cm diameter, divided to about half way into seven
or nine segments, each deeply toothed. Flowers are rather flat in form, up to 4.5 cm
across, dark purplish-blue with notched petals and darker veins.
Native to Turkey and Iran, this species first flowers in early summer and may produce a further flush later in the season.
G.  magnificum Hylander: This is a vigorous sterile hybrid between G. ibericum and
G. platypetalum reaching up to about 70 cm in height, with leaves divided to about
75 per cent into seven to nine deeply toothed divisions which are slightly overlapping.
Flower are a rich bluish purple.
G. renardii Trautvetter: This is a low growing perennial plant with rounded gray-green
felted leaves up to 10 cm across, divided to half way into five or seven broad toothed
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divisions. Flowers are white, or very pale purple, with notched petals and conspicuous
bluish-purple veins.
This is a summer flowering species native to the Caucasus region.
Subgenus Robertium
This is composed of about 30 species. Both annual and perennial species of the subgenus have a fruit discharge described as carpel projection. In this subgenus, the mericarp
containing the seed is projected some distance from the plant and the awn is separated
from the mericarp at the time of the explosive discharge. The mericarp base is rounded
and has no hardened point.
Section Batrachiodes

This includes annual and perennial hairy plants with notched petals and a very small
mucronate apex to the sepals are included in this section. The mericarps are ribbed,
sometimes slightly.
G. pyrenaicum N.L. Burman: This is a perennial up to about 50 cm or so with rounded
leaves up to 10 cm across divided into seven or nine divisions. Flowers are up to 2 cm
wide on long trailing stems, petals being dark pinkish-purple, white at the base with
darker veins and are produced from late spring to early autumn.
It is native to south-western and southern Europe and a white flowered form is also
grown.
Section Unguiculata

This includes perennial plants with glandular hairs. Sepals are erect, petals clawed but
not notched and mericarps are ridged.
G. macrorrhizum Linnaeus: This is an aromatic rather sticky perennial up to 50 cm tall
with leaves up to 20 cm across divided to 75 per cent into seven shallowly divided
lobes. It flowers in summer, with a reddish swollen calyx and clawed white or pink
petals in a dense inflorescence. Stamens are about twice as long as sepals.
This species is native to southern Europe and a number of cultivars with darker (Bevans
Variety) or paler (Album) flowers or variegated leaves (Variegatum) are grown.
G. dalmaticum (Beck) Rechinger: This is a low growing aromatic perennial up to 15 cm
tall. Stems are trailing with small rosettes at the ends of hairless glossy leaves up to
4 cm wide. Flowers are bright pink up to about 2 cm across.
This is a summer flowering plant native to south-western Yugoslavia and Albania.
G.  cantabrigiense Yeo: This is a hybrid between G. macrorrhizum and G. dalmaticum
and this plant is aromatic and low growing up to 20 cm or more tall with light green
leaves intermediate between the parents and pink or white flowers up to 2.8 cm wide.
Section Lucida

This includes plants which are annual with mostly glandular hairs. Sepals are erect,
petals clawed and mericarps glandular hairy with longitudinal ridges.
G. lucidum Linnaeus: This is an annual plant up to about 50 cm with red stems and
somewhat succulent glossy leaves up to 5 cm across, deeply divided into five divisions.

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Diana Miller

Flowers are up to 1 cm across, erect and deep pink. It is found wild from Europe and
North Africa to Asia.
Section Ruberta

This includes annual, biennial or perennial plants with mostly glandular hairs and leaves
divided to the base. Petals are clawed, barely notched and the mericarps are ridged.
G. robertianum Linnaeus: This is an annual, usually overwintering, unpleasant smelling,
with red to reddish-brown hairy stems and leaves. Leaves are over 10 cm across, divided to the base into five-stalked, deeply pinnately divided sections. Flowers are small
up to 1 cm wide, pink, flowering over a long period from spring to autumn.
It is found wild across northern hemisphere from Europe to China and also in North
America where it may have been introduced. Several cultivars with differing flower
colours are grown, especially ones with pure white flowers such as Celtic White. It has
been used medicinally in the past.
Section Anemonifolia

This includes short lived perennials forming very large rosette plants with leaves divided
to the base. Petals are clawed and mericarps ridged. They originate from Madeira.
G. maderense Yeo (Figure 3.1): This is the largest species reaching up to 1.5 m in height
in flower, with leaves up to 60 cm across, each divided to the base into deeply divided
lobes. The stem is over 50 cm tall and produces a rosette of leaves from the centre of
which the tall flowering stem emerges bearing numerous purplish-pink to magenta
flowers, up to 3.5 cm wide, in winter to early spring.
G. palmatum Cavanilles: This is also from Madeira and is not dissimilar but smaller with
less divided leaves up to 35 cm across and slightly larger flowers, with stamens about
twice as long as the sepals. This species flowers in summer.

Figure 3.1 Geranium maderense.

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The taxonomy of Geranium species and cultivars

19

Subgenus Erodioideae
In the third subgenus, the plants are perennial. The fruit discharge is termed Erodium
type where the awn remains attached to the mericarp, containing the seed, as it is
released and becomes coiled but not plumed. The mericarp has a horny point and is
covered with bristles on the sides. There are about 15 species in this subgenus.
Section Erodioideae

This section includes tall branching plants with nodding flowers and spreading or
reflexed petals. The mericarp apex has three to five ridges.
G. phaeum Linnaeus: This is a perennial up to about 80 cm, flowering in late spring to
early summer. Basal leaves are up to 20 cm wide, toothed but not deeply divided, persistent in winter. Flowers are rather flat, over 20 mm diameter, nodding in a one-sided
inflorescence, with slightly reflexed, deep purple to pale purple to grayish lilac petals.
A native to southern and central Europe, this species is naturalised in many countries
further to the North where it may be found in semi-shaded areas such as wood margins,
or in meadows.
A number of cultivars may be found in cultivation which have been selected for their
flower colour from white to very dark purple and at least one has variegated foliage.
Section Subacaulia

This includes mostly low growing alpine plants with silvery or gray green foliage.
Flowers are erect and petals not reflexed. The mericarp apex has one to three ridges.
G. cinereum Cavanilles var. cinereum: This is a rosette forming perennial with a stout rootstock and gray-green basal leaves up to 5 cm across deeply divided into five to seven
three-lobed divisions. It flowers in summer, the flowers being 2.5 cm across, petals
notched, white or pink with bright pink netted veins.
This is a species from Central Pyrenees, which has resulted in a number of cultivars
such as Ballerina with gray leaves and purplish pink flowers.
G. cinereum Cavanilles var. subcaulescens (De Candolle) Knuth: This differs in the dark
green leaves and deep purplish-red flowers with a black mark at the base of each petal.
This variety is native to Turkey and the Balkan region.
G.  lindavicum Knuth: This hybrid, between G. argenteum and G. cinereum, is more vigorous than either parent, with more deeply divided silky leaves compared to those of
G. cinereum and pale pink, net veined petals. A number of named cultivars are grown such as
Apple Blossom with silver-gray leaves and almost white, less conspicuously veined petals.
REFERENCES
Knuth, R. (1912) Geraniaceae, Das Planzenreich, 4, 129.
Yeo, P.F. (1984) Fruit discharge type in Geranium (Geraniaceae): its use in classification and its
evolutionary implications. Bot. J. Linn. Soc., 89, 136.
Yeo, P.F. (1985) Hardy Geraniums, Batsford, London (Reprinted below).
Yeo, P.F. (1992) Hardy Geraniums (2nd edition), Batsford, London.

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Phytochemistry of the genus Geranium


Jeffrey B. Harborne and Christine A. Williams

INTRODUCTION

The phytochemistry of Geranium, a genus of some 300 temperate species (Mabberley,


1997) is reasonably well known today. According to Hegnauers dictionary of plant
chemistry (Hegnauer, 1966, 1989), at least 55 species have been investigated chemically. Furthermore, detailed studies have been carried out on at least three well known
species: G. macrorrhizum, an essential oil plant; Herb Robert, G. robertianum, a European
medicinal plant; and G. thunbergii, a Japanese medicinal plant.
The most characteristic single chemical in the genus is undoubtedly the ellagitannin
geraniin, named as such following its crystallisation from Geranium thunbergii. This substance (see below) is universally present in the leaves of Geranium species. Geraniin,
unlike almost all other hydrolysable tannins, fails to produce an astringent taste when
leaf extracts of G. thunbergii are taken orally (Okuda et al., 1992). This does not mean
that other mammals are not affected by the taste properties of this major chemical.
Geranium plants are well known to be rabbit-proof and one suspects the reason for this
is the high content of leaf tannin.
Another natural compound which presumably takes its name from the genus, is
germacrone. This is a sesquiterpene isolated in quantity from the essential oil of
G. macrorrhizum. This plant oil also yields the monoterpene, geraniol, which is named
after geraniol oil, which is actually derived from plants of the closely related genus
Pelargonium (see Chapter 11). Geranium oil itself is so widespread in nature in the essential oil of hundreds of plants, that it cannot be regarded as characteristic of Geranium or
Pelargonium. Furthermore, the derived monoterpene radical, geranyl, occurs attached to
a variety of other natural products, including a number of flavonoids and coumarins.
In fact, there is little evidence available at present to suggest that either germacrone
or geraniol are widely distributed in Geranium. It is the flavonoid constituents and
particularly two classes of phenolic tannins that have been most widely investigated.
The present account describes the whole range of plant polyphenols that have been
encountered in the aerial parts and roots of these plants.
ESSENTIAL OILS

Aerial parts of G. macrorrhizum have yielded an essential oil containing two well
known monoterpenoids, geraniol (1) and -citronellol (2), together with several
sesquiterpenes. These include germacrone (3), which makes up to 50 per cent of the

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Phytochemistry of the genus Geranium 21

(1) Geraniol

(2) -Citronellol

(3) Germacrone

(4) -Elemene

(5) -Curcumene

Figure 4.1 Essential oil components of Geranium.

oils, -elemene (4) and -curcumene (5) (Ognyanov et al., 1958) (Figure 4.1). Little
has been reported about the essential oils of any other Geranium species.

MONOMERIC FLAVONOIDS

Leaf flavonoids
The leaf flavonoids of Geranium are typical of the Geraniaceae and related dicotyledonous families. They are predominantly flavonols and the commonly occurring quercetin
(6) is universally present. In a survey of acid-hydrolysed leaf tissue of 78 species, BateSmith (1972) reported that quercetin is generally accompanied by the lower homologue
kaempferol (7) (in 93 per cent of the sample) and by the higher homologue myricetin
(8) (Figure 4.2) (in 13 per cent of the sample). Variation in this basic flavonol pattern
is to some extent correlated with the geography of the genus. A primitive pattern,
including myricetin, predominates in plants from the central Eurasian area, while an
advanced pattern, represented by high concentrations of kaempferol, is present in
Mediterranean and American species.
Although it is apparent that the above three flavonols occur in Geranium in glycosidic combination, relatively little is known of the glycosidic pattern of most species.
However, there is one report of an high performance liquid chromatography (HPLC)
survey of Geranium leaves by Okuda et al. (1980). These authors found that quercetin
occurs regularly in the genus as the 3-galactoside, called hyperin (9) Figure 4.2. This was
detected in direct alcoholic leaf extracts of 12 out of 15 species surveyed (Table 4.1). The
content of hyperin varied from 0.03 to 1.6 per cent dry weight, with an average value of
0.43 per cent.
One species apparently lacking in quercetin 3-galactoside is the Japanese G. thunbergii (Table 4.1). Instead, leaves of this plant contain either kaempferol 3-rhamnoside

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Jeffrey Harborne and Christine Williams

(6) Quercetin

(7) Kaempferol

(8) Myricetin

(9) Hyperin

(10) Kaempferol 3-rutinoside


4-glucoside

(11) Quercetin 3-glucuronide

(12) Vitexin

Figure 4.2 Leaf flavonoids of Geranium.

or a mixture of kaempferol 3-arabinoside-7-rhamnoside and kaempferol 3,7-dirhamnoside (Kawamura et al., 1995). There are thus two chemical races in flavonoid content,
but the occurrences of the two races do not correspond with any other variable features
of this plant species.

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Phytochemistry of the genus Geranium 23


Table 4.1 Geraniin and hyperiin content of the dry leaves of Geranium species
Species

Geranin (%)

Hyperin (%)

Month of collection

G. eriostemon Fisch. var reinii Maxim


G. erianthum DC.
G. soboliferum Komar.
G. krameri Franch. et Savat.
G. yoshinoi Makino
G. yesoense Franch. et Savat.
G. yesoense Franch. et Savat. var. nipponicum Nakai
G. shikokianum Matsum.
G. sibiricum L. var. glabrius Ohwi
G. thunbergii Sieb. et Zucc.
G. wilfordii Maxim.
G. wilfordii Maxim. var. hastatum Hara*
G. tripartitum R. Knuth
G. robertianum L.
G. carolianum L.

7.5
7.6
6.8
6.8
9.8
12
12
6.0
8.1
12
9.5
0.50
12
9.8
11

0.15
0.13
0.16
0.19
0.55
0.18
0.09
0.59

0.21
0.03
1.3

1.6

July
August
October
October
September
August
October
August
October
August
September
September
September
September
May

Note
* Fresh aerial tissue.

Herb Robert, G. robertianum, a plant of medicinal interest, has been examined in


some detail for its flavonol glycosides. Aerial parts yield a mixture of six monoglucosides: kaempferol and quercetin 3-galactoside, quercetin 3-glucoside, quercetin
4-glucoside, quercetin 7-glucoside and quercetin 7-rhamnoside. Accompanying
these monoglycosides are seven 3-diglycosides. Only four of the seven were fully
characterised as the 3-rutinosides and 3-rhamnosylgalactosides of kaempferol and
quercetin (Kartnig and Bucar-Stachel, 1991). Whether Herb Robert varies in its
flavonol glycoside content is not yet clear, but it may be noted that Okuda et al.
(1980) failed to find the quercetin 3-galactoside reported by Kartnig and BucarStachel, 1991) in their particular sample (Table 4.1).
A further four flavonol glycosides, not described so far, have been characterised variously in five Geranium species native to Egypt (Table 4.2). The most distinctive is
kaempferol 3-rutinoside-4-glucoside (10), recorded in G. yemense and G. rotundifolium.
The presence of quercetin 3-glucuronide (11) in G. dissectum is noteworthy (Saleh et al.,
1987) Figure 4.2. The apparent absence of quercetin 3-galactoside from these five
Egyptian species should also be noted.
Table 4.2 Flavonol glycosides of five Egyptian species of Geranium
Species

Major flavonols present

G. yemense
G. rotundifolium

Kaempferol 3-rutinoside-4-glucoside
Kaempferol 3-rutinoside-4-glucoside
Kaempferol 3-rhamnoside
Quercetin 3-glucoside
Myricetin 3-rutinoside
Quercetin 3-glucuronide
Quercetin 3-glucoside
Quercetin 3,7-diglucoside

G. trilophum
G. mascatense
G. dissectum

Source: Data from Saleh et al. (1983).

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Jeffrey Harborne and Christine Williams

(13) Malvidin 3,5-diglucoside

(14) Kaempferol 3-sophoroside

(15) Quercetin 3,7,3,4-tetramethyl ether

Figure 4.3 Floral and exudate flavonoids of Geranium.

Other classes of flavonoid such as glycosylflavones are also present in Geranium according to Bate-Smith (1977) but they have not in general been investigated further. They have
been found to dominate in the case of Geranium phaeum. Here, the flavonol glycosides based
on quercetin are minor components, compared to the five glycosyl flavones: vitexin (12)
(Figure 4.2), isovitexin, orientin, iso-orientin and vicenin (Boutard and Lebreton, 1975).
Floral flavonoids
Most Geranium species have attractive flowers, with colours ranging from blue, purple
and red to pink and white. Anthocyanins, together with co-occurring flavonol glycosides are presumably responsible for those flower colours, but surprising little work has
been carried out on these pigments in the genus. A major study has, however, been
devoted to the bluish-purple or bluish-magenta flowers in G. pratense and G. sanguinea
and in the cultivar Johnsons Blue, a hybrid derived from G. himalayense  G. pratense.
The same major anthocyanin is present in the flower of all three plants. It is malvidin
3,5-diglucoside (13), with a labile acetyl substituent at the 6-position of the glucose
residue attached to the 5-hydroxyl. Thus, it is malvidin 3-glucoside-5-(6-acetylglucoside) (Markham et al., 1997).
In the petals of two of these plant species, the anthocyanin co-occurs with four flavonol
glycosides, namely the 3-glucosides and 3-sophorosides of kaempferol and myricetin.
Colour tests in vitro indicate that kaempferol 3-sophoroside (14) is the most important
co-pigment, shifting the mauve colour of the malvidin glycoside (13) Figure 4.3 towards
the blue region. An additional and unusual feature of flower colour production in these

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Phytochemistry of the genus Geranium 25


Table 4.3 Exudate flavonol methyl ethers of G. macrorrhizum and G. lucidum
Kaempferol

Quercetin

Myricetin

3-methyl ether
4-methyl ether*
3,7-dimethyl ether
3,4-dimethyl ether
7,4-dimethyl ether
3,7,4-trimethyl ether

3,7-dimethyl ether
3,3-dimethyl ether
7,3-dimethyl ether
3,7,3-trimethyl ether
7,3,4-trimethyl ether
3,7,3,4-tetramethyl ether

7,3,4-trimethyl ether
3,7,3,4-tetramethyl ether

Notes
*Lacking in G. macrorrhizum;
lacking in G. lucidum; otherwise all compounds present in both species.

Geranium petals is the presence of a cell sap pH of between 6.6 and 6.8, instead of the
more usual pH at 5.6. This appears to be a very rare feature in nature but is important
for the full colour intensity observed in these flowers (Markham et al., 1997).
Exudate flavonoids
Geranium species regularly have glandular hairs or trichomes on the upper leaf surface.
The chemical constituents of these trichomes can be examined separately from the
internal leaf components by brief rinsing of leaf surfaces in a solvent such as acetone.
Besides the terpenoids and hydrocarbons that are commonly present at the surface, leaf
washes occasionally yield mixtures of lipophilic flavonoids, usually flavonol methyl
ethers. Such compounds have been obtained from leaf surfaces of G. macrorrhizum and
G. lucidum. The structures present are almost identical in both plants and consist of
some 14 kaempferol, quercetin or myricetin methyl ethers (Table 4.3) (Ivancheva and
Wollenweber, 1989).
The above report supercedes an earlier paper by Ognyanov and Ivantcheva (1972) in
which a so-called novel flavonol, 3,5,7,2,4,6-hexahydroxyflavone and kaempferol
3-methyl ether were reported at the surface of G. macrorrhizum. Re-examination of
the evidence for the new flavonol suggests that this was a mistaken identification of
a known flavonol. It may also be noted that quercetin 3,7,3,4-tetramethyl ether (15)
was independently identified as a major lipophilic constituent of G. macrorrhizum by
Nakashima et al. (1973). This compound (15) Figure 4.3 crystallised out in 0.4 per
cent yield from the essential oil of this plant.
TANNINS

Hydrolysable tannins
The major hydrolysable tannin of Geranium is the compound geraniin (16) Figure
4.4, first crystallised from leaf extracts of G. thunbergii. This plant has been used
extensively in folk medicine in Japan. A boiling water extract of G. thunbergii
has been taken by numerous people over many years as an antidiarrhetic and for
controlling intestinal function (Okuda et al., 1992). Geraniin makes up more than

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26

Jeffrey Harborne and Christine Williams

(16) Geraniin

(17) Gallic acid

(18) Ellagic acid

(19) Procyanidin

(20) (+)-Catechin

(21) ()-Epicatechin

Figure 4.4 Tannins and their precursors in Geranium.

10 per cent of the weight of the dried leaf. It forms yellow crystals and, remarkably
for an ellagitannin, completely lacks the astringency normally associated with plant
tannins.
In its chemical structure, geraniin (16) is based on a molecule of glucose, which is
disubstituted in the 3,6- and 2,4-positions by two hexahydroxygallic acid residues.
Additionally, there is a galloyl ester group linked at C-1 of the sugar. Biosynthetically,
geraniin is derived from gallic acid (17) via pentagalloylglucose as an intermediate
(Haslam, 1989).
Geraniin would appear to be the characteristic hydrolysable tannin of the genus
Geranium, since it has been detected by HPLC in every one of the 15 species surveyed
(Okuda et al., 1980) (Table 4.2). The richest source is G. thunbergii, with over 12 per cent
of its dry weight made up by geraniin. Other species range from 0.5 per cent up to

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Phytochemistry of the genus Geranium 27

12 per cent with an average of about 10 per cent dry weight. By comparison with the
leaves, the stems of these plants have only 12 per cent dry weight.
In an earlier survey based on a colour test for ellagitannin developed with nitrous
acid in the absence of oxygen, Bate-Smith (1972) found that some 30 species,
representing 16 sections of the genus, contain ellagitannin (presumably geraniin) in
amounts ranging from 1.3 to 20 per cent dry weight. It seems likely that most, if
not all, known Geranium species contain geraniin or an ellagitannin of similar
structure. The same compound, incidentally extends its distribution to other
members of the Geraniaceae and to other families in the order Geraniales. It has
been detected, for example, in 28 plant species of the Euphorbiaceae. It also occurs
in the cocaine-containing Erythroxylon coca (Erythroxylaceae). Geraniin is however
apparently absent from the closely related genus, Pelargonium, in spite of the fact
that ellagitannins are also abundantly present in Pelargonium species (Okuda et al.,
1980) (see Chapter 11).
Co-occurring with geraniin in the leaves of Geranium species is the related structure,
ellagic acid (18). Bate-Smith (1962) records ellagic acid in the leaves of 4 out of 6
surveyed, in G. meeboldii, G. phaeum, G. robertianum and G. sylvaticum. A richer source
of ellagic acid, is however the plant root and rhizome. Here, it has been recorded in
some 61 species (Hegnauer, 1966). Moreover, so much is present in the roots that ellagic acid can be isolated in crystalline form. Gallic acid (3,4,5-trihydroxybenzoic), which
is a presumed precursor of ellagic, has also been recorded regularly in the leaf
(Bate-Smith, 1962) and the root (Hegnauer, 1966). Gallic acid has been isolated, for
example, from roots of G. maculatum, G. nepalensis and G. pratense.

Condensed tannins
Plants of Geranium contain both hydrolysable and condensed tannin, but the distribution in the different organs varies considerably. The main occurrence of condensed tannin (or proanthocyanidin) is in the root stock, according to Bate-Smith (1973). There
is apparently a suppression of this chemical character in the leaves, where ellagitannins
dominate (see above). Only a handful of 60 species of Geranium surveyed have significant amounts of proanthocyanidins in the leaves. These are: G. polyanthes (Eurasia),
G. platypetalum (Armenia), G. renardii (Caucasus), G. sinense (China), G. incanum (South
Africa) and G. lindenianum (Venezuela).
The proanthocyanidins in Geranium are based on either procyanidin or prodelphinidin or a mixture of the two. No detailed chemistry has yet been carried out on
the condensed tannins of these plants. However, it is likely that the procyanidins are
of a common type (e.g. (19)), since the two procyanidin precursors, ()-catechin (20)
and ()-epicatechin (21) Figure 4.4 have been detected in roots of G. pratense and
G. palustre (Hegnauer, 1966).
The content of procyanidin in fresh rhizomes, as compared to the amount of
ellagitannin, has been shown to be about the same in G. sylvaticum. By contrast, there is
only one-seventh the amount of procyanidin, compared to six-sevenths ellagitannin, in
G. pratense (Hegnauer, 1966). The high content of tannins in the roots has meant that
Geranium species have been employed in the past as good sources of tanning material for
the leather industry. At least two species, G. nepalense and G. wallichianum have been used
in this way.

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Jeffrey Harborne and Christine Williams

MISCELLANEOUS CONSTITUENTS

Aerial parts of G. richardsonii and G. viscosissimum characteristically accumulate the


organic acid, tartaric acid. This acid occurs regularly in members of the Geraniaceae
(Stafford, 1961). However, it is not always present in every Geranium species. Thus,
G. robertianum and G. sanguineum, when analysed, showed the presence of malic and
citric acids, but tartaric acid was missing (Kinzel, 1964).
CONCLUSION

The chemistry of Geranium, as is clear from the above summary, is dominated by phenolic constituents. Not only are these two classes of plant tannin proanthocyanidin and
ellagitannin widely distributed in both aerial and underground tissues. But also there
are a wealth of monomeric flavonoids, variously present in the leaf and petal. We are
only just beginning to appreciate the chemical complexity bound up in the phenolic
fraction of Geranium plants and much further work is required to establish the precise
range of structures that are present in any given species.
Since both the monomeric flavonoids (Rice-Evans, 2000) and the various tannins
(Haslam, 1989) have long been considered to be active components of many medicinal
plants, it is likely that the useful properties in terms of human medicine associated with
Geranium plants may be due to the type and quantity of particular phenolics present.
However, there is no doubt that much further biological experimentation is required
before we can adequately explain the curative properties of these plants.
REFERENCES
Bate-Smith, E.C. (1962) Phenolic constituents of plants and their taxonomic significance.
I Dicotyledons. J. Linn. Soc. (Bot.), 58, 3954.
Bate-Smith, E.C. (1972) Ellagitannin content of leaves of Geranium species. Phytochemistry, 11,
17551757.
Bate-Smith, E.C. (1977) Chemotaxonomy of Geranium. Bot. J. Linn. Soc., 67, 347359.
Boutard, B. and Lebreton, P. (1975) The presence of C-glycoflavones in Geranium phaeum. Plantes
Med. Phytotherapi., 9, 289296.
Haslam, E. (1989) Plant Polyphenols. Vegetable Tannins Revisited, 230pp., Cambridge University Press.
Hegnauer, R. (1966) Chemotaxonomie der Pflanzen, vol. 4, pp. 195197, Birkhauser Verlag, Basel.
Hegnauer, R. (1989) Chemotaxonomie der Pflanzen, vol. 8, pp. 511516, Birkhauser Verlag, Basel.
Ivancheva, S. and Wollenweber, E. (1989) Leaf exudate flavonoids in Geranium macrorhizum and
G. lucidum. Indian Drugs, 27, 167168.
Kartnig, T. and Bucar-Stachel, J. (1991) Flavonoide aus den oberirdischen Teilen von Geranium
robertianum. Planta Med., 57, 292293.
Kawamura, T., Hisata, Y., Noro, Y., Nishibe, S., Sakai, E. and Tanaka, T. (1995) Polyphenols, 94,
Palma de Mallorca, INRA, Paris, pp. 301302.
Kinzel, H. (1964) Organic acids in the leaves of some plants. Ber. Deut. Botan. Ges., 77, 1421.
Mabberley, D.J. (1997) The Plant Book, Cambridge University Press.
Markham, K.R., Mitchell, K.A. and Boase, M.R. (1997) Malvidin 3-glucoside-5-(6-acetylglucoside) and its colour in Geranium Johnsons Blue and other Blue Geraniums. Phytochemistry,
45, 417423.
Nakashima, R., Yoshikawa, M. and Matsuura, T. (1973) Quercetin 3,7,3,4-tetramethyl ether
from Geranium macrorrhizum. Phytochemistry, 12, 1502.

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Phytochemistry of the genus Geranium 29


Ognyanov, I.V. and Ivantcheva, S. (1972) A new hexahydroxyflavone and isokaempferide in
Geranium macorrhizum. Dokl. Bulg. Akad. Nauk., 25, 10571059.
Ognyanov, I., Ivanov, D., Herout, V., Hovak, M., Pliva, J. and Sorm, F. (1958) Structure of germacrone. Chem. Listy, 52, 11631173.
Okuda, T., Mori, K. and Hatano, T. (1980) The distribution of geraniin and mallotusinic acid
in the order Geraniales. Phytochemistry, 19, 547551.
Okuda, T., Yoshida, T. and Hatano, T. (1992) Pharmacologically active tannins from medicinal
plants. In: Plant Polyphenolsi (Hemingway, R.W. and Laks, P.E., eds), pp. 539569, Plenum
Press, New York.
Rice-Evans, C. (ed.) (2000) Wake up to Flavonoids, 74 pp., Royal Society of Medicine Press,
London.
Saleh, N.A.M., El-Karemy, Z.A., Mancour, R.M. and Fayed, A.A. (1987) A chemosystematic
study of some Geraniaceae, Phytochemistry, 22, 25012505.
Stafford, H.A. (1961) Distribution of tartaric acid in the Geraniaceae. Amer. J. Bot., 48, 699701.

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Cultivation and harvesting


of Geranium macrorrhizum and
Geranium sanguineum for
medicinal use in Bulgaria
Tatyana Stoeva

INTRODUCTION

Species belonging to the genus Geranium are known as hardy geraniums and a number
of them are broadly used as ornamental, medicinal and melliferous plants. The most
economically important for their healing and/or aromatic properties are G. macrorrhizum L.
and G. sanguineum L., which are cultivated in Bulgaria.

GERANIUM MACRORRHIZUM L. (SYN. BIGROOTED GERANIUM,


LONGROOTED CRANESBILL)

Introduction
G. macrorrhizum is a perennial herbaceous plant with a long, nodulous, horizontal,
superficial over- and under-ground rhizome, covered with dry brown scales. Basal
leaves are 410 cm wide, fragrant, divided into 57 lobes on 25 cm long petioles
growing in clumps; stem leaves are opposite, on short petioles or cauline. Stems are
1550 cm high, erect, straight with magenta flowers on top. All leaves and stems are
covered with simple and glandular hairs (Webb and Ferguson, 1968; Petrova and
Kozhuharov, 1979; Assenov et al., 1998). The species is distributed in temperate zones
of Europe: Southern Alps, Apennines, south and central Carpathians and Balkan
Peninsula. The plant has become naturalized in Central and Northern Europa, where
it is grown for ornamental or medicinal purposes and for the feeding of bees
(Hegi, 1924; Webb and Ferguson, 1968; Petrova and Kozhuharov, 1979).
The plant is highly valued in Bulgaria for its ornamental, aromatic, melliferous and
variety of healing properties which makes it a garden favourite. It is an emblematic plant
in the Bulgarian folk tradition: a symbol of health, wealth and longevity: its folk name
Zdravetz means health (Ivancheva, 1998). G. macrorrhizum is the source for production of
the Bulgarian geranium essential oil (EO) called Zdravetz oil, which is distilled from the
overground parts of the plant and possesses a very pleasant odour reminiscent of clary
sage, orris, and particularly of rose (Guenther, 1950; Gildemeister and Hoffman, 1959).
Cultivation
The first experiments on the industrial cultivation of G. macrorrhizum in Bulgaria were
carried out during 19241931 at the State Experimental Field for Roses, Essential oil

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Cultivation and harvesting of Geranium species for medicinal use

31

and Medicinal Plants in the town of Kazanlik (Rose Valley). Rhizomes of wild geranium were transfered to the field conditions of the Rose Valley but survived for 3 years
only, because of the hot summers and low air and soil humidity in this area (Georgieff,
1933). The abundance of natural high qualitative resources for the plant all around the
southern slopes of the Central Balkan Mt., as well as the northern ones of the Sredna
Gora Mt. which were in the immediate vicinity of the distillers in the Rose Valley,
made the oil production from wild sources more profitable than those from cultivated
plants (Georgieff, 1933; Irinchev, 1956). Recently a large part of the commercially
valuable populations of G. macrorrhizum in the region, were protected within the
Central Balkan National Park, which forced the development of primary technology
for large-scale cultivation for EO production. Experiments were carried out at the
Institute of Botany in Sofia and various soil-types were assessed under different environmental conditions.
Climatic and soil requirements
In the wild, the species inhabits humid, shady, shrubby and rocky places, among rock
fragments where soil is scanty, preferentially on steep slopes facing north, generally on
limestone. The species is sciophylic and cold-resistant and takes part in the herbaceous
canopy of forestal coenoses in mountains and lower mountain slopes from 300 to 2500 m
(Webb and Ferguson, 1968; Petrova and Kozhuharov, 1979; Genova, 1995;
Assenov et al., 1998).
Choice of the correct place for plantation is of great importance. The species has no
special requirements as to soil-type but it prefers semi-permeable to well-drained
soils. It needs high humidity and its cultivation on open and sunny places have to be
compensated by irrigation, spraying or a showering system. This could be of great
advantage in the utilization of terrains in mountain regions which are unsuitable for
main crops (near the forests, slopes), and out of crop rotation. As an intercrop in
orchard gardens it could be used as a melliferous plant as well. The crop performs best
in areas with an average daily temperature of 1822 C (Yankulov et al., 1993).
Propagation
Plant multiplication in nature occurs both vegetatively, by rhizome sprouts (suckers),
and by seeds. Plants form large clumps and a common garden practice is to divide them
into single main rhizomes (Genova, 1995). Despite the almost unlimited rooting
capacity of the plant and possibility to produce single-node cuttings, conventional
vegetative propagation using the overground part of rhizomes from the previous
crop, still remains the only method used at the horticultural level.
Planting and aftercare
Preliminary soil-cultivation: deep ploughing, 3035 cm deep, after a previous crop
(cereals, earthed-up crops), harrowing and cultivation. Suckers (rhizome tips with 36
leaves) 1015 cm long are planted at 46 cm depth in rows and covered with soil (this
could be performed mechanically). The recommended spacing is 50 cm between rows
and 30 cm between plants. The rate of planting material is 15002200 kg/ha, which
yields 66 00070 000 plants per hectare. The best time to plant is late autumn from

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Tatyana Stoeva

15th October to 15th November, which ensures sufficient soil humidity, 90 per cent
rooting occurs and plants spend the winter successfully (Yankulov et al., 1993).
Aftercare during the first and second year includes: 35 times of earthing up (weeding) and abundant watering (78 times). From the third year, plants form wide clumps
merged into continuous compact rows and suppress weeds. Irrigation remains to be the
main aftercare during the further exploitation of the plantation, which is up to 78
years (Yankulov et al., 1993).
Fertilization
G. macrorrhizum is responsive to fertilization. Incorporation of 600800 kg/ha of superphosphate and 150200 kg/ha K2O at the time of ploughing and land preparation or
mixing half of these amounts with 3040 t per hectare of cattle manure is the usual
method. In the first spring, when rows are well outlined by developed plants, 200300
kg/ha of N fertilizer has to be applied with the first earthing up. Annually, in the
spring, plants require full mineral fertilization (Yankulov et al., 1993).
Harvesting and yields
Harvesting begins in the second year after planting and a regular yield could be
obtained after the third. The above-ground mass is harvested twice a year: before flowering (end of May to the beginning of June) and at the end of vegetation in late autumn
(end of September to the beginning of October) when accumulation of phytomass is
highest. The EO content varies from 0.02 to 0.13 per cent depending on the plants origin and the vegetative stage.
Different Bulgarian populations were studied for their EO productivity and a high
oil-yielding selection (from Rila Mt.) was used for estimating the possible harvest of
EO from the species under conditions of large-scale cultivation; however, breeding has
still not been carried out. Herbage has to be cut (reaped) with a sickle 45 cm above
the overground rhizome, so as to ensure new growth. Fresh herbage is used for distillation and it withstands pressing, wilting but should not be stored for more than 3 days.
After the first harvest, the plantation needs irrigation and earthing.
The annual yield (two harvests) of phytomass varies from 4000 to 6000 kg/ha, which
at an average EO content of 0.05 per cent could yield 23 kg/ha of EO (Yankulov et al.,
1993).
Use of G. macrorrhizum
Phytotherapy of some Balkan countries makes use of both herbage and rhizomes of
G. macrorrhizum mainly for their hypotensive, sedative, astringent, cardiotonic and
antiatheromatous effects. This biological activity is due to: EO with about 0.1 per cent
of the main compound, the sesquiterpenic ketone germacrone, which makes up to 50
per cent of the EO; there are also tannins, flavonoids, phenolic acids and waxes in the
herbage and tannins (about 16 per cent), flavonoids and phenolic acids in the rhizomes
(Mihailov and Tucakov, 1974; Petkov, 1982; Assenov et al., 1998). Phytotherapy
prescriptions involve the water-soluble extract (cool extraction of dry rhizomes at a
ratio of 1:10 for 8 h) per os: 400 ml daily split into four doses, as well as externally as
compresses (Petkov, 1982).

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Cultivation and harvesting of Geranium species for medicinal use

33

Pharmacological effect
The extracts and aromatic products of G. macrorrhizum have been studied in detail in
Bulgaria. The main pharmacological effects of the two herbal drugs was proved experimentally to be due to their water-soluble, ethanolic and methanolic extracts (Manolov
et al., 1977; Petkov, 1982). Isolated flavonoid fractions possess hypotensive and spasmolytic activity as well (Ivancheva et al., 1976). Different fractions of the rhizome
methanolic extract demonstrate sedative and moderate central myorelaxing effects
(Manolov et al., 1977; Petkov, 1982). After the EO extraction, a polymeric phlobaphen
complex was obtained from the herbage as a durable (stable) product which clinical
tests showed it to have a hypotensive effect (Petkov, 1982). The antimicrobial activity
of polyphenols was also reported (Ivancheva et al., 1992).
GERANIUM SANGUINEUM L. (BLOODY CRANESBILL)

Introduction
Geranium sanguineum is a perennial plant with stout, horizontal rhizomes. Stems are
diffused, branched, erect to decumbent, with long white, patent hairs and sessile glands.
Leaves are mostly cauline, 35 cm wide, divided into 57 lobes, each with 13 linear,
oblong, acute segments on each side. Flowers are single on a 715 cm peduncle and stick
out from nodes (Webb and Ferguson, 1968; Petrova and Kozhuharov, 1979; Assenov
et al., 1998). The species is distributed in most of Europe and the Caucasus, southwards
from c. 60N (Hegi, 1924; Webb and Ferguson, 1968; Petrova and Kozhuharov, 1979).
The species is a valuable ornamental, but in Bulgaria it is valued mostly for its
medicinal properties. Because of the red colour of its rhizomes, the plant was considered
to be a blood-strengthener and in folk medicine, the water-soluble extracts of rhizomes
are prescribed as a remedy for malignant illness of the blood-generated organs (Assenov
et al., 1998). Some aspects of large-scale cultivation, for production of both rhizomes
and herbage, were examined in the field, in the Sofia Plain, where plant samples of wild
origin were introduced and propagated for the field studies.
Cultivation
Species occur on rocky or sandy ground or on well-drained soils, in herbaceous places,
among shrubs and sparse woods in lowlands, mountains and base of mountains up to
1700 m (Webb and Ferguson, 1968; Petrova and Kozhuharov, 1979; Assenov et al.,
1998).
The species have no special requirements of soil under conditions of cultivation. The
crop is sensitive to waterlogging, so terrains for plantations have to be well-drained and
sunny. It grows well on sandy to clayey and alluvial-meadow soils as well.
Propagation
In nature, plant propagation occurs both by seeds and vegetatively by rhizome sprouts
(suckers). As an ornamental, which could be kept at the same place for years, the plant
forms a large round clump (up to 5060 cm in diameter and up to 50 cm in height)
which is due both to new suckers and seedlings growing up inside the clump. Seedlings

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34

Tatyana Stoeva

were used in the studies, produced under green-house conditions from the end of
January/early February to mid-April.
Planting and aftercare
Normal preliminary soil cultivation and fertilization conditions for G. macrorrhizum
were applied. Seedlings were planted in rows spaced 70 cm apart and with a 30 cm
distance between individuals and irrigation was supplied. A 1 ha plot was covered by
50 000 seedlings. The plantation needs 12 times of irrigation to be applied and weed
control (regular earthing up) during the growth period.
Harvesting and yields
There are two approaches to the utilization of plantations depending on which of the
herbal drug is to be produced: herbage or roots and rhizomes.
Roots and rhizomes: The crop is ready for harvest in the third year after the end of
vegetation. Yield of fresh rhizomes reaches 20 000 kg/ha (4000 kg/ha dry rhizomes).
During these years, overground parts could be used for seed production.
Herbage: Experimental data shows that on the third year of cultivation, the yield of fresh
above-ground mass of 12 000 kg/ha (300350 kg/ha dry weight) could be achieved.
Possibilities for simultaneous utilization (rotation) of the plantation for production
of both sources and duration of exploitation have to be studied.
Use of G. sanguineum
Bulgarian phytotherapists apply Rhizoma et Radix Geranii sanguinei for their astringent,
vasodilatant, anti-inflammatory, hypotensive, cardiotonic and slight sedative effect
(Petkov, 1982; Staneva et al., 1982; Assenov et al., 1998). It contains catechin tannins
(up to 29 per cent), leucoanthocyanidins, the bitter substance geraniin, resins, etc.
(Assenov et al., 1998). Phytotherapists prescribe water-soluble extracts (cool extraction
of dry rhizomes at a ratio of 1:10 for 8 h) per os: 400 ml daily split in four doses. It is
also applied externally (Petkov, 1982). Numerous investigations have been reported about
the healing effect of the plant extracts and the polyphenolic complex obtained from
herbage and rhizomes of this species, which possess antimicrobial (Ivancheva et al., 1992)
antiviral, against Herpes simplex (Zgorniak-Nowosielska et al., 1989; Serkedjieva, 1995,
1997; Serkedjieva and Ivancheva, 1999) and influenza (Manolova et al., 1986; Serkedjieva
et al., 1986; Serkedjieva and Manolova, 1987, 1988; Serkedjieva, 1997; Serkedjieva and
Hay, 1998) viruses and also its radio-protective activity. Three Bulgarian patents were
taken out on the basis of G. sanguineum extracts, concerning the main pharmacological
effects of the plant: i.e. its hypotensive, antiinfluenza and radio-protective (immunostimulative) functions (Ivancheva, 1998).

REFERENCES
Assenov, I., Gussev, C.H., Kitanov, G., Nikolov, S. and Petkov, T. (1998) Bilkosabirane. BILER, Sofia.
Georgieff, C. (1933) Annual Report of the State Experimental Field for Roses, Etherial and
Medicinal Plants in Kazanlik (for 19291932), Publ. house Gutenberg Kazanlik.

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Cultivation and harvesting of Geranium species for medicinal use

35

Genova, E. (1995) Geranium macrorhhizum L. In: Chorological Atlas of Medicinal Plants in Bulgaria,
I. Bondev (ed.), Acad. Press Prof. M. Drinov, Sofia, 9495.
Gildemeister, E. and Hoffmann, Fr. (1959) Die therischen le. Bd. 5, Academie Verlag Berlin.
Guenther, E. (1950) The Essential Oils, Vol. 4, D. Van Nostrand Company, Inc., Toronto, New
York, London.
Hegi, G. (1924) Ilustrierte Flora fon Mittel-Europa, IV Bd., 3 Teil, J.F. Lehmanns Verlag,
Mnchen, p. 1708.
Irinchev, I. (1956) Zdravetzovo maslo. Priroda, 5(2), 6567.
Ivancheva, S. (1998) Zdravetzut bilka i poema. Integral G, Sofia.
Ivancheva, S., Zapessotchnaya, G. and Ognyanov, I. (1976) Flavonoids and other substances in
roots of Geranium macrorrhizum L. Compt. rend. de lAcad. bulg. des Sci., 29(2), 205208.
Ivancheva, S., Manolova, N., Serkedjieva, J., Dimov, V. and Ivanovska, N.(1992) Polyphenols
from Bulgarian medicinal plants Geranium macrorrhizum and G. sanguineum with anti-infectious activity. Basic Life. Sci., 59, 717728.
Manolov, P., Petkov, V. and Ivancheva, S. (1977) Studies on the central depressive action of
methanol from Geranium macrorrhizum L. Compt. rend. de lAcad. bulg. des Sci., 30(11),
16571659.
Manolova, N., Gegova, G., Serkedjieva, J., Maksimova-Todorova, V. and Uzunov, S. (1986)
Antiviral action of a polyphenol complex isolated from the medicinal plant Geranium
sanguineum L. I. Its inhibiting action on the reproduction of the influenza virus. Acta Microbiol.
Bulg., 18, 7377.
Mihailov, M. and Tucakov, J. (1974) Pharmacognostic study of long-rooted geranium (G. macrorrhizum) in Yugoslavia. Preliminary communication. Glas Srp. Akad. Nauka (Med.), 25, 919.
Petkov, V. (1982) Ed. Modern Phytotherapy, Medicina i Fizkultura, Sofia.
Petrova, A. and Kozhuharov, S. (1979) Geranium L. In: Flora Republicae popularis bulgaricae,
vol. VII, (B. Kuzmanov, Ed.), Aedibus Academiae Scientiarum bulgaricae, Sofia, 3134.
Serkedjieva, J. (1995) Inhibition of influenza virus protein synthesis by a plant preparation from
Geranium sanguineum L. Acta Virol., 39(1), 510.
Serkedjieva, J. (1997) Antiinvective activity of a plant preparation from Geranium sanguineum L.
Pharmazie, 52(10), 799802.
Serkedjieva, J. and Ivancheva, S. (1999) Antiherpes virus activity of extracts from the medicinal
plant Geranium sanguineum L. J. Ethnopharmacol., 64(1), 5968.
Serkedjieva, J., Manolova, N., Gegova, G., Maksimova-Todorova, V. and Ivancheva, S. (1986)
Antiviral action of a polyphenol complex isolated from the medicinal plant Geranium
sanguineum L. II. Its inactivating action on the influenza virus. Acta Microbiol. Bulg., 18, 7882.
Serkedjieva, J. and Manolova, N. (1987) Antiviral action of a polyphenol complex isolated from
the medicinal plant Geranium sanguineum L. V. Mechanism of the anti-influenza effect in vitro.
Acta Microbiol. Bulg., 21, 6671.
Serkedjieva, J. and Manolova, N. (1988) Antiviral action of a polyphenol complex isolated from
the medicinal plant Geranium sanguineum L. VI. Reproduction of the influenca virus pretreated
with the polyphenol complex. Acta Microbiol. Bulg., 22, 1621.
Serkedjieva, J. and Hay, A.J. (1998) In vitro antiinfluenza virus activity of a plant preparation
from Geranium sanguineum L. Antiviral Res., 37(2), 121130.
Staneva, D., Panova, D., Raynova, L. and Assenov, I. (1982) Bilkite vuv vseki dom. Medicina i
Fizkultura, Sofia.
Webb, D. and Ferguson, A. (1968) Geranium L. In: Flora Europaea, Univ. Press, Cambridge, p. 195.
Yankulov, Y., Taleva, R. and Stoeva, T. (1993) Obiknovenniyat zdravetz e eterichnomaslena
kultura. Zemedelie, 91 (11/12), 6.
Zgorniak-Nowosielska, I., Zawilinska, B., Manolova, N. and Serkedjieva, J. (1989) A study on
the antiviral action of a polyphenol complex isolated from the medicinal plant Geranium
sanguineum L. VIII. Inhibitory effect on the reproduction of Herpes simplex virus type 1. Acta
Microbiol. Bulg., 24, 38.

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Essential oil of Geranium


macrorrhizum L. production,
extraction, distillation and use
Tatyana Stoeva

INTRODUCTION

The essential oil (EO) of Geranium macrorrhizum is produced solely in Bulgaria and
the industry dates back to the end of the nineteenth century (Guenther, 1950;
Gildemeister and Hoffman, 1959; Irinchev, 1956). The above-ground herbage is harvested in the autumn (SeptemberOctober). In post-flowering plants, the EO content
was found to be higher (0.0830.13 per cent) than during flowering (0.05 per cent).
Herbage consists of 4349 per cent leaf blades, 3943 per cent leafstalks, 48 per cent
yellowing or withered leaves and flowers and 510 per cent rhizomes (Irinchev, 1956;
Georgiev, 1995). In recent years, the availability of the wild source of G. macrorrhizum
became scarce and is unavailable for industrial usage due to the new biodiversity protection laws and conservation strategies. The only way to solve the lack of resource was
to amend the cultivation and increase plant productivity.
ESSENTIAL OIL DISTILLATION

Essential oil distillation is done in the same distillation vessels as those where peppermint and lavender are processed. The main methods used are: water distillation, steam
and water distillation and steam distillation.
During steam distillation, the herbage is preventing from immersion by supporting
it, without compaction, or by the use of 12 perforated grids, and the process proceeds
at 120 kg/cubic meter.
In water plus steam distillation, it requires 8085 kg herbage per cubic meter, the
boiling water being poured in at a rate of 1:56. Distillation is continued for 3.44.5 h
at a speed of 56 per cent and a temperature of the distillation of 4550 C as the EO
components crystallise out at lower temperatures. About 48 per cent of the oil is
obtained during the first hour, with 1722 per cent obtained after the second and third
hour. Since the distillate waters contain 1520 per cent of the total oil, they are cohabated for 1.52 h and 80 per cent of the EO in the water is isolated during the first
hour (Irinchev, 1956; Georgiev, 1995).
Primary and secondary oils are rectified separately. They are left in a warm place for
precipitation of admixtures to occur and then are filtered while hot. The commercial
EO is prepared by combining the primary (raw) and secondary (cohabated) oils in a proportion of 8:1. According to the temperature, the EO is a yellow-green to dark green
liquid (above 35 C) or a semi-solid mass which consists of a mixture of colourless to

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Essential oil of Geranium macrorrhizum 37

pale-yellow crystals (stearoptene) with a liquid (eleoptene) at room temperature


(Irinchev, 1956; Georgiev, 1995; Ivanov et al., 1952).
The odour is typically zdravetz: it is a pleasant, reminiscent of clary sage, orris and
rose (Guenther, 1950). The Physico-chemical characteristics of G. macrorrhizum are as
shown in Table 6.1.
ESSENTIAL OIL COMPOSITION

The EO is typically sesquiterpenic, as the major component is germacrone (5055 per


cent) which constitutes the stearoptene. The other terpenes are mainly ketones: - and
-elemenone, germazone etc. Hydrocarbons account for 1113 per cent, comprising:
- and -selinene; -elemene, ar-curcumene, -santalene, caryophyllene, -humulene,
-muurolene, -cadinene, calamenene etc. Alcohols make up 1020 per cent, including:
juniperic camphor, junenol, -eudesmol, elemol. Monoterpenic compounds amount to
710 per cent, consisting of -terpinene, terpinolene,
-cymene, -pinene, -3-carene,
-phellandrene, limonene and borneol. The green colour of the oil is due to azulenes
(Georgiev, 1995; Georgiev et al., 1989; Ivanov et al., 1952; Ivanov and Ognyanov, 1955;
Ognyanov and Ivanov, 1958a,b; Tsankova and Ognyanov, 1972). The EO should be
stored in 5 kg copper canisters (kumkuma) under standard conditions for unlimited
periods. The oil is usually semi-crystalline at room temperature.
The zdravetz oil is used for its excellent fixative properties in fougeres, chypres,
oriental bases, colognes and fantasy fragrances. It blends well with oakmoss, labdanum,
olibanum, sandalwood, clary sage, lavender and bergamot (Arctander, 1960).
CONCRETE AND ABSOLUTE OF G. MACRORRHIZUM

Concrete
This is obtained by extraction using petroleum ether at room temperature through
a three-step extraction: the first lasts for 4060 min, the second lasts 2030 min and
the third lasts for 515 min at a rate of 120 kg zdravetz herbage per cubic litre

Table 6.1 Physico-chemical characteristics of G. macrorrhizum

Relative density at 20 C
Refractive index at 20 C
Optical rotation
Melting point
Ester value
Ester after acetylation
Free alcohols (as geraniol)
Total alcohols (as geraniol)
Stereopten content
Notes
*Ognyanov and Ivanov (1958);
** Georgiev et al. (1989).

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Commercial sample 1*

Sample 2**

0.9300.952
1.50241.5135
4.8 to 8.6
3450 C
4.977.91
20.849.8
5.811.9
7.714.5
not given

0.93800.9680
1.50031.5189
not given
3450 C
715
2555
27.5
6.820.7
41.752.8

38

Tatyana Stoeva

Figure 6.1 Geranium macrorrhizum.

solvent. The herbage is distributed on 46 perforated grids. The concrete yields


0.350.40 per cent. It looks like a vaseline-like green to yellow-green mass with
a strong typically zdravetz odour but much milder, fuller and more lasting than the
EO produced by distillation.
The concrete contains: geraniol, germacrol, mono and bicyclic sesquiterpenes; sesquiterpene alcohol, free acids, paraffins, dyes etc. It should be stored in 5 kg tin-plated
containers for up to 2 years (Guenther, 1950; Gildemeister and Hoffman, 1959;
Georgiev, 1995; Georgiev et al., 1989).
Applications in perfumery: as a rose-scented aromatic with green and fresh notes,
exhibiting good fixative values.

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Essential oil of Geranium macrorrhizum 39

Absolute
The absolute is applied in different perfume compositions (Zhelev, 1971; Nikolov et al.,
1971). It is a dark green thick liquid obtained from zdravetz concrete by extraction with
95 per cent ethyl alcohol. The absolute has strong, penetrative powers but a gentle
zdravetz odour with strong fixative properties.
The remaining mass after the absolute is extracted consists of a dark green solid matter containing mainly n-triacontane. It is fatty, tasteless, with a pleasant zdravetz odour
and possesses strong photoprotective properties (Georgiev, 1995; Toleva et al., 1971;
Toleva and Tolev, 1956). The zdravetz oil and concrete also had antibacterial and
antimycotic activity. (Zhelev, 1971; Nikolov et al., 1971; Toleva et al., 1971).
Figure 6.1 shows a typical example of Geranium macrorrhizum.
REFERENCES
Arctander, S. (1960) Perfume and Flavor Materials of Natural Origins, Elisabeth, New Jersey.
Georgiev, E. (1995) Technologia na estestvenite I sintetichni aromatni producti, Zemizdat, Sofia.
Georgiev, E., Dimitrov, D. and Angelakova, M. (1989) Spravochnik na specialista po aromatichnata
I kozmetichna promishlenost, Technika, Sofia.
Gildemeister, E. and Hoffmann, Fr. (1959) Die therischen le. Bd. 5, Academie Verlag Berlin.
Guenther, E. (1950) The Essential Oils, vol. 4, D. Van Nostrand Company, Inc., Toronto,
New York, London.
Irinchev, I. (1956) Zdravetzovo maslo. Priroda, 5(2), 6567.
Ivanov, D., Ognyanov, I. and Nikolov, N. (1952) Sur lhuile de zdravetz bulgare, Compt. Rend.
Acad. Bulg. Sci., 5, 3336.
Ivanov, D. and Ognyanov, I. (1955) Bulgarian zdravetz oil. II. Sesquiterpenic hydrocarbons from
oil, Compt. Rend. Acad. Bulg. Sci., 8, 4548.
Nikolov, N., Blagoeva, I. and Boyadzhiev, P. (1971) Aromatnie produkti iz Geranium macrorrhizum. In: Congress International des huilles essentielles, Tbilissi (USSR), Sept. 1968, vol. 1,
Chimie et Technologie des huilles essentielles et des substances odorantes. Pishchevaya promishlenosti,
Moscow, p. 248
Ognyanov, I. and Ivanov, D. (1958a) Bulgarian zdravetz oil III. Its terpene compounds, Compt.
Rend. Acad. Bulg. Sci., 11, 379382.
Ognyanov, I. and Ivanov, D. (1958b) Bulgarian zdravetz oil IV. Sesquiterpene oxygen compounds in the oil is eleoptene. Compt. Rend. Acad. Bulg. Sci., 11, 469472.
Toleva, P. and Tolev, I. (1965) Des possibilities dutilizer lhuile essentielles et la concrete de
Geranium dans la preparation de produits de cosmetique. Travaux Scientifiques de ITSIA, 12,
133136.
Toleva, P., Hristov, D., Georgieva, A. and Surtalova, T. (1971) Issledovanie sostava voskov iz
konkretov zdravetz I akatzii I vozmozhnosti ih ispolizovaniya. In: Congress International des
huilles essentielles, Tbilissi (USSR), Sept. 1968, vol. 1, Chimie et Technologie des huilles
essentielles et des substances odorantes. Pishchevaya promishlenosti, Moscow, pp. 362367.
Tsankova, E. and Ognyanov, I. (1972) Sesquiterpene hydrocarbons in the Bulgarian zdravetz
(Geranium macrorrhizum L.) oil. Compt. Rend. Acad. Bulg. Sci., 25, 12291231.
Zhelev, Z. (1971) Aromatischeskie produkti iz zdravetza In: Congress International des huilles
essentielles, Tbilissi (USSR), Sept. 1968, vol. 1, Chimie et Technologie des huilles essentielles et des
substances odorantes. Pishchevaya promishlenosti, Moscow, pp. 9799.

2002 Edited by Taylor & Francis

Use of Geranium species extracts


as herbal medicines
Elizabeth M. Williamson

INTRODUCTION

Geranium species are common throughout temperate regions and are used in many
different parts of the world in traditional systems of medicine. Geranium oil is also
widely used, however this normally refers to the essential oil (EO) distilled from
Pelargonium species rather than Geranium. In general, most species are used for similar
disorders, although some of the different local indications for each are given in Table
7.1. Geraniums used medicinally usually contain high levels of tannins, which are
responsible for the folklore use as haemostatics and astringents. They are used internally
for haemorrhage and diarrhoea, and externally for wounds, grazes, sores and fissures
(British Herbal Pharmacopoeia, 1983; Brendler et al., 1999). More recently various
tannin-containing drugs, including Geranium species, have been used as antiinfective
agents particularly for viral diseases (Serkedjieva and Hay, 1998) and antioxidant
activity, which would be expected from the content of polyphenolic compounds, has
also been demonstrated (Lamaison et al., 1993).
EUROPEAN AND AMERICAN HERBAL MEDICINE

Geranium maculatum L.
The species most commonly used worldwide is probably G. maculatum L., variously
known as American cranesbill, storksbill, spotted cranesbill, crowfoot and others.
This species is found in shady and moist ground throughout the whole of Europe and
in North America from Newfoundland to Manitoba and as far south as Missouri.
Both the rhizome and the herb have been used for medicinal purposes since antiquity
to treat fever, including malaria, abdominal and uterine disorders, inflammation and
as an external application for wounds, excessive bleeding, and sores. Internally it was
used as a styptic for metrorrhagia, menorrhagia, haematuria and haemorrhoids; and
particularly for diarrhoea, peptic and duodenal ulcers and dysentery. These are still
the most important indications. In the middle ages, Paracelsus described it as having
cardiotonic and antidepressive activity, and there are other uses for which Geranium
has been suggested, including worms, leucorrhoea and as a mouthwash (Brendler
et al., 1999).

2002 Edited by Taylor & Francis

Table 7.1 Species of Geranium used medicinally


Geranium sp.

Local names

Locality

G. aconitifolium
G. core-core
G. japonicum

Palto
Core-core
Cranesbill Storksbill

Ladakh
Mexico
Japan, China

G. macrorrhizum

Bulgarian Geranium,
Zdravetz
American or Spotted
Cranesbill, Storksbill,
Crowfoot
Mano de Leon, Pata de
Leon, Agujas

Bulgaria, Romania,
Poland
North America, Europe

G. maculatum

G. mexicanum
G. nepalense
G. niveum
G. pratense

Mexico, Venezuela

G. sanguineum

Bloody geranium

N. India, Nepal
Mexico
China, Japan, Europe,
temperate regions
worldwide
Eastern Europe

G. robertianum
(Geranium foetidum
Gilib)
G. thunbergii

Herb Robert, Herb Robin,


Dragons Blood, Wild
Cranesbill, Storkbill.
Gen-No-Shoko

Europe, USA, China, Japan,


North Africa, USA, India,
South America
China, Japan

G. wallichianum

Wallich Cranesbill, Laljhari

G. wilfordii

Lao Kuan Tsao

Northern India, Punjab,


Kashmir
China

Meadow Cranesbill,
Cao-Yuan-Lao-Guan-Cao

2002 Edited by Taylor & Francis

Internal use

Shock, fever, cataract


Rheumatism, numbness
of limbs, pain
See G. maculatum;
antiviral
Diarrhoea; dysentery;
GI ulcers; styptic in
menorrhagia and haematuria
Laxative in infants,
antispasmodic
Diarrhoea, endometriosis
Infectious diarrhoea
Acute bacillary dysentery

External use

References

Insect bites, ulcers


Toothache, inflammation

Srivastava et al. (1982)


Rodriguez et al. (1994)
Perry (1980)

Oil used in
aromatherapy
Haemorrhoids; wounds;
sores; bleeding; as a
mouthwash
Infant bathing to treat
rashes and wounds

Serkedjieva, 1997;
Tisserand et al. (1995)
Brendler et al. (1999);
British Herbal
Pharmacopoeia, (1983)
Morton (1981)
Perry (1980)
Calzada et al. (1998)
Yau et al. (1999)

Haemorrhage, diarrhoea
Diarrhoea, haemorrhage,
jaundice, dispersal of milk,
kidney and gall stones
Inflammation of GI system,
diarrhoea, haematological
and liver disorders
Astringent, diarrhoea
Chronic rheumatism

Gargle, mouthwash,
burns, wounds

Serkedjieva (1996,
1997)
Brendler et al. (1999)
Ambasta (1986)

Cataract

Kimura et al. (1994)

Toothache and eye


disorders

Ambasta (1986)
Pei-gen (1989)

42

Elizabeth Williamson

Constituents and preparations

G. maculatum contains gallotannins. The dried herb and the root are used at the same dose,
which is normally 12 g powdered drug taken 3 times daily. The herb may be taken as
an infusion, and the root as a decoction, liquid extract 1:1 (45 per cent ethanol) or tincture
1:5 (45 per cent ethanol). G. maculatum is often found in preparations combined with
other herbs such as Geum urbanum, Agrimonia eupatoria for duodenal ulcer, and Bidens pilosa
for bleeding of the digestive tract (British Herbal Pharmacopoeia, 1983). Few side effects
have been observed, although patients with sensitive stomachs may feel nauseous because
of the high tannin content, and theoretically it should not be taken with certain other
medicines because of the possibility of the formation of tannin-drug complexes.
Homoeopathic preparations are also used, including drops, tablets or injections, to treat
stomach ulcers and bleeding of the mucus membranes (Brendler et al., 1999).
Geranium robertianum L.
G. robertianum L., also known as Herb Robert, Herb Robin, Dragons Blood and others
(see Table 5.1) is indigenous to a large area covering Europe to China and Japan; most
of North America; Africa as far south as Uganda, and temperate parts of South America.
Historically, it was used as an astringent in diarrhoea and excessive bleeding from
various causes in much the same way as G. maculatum, but it also had a reputation for
resolving or dispersing milk in women after parturition, and as a coolant and pain
reliever. It was even recommended as a gargle for angina. The Indians of western North
America are said to have used the root as a cure for syphilis. It is now used as a
mouthwash for inflammation of the mouth and pharynx; topically for burns and
wounds, and internally for haemorrhage, kidney and bladder stones, and for liver and
gall bladder problems. It is used in India for similar purposes and particularly for
jaundice (Ambasta, 1986) and has been used in veterinary medicine for dysentery and
haematuria. Modern usage also centres on the antiviral effect of extracts of the plant,
which has been confirmed in some studies but not in others. No activity was shown
against polio type 1, measles, coxsackie-B2, adeno- or Semliki forest viruses, but a mild
effect was demonstrated against a stomatitis virus. Extracts also have inhibitory effects
on some types of pathogenic microbial growth in vitro (Brendler et al., 1999) The effects
of geraniin will be discussed later in connection with the effects of G. thunberghii.
Constituents and preparations

G. robertianum contains tannins including geraniin; isogeraniin; -penta-O-galloyl


glucose; and flavonoids such as rutin, hyperoside and others. The dried aerial parts of the
herb are used at a dose of 1.5 g, taken as an infusion up 3 times daily. This may be used
internally or externally. Fresh cleaned leaves have been chewed to relieve inflammation
of the oral cavitiy. Occasionally the herb may be found adulterated with G. palustre,
or G. pratense.
Geranium macrorrhizum L. and G. sanguineum L.
Bulgarian folk medicine and that of other Eastern European countries such as Poland
and Romania, use G. macrorrhizum (known as zdravetz in Bulgarian) and G. sanguineum
for similar astringent purposes in diarrhoea and haemorrhage to those outlined for

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Use of Geranium species extracts as herbal medicines 43

G. maculatum. G. sanguineum is known to contain a number of polyphenolic compounds


including gallotannins, catechins and flavonoids, and has been shown to inhibit
replication and synthesis of the influenza virus in vitro and in vivo in mice (Serkedjieva,
1996, 1997) and Herpes, Vaccinia and HIV viruses in vitro (Serkedjieva, 1996, 1999).
It appears to work by inhibiting influenza virus neuramidase enzyme (Serkedjieva,
1995a) and protein synthesis (Serkedjieva, 1995b). Other susceptible organisms
included Staphylococcus aureus and Candida albicans (Serkedjieva, 1997). The EO of
Zdravetz (G. macrorhizum) is occasionally used in aromatherapy and contains about
50 per cent of germacrone (Tisserand and Balacs, 1995).
ORIENTAL MEDICINE

Geranium thunberghii Sieb et Zucc.


G. thunberghii, known as Gen-no-shoko in Japanese, is used in Kampo (traditional
Japanese medicine) particularly as a remedy for diarrhoea induced by inflammation of
the small intestine and also for liver and haematological disorders (Kimura et al., 1984).
It also has been used to treat cataract (Fukaya et al., 1988). The biological activity is
usually ascribed to the tannin content, particularly geraniin. Extracts of the plant have
been shown to reduce gastro-intestinal motility in isolated rat intestine (Kan and
Taniyama, 1992); have inhibitory effects on cholera toxin-induced secretion from rat
gastric mucosa and other astringent effects (Ofuji et al., 1998), giving support to the
traditional usage of Geranium for diarrhoea. They also exhibit strong antimutagenic
effects against direct acting mutagens (Okuda et al., 1984). Like other tannin-containing drugs, extracts reduced levels of ureamic toxins, including creatinine, methylguanidine and guanidinosuccinic acid, in rats with renal failure (Yokozawa et al., 1995).
A considerable amount of research has been done on isolated geraniin, which has been
shown to protect against experimental hepatic injuries in rats induced by galactosamine,
carbon tetrachloride and thioacetamide (Nakanishi et al., 1998a). Geraniin also
prevented the accumulation of liver triglycerides and lipid peroxide levels and lowered
serum levels of hepatic enzymes associated with liver damage in the rat (Nakanishi et al.,
1999a). A protective effect on oxidative damage to mouse ocular lens supports the
traditional use for cataract to some extent (Fukaya et al., 1988). Haematological effects
of geraniin in rats have also been studied, and a decrease in serum lipid levels observed
as well as a reduction in erythrocytes and leucocytes (Nakanishi et al., 1998b). The
effects of geraniin on aminonucleoside nephrosis in rats included a reduction in proteinuria, and in serum and cholesterol levels produced by puromycin (Nakanishi et al.,
1999b). Macrophages are known to be affected by geraniin, and marked increases in
phagocytosis observed in in vitro cultures (Ushio et al., 1991). The clinical significance
of some of these findings is not clear, and few human studies on Geranium herb are to be
found in the literature, however the results of these various experiments show that the
tannins it contains have pharmacological effects which may support its therapeutic use.
Constituents and preparations

G. thunberghii contains tannins, the most important being geraniin, corilagin,


dehydrogeraniin, furosin and furosinin, ellagic and gallic acids, geraniic acids B and C and
phyllanthusiin F (Kan and Taniyama, 1992; Okuda et al., 1982; Ito et al., 1999).

2002 Edited by Taylor & Francis

44

Elizabeth Williamson

Geranium wilfordii Maxim, G. pratense L. and G. nepalense Sweet


G. wilfordii, or Lao-kuan-tsao is used in Chinese medicine to treat chronic rheumatism,
often steeped in wine and taken orally, either alone or in combination with other
antirheumatic drugs. Erodium stephanium, also known as Lao Guan Cao, is considered
interchangeable and used in a similar way (Pei-gen, 1989). The closely related Meadow
Cranesbill, G. pratense (Cao Yuan Lao Guan Cao) is used in traditional Chinese medicine
to treat acute bacillary dysentery (Yau et al., 1999). G. nepalense is used in a similar manner
to G. thunberghii, which is sometimes considered a variety of it (Perry, 1980).
ASIA

Geranium aconitifolium LHerit.


This plant is known as palto by the traditional medical practitioners of Ladakh in the
Himalayas. The Tibetan system of medicine is known as Amchi and is a form of
Ayurveda. The flowers of G. aconitifolium are used in the form of a paste to soothe insect
bites, and the root paste is used for ulcers, and to treat cattle wounds, especially when
an insect repellent action is needed (Srivastava and Gupta, 1982).
Geranium wallichianum D. Don.
The Wallich Cranesbill (locally called Laljhari or Liljhari, and in Kashmir, Kao-ashud)
is used in Uttar Pradesh, India; and in Kashmir and Punjab as an astringent,
particularly for eye problems, and toothache. The root has been substituted for Coptis
teeta (Ambasta, 1986) and like many other species of Geranium is also used for tanning. Other species used in a similar way in India include G. robertianum (see above),
G. pusillum, G. rotundifolium and G. sibirica; all are used as astringents and for wound
dressing (Ambasta, 1986).
SOUTH AND CENTRAL AMERICA

Geranium core-core L.
An infusion of the leaf of this plant, known as core-core, is used in Chile by the
Mapuche Amerindians to treat cataract, shock and fever. The root, considered
astringent, was used to treat toothache and the whole plant used as an antiinflammatory
agent (Rodriguez et al., 1994). It is not normally used for diabetes, but the
hypoglycaemic effects of an extract of the whole plant was assessed in normoglycaemic
and alloxan diabetic rats and the activity found to be significant, but less than that
produced by tolbutamide (Rodriguez et al., 1994).
Geranium mexicanum HBK.
In Mexico, the juice of this plant is used as a laxative in infants although it is reputed
to have no effect in adults. A decoction is used to bathe babies to prevent and treat
rashes and wounds. In parts of Venezuela, the leafy stems are sold by herb vendors to
make a decoction, which is drunk for digestive spasms (Morton, 1981).

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Use of Geranium species extracts as herbal medicines 45

Geranium niveum
This plant is used in Mexican traditional medicine to treat infectious diarrhoea, which
is usually amoebic dysentery, and has recently been tested as for antiprotozoal activity
against Entamoeba histolytica and Giardia lamblia. Activity was confirmed to support
this usage, although the plant extract was less effective that metronidazole (Calzada
et al., 1998). Bioassay-guided fractionation led to the isolation of two new antiprotozoal constituents, identified as A-type proanthocyanins and named geranins A and B
(Calzada et al., 1999).

CONCLUSION

The use of Geranium species throughout the world demonstrates reassuring evidence
that even in a wide variety of systems of medicine, with different original philosophical
principles, traditional use shows very similar indications and supports the
pharmacological studies carried out more recently. There is very little discrepancy
between usage in different parts of the world and these depend usually upon the
astringent effect of the tannins contained in the herb, present in whichever species
grows locally. The more recent studies on the antiviral effects and other antimicrobial
actions will add to the supporting data for the traditional use of this species.

REFERENCES
Ambasta, S.P. (ed.) (1986) The Useful Plants of India, CSIR, New Delhi, India.
Brendler, T., Gruenwald, J. and Jaenicke, C. (eds) (1999) Heilpflanzen/Herbal Remedies. Deutcher
Apotheker Verlag, Stuttgart, Germany.
British Herbal Pharmacopoiea (1983) British Herbal Medicine Association, Keighley, UK.
Calzada, F., Meckes, M., Cedillo-Rivera, R., Tapia-Contreras, A. and Mata, R. (1998) Screening
of Mexican medicinal plants for antiprotozoal activity. Pharmaceutical Biology, 36(5),
305309.
Calzada, F., Cerda-Garcia-Rojas, C.M., Meckes, M., Cedillo-Rivera, R., Bye, R. and Mata, R.
(1999) Geraniins A and B, new antiprotozoal A-type proanthocyanins from Geranium niveum.
J. Nat. Prod., 62(5), 705709.
Fukaya, Y., Nakazawa, K., Okuda, T. and Iwata, S. (1988) Effect of tannin on oxidative damage
of ocular lens. Jap. J. Opthalmol., 32(2), 166175.
Ito, H., Hatano, T., Namba, O., Shironon, T., Okuda, T. and Yoshida, T. (1999) Constituents of
Geranium thunbergii Sieb. et Zucc. XV. Modified dehydroellagitannins, geraniic acids B and C
and phyllanthusiin F. Chem. Pharm. Bull., 47(8), 11481151.
Kan, S. and Taniyama, K. (1992) Mechanism of inhibitory actions of Geranium thunbergii, tannic acid and geraniin on the motility of rat intestine. Jap. J. Pharmacognosy, 46(3), 246253.
Kimura, Y., Okuda, H. and Mori, K. (1984) Studies on the activities of tannins and related compounds from medicinal plants and drugs IV. Effects of various extracts of Geranii Herba and
geraniin on liver injury and lipid metabolism in rats fed peroxidised oil. Chem. Pharm. Bull.,
32(5), 37553758.
Lamaison, J.L., Petitjean-Freitet, C. and Carnat, A. (1993) Tannin in polyphenols and antioxidant activity in French Geraniaceae. Plantes Medicinales et Phytotherapie, 26(2), 130134.
Morton, J. (1981) Atlas of Medicinal Plants of Middle America. Charles C. Thomas, USA.
Nakanishi, Y., Kubo, M., Okuda, T., Oruda, M. and Abe, H. (1998a) Hematological effects of
geraniin in rat. Natural Medicines, 52(2), 179183.

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46

Elizabeth Williamson

Nakanishi, Y., Orita, M., Okuda, T. and Abe, H. (1998b) Effects of geraniin on the liver in rats
I. Effects of geraniin compared to ellagic acid and gallic acid on hepatic injuries induced by
CCl4, D-galactosamine and thioacetamide. Natural Medicines, 52(5), 396403.
Nakanishi, Y., Kubo, M., Okuda, T. and Abe, H. (1999a) Effect of geraniin on aminonucleoside
nephrosis in rats. Natural Medicines, 53(2), 94100.
Nakanishi, Y., Okuda, T. and Abe, H. (1999b) Effects of geraniin on the liver in rats III.
Correlation between lipid accumulation and liver damage in CCl4-treated rats. Natural
Medicines, 53(1), 2226.
Ofuji, K., Hara, H., Sukamoto, T. and Yamashita, S. (1998) Effects of an antidiarrhoea
containing an extract from Geranium herb on astringent action and short-circuit current
across jejunal mucosa. Folia Pharmacol. Jap., 111(4), 265275.
Okuda, T., Hatano, T. and Yazaki, K. (1982) Dehydrogeraniin, furosinin and furosin,
dehydroellagitannins from Geranium thunbergii. Chem. Pharm. Bull., 30(1), 11101112.
Okuda, T., Mori, K. and Hayatsu, H. (1984) Inhibitory action of tannins on direct acting
mutagens. Chem. Pharm. Bull., 32(9), 37553758.
Pei-gen, X. (1989) Excerpts from the Chinese Pharmacopoeia. In: L.E. Craker, J.E. Simon (eds)
Herbs, Spices and Medicinal Plants, Vol. 4. Oryx, USA, pp. 4385.
Perry, L.M. (1980) Medicinal Plants of East and South East Asia, MIT Press, USA, p. 159.
Rodriguez, J., Loyola, J.T., Maulen, G. and Schmeda-Hirschmann, G. (1994) Hypoglycaemic
activity of Geranium core-core, Oxalis rosea and Plantago major in rats. Phytother. Res., 8(6),
372374.
Serkedjieva, J. (1995a) A polyphenolic complex isolated from Geranium sanguineum L. inhibits
influenza virus neuramidase. Fitoterapia, 63(2), 111117.
Serkedjieva, J. (1995b) Inhibition of influenza virus protein synthesis by a plant preparation
from Geranium sanguineum L. Acta Virologica, 39(1), 441443.
Serkedjieva, J. (1996) A polyphenolic extract from Geranium sanguineum L. inhibits influenza
virus protein expression. Phytother. Res., 10(5), 441443.
Serkedjieva, J. (1997) Antiinfective activity of a plant preparation from Geranium
sanguineum L. Pharmazie, 52(10), 799802.
Serkedjieva, J. (1999) Anti herpes virus activity of extracts from the medicinal plant Geranium
sanguineum L. J. Ethnopharmacol., 64(1), 5968.
Serkedjieva, J. and Hay, A.J. (1998) In vitro anti-influenza activity of a plant preparation from
Geranium sanguineum L. Antiviral Res., 37(2), 121130.
Srivastava, T.N. and Gupta, O.P. (1982) Medicinal Plants used by Amchies in Ladakh. In: C.A.
Atal and B.M. Kapoor (eds) Cultivation and Utilization of Medicinal Plants, Regional Research
Laboratory, CSIR, Jammu-Tawi, India, 519526.
Tisserand, R. and Balacs, T. (1995) Essential Oil Safety. Churchill Livingstone, Edinburgh, UK.
Ushio, T., Okuda, T. and Abe, H. (1991) Effect of geraniin on morphology and function of
macrophages. Int. Arch. Allergy Appl. Immunol., 96(3), 224230.
Yau, X., Zhou, J. and Xie, G. (1999) Traditional Chinese Medicines. Ashgate Publishing, UK.
Yokozawa, T., Fujioka, K., Oura, H., Tanaka, T., Nonaka, G. and Nishioka, I. (1995)
Confirmation that tannin-containing crude drugs have a uraemic toxin-decreasing action.
Phytother. Res., 9(1), 15.

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Part 2

Pelargonium

2002 Edited by Taylor & Francis

The taxonomy of Pelargonium


species and cultivars, their origins
and growth in the wild
Diana M. Miller

CHARACTERISTICS OF THE GENERA WITHIN


THE FAMILY GERANIACEAE

The genera Geranium and Pelargonium are classified in the family Geraniaceae and like
the three other genera included in Geraniaceae they also have a similar elongated fruit
with five mericarps, each containing a single seed. When the seeds mature, the
mericarps split apart and the plumed seed is released. Monsonia is found mainly in
Africa with a few species in Asia. The fleshy stemmed Sarcocaulon is limited to southern
Africa where it is called Bushmans candle. The remaining three genera were included
by Linnaeus in the one genus Geranium named from the resemblance of the fruit to a
cranes bill. The true Geranium has a wide distribution throughout the temperate
regions of the world but the genus of plants with irregular flowers was later separated
from Geranium and named Pelargonium for the Greek word for stork, pelargos. The
third genus, Erodium, mainly found around the Mediterranean, was later separated and
renamed from the Greek for heron. The differences between Geranium and Pelargonium
are compared in Table 8.1.
The majority of Pelargonium species are found in the Southern hemisphere mainly in
South Africa with a few in Australia, eastern Africa and on some islands including
St. Helena, Tristan de Cuhna and Madagascar. On the other hand Geranium grow wild
in the Northern hemisphere in North America, Europe and Asia. Although, as Table
8.1 indicates, the species of each genus should be readily distinguished, confusion has
arisen over the nomenclature of Pelargonium. When first introduced into Europe in the
seventeenth century, all pelargoniums were called geraniums, presumably because of
the similar fruit structure. However, later botanists noted distinct differences and the
two genera were separated about 200 years ago. However, the name geranium has
become re-established during the twentieth century as a vernacular name for
pelargoniums especially for the zonal cultivars so widely used in bedding.
HISTORY OF DISCOVERY

As with the majority of plants, the discovery and introduction of the first Pelargonium
species into the great gardens of Europe is closely connected with the history of
exploration and the opening up of trade routes. Once the route around the southern tip
of Africa to the East had been discovered and the spice trade was established, the East
India Companies of Britain and Holland were set up to create permanent trading posts

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50

Diana Miller

Table 8.1 The distinctions between Pelargonium and Geranium


Pelargonium

Geranium

Flowers irregular, the upper two petals different


in shape and size to the lower three
Hypanthium present
Fertile stamens less than ten
Habit various
Mostly frost tender
Mostly from the Southern hemisphere

Flowers regular, all petals more or less the


same in shape and size
No hypanthium present
Fertile stamens ten
Mostly herbaceous
Mostly hardy
Mostly from the Northern hemisphere

in southern Africa. Naturalists on board collected plants for possible food or medicine
for the sailors and plants were brought back to Europe to botanic gardens such as the
one at Leiden, established in 1577.
The earliest plants from South Africa were bulbs and the first recorded Pelargonium
was the tuberous rooted, P. triste. It is found wild in the regions near the early
settlements on the coast. Other pelargoniums grow in similar areas with much more
showy flowers, but P. triste with a tuber would have been more able to survive the long
journey back. It may have been collected as a medicine as it has been used as such in its
native land, or as a possible food source, or simply for the night-scented flowers. It was
first recorded in 1631 by John Tradescant but it was initially considered to be a native
of India, presumably because it was brought back on a ship returning from the East.
Paul Hermann in 1672 was perhaps the first serious collector who pressed examples
of the South African Flora on his way to Ceylon (now Sri Lanka). Seeds were sent to Jacob
Breyne who illustrated one or two Pelargonium species in 1678. On his return to Holland,
Hermann published a catalogue of the plants of the gardens in Leiden which listed nine
pelargoniums, all of which are still grown today. Jan Commelin at the new botanic
garden in Amsterdam, also received plant material and 2 years later was listing one or
two new species and, by 1710, about ten more new species had been added to this
collection.
Exchanges of plants between Britain and Holland were frequent, and records around
the turn of the century show that in London, James Sherard, an apothecary with a large
estate at Eltham in Kent and the Bishop of London, Henry Compton in his famous
contemporary gardens at Fulham included pelargoniums. In South Africa at about this
time, explorations inland to the north and east resulted in the discovery of more new
species of Pelargonium several of which were recorded in European gardens. During the
next 50 years there was a slow but steady introduction of species, but in 1772 a young
collector from Kew, Francis Masson was sent to South Africa and was responsible for
about 20 years, for the introduction of a large number of new species from inland areas
of the southern and south-western Cape.
Another Kew gardener was Anthony Hove. On his way to India in 1795, he collected
17 pelargoniums from near the Bay of Angra, on the south-western coast of Africa,
about 500 miles north of the Cape. Unfortunately only three survived.
The explorer William Paterson in 1777 also collected plants as he travelled
northward along the coast where he discovered the Orange River as well as P. sibthorpifolium and P. klinghardtense. The first Australian species such as P. australe found as
early as 1792, were collected following the expeditions of Captain Cook and Joseph
Banks.

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The taxonomy of Pelargonium species and cultivars

51

Towards the end of the eighteenth century and during the nineteenth century, a large
number of hybrids were grown, at first as accidental seedlings and later as the process
was understood, more deliberately produced. Zonal, regal, scented-leaved and ivyleaved cultivars were well known by the late nineteenth century and an explosion of
interest in these groups throughout the world has occurred during the twentieth
century. New species have been discovered and a number, especially from the section
Hoarea have been named as recently as the 1990s.

GENERAL CHARACTERISTICS OF THE GENUS PELARGONIUM

The flowers of Pelargonium are arranged in an umbel-like inflorescence of one to about


50 individual flowers. Whereas in a true umbel, the youngest flowers are at the centre
of the flower head, in pelargoniums, the oldest flowers are at the centre, so the
inflorescence is normally termed a pseudoumbel.
Each flower has five sepals with the posterior one modified so that a nectary is formed
at the base. The length of this nectary is characteristic for each species and in some is
a mere indentation but in others may be several centimetres long. The nectary is fused
to the pedicel and known as the hypanthium. At the end of the hypanthium is a hump,
sometimes quite pronounced, and the relative lengths of the hypanthium and pedicel
is often important in the classification of species. The five free petals are often clawed
and arranged so that the upper two are separated from the lower three usually with
a distinct difference in size, shape and markings. This distinction becomes less obvious
in the modern zonal and regal cultivars, deliberately bred in Victorian times to bear
regular flowers with rounded petals. The relative sizes, arrangement and positioning of
the petals, together with the differing lengths of pedicel and hypanthium, create the
wide range of flower formation in the genus, each having evolved alongside the
appropriate pollinating insect found in its native habitat.
Of the ten stamens, seven or fewer bear fertile pollen and this number is, another
significant feature in the recognition of the sections. The remaining infertile stamens
are known as staminodes, which may be curved. The filaments are joined at the base,
occasionally for most of their length. The style divides into five stigmas, which open
after the anthers have dehisced, thus avoiding self pollination. Once the flower is
fertilised, the mericarps develop and the plumed seeds are dispersed.
In habit, the species of Pelargonium may be woody, succulent or herbaceous, annual or
perennial, evergreen or deciduous, and some have tubers. All have alternate petiolate
leaves with stipules. The leaf venation may be palmate or pinnate, simple or compound
and of almost any shape. In some sections, the petioles, the stipules or both are
persistent, remaining on the stems for several seasons often hardening to form spines.
The presence of aromatic oils in many species is often a useful tool for identification.
A few species have scented flowers but this scent is usually only emitted at night.

NATIVE HABITATS

The genus Pelargonium includes about 270 distinct species and the majority of these are
to be found in southern Africa. In southern Africa, itself, over 80 per cent of these are

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associated with the Mediterranean type of climate and vegetation found in the southwestern part of Cape Province in an area of winter rainfall. The remaining species are
found in southern and eastern Cape where the rain falls mainly in summer. Approximately
20 or so grow in East Africa. About a dozen species are to be found wild outside Africa,
some in Australia, one or two in New Zealand, two in the Middle East and one or two are
to be found on the islands of Madagascar in the Indian Ocean and St. Helena and Tristan
da Cunha in the southern Atlantic Ocean (van der Walt, J.J.A., 1977).
The characteristic feature of all these localities is the relatively low rainfall which in
most cases falls mainly in one season of the year, either summer or winter. No species
grow in areas of high humidity and those that are found nearer the equator live at
higher altitudes where the temperatures are not excessive. However, in other respects,
all types of habitat are occupied from desert to tall grasslands, on rock faces or amongst
shrubs.
The genus is almost unequalled in the plant kingdom for the enormous diversity of
form created to adapt to these different habitats. The genus includes shrubs, annuals,
succulents and tuberous plants; plants of a few centimetres tall or shrubs reaching
several metres; plants with fragrant flowers or with scented foliage, some of which are
used in the commercial production of aromatic oils; plants which have spines and
a number valued for their medicinal properties.
CLASSIFICATION HISTORY

The first pelargoniums were grouped with geraniums. As early as 1732, Dillenius
suggested that the African species of Geranium with unequal and irregular flowers
might be called Pelargonium but he did not utilise his own epithet. Six years later, in
1738, Johannes Burman of Amsterdam again brought up the name and did employ
Pelargonium for at least some of the species he depicted. Not long after this date, in
1753, Linnaeus published his Species Plantarum which although it established the
binomial system of naming, did not recognise Pelargonium as a distinct genus and
retained the generic name Geranium for the 20 Pelargonium species known at that time
as well as those known today as Erodium and Geranium. Such was the stature of Linnaeus
at the time, that the name Geranium was retained for another 40 years before the name
Pelargonium was finally approved.
Arguably, the most important taxonomic works were the illustrations and
unpublished descriptions of Charles-Louis LHritier, who is given the credit for
publishing the name Pelargonium in Geraniologia 17871788 where he clearly
distinguished between the three genera, Pelargonium, Erodium and Geranium. Although
the generic names were disputed for a few years, they were eventually established and
have remained since.
By the latter part of the eighteenth century, the number of new Pelargonium species
and hybrids had risen so dramatically that a means of classifying them became
imperative. Cavanilles in 1787 subdivided the species of Geranium into groups. He separated the African geraniums, on the basis of their flower shape and further subdivided
these on leaf characters such as the presence of a zone, and then on the degree of lobing.
Aiton in 1789 placed species with similar morphology together but did not attempt to
formalise the groupings with names. The first serious attempt was by Sweet in 1820, in
the first of his five volumes of Geraniaceae. He separated many of the more distinct

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species by creating ten new genera. These differences were obviously recognised, but not
necessarily considered sufficient to merit the status of unique genera, and de Candolle in
1824 soon reduced Sweets genera to sections within the original genus Pelargonium.
Although his classification included many new names for sections which were then
subdivided into series, it made the recognition of a plant easier because each grouping
was smaller to include far fewer species. Different classifications were published in the
following years such as that by George Don in 1831.
Most of the classification systems which followed were variations or amalgamations
of the systems produced by Sweet and de Candolle. Ecklon and Zeyher in 1835, prolific plant collectors in South Africa, reinstated the generic status for several sections
and created other new ones as well but they seem to have little influence on classification as these names were soon discarded by Harvey in Flora Capensis. William
Harvey, Colonial Treasurer at the Cape in 1835 produced his Flora Capensis in 1860
where he separated the genus into 15 sections, many of which were combinations of
those proposed by Sweet and de Candolle. Reinhard Knuth, who published an important work on Geraniaceae in 1912, basically followed Harveys naming but included
a number of new species.
Harveys division of the genus into sections was followed in principle for over a 100
years until the last 20 years when the taxonomists in South Africa began a major study
of the genus. This investigation is still being carried out by botanists in several parts of
the world looking at all aspects of taxonomy. These modern methods investigate all
aspects of the species, including location, habitat, chromosome size and number, pollen
characteristics, alkaloid and protein content, external morphology and internal
anatomy. In many cases, the original classifications have remained very similar although
the recent work has solved many anomalies and is able to show evolutionary trends and
relationships. Even more recently a group or researchers have made a detailed phylogenetic study, the results of which are not completely published, and their latest
classification has been followed in this publication.
SYNOPSIS OF SECTIONS

The most recent classification is based on the molecular work but has initially been
divided into two subgenera based on the chromosome size. Each subgenus is further
divided into a number of sections. These divisions into sections in most cases matches
the morphological-based classification of the older botanists and closely relates to areas
of similar climatic conditions with a characteristic type of vegetation. It does solve
a number of apparent past anomalies. All species of the section Cortusina, for example,
are to be found in southern Namibia and the north-western part of Cape Province in
desert or semi-desert regions where the winter rainfall may not exceed 23 cm a year
and plants may be found protected by rocks or in loose sand. However, the species of
section Reniformia, until relatively recently classified in the same section, are to be
found towards the southern and eastern part of South Africa in areas of summer rainfall, up to 2030 cm a year, some in long grass and others at the edges of forest. The
adaptation of each species to the microclimate in which it is found, explains the enormous variation in habit. Even within a single species in the wild, the variation in the
habit of the plant collected from different localities can reflect the conditions under
which it was growing, especially availability of water and light. This adaptability can

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cause some problems with identification. Hybrids between subgenera are not known
and hybrids between the sections are extremely rare.
Subgenus Ciconium
This subgenus representing about 23 per cent of the species in the genus has large
chromosomes and is divided into six sections. Most of the species are found in eastern
and southern Cape Province and East Africa, Yemen to the Middle East.
Section Ciconium

This extremely important section for horticulture, includes several species involved in
the ancestry of both the zonal and ivy-leaved pelargoniums. Earlier, botanists separated
species with the trailing habit of P. peltatum into a distinct genus, Dibrachya. Nowadays,
this section is merged with Ciconium (van der Walt and Vorster, 1988) and more
recently species have been added from other sections such as Ligularia. All have large
chromosomes with a basic number x 9. If not pruned back for the winter, nearly
all are evergreen in cultivation, with simple, palmately lobed, but not repeatedly
divided, leaves.
The flowers tend to be in shades of red and pink or white but less frequently in the
purplish shades associated with species in other sections. Unusually the lower petals
may be equal in size or sometimes even larger than the upper. There are seven or fewer
fertile stamens of which two or more may have extremely short filaments or all the
filaments may be united for almost their whole length. The hypanthium is long, mostly
over five times the pedicel length.
The majority of the species grow wild in the eastern or southern parts of Cape
Province. Two important species are P. zonale and P. inquinans, considered to be
the major parents of the zonal cultivars. Both are among the early introductions of
the genus at the beginning of the eighteenth century but the main development of the
zonals did not begin until well over a 100 years later. Sports and selections of P. peltatum
on the other hand resulted in the ivy-leaved pelargoniums with probably little or no
influence from other species.
P. acetosum (Linnaeus) LHritier: A branching, subshrub with hairless brittle stems and
fleshy, glaucous leaves, sometimes with a reddish crenate margin. The pale to salmonpink flowers have very narrow petals and five fertile stamens. This was one of the very
early species of Pelargonium from eastern Cape Province which was included in
illustrations by Casper Commelin of the plants in the medicinal plant garden in
Amsterdam in 1703. Perhaps it was thought that the sorrel tasting leaves had some
curative properties although they have no known medicinal value.
P. articulatum (Cavanilles) Willdenow: A plant with a very short stem above ground but
an underground rhizome which is alternately thick and thin. The more or less orbicular
leaves usually have a narrow dark zone towards the margin with deeply cordate base and
large cream to white flowers have upper petals veined with purple, much narrower lower
petals and seven fertile stamens. This species has recently been used in Australia with
zonal cultivars to produce a range of interesting hybrids. It is thought that Thunberg
was the first to collect this species in the early 1770s from the western part of Cape
Province.

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P. frutetorum R.A. Dyer: A spreading, branching plant with thick reddish-brown stems
and shallow five-lobed, green leaves with a very distinct dark brown-purple ring-shaped
zone towards centre of lamina. The pale salmon pink flowers have seven fertile stamens.
This species from the eastern Cape Province has been used in hybridisation to create
zonal type cultivars with attractive foliage. It is less robust than P. zonale but has a much
more clearly defined zone on the leaf. The Boar is almost certainly derived from this
species.
P. inquinans (Linnaeus) LHritier: An erect, branching, subshrub to about 2 m tall with
red glandular hairs and unmarked, almost circular shallow lobed leaves. The flowers are
scarlet, occasionally pink or white, almost regular in shape, the upper petals slightly
smaller than lower. The stamens and style are barely exserted and the filaments with
seven fertile anthers are joined for most of their length.
This species and P. zonale are generally considered to be the main parents of the
modern zonal pelargoniums, and both were very early introductions from the Eastern
Cape into the great gardens of Europe in the early eighteenth century. Many plants
found under this name are early hybrids but the true species is easily recognised by the
red glandular hairs found on the stems and leaves which leave a red-brown stain on the
hands. The plant is another of those that has been used in the past for its medicinal
properties.
P. peltatum (Linnaeus) LHritier: A trailing or climbing, variable perennial with somewhat fleshy, slightly aromatic leaves, usually peltate, with five triangular lobes, either
glossy and glabrous or with a short soft velvety pubescence, often with a darker circular
zone. The flowers are strongly zygomorphic, white, pink or pale purple, up to 4 cm
across, the upper petals larger and veined darker; fertile stamens seven, two of which
are very short.
Typically P. peltatum is found scrambling through other shrubs, able to reach to 2 m
or more. It grows wild over a large area of the winter rainfall zone in Cape Province but
the distribution extends much further east into the regions of summer rainfall of Natal
and eastern Transvaal. It was apparently introduced into Europe in 1700. The leaves
have been used as an antiseptic and a deep blue dye, which has been used in painting,
may be obtained from the petals but the species is most important as the parent of the
ivy-leaved pelargoniums.
P. quinquelobatum Hochstetter: A herbaceous, hairy, perennial plant with dull green,
bluish-tinged deeply lobed leaves which are broadly triangular in outline. The flowers
are pale yellowish-green to grayish green-blue, the upper petals faintly lined with pink,
and three of the seven fertile stamens have very short filaments.
The unusual colour of the flowers of this species from Tanzania and Kenya to
Ethiopia, has encouraged the use of this plant for hybridisation although few have
proved successful so far.
P. salmoneum R.A. Dyer: A weakly erect, branching subshrub to about 1.5 m or more
with semi-succulent stems and thick, green to glaucous, unmarked leaves which are
somewhat folded upwards. The narrow petals of the salmon pink flowers are almost
equal and there are five fertile stamens.
P. salmoneum was first found in a garden in Port Elizabeth and described in 1932. For
many years it was considered to be a species but later, because it was only known in
cultivation, it was listed as a cultivar.

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P. zonale (Linnaeus) LHritier: An erect usually hairy subshrub but often found scrambling through bushes. The orbicular leaves, often have a darker brownish-purple
horseshoe-shaped mark. The inflorescence has up to 50 pink, sometimes white or red,
flowers with more or less equal petals, marked with darker veins and seven fertile
stamens, two of which are very short. In the wild, this species is widespread from
eastern to western Cape Province and Commelin, records how it was grown in 1700 in
the medicinal garden of Amsterdam.
It has lent its name to the enormous group of modern cultivars, the zonals, named
on account of the zoned leaf, and it was certainly involved in their parentage.
Section Chorisma

Old references, especially in German, placed P. tetragonum in the genus Chorisma which
was later referred to as a section by de Candolle. Harvey transferred the species to
section Jenkinsonia but recent studies indicate that the section Chorisma should be reinstated and include three other less well-know species, until recently classified in the
section Ligularia (Albers et al., 1995). These are all shrubs or subshubs with herbaceous
or semi-succulent stems. The simple leaves have petioles usually longer than the
lamina. The inflorescence has up to six flowers on short pedicels, each with two very
large upper petals and two or three very much smaller lower ones. There are five or
seven fertile stamens. All have very large chromosomes with a basic number x 11.
The species may be found wild in the southern part of Cape Province from the western
to eastern Cape.
P. tetragonum (Linnaeus f.) LHritier: A sprawling or upright tufted plant with brittle
green, three or four-angled, succulent stems jointed at the nodes. The rounded or
reniform dark green, often marked with a darker zone leaves are quickly deciduous. The
flowers are large, cream or pale pink, one or two at the ends of the branches with the
upper petals veined dark red, a hypanthium up to 6 cm long and seven strongly exerted
fertile stamens, the filaments bent sharply upwards.
It was collected by Francis Masson on his second expedition around the Cape
Peninsula and introduced to Kew in 1774 and also grows wild in dry rocky ground
from the west coast to Grahamstown.
Section Myrridium

Most species in this section are herbaceous plants with pinnately divided leaves and
rather long straggly stems sometimes woody at the base. The flowering stems become
very elongated, with smaller leaves along their length, while long peduncles hold the
flowers above the foliage. The inflorescence is few flowered and each flower is very
irregular in shape with two very large upper petals, usually with long claws, but three
or sometimes only two, small lower ones. The sepals have a membranous texture and
are conspicuously veined and ribbed. The hypanthium may be quite long and the fertile stamens five or seven. The fruits enlarge quite considerably as they ripen (van der
Walt and Boucher, 1986). The plants are often found as sprawling roadside weeds and
many are pioneer plants colonising disturbed ground. Most grow wild in the winter
rainfall areas of south-western Cape Province, though some species extend further east
and north into the summer rainfall regions. The basic chromosome number is x 11.

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P. longicaule Jacquin: These are low growing, spreading, herbaceous plants with dark green
leaves, often tinged red, deeply pinnately divided to bi-pinnatisect. The white to pale pink
flowers, often tinged yellow in bud, have upper petals with conspicuous red feathering and
seven fertile stamens. The first reference to this plant in 1767 described this species as
a form of P. myrrhifolium but there has been much confusion about the nomenclature of
members of this section. It grows in mountainous regions of south-western Cape Province.
P. caucalifolium Jacquin: Superficially this species might be mistaken for P. longicaule but
in P. caucalifolium the stems tend to be woodier and the flowers rarely have more than
four petals and there is usually only one flower, rarely two on each flower stem.
P. myrrhifolium (Linnaeus) LHritier: This is a low growing, short lived subshrub with
pinnatifid or bi-pinnatisect leaves. Flowers are white to pale purplish-pink, each
peduncle bearing up to five flowers, the upper petals with long claws and deep red
feathered markings and five or seven fertile stamens. This species is very variable in the
wild being found from Namaqualand through south-western Cape Province to Port
Elizabeth in southern Cape Province. It was one of the earliest pelargoniums to be
introduced and it was first illustrated in 1678. The variety coriandrifolium has more
finely divided leaves and larger flowers but many plants found in cultivation under this
name are the larger flowered P. longicaule.
P. candicans Sprengel: This species shows some resemblance to P. myrrhifolium var. myrrhifolium with rather small pinkish coloured flowers. It is however distinguished by leaves
which are a gray almost silvery green, often with a darker blotch in the centre and with
two lobes at the base. The flowers always have four petals and five fertile stamens.
P. suburbanum Clifford ex Boucher: This is a sprawling herbaceous perennial, and the
leaves have long conspicuous hairs. The flower buds are large and the flowers bright
pink or white to pale yellow held well above the foliage, the upper petals with dark red
feathered markings and with seven fertile stamens. Two subspecies are easily distinguished in flower as ssp. suburbanum, which has bright pink flowers with a shorter
hypanthium, while the flowers of ssp. bipinnatifidum are cream with the hypanthium
exceeding 15 mm. Whereas ssp. suburbanum is found in eastern Cape Province, ssp.
bipinnatifidum grows in the south-west.
Section Jenkinsonia

In his first volume of Geraniaceae in 18201822, Robert Sweet proposed a new


genus, Jenkinsonia, which he named after Robert H. Jenkinson, one of the well known
collectors of members of the family Geraniaceae in the early nineteenth century. He
included in this genus, species now reclassified in the related sections Myrrhidium and
Chorisma (van der Walt et al., 1997). Most of the species in this recently redefined section
are subshrubs, some with tubers although two species, P. senecioides and the recently
described P. redactum are annuals, rarely seen in cultivation. The leaves, sometimes soon
deciduous, are palmately or pinnately divided and in several species, aromatic. The
length of the hypanthium may be shorter or longer than the pedicel, the petals four or
five, the upper usually larger and sometimes rolled to form a tube-like structure. There
are two, three, five or seven fertile stamens. The species of this section with a basic
chromosome number x 9, are distributed through most of southern Africa including
Namibia and Botswana but the majority may be found in the north-western area.

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Figure 8.1 P. praemorsum. (See Colour plate 1)

P. antidysentericum (Ecklon and Zeyher) Kosteletzky: This is an erect branching shrub


with a very large, partly underground tuber and thin branches becoming woody
with age and often with hard curved spines formed from persistent stipules.
Rounded, five-lobed, aromatic leaves are produced in clusters on short branches. The
flowers have five purplish-pink or white petals veined with purple, a long
hypanthium up to 30 mm and seven prominently exserted fertile stamens, the filaments slightly curved upwards. This unusual species is found growing in very arid
regions of Namibia and Namaqualand. The enormous tubers were used by the
Hottentots as a medicine in cases of dysentery and anaemia. First described in 1835,
it was known to be in cultivation a few years later but is only seen in a few specialist
collections today.
P. praemorsum (Andrews) Dietrich: This is a branching subshrub up to 30 cm or so in
height with rather thin brittle stems (Figure 8.1). The leaves are almost round, deeply
divided into five, sometimes clustered at the nodes, soon deciduous but the stipules
persistent and rigid. The flowers are cream or pink to purple, the upper petals are very
large, veined with deep red or purple, the lower petals two or three and the seven
exserted fertile stamens have filaments strongly curved upwards.
It is thought to have been first introduced into cultivation in England from
Namaqualand at the end of the eighteenth century and although not common is
spectacular in flower.
P. trifidum Jacquin: This is a scrambling herbaceous plant woody at base with bright
green trifoliate to trifid leaves, strongly scented when touched. Flowers large, cream to
almost white, the larger upper petals with conspicuous red veining, the hypanthium
long and seven fertile stamens (Figure 8.2).
This freely seeding plant is found wild in arid regions from the south-western to the
eastern regions of the Cape Province, and was first introduced into cultivation at Kew

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Figure 8.2 P. trifidum. (See Colour plate 2)

in 1790. Several forms, differing slightly in leaf and flower size are seen in cultivation,
some with a more pleasant scent than others.
Section Subsucculentia

The four species of this recently proposed section with large chromosomes and a basic
number x 10, have been separated from the section Ligularia (van der Walt et al.,
1995). All are rare in cultivation but in the wild may be found on the west coast of
southern Africa from Namibia to the western Cape. They form deciduous, shrubs or
subshrubs with woody or somewhat succulent stems, often covered with spines formed
from the persistent remains of the petioles. The inflorescence of up to ten flowers, each
with five petals, the upper and lower more or less similar in size, five or seven fertile
stamens and the hypanthium long, usually exceeding the pedicel.
Section Quercetorum

As a result of recent investigations, it has been proposed that a number of species from
the Sections Ciconium, Ligularia or Jenkinsonia are included in this new section Although
this grouping reflects their phylogenetic identity, the four species are geographically and
morphologically very diverse. Two more or less hardy species from the Middle East in
Iraq and Turkey, (P. endlicherianum and P. quercetorum), have swollen roots with two very
large magenta coloured upper petals but with minute or absent lower petals and seven
fertile stamens. One species from the south-western Cape Province (P. karooicum) is
a small woody plant with long semi-succulent branches becoming woody with age,
deciduous leaves, white pink or pale yellow flowers, the upper petals slightly larger than
the lower and five fertile stamens (Figure 8.3). The fourth species from Madagascar
(P. caylae) is a tall evergreen shrub with pale purple-pink flowers with somewhat undulate petals and five fertile stamens. All are extremely rare in cultivation in Europe.

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Figure 8.3 P. karooicum. (See Colour plate 3)

Subgenus Pelargonium
All members of this subgenus have small chromosomes and it is now separated into
eight sections, several of which have been subdived into subsections. About 77 per cent
of the recognised species belong in this subgenus. The majority are found in the winter
rainfall areas of the south-western Cape and Western areas of southern Africa although
members of the Section Peristera are geographically spread from Australia or several
Oceanic islands and through southern and eastern Africa.
Section Campylia

Initially, the name for this section was used by Sweet in 1820 for a new genus to include
P. ovale, on account of the two bent staminodes. Others of the present section such as
P. tricolor, with erect staminodes and shiny raised bumps at the base of the two upper
petals, he assigned to yet another genus, Phymatanthus, meaning wart-flower. These
patches are false nectaries to attract insects for pollination (MacDonald and van der
Walt, 1992). The two genera were then amalgamated into one section, Campylia, by
de Candolle a few years later and the recent work in South Africa has added the newly
described species, but as yet rarely cultivated, P. ocellatum, as well as some from other
sections (van der Walt and Roux, 1991).
The plants are small, with short stems and all have an extensive root system enabling
the plants to tap water from well below the surface. The leaves have long petioles with
conspicuous membranous stipules at the base. The flowers are often rather open or flat
in shape with five, occasionally four, usually broad petals, a long pedicel and five or seven
fertile stamens. The hypanthium is usually very short and in some cases the only sign is
a slight depression at the base of the upper sepal. In some species such as P. ovale, the
upper petals have constricted or auricled bases. The basic chromosome number is
x 10. There appears to be some affinity between this section and the section Pelargonium. Campylia includes some of the most difficult species of the genus to grow. In the
wild, this section is centred in south-western and southern parts of Cape Province where

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Figure 8.4 Splendide a hybrid between P. tricolor and P. ovale. (See Colour plate 4)

the plants tend to grow in mountainous regions with very freely draining soils. Of about
ten species in the genus, about three are found in general cultivation.
P. elegans (Andrews) Willdenow: This is a small erect tufted plant with green, hairy or
glabrous, broad ovate to almost rounded leaves, the margin often reddish. The flowers
large, to 3 cm across, pale to deep pink, the upper petals with darker markings, and
with seven fertile stamens. P. elegans introduced by the British nursery firm of Lee and
Kennedy in 1795, is found in south-western Cape Province, often near the coast.
P. ovale (Burman filius) LHritier: This is a low growing plant with hairy, often graygreen, almost rounded to lanceolate leaves. The flowers, about 4 cm across, are white to
deep pink, the upper petals with darker markings and have five fertile stamens. This is
a variable species and several subspecies have been named (van der Walt, J.J.A. and Van
Zyl, L., 1988). In the wild, it is found in mountainous regions of Cape Province and
Francis Masson collected slightly different plants for Kew on at least three of his expeditions in 1774, 1790 and 1794. It is one of the easier of the section to cultivate.
P. tricolor Curtis: This is a small plant to about 30 cm high. The leaves are gray-green,
hairy, narrow with sharp irregular teeth and often two larger lobes at the base. The
flowers c. 2 cm across, resemble a wild pansy, the upper petals deep red with a glossy
black raised spot and the lower petals white. Fertile stamens are five in number. P. tricolor
is found growing wild, often under other shrubs, in dry sandy soils in the foothills of
the mountains in south-western Cape Province.
It was first collected by Francis Masson on his expedition of 1791. Plants are
occasionally found with unicoloured white or mauve-pink flowers still bearing the dark
patches at the base of the petals. The true species is rare in cultivation and difficult to
grow but the cultivar Splendide, a hybrid with P. ovale, is easier and may be
distinguished by the long petioled, gray-green, hairy leaves which are broadly ovate and
more regularly serrated, the slightly larger flowers and dark purple stamens (Figure 8.4).

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Figure 8.5 P. alternans. (See Colour plate 5)

Section Otidia

This small section is well defined by the succulent habit of the species, totally unlike
other pelargoniums, showing some resemblance to members of the families
Crassulaceae or Euphorbiaceae. For this reason Sweet in 1822, adopted the genus Otidia
proposed earlier by Lindley for P. carnosum. This was later demoted to a section within
Pelargonium. All but one of these species are found in the arid regions of the western side
of South Africa and Namibia in areas where the winter rainfall may be under 100 mm
a year. The plants shed their leaves, becoming more or less dormant during the hot, dry
summers. Some grow near the coast and have to withstand salt-laden winds from the sea.
The plants grow in rocky areas but do survive in shifting sand dunes.
The plants have succulent stems, fleshy pinnate, often compound leaves and very
small stipules but the habit may be variable, especially so in cultivation when water is
less scarce. The leaves are usually clustered towards the top of stems as the lower ones
fall in previous seasons. The inflorescence is often branched, each branch bearing a few
white or cream flowers. The petals are not markedly dissimilar in size and shape,
although in most species, the upper two have reddish marks while the lower three are
plain. The flowers have five fertile stamens and a short hypanthium. The basic
chromosome number is x 11.
P. alternans Wendland: This is a succulent branching plant with deeply lobed, hairy,
pinnate leaves (Figure 8.5). The white flowers c. 1.5 cm across, have narrow reflexed
petals, the upper marked with red lines. Plants in cultivation tend to be more vigorous
whereas in the wild the old plants are stunted and woody. The species may be found in
the dry and mountainous regions of south-western Cape Province and is said to have
been introduced to Kew by F. Masson in 1791.
P. carnosum (Linnaeus) LHritier: This is a succulent plant 30 cm or more tall with very
variable oblong, more or less succulent, gray-green to green leaves, to c. 15  5 cm.
The white, sometimes greenish-tinged flowers are almost regular in shape, about
1.5 cm across with slightly reflexed upper petals marked with reddish-purple lines.

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This, the first known member of the section first illustrated by Dillenius as early as
1732, is still the most widely grown today. With its very wide natural distribution in
southern and south-western Africa, it is variable in its morphological characteristics
and has been collected on many expeditions.
P. ceratophyllum LHritier: This is a much smaller plant with thinner stems and almost
rounded succulent leaf segments and small petals barely longer than the sepals. This is
one of several species which grows wild in south-western Namibia and north-western
Cape Province. It was first collected in 1786 by A.P. Hove, a collector for the Royal
Botanic Gardens of Kew.
P. dasyphyllum Meyer, E.: This species forms a branching succulent which has been
mistaken for P. alternans, but is less visibly hairy with a less woody appearance. The
narrow, unmarked, strongly reflexed petals give the flowers an asymmetric appearance.
It grows in the north-western part of Cape Province and was first collected in
about 1830.
P. laxum (Sweet) Don, G.: Apart from the much more irregular appearance of the
flowers, this species might superficially be mistaken for P. carnosum. It is the only
species of the section to be found in the summer rainfall zones of central and eastern
Cape Province. It is said to have been cultivated from seed sent to Colvill in 1821.
Subsection Cortusina

This section has recently been split and several species have been transferred to the new
section, Reniformia (Dreyer et al., 1992). However the most recent work by Bakker et al.
(2000) from the most recent phylogenetic analyses, has proposed that as this group of
plants are so closely related to members of the section Otidia that a subsection is more
appropriate. Many distinct morphological characteristics as well as the karyological evidence and very widely separated geographical locations, made this an obvious division.
In 1824, de Candolle created a subseries for species such as P. echinatum. Ecklon
and Zeyher and raised it to the status of genus in 1835, but Harvey in Flora
Capensis in 1859 used the name as a section. The species are from the desert and
semi-desert areas of north-western part of Cape Province and Namibia where the
winter rainfall is exceedingly low, often under 10 cm annually. The stems of all
except one, are succulent for the storage of water and often covered with the remains
of persistent hard stipules or petiole bases, giving extra protection. The long petioled, simple, usually almost rounded leaves, are shed in periods of drought. Several
species have the added advantage of tuberous or thickened roots. The inflorescence
is rarely branched, but each peduncle bears several flowers. Each flower has an
almost regular appearance with six or seven fertile stamens and, except for P. desertorum, the hypanthium is always conspicuously longer than the pedicel. The basic
chromosome number is x 11.
P. cortusifolium LHritier: This is a branching plant to 30 cm with thick succulent stems
and almost rounded hairy leaves with a silvery sheen. Flowers are white to pale pink or
lilac in inflorescence of about ten flowers, the lower petals often darker in colour than
the upper; fertile stamens six. This species is found along the coastal areas of southern
Namibia in desert conditions. It was first collected by A.P. Hove in 1786 during an
expedition to the south west coast of Africa.

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Figure 8.6 P. echinatum. (See Colour plate 6)

P. crassicaule LHritier: This is a low growing plant with thick brown knobbly succulent
stems and very broad ovate gray-green leaves with a soft velvety texture. It has white to pale
pink or lilac flowers in inflorescence of about eight flowers which are slightly scented. The
reflexed upper petals are often blotched and lined with purple; fertile stamens six or seven.
Like P. cortusifolium, this species was introduced by Hove in 1786 from southern Namibia.
P. desertorum Vorster: This species is very similar to P. xerophyton, but with strongly aromatic foliage and the hypanthium shorter than the pedicel.
P. echinatum Curtis: This is an erect subshrub with thick spines on stems from persistent petioles and ovate, shallow 35 lobed, gray-green, leaves paler and hairy
below, up to 6 cm across. Flowers are usually white in cultivation but also pink to
purple in wild, 1.52 cm across; ovate upper petals each have a dark red blotch and
lines and 67 fertile stamens (Figure 8.6).
The species grows wild in the north-western regions of Cape Province and a white
flowered specimen was first collected by F. Masson for Kew in 1789. Miss Stapleton
which has bright purplish pink flowers spotted on each petal with longer straighter
spines, was raised from seed collected at Colvills nursery and first flowered in 1823.
P. xerophyton Schlechter ex Knuth: This is a low growing plant with numerous thick and
almost woody branches with dull to blue-green broad ovate leaves. It has white, usually

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solitary flowers, the upper petals are narrow and spotted red; there are seven fertile
stamens. This species, first recorded in 1897, is native to southern Namibia and
north-western Cape Province, surviving in the shelter of rocks.
Section Pelargonium
This is a large section which contains some very important plants for both the horticultural industry and as a crop for the commercial production of Geranium oil. It
includes the parents of most of the scented leaved cultivars, the angel pelargoniums and
the Uniques, as well as the species, P. cucullatum, from which all the regal pelargoniums
have been developed. These species may usually be found in areas where there is at least
some water, either in the subsoil or near streams or rivers, even though these are often
dry for part of the year. The majority are to be found in the winter rainfall regions of
south-western or southern Cape Province, many near to the coast. Unpruned, most will
become large and eventually, quite woody shrubs. The foliage is often aromatic and
sometimes viscid. The flowers, in few flowered inflorescences are white, pink or purple
but none are a true red or yellow. The upper petals are larger in size and often a different shape compared to the lower petals and are marked with darker spots or lines. There
are seven fertile stamens and the hypanthium may be longer or shorter than the pedicel
(van der Walt, 1985). The basic chromosome number is x 11. They appear closely
related to the subsection Glaucophyllum but do not grow in such arid situations.
The cultivars grown for rose-scented Geranium oils have been developed from species
such as P. capitatum and P. radens, and several other species have scented foliage which
have been considered as possible sources of aromatic oils, may be used in pot pourri and
in some cases for culinary flavouring.
P. betulinum (Linnaeus) LHritier: This is an upright or decumbent branching woody
plant with rather stiff, toothed leaves c. 20  15 mm. Flowers are pink or purplishpink, sometimes white, 3 cm or more across, upper petals heavily veined with
purplish-red, lower petals unmarked or with faint markings, narrower than upper.
This species, which is found near the south-western and southern coast line of South
Africa, was known in European gardens in the mid-eighteenth century. Natural
hybrids with P. cucullatum are found in the wild and it is almost certainly one of
the ancestors of some of the regal and Unique pelargoniums, as a result of accidental
crosses in the early days of the eighteenth century. It has been used for the treatment of chest complaints in its native land.
P. capitatum (Linnaeus) LHritier: This is a decumbent, somewhat spreading, or weakly
erect, softly hairy plant and densely hairy, strongly rose-scented foliage to 28 cm
across. Flowers measure to 15 mm across, usually mauve-pink in very dense compact
heads of 1020 flowers, upper two petals narrow obovate, veined darker pink. P. capitatum found in many areas along the coasts of South Africa, was one of the earlier species
imported to Europe and records indicate that it was brought into England from
Holland in 1690. The true species is quite rare in gardens but is represented by the cultivar Attar of Roses with a more upright habit and rougher but strongly aromatic
foliage and pinker flowers.
P. citronellum J.J.A. van der Walt: This is a rough, hairy, strongly lemon-scented shrub
to 2 m with irregularly toothed leaves (Figure 8.7). Flowers are pale pinkish-purple in

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Figure 8.7 P. citronellum. (See Colour plate 7)

an open branching inflorescence, upper petals reflexed, marked with dark purple lines
and blotches. Until recently, this plant was not recognised as a distinct species because
of its similarity to P. scabrum. It normally grows near streams in a small area of southern
Cape Province. The popular, lemon-scented cultivar Mabel Grey is very similar.
P. crispum (Bergius) LHritier: This is a very upright plant, the base of the stems becoming woody with small strongly lemon-scented, rough leaves up to about 7 mm across with
crisped margins. The large flowers are usually pink, the upper petals with darker markings and notched at the apex. The species was first described in 1767 and grows wild in
south-western Cape Province. Garden plants show a wide range of leaf size and a number
of cultivars are grown for their lemon-scented foliage such as the smaller leaved, Minor,
the more vigorous Major and Variegatum with leaves edged with creamy white.
P. cucullatum (Linnaeus) LHritier: This is a large, erect, branched, hairy, shrub up
to over 2 m in height. Leaves rounded to triangular in shape, toothed and sometimes
shallow lobed, usually hood- or cup-shaped with long hairs, sometimes aromatic,
c. 4.5  50 cm. Flowers measure to over 4 cm or more across, and are bright purplish
pink in a large branching inflorescence, with the upper two petals veined deeper pink,
lower petals slightly smaller, narrower.
P. cucullatum grows wild in Cape Province and was introduced into cultivation in the
early part of the eighteenth century. Three subspecies, for many years treated as
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distinct, are found in geographical areas that rarely overlap (Volschenk et al., 1982). It
is almost certain that ssp. cucullatum and ssp. strigifolium are parents of the regal or
fancy pelargoniums. P. cucullatum ssp. tabulare with softly hairy, distinctly cup-shaped
and strongly scented leaves was involved in early hybrids such as Purple Unique.
In cultivation, it is sometimes difficult to decide which subspecies to assign a plant,
probably because of the hybridisation between the subspecies.
P. denticulatum Jacquin: This is an erect branched shrub up to over 1.5 m, with strongly
balsam-scented, sticky dark green leaves which are bi-pinnatisect, the ultimate segments being irregularly toothed. Flowers are purplish-pink, up to 2 cm across; the
peduncle measures up to 5 cm, bearing about six flowers; upper petals are narrow and
spathulate, veined darker pink, with the apex usually notched, c. 18  6 mm; lower
petals are slightly smaller, unmarked; the hypanthium is c. 89 mm; the pedicel up to
2 mm; there are seven fertile stamens. It comes from south-western and southern Cape
Province growing in the moister areas especially beside streams and in deep valleys and
was introduced into cultivation in 1789. The cultivar Filicifolium with very finely
divided leaves is a form of this species.
P. glutinosum (Jacquin) LHritier: P. glutinosum also has the viscid, strongly scented
foliage of P. denticulatum and P. quercifolium but has a far wider distribution in the
wild. The leaves are less rough than in these species. The flowers are pale to dark pink,
c. 1.5 cm across. It shows a range of variation in both its leaf and flower characteristics.
Some scented-leaved cultivars such as Viscosissimum are probably forms of this
species.
P. Graveolens: It is a vigorous, branching, rose-scented, shrub to over 1.5 m in height with
somewhat rough, deeply divided green leaves c. 4  6 cm, with the ultimate segmented
margins slightly curved under. Flowers are pink to pale purplish-pink, up to 15 mm across
in inflorescence of 510 flowers, the upper petals are narrow with rounded or notched apex,
veined dark purplish-pink, and have stamens with stunted anthers rarely bearing pollen.
The naming of this old and exceedingly well known rose-scented Pelargonium grown
on the window sills of so many houses in this country, Europe and North America, is
not easy to resolve. In 1792, a plant was illustrated by LHritier which is more or less
identical morphologically with the plant most commonly grown today as Graveolens
and it was almost certainly a hybrid.
Ros, the cultivar widely grown for the production of rose-scented Geranium oil has
been shown to be a hybrid between P. capitatum and P. radens (Demarne and van der Walt,
1989) and is very similar morphologically to Graveolens, Radula, Little Gem and the
variegated Lady Plymouth. The species P. graveolens found wild in the northern part of
South Africa, has white flowers and deeply divided, softly hairy, somewhat peppermintrose scented leaves. The flowers are larger, fewer with longer pedicels and hypanthia
giving the inflorescence a more open appearance also bears seven fertile anthers.
P. quercifolium (Linnaeus f.) LHritier: This is an erect, branching viscid shrub
with a strong balsam scent. Leaves are rough with long glandular hairs, usually up
to 5  5 cm, pinnately lobed to pinnatisect. Flowers are pale pink to darker purplishpink, in inflorescence of 36; the upper petals have a notched apex and darker
purplish-pink lines and blotches (Figure 8.8). This species, from southern Cape
Province, was first introduced to Kew about 1774. It is variable in leaf and flower
characteristics in its native habitat and some forms resemble cultivars seen in gardens
such as Royal Oak.
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Figure 8.8 P. quercifolium. (See Colour plate 8)

P. radens H.E. Moore: Erect branched aromatic shrub to over 1 m in height. The very
rough grayish-green leaves are deeply divided into narrow segments, the margins of
each segment rolled under giving an even narrower appearance. The pale or pinkishpurple flowers are in a loose inflorescence of about five, the upper two petals with
darker markings. This species from south-western Cape Province to Transkei, was first
introduced to Kew by Masson in 1774. It is not common in cultivation and should not
be confused with the rose-scented cultivar Radula. P. radens has very rough leaves and
the segments are exceedingly narrow as the margins are rolled under. This species is
considered with P. capitatum to be a parent of the cultivar Ros grown in great
quantities for the commercial production of Geranium oil on the island of Reunion.
P. tomentosum Jacquin: This is a low growing, but wide-spreading, branched subshrub
strongly scented of pepperment. Leaves with three or five round lobes 4 6  5 7 cm,
have long, soft, velvety hairs. The white flowers in a loosely branched inflorescence are
small, the upper two petals obovate, with purple lines. This species is a popular ornamental plant and has also been used as a culinary flavouring and for the production of
peppermint oil. It has been cultivated continually since its introduction by Francis
Masson in 1790. Unlike many Pelargonium species, it will grow in more slightly shaded
and moist situations.
Subsection Glaucophyllum

This is rather a small section and is very close to section Pelargonium and hybrids
between the two sections may even be found occasionally in the wild. Bakker et al.,
2000 have proposed that the section Glaucophyllum be demoted to a subsection within
section Pelargonium. The leaves are usually glaucous, as the name suggests, and often
rather leathery, simple or divided. The white, cream or purplish-pink flowers in a
few flowered inflorescence, are very irregular in shape with a hypanthium usually
considerably longer than the pedicel. Five to seven fertile stamens are present. The
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plants are subshrubs, either upright or trailing and the lower parts of the stems are
woody. The basic chromosome number is x 11. The species are found in the rocky,
mountainous regions of southern and south-western regions of Cape Province in the
winter rainfall region (van der Walt et al., 1990).
P. grandiflorum (Andrews) Willdenow: This is an erect, almost hairless plant with glaucous deeply 57 palmately lobed, sometimes zoned leaves. Flowers 23, pink to pale
purple-pink or sometimes creamy white, the upper petals marked with darker blotches
and streaks (Figure 8.9). It is thought to have been introduced in 1794 by Francis
Masson and was used in the early nineteenth century in hybridising.
P. tabulare (Burman filius) sensu J.J.A. van der Walt and P. patulum Jacquin.
These are similar but with smaller flowers. P. tabulare is an erect plant but shorter
than P. grandiflorum whereas P. patulum has a trailing habit.
P. laevigatum (Linnaeus filius) Willdenow: This is a small, very variable, often rather
straggling, usually glabrous plant with variable, usually glaucous, slightly fleshy leaves
divided into three linear or rounded segments, themselves three parted, with almost spinelike apices. The white or pale pink flowers are normally single, the upper petals reflexed
and marked with red. First collected by Thunberg around 1773, described in 1781,
illustrated in several early books and easy to cultivate, this species is not widely grown.
P. lanceolatum (Cavanilles) Kern: This is an upright branching plant with lanceolate,
untoothed, glaucous leaves (Figure 8.10), Flowers one to two in number, are cream to
pale yellow with the upper petals marked with red and strongly reflexed. In leaf, this
species is very atypical but the flower is quite typical of the section.
Section Hoarea

In the wild, the species of this section grow mainly in the arid inhospitable areas of
winter rainfall of west and south-west Cape Province with a few extending into

Figure 8.9 P. grandiflorum. (See Colour plate 9)

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Figure 8.10 P. lanceolatum. (See Colour plate 10)

southern Cape Province. This is the largest section within the genus containing about
80 species. The plants die down immediately after flowering and pass most of the year
underground in a dormant state. The foliage appears after the winter rain but the flowers
do not develop until the leaves have died down, although in cultivation the leaves may
remain during flowering. All are geophytes with one or more tubers covered with
papery sheaves which help to prevent the tuber drying out in summer. The
inflorescence, often branched, usually has many flowers and each flower may have either
two, three, four or five petals and five, sometimes two, three or four fertile stamens. The
flowers are very irregular and have a hypanthium exceeding the pedicel in length.
The basic chromosome number is x 11.
P. appendiculatum (Linnaeus filius) Willdenow: This is a plant with a large underground
tuber and gray-green, densely hairy, aromatic, feathery leaves, to 10  5 cm. Yellow
flowers about 4 cm across, borne on a long stem, have very narrow petals, the upper
petals spotted with red (Figure 8.11). It was collected by Thunberg in the late
eighteenth century. Although not common in cultivation, it is worth growing for its
tall many-flowered inflorescence.
P. auritum (Linnaeus filius) Willdenow: This is a rather small tuberous plant with
very variable leaves from simple to bi-pinnatifid, the lamina up to 12 cm or more
long. The flowers may be very dark purple, pink or white, in many flowered heads
with linear petals and long exserted stamens giving a star-like appearance. It may be
found growing wild in south-western Cape Province and has been known in Europe
since 1697.
P. incrassatum (Andrews) Sims: This is a plant with a large fleshy underground tuber and
deeply pinnately lobed leaves with soft grayish-white hairs. The 2040 bright magenta
flowers are borne terminally on long stems, and have three lower petals with in-rolled
edges. It was first collected by Francis Masson in 1791 from the coastal regions of
western Cape Province and Namaqualand.

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Figure 8.11 P. appendiculatum. (See Colour plate 11)

P. pinnatum (Linnaeus) LHritier: This stemless tuberous plant has bluish-green leaves,
oblong in outline, pinnate with elliptic pinnae each c. 10  5 mm. The flowers, each
about 2 cm across, are clear pink but pale yellow and white forms may be found in the
wild. It is not uncommon in the south-western Cape Province and has been known
since the early eighteenth century.
P. rapaceum (Linnaeus) LHritier: This is a stemless plant with a large and several smaller
tubers. The leaves are hairy, linear, pinnate, the pinnae further divided into linear
segments forming whorls along the rachis. The flowers are similar in shape to a legume,
pink or yellow, in heads of ten or more. The upper petals are held together erect, while
the lower petals are held together enclosing the stamens. It was one of the earliest of
the section to be collected with early references of Commelin and Hermann at the end
of the seventeenth century and in the wild has a very wide distribution through Cape
Province.
Subsection Ligularia

This section as circumscribed by Knuth is one of the most diverse both morphologically and geographically. However a karyological study together with attempts to
hybridise species of this section and others, has shown that many of the species should
be moved to other sections and for some new sections created (Albers et al., 1992). In

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most cases, the results were confirmed by morphological similarities and also by their
natural geographical locations. The remaining members of the existing section have
small chromosomes with a basic number x 11. All have fleshy stems, often covered
with the remains of stipules, sometimes becoming quite hard. The leaves in most
species are adapted to survive in regions of quite low rainfall on the western side of
South Africa.
It is interesting to note that some of the species included in this section and others
originally included but now moved, are of more recent introduction and were not
known to the early botanists at the height of the interest in these new Cape introductions. More recently phylogenetic work by Bakker et al. (2000) have suggested that
the remaining species within this reduced section are classified as a subsection of
Hoarea.
P. fulgidum (Linnaeus) LHritier: This is a spreading or scrambling, softly hairy plant
with somewhat succulent stems. The pinnately lobed leaves often have two almost free
lobes at base and a silver sheen. Flowers are scarlet in a branched inflorescence with 49
flowered heads; upper petals veined darker red, strongly reflexed; the hypanthium is
long, often dark brownish-red, very conspicuous and swollen at the base and it has
seven fertile stamens (Figure 8.12).
This is one of the older species to be introduced into Holland in the early eighteenth
century and from there sent to Italy and England. It appears to be one of the few
members of the genus which is able to hybridise with species of several other sections

Figure 8.12 P. fulgidum. (See Colour plate 12)

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such as Polyactium, and Pelargonium. It is involved in the parentage of some red flowered
cultivars such as Scarlet Unique and possibly the regal pelargoniums but is not part of
the parentage of the zonal or ivy-leaved cultivars. It grows along the west side of South
Africa, near to the coast.
P. pulchellum Sims: This is a hairy plant with a very short, rarely branched, thick semisucculent stem and thickened root. The leaves are softly hairy and pinnately lobed to
pinnatifid. Many white flowers are held in a branching inflorescence, the upper petals
with faint red lines at base, sometimes red blotched, while unusually the lower petals
have a prominent red blotch; the hypanthium is long and fertile stamens seven in
number. This is one of the most striking species of the genus and will flower early in
the season. It grows wild in Namaqualand.
Section Peristera

The section includes some of the more insignificant short-lived, dwarf herbaceous
plants, often with straggly or weedy, trailing habits. Initially the plants are usually
quite compact, but at flowering, elongate to produce many spreading branching stems
with long internodes. The flowers are usually small, rather regular in shape, the petals
often barely longer than the sepals, and borne on very fine pedicels in many flowered
heads. The fertile stamens are five or seven, occasionally four and the hypanthium often
very short or more or less non-existent. The leaves may be simple or divided, pinnately
or palmately veined but usually with rather long petioles. This section representing
about 17 per cent of the total number of species of Pelargonium, is more extensive than
any other with species found in Australia, east Africa, islands such as Madagascar and
Tristan da Cunha as well as in South Africa. Many individual species themselves have a
very wide geographical distribution which is unusual within the genus as is the variable chromosome number.
P. australe Willdenow: This is a herbaceous perennial with a short erect stem, but with
leafy flowering stems extending to about 30 cm long. Leaves are hairy or more or less
glabrous sometimes flushed purple below. Flowers are white or pale pink, in a fairly
compact inflorescence, the upper petals veined red; fertile stamens seven in number.
This very variable species may be found in several parts of Australia, eastern Tasmania
and New Zealand growing in a range of different habitats, usually in sandy dunes in
coastal areas but also inland. Before flowering, the plants make rather neat rosettes but
as the flower stems elongate and branch, the whole plant becomes straggling.
P. drummondii Turczaninow: This is a plant with semi-succulent thick stems covered
with persistent brown membranous stipules and dark green, more or less orbicular
leaves. Flowers are white to very pale pink, the upper petals veined dark pink; fertile
stamens seven in number. This is a little known species that grows in a restricted location in rocky conditions of inland areas of western Australia and was first discovered
about 150 years ago.
P. grossularioides (Linnaeus) LHritier: This is a spreading, short lived, herbaceous
plant often with red-tinged stems. The rounded to reniform shallow 35 lobed leaves
have a fruity scent variously described as peach, blackcurrant or coconut. Many tiny,
usually purplish-red, flowers in a rather tight head, are about 8 mm across, and
almost regular in shape; fertile stamens seven in number. It may be found over a wide

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area of southern Africa as well as Tristan da Cunha and was cultivated as early as
1731.
P. minimum (Cavanilles) Willdenow: This is a prostrate small plant with numerous small
tubers, gray green pinnately divided leaves. Minute white flowers are in a cluster of 36
and have almost no hypanthium; fertile stamens five in number. It has been known
since the late eighteenth century, and in the wild it is found in arid conditions
throughout southern Africa where it is used in folk medicine.
P. rodneyanum Mitchell ex Lindley: This is a plant with brown tuberous roots and
short aerial stems. Leaves are shallowly lobed on a petiole measuring up to about
twice the length of the lamina. Flowers are dark rose or purplish-pink, in a branched
inflorescence of about five flowers, the upper petals with darker pink markings; fertile stamens seven in number. This may be found in south-eastern and South
Australia, often growing among rocks, and was first collected in 1836.

Subsection Isopetalum

P. cotyledonis (Linnaeus) LHritier: This is the only species in the section which Sweet
assigned to its own genus and gave it the name Isopetalum. However, de Candolle in
1824 reduced the genus to a section. Although the remote geographical location as well
as many unique characters of the only species, phylogenetic studies indicate a close
relationship to section Peristera and section Isopetalum it is now considered to be more
correctly classified as a subsection (Bakker et al., 2000). It is a short, slightly branched
plant with stout, succulent stems covered with scaly rough bark about 30 cm tall. The
deciduous leaves, clustered at the ends of branches usually turn red before falling, are
rounded 25 cm across, leathery, glossy dark green above and, gray hairy beneath. The
numerous white unmarked flowers are regular, 1.5 cm across and have five, occasionally
six, fertile stamens but the hypanthium is exceedingly short. The plants have 22
chromosomes. This species is endemic to the island of St. Helena in the southern
Atlantic where it grows on rocky cliffs often exposed to salt sea spray. Unfortunately
like many species of the native flora, it has become very rare in its native country and
wild goats appear to have been one of the major causes of its decline. Grown as a
curiosity and known as old man live forever, it has not lost its appeal since introduced
to Kew in 1765 by John Bush.

Subsection Reniformia

The species found wild in the region of summer or all year round rainfall in the central
and eastern parts of South Africa were assigned to the section, Reniformia (Dreyer et al.,
1992). However, the most recent proposed classification suggests that this section is very
close to Peristera and should be included as a subsection (Bakker et al., 2000). Most grow
in areas receiving over 50 cm of rain during the summer and some have additional rain
in winter. They are mostly small subshrubs, occasionally with fleshy stems. The stipules
or leaf bases are persistent and the leaves simple, lobed and frequently aromatic. The
many-flowered inflorescence is branched, each individual branch bearing relatively few
small flowers but over quite a long season. The flowers are irregular in shape with the

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rather narrow upper two petals, held distinctly together and erect while the lower three
are usually slightly broader and widespread. The hypanthium is long, the pedicel short
and there are seven fertile stamens. The basic chromosome number is x 8. Most
species of this section are valued for their aromatic foliage and have been cultivated for
nearly 200 years.
P. abrotanifolium (Linnaeus f.) Jacquin: This is a branching, erect somewhat straggly
plant, with stems becoming woody with age and bearing remains of leaf stalks.
Aromatic, gray-green leaves are deeply divided more or less to the midrib into linear
segments. Flowers in cultivation are usually white but pink flowered plants are
common in the wild. The typical white flowered form known in cultivation in Europe
for over 200 years, is found over quite a wide area of Cape Province in dry often rocky
situations in areas of mainly winter rainfall.
P. album J.J.A. van der Walt: This is an erect herbaceous plant with thick fleshy
branching stems and aromatic rather viscid leaves, with whitish tinge. Flowers are
white in branched inflorescence, each peduncle bearing about eight flowers, the upper
petals are sometimes with small red markings. This recently described species may be
found in the eastern Transvaal.
P. exstipulatum (Cavanilles) LHritier: This is a branching, woody subshrub with
aromatic viscous, gray-green leaves Flowers are pale pink, 23 on an unbranched
inflorescence, the upper petals with dark red feathered markings. It is known to have
been grown by the Countess of Strathmore as early as 1779 and is found wild in
southern Cape Province.
P. fragrans Willdenow: This is a small erect branching plant with gray-green, soft
velvety leaves and a spicy aromatic scent. Flowers are white in a branched inflorescence,
the upper petals erect, feathered with red. There has always been a question about
whether this plant is a true species or not and for many years has been considered to be
a hybrid between P. odoratissimum and P. exstipulatum. It was first discovered in Berlin
in the early nineteenth century by Willdenow who considered it to be a true species,
but has not been found in the wild.
P. odoratissimum (Linnaeus) LHritier: This is a low growing herbaceous plant with
short thick main stem, the light green, usually apple-scented leaves arising from the
top, but with spreading or trailing flowering stems. Flowers are white, inflorescence
branching with small leaves, upper petals are finely marked with red. This popular
species has probably been grown continually since its first introduction into Europe in
1724. Many have apple-scented foliage but in other plants the scent may be more
pungent or spicy. In the wild it grows over a large area in the southern and eastern
South Africa.
P. reniforme sensu J.J.A. van der Walt: This is an erect or trailing subshrub with small
tuberous roots. Leaves are gray-green with velvety texture, silvery below and slightly
aromatic. Flowers are bright pink to magenta; inflorescence branched; fertile stamens
seven in number, sometimes six (Figure 8.13). The first introduction was by Francis
Masson to Kew in 1791 from southern and eastern Cape Province. The tuberous roots
of both this species and P. sidoides have been used medicinally for a variety of purposes
in their native country and are now developed and used as a drug in Europe against
tuberculosis (see Chapter 25).

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Diana Miller

Figure 8.13 P. reniforme. (See Colour plate 13)

P. sidoides de Candolle: This plant, with thick underground roots and a short erect
stem, is covered with persistent petioles and stipules, from which arises a rosette of
gray-green slightly aromatic leaves with silvery sheen. Flowers are a distinctive deep
blackish-purple colour, the upper petals narrow, oblong, often twisted and curled
backwards. This species growing from the Transvaal to southern Cape Province, was
collected by the Swedish botanist Thunberg in 1772 and also by F. Masson.

Section Polyactium

The section includes species which are found in the winter rainfall area of south-west
large, not covered by the papery sheaves typical of members of the section Hoarea. The
leaves are lobed or pinnately divided and are produced, at least in the wild, at the same
time as the flowers. The almost regular yellowish, greenish, dark brown or purple
night-scented flowers each with a long hypanthium are formed on a many-flowered
scape and have six to seven fertile stamens. The basic chromosome number for the
section is x 11.
P. lobatum (Burman filius) LHritier: This is a plant with a very large irregular tuber
covered with a rough bark and a very short aerial stem and leaves variable in shape and

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degree of lobing, up to 30 cm long in the wild. Flowers are very dark purple-black
c. 2 cm across, sweetly night-scented in umbels of 520 on a branched inflorescence,
rounded petals, margined yellowish-green; fertile stamens seven in number. Tubers of
this species were first sent to Holland from the Cape in 1698 from its natural habitat
in south-western and southern Cape Province.
P. triste (Linnaeus) LHritier: This is a geophytic plant with a large tuber as well as
several smaller ones and a very short succulent aerial stem. Basal leaves are hairy,
somewhat carrot-like, deeply divided into narrow segments. Flowers are night-scented,
brownish-purple, sometimes yellow or brown, with a broad yellowish margin about
1.5 cm across, upper petals, slightly reflexed; fertile stamens seven in number. This
species was the first Pelargonium to have been introduced into cultivation in Europe in
about 1630. It is found in sandy soils, often in colonies in the south-western and western
regions of the Cape Peninsula. The tuber has been used as a remedy for dysentery.
Subsection Gibbosum

The distinct habit of the only species included in this subsection has resulted in the
creation of this subsection.
P. gibbosum (Linnaeus) LHritier: This is a spreading or scrambling almost hairless plant
with succulent stems swollen at the nodes, becoming woody later. Leaves are somewhat
succulent, glaucous, pinnately lobed with one or two pairs of unevenly toothed or lobed
leaflets. Up to 15, greenish-yellow flowers, 1.52 cm across, are sweetly scented at
night, the upper petals slightly reflexed; fertile stamens seven in number. In the wild,
along the western coast of South Africa, this species may often be found scrambling for
several metres through shrubs.
Section Magnistipulacea

This is a small section separated from Polyactium, with species found in the southern
and eastern Cape Province and east Africa. The flowers have a long hypanthium, seven
fertile stamens and the petals are often fringed. The plants are tuberous and the basic
chromosome number is x 11.
P. bowkeri Harvey: This is a perennial plant with an underground tuber and a very short
aerial stem with attractive erect, soft, gray-green feathery foliage. Flowers are pale
yellowish-green, the lower petals flushed purple, c. 4 cm across, with all petals deeply
cut into linear segments.
Introduced in 1863 from the grassland of eastern Cape Province and Natal. The
leaves are said to have been eaten by some of the local people and it has also been used
a medicinal plant.
P. luridum (Andrews) Sweet: This is a stemless plant with an underground tuber and
extremely variable hairy leaves, the early ones shallow pinnately lobed becoming more
deeply divided into linear segments as the season progresses. The night-scented white,
pink, yellow or occasionally red flowers reach 2.53 cm across with broad almost equal
petals. This is a species that shows considerable morphological variation with a wide
geographic distribution from Tanzania to the southern coast of South Africa. It has also
been used medicinally and in concoctions for courtship rituals.

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P. schizopetalum Sweet: This geophyte has a large tuber covered with brown scales and a
very short aerial stem with shallow to deeply pinnately divided and pubescent basal
leaves. The pale yellow or yellowish-green flowers, often flushed reddish-purple are
about 3 cm across, and are unpleasantly scented at night; all the petals are similar and
deeply cut into linear segments. The leaves of plants collected from different locations
in eastern Cape Province may show considerable variation. It was first collected in
1821.

REFERENCES
Albers, F., Gibby, M. and Austmann, M. (1992) A reappraisal of Pelargonium section Ligularia
(Geraniaceae). Plant System. Evolution, 179, 257276.
Albers, F., van der Walt, J.J.A., Gibby, M., Marschewski, D.E., Price, R.A. and du Preez,
G. (1995) A biosystematic study of Pelargonium section: 2. Reappraisal of section Chorisma.
S. Afr. J. Bot., 61, 339346.
Aiton, W. (1789) Hortus Kewensis, Ed 1, Vol. 2., London.
Bakker, F.T., Culham, A. and Gibby, M. (2000) Phylogenetics and diversification in Pelargonium.
Adv. Plant Mol. System. 57, 353374.
Bakker, F.T., Culham, A., Daugherty, L.C. and Gibby, M. (1999) A trnL-F based phylogeny for
species of Pelargonium (Geraniaceae) with small chromosomes. Plant System. Evolution, 216,
309324.
Burman, J. (1738) Rariorum africanarum plantarum, Amsterdam.
Cavanilles, A.J. (1787) Monadelphiae classis dissertationes decem; Quarta dissertatio botanica de
Geranio, Paris.
De Candolle, A.P. (1824) Prodramus systematis naturalis regni vegetabili, Vol. 1., Paris.
Demarne, F. and van der Walt, J.J.A. (1989) Origin of the rose-scented Pelargonium cultivar
grown on Runion Island. S. Afr. J. Bot., 55, 184191.
Dreyer, L.L., Albers, F., van der Walt, J.J.A. and Marschewski, D.E. (1992) Subdivision of
Pelargonium sect. Cortusina (Geraniaceae). Plant System. Evolution, 183, 8397.
Harvey, W.H. (1860) Flora Capensis, Hedges, Smith & Co., Dublin.
Knuth, R. (1912) Das Pflanzenreichi, 4, 129, Berlin.
LHritier de Brutelle, C.-L. (1787) Geraniologia, sue Erodii, Pelargonii, Monsoniae et Grieli historia
iconibes illustrata, Paris.
MacDonald, D.J. and van der Walt, J.J.A. (1992) Observations on the pollination of Pelargonium
tricolor, section Campylia (Geraniaceae). S. Afr. J. Bot., 58, 386392.
Sweet, R. (18201830) Geraniaceae, vol. 15, London.
van der Walt, J.J.A. (1985). A taxonomic revision of the section Pelargonium LHerit.
(Geraniaceae) Bothalia, 15, 345385.
van der Walt, J.J.A., Albers, F., Gibby, M., Marschewski, D.E. and Price, R.A. (1995) A biosystematic study of Pelargonium section: 1. A new section Subsucculentia. S. Afr. J. Bot., 61, 331338.
van der Walt, J.J.A., Albers, F. and Gibby, M. (1990) Delimitation of Pelargonium sect.
Glaucophyllum (Geraniaceae). Plant Syst. Evolution, 171, 1526.
van der Walt, J.J.A., Albers, F., Gibby, M., Marschewski, D.E., Hellbrugge, D., Price, R.A. and
van der Merwe, A.M. (1997) A biosystematic study of Pelargonium section: 3. Reappraisal of
section Jenkinsonia. S. Afr. J. Bot., 63, 421.
van der Walt, J.J.A. and Boucher, D.A. (1986) A taxonomic revision of the section Myrrhidium
of Pelargonium (Geraniaceae) in southern Africa. S. Afr. J. Bot., 52, 438462.
van der Walt, J.J.A. and Roux, J.P. (1991) Taxonomy and phylogeny of Pelargonium section
Campylia (Geraniaceae). S. Afr. J. Bot., 57, 291294.
van der Walt, J.J.A. and Van Zyl, L. (1988) A Taxonomic revision of Pelargonium section
Campylia (Geraniaceae). S. Afr. J. Bot., 54, 145171.

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van der Walt, J.J.A (1977) Pelargoniums of Southern Africa, vol. 1. Purnell and Sons, Cape Town.
van der Walt, J.J.A. and Vorster, P.J. (1981) Pelargoniums of Southern Africa, vol. 2. Juta and Co.
Ltd., Cape Town.
van der Walt, J.J.A. and Vorster, P.J. (1988) Pelargoniums of Southern Africa, vol. 3. National
Botanic Gardens, Kirstenbosch.
Volschenk, B., van der Walt, J.J.A. and Vorster, P.J. (1982) The subspecies of P. cucullatum
(Geraniaceae) Bothalia, 14, 4551.

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Cultivation and sales of


Pelargonium plants for ornamental
use in the UK and worldwide
Janet James

INTRODUCTION

Historical survey
The Pelargonium family first reached Europe some 350 years ago, when sailing ships
were beginning to travel further afield. The ships surgeon was usually the person most
interested in botany, and he would explore the new countries in search of unknown
plants. The probable incentive was to use the plants for medicinal purposes.
In Europe, it became fashionable for rich people to build glasshouses to accommodate plants from warmer climates that would not have survived frosts. The lifting of the
tax on glass in 1851 had an impact on this activity. Pelargoniums became popular subjects for hybridising, because cross-pollination was not difficult, and they have the
advantage of growing all the year round, so there was no dormancy to interrupt the
work. The length of the flowering period was also a bonus and inspired gardeners to use
the results of the breeding work as long lasting summer bedding.
By the time Queen Victoria was on the throne, pelargoniums, or geraniums as they
were popularly known, were very fashionable plants. The misnomer of geranium came
about because the seed of the pelargonium is very similar to the seed of the geranium,
and at first the botanists decided that the pelargoniums were, in fact, closely related to
European geraniums, and named them accordingly. As science progressed, this was
found not to be true, and it was later on that the term pelargonium was applied to
these plants. But by then it was too late the word geranium was well and truly part
of the English language for what we now know as a zonal pelargonium.
Cost of pelargoniums
One indication of the value put on these plants in the nineteenth century days, was the
fact that a zonal variety called Paul Crampel was put on the market in 1896 at 1
a plant compared to the price of bread at that time (about 2d a loaf 1 240d),
this was an enormous amount of money. We know from nurserymens catalogues of the
day that pelargoniums were plentiful in a great number of varieties. The Pelargonium
section of Cannells Nursery, of Swanley in Kent, catalogue in 1910 listed 810 varieties.
A great many mutations occurred during this period of cultivation, and many of the
coloured-leaf varieties that we still grow heralded from the nineteenth and early twentieth century. Caroline Schmidt, for instance, came from Germany in1898 and is still

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going strong on the Continent it is known as Wilhelm Langguth. During the First
World War, when anti-German feeling was running high in Britain, the plant was
called Caroline Smith, and reverted to Schmidt once feelings had calmed down.
Mrs Parker is a pink sport from Caroline Smith, and has identical leaves and tallish
robust growing habit. Chelsea Gem (1880) is paler and more compact in its growth
habit, but is frequently mistakenly labelled as Mrs Parker.
First World War: effects on plants grown
The First World War heralded a disaster for many tender plants. It was the law that
glass could only be used to grow food. Therefore many varieties were lost to
cultivation, but fortunately many novelty varieties were preserved by amateur
growers. After the war all things Victorian went out of fashion, wealth had largely
dissipated and labour was short. All these things led to a decline in the popularity of
the Pelargonium family.
The war did not have such an impact in North America, and breeding work
continued there. About the 1960s a new strain was introduced called Irene
variety. The original Irene was raised by Charles Behringer and was named after his
wife. (Shellard, 1981). These were short-jointed, bushy, floriferous plants and soon set
criteria by which all varieties were judged. It did not take long for them to arrive
in England, and these became the standard bedding varieties. At this time new plants
were obtained by cuttings taken from mother stock, and seed raised varieties were
only in the hands of the hybridisers.
F1 hybrid seeds
The drawback to cultivation by cuttings was the cost of maintaining the stock, the cost
of labour and the fact that viruses and disease could be perpetuated from one generation
to the next. Therefore much breeding work was aimed at producing plants that could
be satisfactorily raised from seed. The first series of F1 hybrid seed zonal pelargoniums
to be taken up by commercial growers was called the Carefree strain and this was soon
followed by the Sprinter range. In the 1970s, the traditional Gustav Emich variety
that had always graced the flower beds outside Buckingham Palace was replaced by
a scarlet Sprinter variety. The more modern seed strains now used are the multibloom types.
Problems raised by hybrid seeds
Seed-raised plants became the norm for local authority parks departments, as they were
more cost effective than plants raised from cuttings. But they also had drawbacks. More
time was needed to grow the plants than with cutting material, and in order to get
them into bloom for early summer they had to be given high temperatures early in their
life. For instance, from a January sowing it would be necessary to give a night temperature of 64 F for several weeks. Also the blooms tended to shatter and petal drop was
a problem. This was overcome by spraying the blooms with silver thiosulphate.
Another problem was the fact that because they came from seed, they tended to form
seed heads rapidly sometimes before the whole bloom had opened up. This gave

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unsightly beds of half-formed flowers. However, breeding work is still continuing in


this field and improvements are being made all the time. The plants raised from seed
are single zonal varieties (as doubles do not readily form seed), and they are basically
green leaved varieties, though many do have an attractive dark zones.
Cuttings and big-business companies
Now-a-days many plants are raised for the commercial market from cuttings taken
from mother stock. There are a number of large wholesale nurseries situated on the
Continent, such as Fischers and Elsners in Germany, Enthoven and van Veen in the
Netherlands, and Philomel in France, that are supplying the garden centres of Europe.
They concentrate on breeding varieties that will perform well by being short jointed
and bushy and very floriferous, which suits the needs of the vast majority of garden centre customers. Ideally a plant is approximately 2 ft high, 2 ft across and full of flower
at the end of May. Fortunately for the horticulture trade, many people will discard the
plants at the end of the season and expect to buy more the following year. The balconies
of Bavaria, Austria and Switzerland will be filled with cascading ivy-leaf geraniums all
summer long, but most amateurs make very little attempt to preserve the plants for use
in the following year.
In order to keep costs down, many stock plants will be grown in a climate more equitable to the needs of the plants. The Canary Islands and Kenya are two places chosen
for the growing of stock plants. The Canaries are particularly suitable because they are
isolated from possible viruses and disease. The wholesale nurserymen take great care to
see that the mother stock is free from all viruses, and they have laboratories where
micro-propagation takes place. Cuttings are only taken one generation down from this
cleaned up material. The wholesale nurseries are run like factories, with every square
metre contributing to production, and timetables are strictly adhered to. Production is
labour intensive, and costs are kept to a minimum.
Many unrooted cuttings from wholesale nurseries are sold to nurserymen all over
Europe, being sent in insulated boxes by air. So the source of most of the plants in
garden centres is the same, even though the plants have been grown locally.
Small, family-run nurseries
In a different ball game are the small nurseries, mostly family concerns, that are
preserving the many old varieties which are still in existence. They cannot possibly
compete with the wholesalers, so instead of growing a vast number of a few varieties,
they do the opposite and grow a few of a vast number of varieties. These nurseries
are aiming their products at the amateur growers who are interested in finding
plants that are not readily available.
Different types of pelargoniums on offer
The types of pelargonium became known under the following sections: zonals, regals,
ivy-leaf and scenteds.
Zonals are the ones commonly called geraniums and are largely used as bedding
plants and for urns and tubs to decorate buildings.

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Ivy-leaf these are Pelargonium peltatum derivatives and are used mainly in hanging
baskets, urns and tubs, but rarely for bedding. Recently there has been a distinction
made between the cascade (or windowsill) varieties and the normal types. The cascades
are multi-flowering single varieties in a limited number of colours, and some have
variegated leaves.
Regal are very different from zonals, and known commonly as pelargoniums,
having large open blooms and only blooming in their season (when there is 14 h of
daylight). In the USA, they are known as Martha Washingtons.
Zonals can be subdivided into basic, dwarf and miniature according to their
growing habit. In each subdivision, they can have flowers that are either single,
semi-double or double. The singles have florets made up of exactly five petals, the
semi-doubles have between six and nine petals, and the doubles have ten or more
petals to each floret. They can also be sub-divided according to their leaf colour or
flower formation. There are golden, bicolours and tricolours in the leaf sub-divisions
and cactus, tulip and rosebud in the flower sub-divisions. There are also some
varieties which are a cross between the zonal and ivy-leaf varieties, and these are
known as hybrid ivies.
The species and primary hybrid plants are not produced in any great numbers commercially, except when they have scented leaves. There is also a wide range of scented
leaf cultivars, with odours ranging from apple to camphoric. These are becoming
increasingly popular and are the subject of many articles in gardening magazines.
The small nurseries are in some ways altruistic in that they aim to preserve plants that
would otherwise be lost for ever, but they also introduce new varieties that have been
bred by enthusiastic amateurs. Some dedicated amateurs can produce amazing results
with very few facilities at their disposal. Ian Gillam of Canada lives in a flat in
Vancouver, but has managed to produce some Stellar varieties which are now renowned
throughout the world. The late Reverend Stanley Stringer in Suffolk spent his retirement concentrating mostly on dwarf or miniature growing plants, and left a fine heritage of superb varieties. Bert Pearce of Fareham left a fine series of regal pelargoniums
behind when he died recently. Even now Brian West is working in his two greenhouses
on the Isle of Wight, taking careful notes, and breeding new plants of distinction. There
are many such people working in a small way to increase the family of pelargoniums, to
the advantage of us all.

DEVELOPMENT OF PERSONAL NURSERY BUSINESS

Historical background: the Vernon Geranium nursery


On a personal basis, our own nursery developed from a back garden hobby, inspired by
the collection of pelargoniums inherited from parents in about 1972 it would have
seemed such a shame to let the plants die, and once hooked on the beauty and diversity of this family of plants, things progressed from there. Grandad was a nurseryman
who discovered the joys of the Pelargonium family after he retired, and on his death left
a considerable collection of varieties. This was the basis of the nursery.
The back garden soon proved to be too small, so the family (including four children
still at school) was uprooted and moved to an ancient pub (The Vernon Arms hence
the name) that the brewery was selling off for use as a private house. This was situated

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near to Harefield Hospital in Middlesex, and mother continued her teaching career in
the local primary school.
By 1979, the teaching career was abandoned in favour of the geraniums, and by
chance fathers firm (where he had worked for over 30 years as a civil engineering
draughtsman) decided to uproot and move away. At this point care was thrown to the
wind and both parents opted for the nursery with hindsight this was a very foolhardy
decision, and not one to be recommended!
In 1983, two sons were fired with enthusiasm and volunteered to join the venture
one was a qualified plumber and the other had been to agriculture college. The site
at Harefield was proving to be too small, so the two sons moved to a leasehold nursery at Cheam in Surrey. The drawback to Cheam was that it was to be used
for wholesale growing only, so we had hoped to keep Harefield for our main retail
outlet.

Initial mail-order business


This was not to be, as the debts mounted, and we had to sell the Harefield nursery. This
meant that we had to concentrate all our efforts on our mail-order sales, as the only outlet we had for potted up plants was the wholesale market and shows. The wholesale
market was not really our scene as garden centres were only interested in a limited
number of varieties for a very few weeks of the year. Shows were more successful, as
people appreciated being offered a wide range of plants, and we found that by keeping
up a good supply of the more unusual varieties, we could sell plants right on into
September.
One morning in 1987, we read that Gambles geraniums of Derbyshire was closing
down. This was a nursery famous for introducing some of the best American and
European varieties to this country, and for their own breeding of some excellent zonals.
We wondered what would happen to the mother plants, so it was decided to approach
Mr Ken Gamble as to their fate. We were invited to make him an offer for the complete
stock, which was accepted, and the stock was added to our ever increasing collection of
geraniums.

Acquisition of retail facility


In 1991, we managed to re-negotiate our lease, so now we are able to sell plants from
the nursery, and are open every day from the beginning of March to the end of July. We
hold our open weeks during the last week in July, when tours of the nursery are
conducted twice a day.

Publicity
We started exhibiting at the Royal Horticultural Society (RHS) summer shows at the
Halls in Vincent Square in 1981, and exhibited at the Chelsea flower shows regularly.
But in 1989, we decided not to apply for Chelsea any more, as we found that we were
a very small fish in a huge sea, and the show came just at the time of year when we were

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busiest at the nursery. By about 1990, we determined to stop using flower shows as
a means of marketing our plants because the amount of time and effort involved was
not justified by the monetary return.
Our catalogue is produced in relatively large numbers (100 000 copies) and is now
also on the Internet (under www.GeraniumsUK.com), so hopefully, it will reach a much
wider public that we are able to by posting out catalogues.
Seed versus cutting-raised plants
The mass sales of pelargoniums (geraniums) has largely gone over to the seed-raised
varieties in the last decade, and this is due in no small extent to the marketing power
of the seed firms. We have produced our coloured catalogue with the intention of
redressing the balance somewhat. The general public do not even seem to be aware that
there are such things as miniature, dwarf or golden-leaved geraniums probably
because they rarely read about them, and even more rarely find them offered for sale in
their local Garden Centre.
Seed firms market geraniums as an annual plant, as it is, of course, in their interest
to do so but the public do seem to be aware that they are a tender perennial, and that
with a minimum of care in the winter, the plants can live for many years.

THE VERNON GERANIUM NURSERY: SITE AND RUNNING PROTOCOL

Lighting and temperature maintenance


Our site in Surrey that occupies just 1.8 ha, of which some 0.5 ha is under glass or
polytunnel. We sell our plants mainly as rooted cuttings via mail-order throughout
Europe. Stock plants are kept throughout the year, and are given supplementary lighting during the winter months. The trade is very seasonal, with the vast majority
of customers wishing to receive their orders during the first 4 months of the year,
which is why we have to spur on the growth with the high pressure sodium lights. An
environmental computer measures the lux levels during the day, and brings on the
lights in the night to make up the inevitable deficiency during the winter months. By
this means we have material growing to be taken as cuttings throughout the year.
Coloured leaf varieties, which are lacking in chlorophyll to support growth, are in a
special area where there are extra lights, and the temperatures are kept higher than
elsewhere. The normal minimum temperatures in the stock house are 10 C daytime
and 7 C at night. Below 5 C, the plants will not continue to grow (and at below 0 C,
they will die!). Higher minimum temperatures would speed growth, but the cost
would be prohibitive.
Watering and feeding
Watering and feeding of stock is by means of a drip feed system i.e. each pot has a fine
tube attached, and the amounts given are regulated by water meters on the taps. The
watering is not computerised, as we feel this is best left to personal judgement. The
feed is drawn into the hose lines from a central location.

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Cuttings
Cuttings are taken in batches according to the time of year and orders pending. For
servicing the main mail-order catalogue, batches of 30 or 60 of each variety is taken, so
that there is a continuous supply, and orders can be despatched soon after receipt. The
orders are entered into a computer, and from this we can ascertain which are the more
popular varieties, so that production can be geared accordingly.
We produce a smaller collections catalogue, which is sent out to a larger number of
people, using a direct marketing approach. We exchange and buy lists of names and
addresses from firms in a similar line of business, so that we know we are targeting
people who have gardens, and who have previously bought plants or seeds by mailorder. This means that there is a large number of orders going out during March, April
and early May, so cuttings are taken en masse for these, and extra staff are employed
at that time of the year to service these orders.
Methodology of taking cuttings
Because we grow from cuttings, production is very labour intensive. Each plant has to be
trimmed neatly below a node before insertion into a growing medium. We have found it
beneficial to dip each one into a solution of ascorbic acid (Vitamin C) 1 g/85 ml
of cold water. Rooting takes place on heated benches most of the year from May to
August it is not necessary to heat the benches and the heat is provided by domestic boilers servicing hot pipes running along under the cuttings.
The time taken to form roots can vary with each variety, some are quicker than others,
but on the whole it is 23 weeks for the zonal types, and 45 weeks for the regal types.
We do not use chemical growth inhibitors (like cycocel) as we feel this would be
cheating our amateur customers, who do not have access to these products. There are
plenty of varieties that will grow in a short jointed, bushy habit without the need for
artificial aids. Also there are people who would like to have tall growing plants, and
these are no longer available from wholesale growers.
Unrooted cuttings bought from outside
In some instances, it is more economical to buy certain varieties from wholesale nurseries
to supplement our own production. This is usually by unrooted material, which we then
root ourselves, but occasionally with ready rooted plants. The latter can cause problems
because the plants might not be suited to our packaging boxes. When we purchase
material from continental wholesalers it is flown in insulated boxes to Heathrow airport,
and we collect it from there, so our location in Surrey is a great asset.
Use of insecticides and predators to control insect pests
We use both insecticides and natural predators to control insect pests and fungi.
Technical advice is sought from our supplier of these products: Fargro Ltd.,
Toddington Lane, Littlehampton, West Sussex BN17 7PP. They in turn are suppled
with the predators by Novartis BCM (UK) Ltd., Aldham Business Centre, Alham,
Colchester, Essex CO6 3PN.

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Aphids
Nicotine liquid (95 per cent w/w)
Nemolt 150 g/litre (13.6 per cent w/w) teflubenzuron
Chess 40 g/100 litres (25 per cent w/w) pymetrozine
Pirimor (50 per cent w/w) pirimicarb
Biological control
Encarsia formosa
Macrolophus
Hypoapsis
Aphidius colemani
Mycotel (this contains spores of the entomopathogenic fungus Verticillium lecanii
which is highly infective to whitefly)
Red spider mite
Dynamec 18 g/litre (1.8 per cent w/w) abamectin also contains hexan-l-ol
Fungicides
Dorado 200 g/litre (20.8 per cent w/w) pyrifenox
Rovral (50 per cent w/w) iprodione
Plantvax 75 (75 per cent w/w) oxycarboxin
A spreader is used to reduce the amount of chemical needed per application:
Celect 95 per cent rapeseed oil. Feed is used regularly and is applied via a Dosatron
system.
Fertilisers
Early in the year, after the stock plants have been cut once, a higher nitrogen feed will
be used to boost growth (along with a minimum temperature of 7 C and supplementary lights):
Solufeed, NPK 28:7:14 with magnesium and trace elements.
This is followed by a more balanced formula:
Sangral NPK 21:7:24  2MgO
The complete feed is:
Total Nitrogen (N) 21 per cent
Ureic Nitrogen (N) 15 per cent
Phosphorus Pentoxide P2O5 soluble in neutral ammonium citrate and water 7 per cent
(3 per cent P)
Potassium oxide (K2O) soluble in water 24 per cent (19.9 per cent K)
Magnesium oxide (MgO) soluble in water 2 per cent (1.2 per cent Mg)
Boron (B) soluble in water 0.0022 per cent
Copper (Cu) soluble in water, chelated by EDTA 0.0016 per cent
Iron (Fe) soluble in water, chelated by EDTA 0.007 per cent
Manganese (Mn) soluble in water, chelated by EDTA 0.0042 per cent
Molybdenum (Mo) soluble in water 0.0014 per cent
Zinc (Zn) soluble in water, chelated by EDTA 0.0014 per cent.

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Janet James

Compost
For many years we mixed our own compost, but recently it was decided that it
was more economical to buy in a ready prepared mixture. After several not too
successful mediums, we have settled for a crop-specific compost from William
Sinclair Horticulture Ltd. But the specific crop is poinsettia! We have found it
suits our purpose very well, the plants easily send their roots through the open
texture, and it retains moisture without becoming waterlogged. The bag states
a purpose designed compost prepared from a blend of different peat types and a
balanced base fertiliser to provide optimum plant growth. Includes an efficient
wetting agent. A low initial nutrient charge has been used to allow rapid root
establishment and early liquid feeding will be necessary to maintain desired
growth rates.
As commercial nurserymen we have learned by experience how to succeed with this
family of plants, but there are technical works on many aspects of their culture. We
know that the main conditions that ensure success are a dry atmosphere, moist roots
and an abundance of light. Cold, damp conditions will cause pelargoniums to rot, and
warm compost is essential to the rooting process.

ALTERNATIVE ROOTING AGENTS

For less perfect conditions, when basal heat cannot be provided and the temperature is
low, antioxidants can be used as alternative rooting agents (Lis-Balchin, 1988). Use 1
tablet of Vitamin E and/or the food preservatives, BHT and BHA (butylated hydroxytoluene and anisole respectively), using a pinch. These are first dissolved in a little alcohol and then diluted with water to 100 ml. Use sparingly for dipping the cut edge of
cuttings for a few seconds before rooting.

TOP FIVE PELARGONIUMS

In 1999, the top five pelargoniums from each section sold from the nursery:
Zonals
Single: Mr Wren
Paul Crampel
Simplicity
First Love
Skellys Pride
Double: Carol Gibbons
Beryl Gibbons
Brenda Kitson
Betty
Regina

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Cultivation and sales of Pelargonium plants for ornamental use

Dwarf: Nettlestead
Rosina Read
PAC Millenium Dawn
Jean Beatty
Petite Blache
Miniature: Cotton Tails
Garnet Rosebud
Royal Norfolk
Eileen
Red Black Vesuvius
Rosebud: Appleblossom Rosebud
Red Rambler
Westdale Appleblossom
Happy Appleblossom
Wedding Royale
Fancy leaf: Mrs Pollock
Mrs Henry Cox
Retahs Crystal
Encore
Madame Salleron
Regal: Lord Bute
Springfield Black
Mohawk
Askham Fringed Aztec
Sunset Snow
Angels: The Barle
Swedish Angel
Imperial Butterfly
Black Knight
Velvet Duet
Deacons: Deacon Birthday
Picotee
Lilac Mist
Suntan
Arlon
Scented: Sweet Mimosa
Prince of Orange
Pelargonium dichondraefolium

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Janet James

Crispum variegatum
Clorinda
Ivy-leaf: Jack Gauld
Barbe Bleu
Bonito
Snowdrift
Rio Grande

PELARGONIUMS GROWN ELSEWHERE IN THE WORLD

Commercial growing of the Pelargonium family is buoyant throughout the world, and
particularly so in the USA, where propagation has increased by almost 60 per cent from
1979 to 1990. There are some 120 million plants grown in the USA and some 70 million in Germany as opposed to some 2 million in the UK. Of course, these figures are
meaningless unless compared to the population figures of these countries. But generally,
where there are large urban populations, particularly in the western civilisation, there
will be a great demand for these plants.
We, ourselves, have a visit at least annually from touring Japanese nurserymen who
always show a great interest in our diverse selection of varieties, showing more worldwide appeal.

LITERATURE ON PELARGONIUMS FOR GROWERS

There are considerable number of books and papers written on the cultivation of
pelargoniums, with an abundant diversity of opinions on some aspects of their cultivation. Even the scientific works rarely comes to an undisputed conclusion on the best
conditions for the propagation and growing of these plants. Possibly the best work to
recommend for a detailed study of these plants is Geraniums: A Growers Manual edited
by John W. White.

APPENDIX

Addresses of Nurseries for cuttings of common geranium


Elsner pac Jungpflanzen, Kipsdorfer Strae 146, D-01279 Dresden, Germany.
Tel: 0351 25591-0; Fax: 0351 2517494; e-mail: info@pac-elsner.com.
M van Veen Export BV, PO Box 73, 1430 AB Aalsmeer, Holland.
Tel: 0031 297 326516; Fax: 0031 297 328001.
Philiomel S.A., Establissement Horticole, 66600 Salse-le-Chateau, France.
Tel: 04.68.38.61.28; Fax: 04.68.38.69.93; e-mail: philiomel@smi-telecom.fr;
www.littlefrance.tm.fr/philiomel.

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M.C.M. Enthoven C.V., Wateringseweg 5, 2685 SP Poeldijk, The Netherlands.


Tel: 0174 245572; Fax: 0174 247977.

REFERENCES
Lis-Balchin, M. (1988) The use of antioxidants as rooting enhancers in the Geraniaceae, J. Hort.
Sci., 64, 617623.
Shellard, A. (1981) Geraniums for Homes and Garden, David & Charles, Newton Abbot.
White, J.W. (1993) Geraniums: A Growers Manual. Sponsored by Pennsylvania Flower Growers.
4th Ed. Ball Publishing, III. USA. Ed. White, ( J.W. published by Ball Publishing, 1 North
River Lane, Suite 206 PO Box 532, Geneva, Illinois 60134, USA, ISBN 0962679658).

2002 Edited by Taylor & Francis

10 Growing pelargoniums in
the garden, conservatory and
for shows
Maria Lis-Balchin

INTRODUCTION

The main types of Pelargoniums (known by most people as geraniums include:


the zonals (Pelargonium  hortorum), regals (P.  domesticum), ivy-leaf (P. peltatum) and
scented-leaf varieties. These can be distinguished by either the leaf shape, flower shape
or scent.
The zonals are descended from P. zonale and P. inquinans and a few other species in
the Section Ciconium; as the name suggests there is a zone, which is darker than the rest
of the leaf and is crescent or horse-shoe shaped. This zone can be very pronounced or
almost indistinguishable, depending on the cultivar. There are probably over 2000
named cultivars, some of which may be synonymous with others, but have been given
a different name, either in the same country in different nurseries, or in a different
country. One of the early varieties is Paul Crampel, which used to be the red-flowered
geranium growing outside Buckingham Palace.
According to the Muslim legend, geraniums were created when Mohammed went for
a walk in an unfrequented place, and in the heat of the sun, took off his shirt, rinsed it
in a nearby pool and hung it over some branches, The water from the shirt dripped onto
some marshmallows growing underneath and turned them into geraniums!
General cultivation of pelargoniums
Pelargoniums, originating in southern Africa, are more adapted to drier and hotter
conditions than most European countries can provide year-round. Cold, wet situations
kill them. In winter, they are best kept on the drier side and at a temperature never
below 4 C. They require good soil, either loam-based John Innes or soil-less compost,
slightly on the acid-side, preferably with sand, grit, perlite or vermiculite and clay-pots
are preferable, as plastic pots retain too much water.
GERANIUMS (i.e. PELARGONIUMS) OF DIFFERENT TYPES

Descriptions of different cultivars has been taken from: Clifford (1958); Wood (1966);
Witham Fogg (1975); Shellard (1981); Clark (1988) and Taylor (1988). These authors
also give instructions on growing, propagating and general tips on the best plants to

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Growing pelargoniums in the garden, conservatory and for shows 93

grow in different areas of the house and garden. For colour photo graphs of 1000
Pelargoniums see Key (2000).
Zonals
The zonals are divided into various groups according to:
1

Size

Colour of the leaf

Gold leaf or bronze leaf, with/without zone e.g. Golden Crest, Bridesmaid,
Morval.
Bicolour with white/cream and green leaves e.g. Chelsea Gem, Frank
Headley, Freak of Nature, which has white stems and is difficult to take
cuttings from.
Tricolour leaf, with gold, red and green e.g. Contrast, Dolly Vardon, Henry
Cox, Mrs Strang.

Number of petals

Large: including Irenes, which were introduced in 1942 by Charles


Behringer in Ohio, USA and were then bred to produce large bushy floriferous plants with huge leaves e.g. Irene, medium red flower; Sentinel, white;
Electra, bluish-rose. These are ideal for filling up space in the conservatory
or garden.
Dwarfs: (plants not exceeding 20 cm from the top of the pot to the tip of the
foliage) e.g. Wendy Read, double pink shading to white; Tom Portas, double empire rose.
Miniatures: Smallest cultivars, known as miniatures (13 cm from pot to tip),
are best exhibited in batches of 46 in baskets, or individually in conservatories. Miniatures include a wide variety of shades of flowers or leaves and also
some scented leaf cultivars e.g. Frills, Variegated Petit Pierre, Silver
Kewense. The original is thought to be a nearly black-leaved Red Black
Vesuvius.

Single (Five petals), e.g. Christopher, Ley, with large orange-red flowers;
Feurriesse, with velvet-red blooms;
Double (more than five), e.g. Shocking, with bright pink flowers, Royal
Flush, with purple flowers. The single bloomed geraniums are best for outside, and are easily raised from seed; the double ones are often damaged by
rain outside, but are more spectacular.

Appearance of the petals

Spitfire (quill-shaped), Apple Blossom Rosebud, Mr Wren (spotted/striped,


white/red), Gemini (stellar/star-like).
Speckled varieties e.g. Gemma raised by Stringer in 1984; Elmsett raised by
Bidwell in 1982.
Patricia Andrea, a tulip-flowered salmon variety, originating from the USA in
1960.

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Maria Lis-Balchin

Colour of the flower (Witham Fogg, 1975): New varieties of Pelargonium cultivars
have appeared over the years, including the Deacon group, derived from miniature zonals  ivy-leaf; these have double flowers and are bushy and floriferous and
were introduced by the Rev. Stringer in the 1970s e.g. Deacon Lilac Mist.
The Highfield group introduced by K. Gamble in the 1970s e.g. Highfields
Festival, with very bushy but with compact habit and pale lavender-pink blossom.
More recently the PAC group (Elsner in Germany) e.g. PAC Rosecrystal, which
looks like an anemone flower, rose with a white centre was introduced. Sometimes
outstanding varieties are on offer for a short time e.g. the yellow-flowered
Bothams Surprise raised in Australia and sold through the PAC label. The
variegated leaf geraniums were studied by Grieve (1853). His book describes
the variegations in other genera, which can be due to cells filled with air or gas in
immediate contact with the chlorophyll or colouring substance and apparently this
could also be true in geraniums.

Regals
Regals have much larger flowers than the zonals and were therefore called pelargoniums by the general public to distinguish them from the other geraniums. They have
been hybridized mainly from P. cucullatum, P. angulosum, P. fulgidum and P. grandiflorum.
In the USA they are known as Martha Washington or Lady Washington and also
Show pelargoniums. They do not do well in the wet summers and have usually a
restricted flowering time, often just once a year. They also attract whitefly ferociously.
Only a few regals have scented leaves.
The regals are grouped into two sections: the ordinary regals and the Angels or
dwarf/miniature regals.
Regals have the most beautifully coloured petals, with a wide range of colours often
appearing together e.g.

Aztec is pale pink with bronze and strawberry pink markings and a fringed margin.
Grand Slam has rose-red petals with dark markings.
Hazel Cherry has cherry-red petals with blackish blotches.
Morwenna is almost totally black.
All My Love, is orchid-mauve and white.
Cezanne has purple upper petals and the rest is lavender.

Angels
Angels have a distinctive pansy-face and have different foliage to the regals, in
general. Many are crosses or back-crosses of Pelargonium species with P. crispum and
P. grossularioides (small-leaved scenteds) often implicated. The early Angels were possibly the old Angelines, catalogued in the 1820s, derived from P. dumosum, which has
since disappeared (Taylor, 1988). The founding father of the Angels was Arthur Langley
Smith, a school teacher, who first started hybridizing in the early 1900s. P. crispum was
thought to have been hybridized with The Shar and his first creation was named
Catford Belle after his place of residence in London (Catford). The Angels all have
mauvish/white or pinkish, cerise/white colourings with different blotches and most
have scented leaves. Like the regals, they attract whitefly.

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Examples of the best known Angels include:

Beromunster, pale pink with cerise blotches towards edges.


Tip Top Duet, mauve base with two top petals maroon.
Velvet Duet is dark purplish-maroon.
Wayward Angel is pale mauve with upper markings of light maroon.

Many new Angel varieties are introduced each year, but have very similar appearances
to the well-known originals.
Ivy-leaved
These are very distinctive, with shiny five angular-lobed, ivy-shaped leaves, all derived
from P. peltatum and are known as trailing, window-box, Swiss/German or balcony
varieties etc. The leaves have a characteristic odour, which is vaguely like that of real
ivy, Hedera helix. Examples include:

Balcon Royal, originating in the 1960s, with bright red petals.


Duke of Edinburgh, with pink flowers and green/white variegated foliage.
Galilee, originating in 1882 in France, with double pink flowers.
LElegante, again early 1860s, with white single flowers in profusion.
Red/Pink/mini Cascade, with small leaves and single primitive flowers on short
branching stems.
Sugar Baby has double candy-pink flowers on a dwarf plant.

Hybrid ivies
These can have the appearance of either an ivy-leaf or a zonal as they have resulted from
a P. peltatum  P.  hortorum cross.
Zonal-type, the Deacon group (see above) e.g. Deacon Lilac Mist, a lilac flowered
variety turning almost white; Deacon Moonlight, Deacon Birthday, Deacon
Regatta, Deacon Regalia.
Ivy-type, e.g. Millfield Gem, amaranth-rose blotches and feathered a rosy red,
Millfield rose, Jack of Hearts, Elsi and Auden Ken an Emil Eschbach.
Other recent innovations (early 1970s) include the Harlequin group, developed
through grafting: these have numerous red/white striped varieties e.g. Rouletta
known also as Mexicarin. There are also veined leaf varieties e.g. Crocodile, White
Mesh; these originated through the innoculation with a beneficial virus, passed on by
insects (possibly whitefly) and thence they were hybridized.
Scented-leaf varieties
There are numerous scented-leaf varieties which originated from hybridizations between
scented-leaf species, e.g. P. denticulatum, P. capitatum, P.  fragrans, P. odoratissimum etc.
The size and shape of the leaf varies greatly from the very large peppermint, furry leaves
of P. tomentosum to the tiny, pungent P.  fragrans (resembling Vicks ointment). The
scenteds have been placed in various groups by different authors, and it appears that
there is an individual aspect to this, based on the persons appreciation of each odour and

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Maria Lis-Balchin

like/dislike of it. Witham Fogg (1975) puts P. denticulatum in the rosy group, but to the
present author it is distinctly pungent/camphoric and Vicks-like. Some species and cultivars are however unanimously appraised e.g. P. odoratissimum is always apple-like;
P. tomentosum is pepperminty; P. capitatum is rosy; P. crispum is citrusy/lemony. There is
often a change in odour of the leaves during the year, with most changes occurring
during flowering e.g. P. graveolens is more minty when not flowering, and more rosy
when flowering.
Some common scented cultivars include:

Chocolate peppermint syn. Chocolate tomentosum, derived from P. tomentosum, with


massive peppermint-smelling green, furry, leaves with a brown blotch centrally
P. filicifolium has a sticky, very finely divided leaf, with a Vicks-like odour;
described by Andrews in his Geraniums around 1805. It is probably a derivative of
P. denticulatum with its divided leaves, but there is some theoretical justification to
include it under a derivative of P. glutinosum, which has the more viscid secretion
(Abbott, 1994).
Clorinda, vigorous, pink-flowered, camphoraceous/exotic leaves.
Lady Plymouth, derived from P. graveolens, with a minty odour and leaves edged
in white. It was described by Andrews in 1805 as Geranium capitatum variegatum
and then in the current name prior to 1880.
Copthorne, similar to Clorinda, but palish pink flowers with bright cerise markings
Village Hill Oak, derived from P. quercifolium.
Bolero, one of the Hartsook hybrids produced in California as Uniques from regal
crosses, this one is salmon-orange with dark brown to black-purple markings. Others
include: Carefree, Hula, Polka and Voodoo. All have huge spectacular flowers.
Purple Unique, one of the original Uniques introduced in the 1880s, has huge
purple flowers. The first Uniques were however in existence before 1820, as they
were mentioned by Sweet in his Geraniaceae volume 1 (Abbott, 1994). One of
the parents for this group is P. fulgidum, but other species were used later. The
P. fulgidum flower markings have been carried across, even where the red colour has
been replaced by mauve etc. as in Rollinsons Unique which has the distinctive
markings in the upper petals. Others in the group include: Unique Aurore,
Crimson Unique.
Jessels Unique, Madam Nonin, Patons Unique, Scarlet Unique and Shrubland
Pet. Many of these have very distinctive, camphoraceous, fruity-exotic leaf odours.
Sweet Mimosa was introduced in USA in the late 1970s, and has similar leaves to
that of P. graveolens, but with a rosy odour, although its origin is unknown.

Seedlings
The first Pelargonium seeds sold were all F1 hybrids which were all zonals and were
initially very expensive e.g. Carefree, which appeared in different flower colours; there
were also F2 hybrids, which were much cheaper but less dependable and of lesser
quality as these had been open-pollinated. The plantlets, sold in garden centres, are all
raised from seed and although the variety has increased over the years, there is still a
lack of the majority of different shapes, sizes and scents available from cuttings. These
seedlings are ideal for gardens.

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Growing pelargoniums in the garden, conservatory and for shows 97

Species
Many species can be grown in the garden, and include a number of the scented-leaf
species, which form huge bushes e.g. P. tomentosum, P. denticulatum and P. quercifolium
hybrids in particular. Most species are however best kept in the conservatory or
greenhouse and include the more succulent or cactus-like species e.g. P. carnosum,
P. hirtum and the geophytes e.g. P. rapaceum, P. longifolium, which have a short life
above ground.
Show plants
Pelargonium and Geranium shows have categories in each of the groups mentioned
and they are judged specifically for each category. There are easier and harder plants
to grow and for shows, it is generally the most easy which are usually exhibited.
These are also in strict order of popularity and according to Shellard (1981) this as
follows:
1 Regina (zonal), introduced in 1964, with pinkish-salmon flowers and is bushy,
self-branching and short jointed.
2 Henry Cox (zonal), a tricolor, first introduced prior to 1879 with red zone over a
pale green centre and yellow margin to the leaf and salmon-pink flowers.
3 Aztec (regal), introduced in 1962, compact and self-branching, white-base with
red/maroon markings in the centre of the petals, shading to strawberry towards the
edge. It flowers for months.
4 Jane Eyre (zonal), a miniature introduced by Stringer in 1970, with deep lavender flowers and glossy dark-green, zoned leaves.
5 Deacon Lilac Mist (zonal), a dwarf introduced by Stringer in 1970, with double
pale lilac petals.
6 Hazel Cherry (regal), introduced in 1971, with cherry-red flowers with
brown/black feathering on all petals; it has a similar habit to Aztec.
7 Highfields Festival (zonal), introduced in 1974, with pale rose-pink flowers with
a white eye on the upper two petals and zoned deep green leaves.
8 LElegante (ivy), old variety from 1860s with white flowers.
9 Mabel Grey (scented), with a very citrusy odour.
10 Burgenland Girl (regal), introduced in 1964, red-pink double florets, and dark
green leaves.
Latest favourites listed from the 1999 Show organised by the British Pelargonium and
Geranium Society include:

Claydon, Tuddenham, Orion miniature zonal


Elmsett, Brackenwood, Clatterbridge, Bold Carmine dwarf zonal
Burghi, Aztec, Georgi, Ginny Reeves regal
Dolly vardon, Mrs. Henry Cox, Silver Delight bi- and tri-colour zonal
Phyllis, Jessels Unique unique
Voodoo hybrid unique
Blooming Gem, Lakeland lvy-leaf
The Lowman, The Culm, The Mole, Spanish Angel, Quantock Rory Angel

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Maria Lis-Balchin

REFERENCES
Abbott, P. (1994) A Guide to Scented Geraniaceae. Hill Publicity Services, West Sussex.
Clark, D. (1988) Pelargoniums. Collingridge Books, The Hamlyn Publishing Group Ltd,
London.
Clifford, D. (1958) Pelargoniums including the popular Geranium. Blandford Press, Ltd, London.
Key, H. (2000) 1001 Pelargoniums, Batsford, B.T. Ltd.
Shellard, A. (1981) Geraniums for Home and Garden. David & Charles, Newton Abbot.
Taylor, J. (1988) Geraniums and Pelargoniums. The Crowood Press, Wiltshire.
Witham Fogg, H.G. (1975) Geraniuims and Pelargoniums. John Gifford Ltd, London.
Wood, H.J. (1966) Pelargoniums: A Complete Guide to their cultivation. A. Wheaton & Co. Ltd,
Exeter.

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11

Phytochemistry of the genus


Pelargonium
Christine A. Williams and Jeffrey B. Harborne

INTRODUCTION

Species of Pelargonium have long been in cultivation because of their attractive scents
and bright colours. Geranium oil, which is derived from several Pelargonuim species, is
an important plant crop. It is among the top 20 of plant volatile oils and the annual
world production is worth nearly 7 million pounds. It is not surprising therefore that
the chemical study of Pelargonium has concentrated on the essential oils present. Over
120 volatile constituents have been detected. Work has also been devoted to producing
these volatiles in shoot-organ culture of Pelargonium material.
The essential oils of Pelargonium leaves are generally located in glandular hairs on both
leaf surfaces. Other classes of chemical have been recorded in these leaf hairs or trichomes.
These include both flavonoid methyl ethers and salicylic acid derivatives. Protection
against herbivory by two-spotted spider mites has already been demonstrated in the case
of the salicylic acid derivatives. However, it is likely that all the various glandular hair
components have some role in protecting Pelargonium plants from herbivory or microbial
attack in the natural environment. An interesting chemical ecology is already beginning
to develop in the case of these plants and their natural enemies.

TERPENOIDS

Essential oils
Many of the Pelargonium species and the cultivars derived from them by artificial
hybridisation have scented leaves. Members of the Sections Pelargonium, Polyactium and
Cortusina are particularly rich in essential oils (Webb, 1984). The Geranium oil of
commerce is in fact obtained from steam distillation of the leaves of several Pelargonium
species, namely: P. graveolens, P. capitatum, and P. radula. It is a complex mixture of over
120 monoterpenes and sesquiterpenes and other low molecular weight aromatic compounds (Vernin et al., 1983). The oil varies in composition depending on the country
of origin. However, the major components, comprising ca. 6070 per cent of the oil,
are citronellol (1), geraniol (2) and linalol (3), either free or in ester combination. Other
terpenoids present in oils from all localities are: isomenthone (4), menthone (5), nerol
(6), cis-rose oxides (7) and trans-rose oxides (8), -terpineol (9), -pinene (10), myrcene
(11) and -phellandrene (12) (Figure 11.1).

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Christine Williams and Jeffrey Harborne

(1) Citronellol

(2) Geraniol

(3) Linalol

(4) Isomenthone

(5) Menthone

(6) Nerol

(7) cis-Rose oxide

(8) trans- Rose oxide

(9) -Terpineol

(10) -Pinene

(11) Myrcene

(12) -Phellandrene

(13) 6,9-Guaiadiene

(14) 10-Epi--eudesmol

Figure 11.1 Some simple terpenoids found in Pelargonium species.

Egyptian oils and Bourbon oil from Runion differ from the Chinese oil in having
much higher levels of geraniol, geranyl esters and linalol and smaller amounts of
citronellol and its ester and the absence of the sesquiterpene hydrocarbon, 6,9-guiadiene (13) Figure 11.1. African oil can be distinguished by the unique presence of 10-epi-eudesmol (14) Figure 11.1 (Teisseire, 1987). The Geranium oil from Runion also
contains some unusual tetrahydropyrans (1517) Figure 11.2 (Naves et al., 1961,
1963). The oils of a number of other scented Pelargonium species, which are not used
commercially have been analysed (Charlwood and Moustou, 1988; Charlwood and
Charlwood, 1991). They also contain complex mixtures of terpenoids. Thus, P.  fragrans produces many different classes of lower isoprenoids including camphene (18),
1,8-cineole (19), p-cymene (20), farnesene (21), fenchone (22), limonene (23) and
sabinene (24) Figure 11.2. By contrast, the oil of P. tomentosum is made up almost

2002 Edited by Taylor & Francis

Phytochemistry of the genus Pelargonium 101

(15) 2-(1,2-Butenyl)-4-methyl
tetrahydropyran

(16) 3-Hydroxy-2,2,6-trimethyl6-vinyltetrahydropyran

(17) 2-Acetonyl-4-methyltetrahydropyran

(18) Camphene

(19) 1,8-Cineole

(20) p-Cymene

(21) Farnescene

(22) Fenchone

(22) Limonene

(24) Sabinene

(25) Geranial

(26) Neral

(27) Carvone

(28) Cadinene

Figure 11.2 Further simple terpenoids found in Pelargonium species.

entirely of isomenthone (96 per cent) and menthone, while that of the cultivar
Pelargonium Mabel Grey contains 88 per cent citral isomers, geranial (25) and neral
(26) Figure 11.2. The former is utilised in the kitchen to provide peppermint flavour,
and the latter to give a lemon flavour to food. The camphoraceous vapour from steamed
leaves of P. betulinum has been used to relieve coughs and chest complaints and the powdered leaves of P. inquinans to cure headaches and relieve the symptoms of the common
cold and as a body deodorant by native tribesmen (van der Walt, 1977). Three
Pelargonium species, P.  fragrans, P. tomentosum and P. graveolens have been grown in tissue culture by Charlwood and Moustou (1988). The callus tissue in all three taxa
failed to form the oil of the parent plant but shootorgan cultures produced 50 per cent
of a qualitatively similar oil to the original plants. Thus, shootorgan cultures of

2002 Edited by Taylor & Francis

102

Christine Williams and Jeffrey Harborne

P.  fragrans accumulated pinene, sabinene, farnesene, carvone (27) and cadinene (28)
(Charlwood and Moustou, 1988) (Figure 11.2), while P. graveolens shoot cultures
produced geraniol, citronellol and citronellyl formate (Katagi et al., 1986). As with the
parent plant P. tomentosum accumulated equal amounts of menthone and isomenthone
(Charlwood and Moustou, 1988; Charlwood et al., 1990). However, shootorgan cultures of P.  fragrans produced much less fenchone and accumulated more - and
-pinene and sabinene and that of P. graveolens significantly less citronellol than the parent plant. However, oil production in shootorgan culture is unlikely at present to
compete successfully with the yields obtained by growing the whole plant.
Sterols and triterpenoids
The well known sterols: cholesterol, campesterol, and sitosterol, have been reported
both in free form and in esterified form from Pelargonium hortorum, while stigmasterol
was found only in the free form. The major triterpenoids in this plant are - and
-amyrin, which also occur both free and esterifed, and a partially identified compound
named, isomultifluorenol. Traces of free cycloeucalenol and its acetate, obtusifoliol
acetate, cycloartenol acetate and 24-methylene cycloartanol acetate were also detected
(Axel et al., 1972).

MONOMERIC FLAVONOIDS

Vacuolar leaf flavonoids


There have been a number of flavonoid aglycone surveys of Pelargonium species but
no records of flavonoid glycosides. In an early study, Bate-Smith (1973) found
wide variation in the flavonoid constituents between the ten taxas he examined with
a preponderance of myricetin (29) and quercetin (30) Figure 11.3 in species from
Sections Hoarea and Pelargonium. In later chemotaxonomic studies of four Sections:
Glaucophyllum, Cortusina, Chorisma and Jenkinsonia, quercetin was found to be universally present. Myricetin and kaempferol (31) Figure 11.3 were detected in 71 per cent
of the taxa in section Glaucophyllum (van der Walt et al., 1990) and myricetin was found
also in all the species examined in section Cortusina except P. dichondrifolium (Dreyer
et al., 1992) but was absent from sections Chorisma (Albers et al., 1995) and Jenkinsonia
(van der Walt et al., 1997). The major components of the section Chorisma were
flavonols but two flavones, luteolin (32) and apigenin (33) Figure 11.3 were additionally
detected in two taxas P. mollicomum and P. tetragonum. In a more definitive survey of 58
Pelargonium species from 19 sections Williams et al. (2000) confirmed that flavonols are
the major leaf vacuolar flavonoid constituents in the genus. Quercetin was present in
all species except P. spinosum, where luteolin was the major component accompanied by
flavone C-glycosides. However, luteolin was more usually present as a trace constituent
in 49 per cent of taxa and flavone C-glycosides as the major flavonoids in 36 per cent
of the species. The regular occurrence of other flavonols, myricetin in 38 per cent and
kaempferol in 50 per cent of taxa, respectively, confirms the previous findings.
Additionally both quercetin 3-methyl ether (34) and isorhamnetin (35) (Figure 11.3)
were detected in 10 per cent of the sample. However, apigenin was not detected in any
taxon examined in this study. The results are presented in more detail in Table 11.1.

2002 Edited by Taylor & Francis

Phytochemistry of the genus Pelargonium 103

(29) Myricetin

(30) Quercetin

(31) Kaempferol

(32) Luteolin

(33) Apigenin

(34) Quercetin 3-methyl ether

(35) Isorhamnetin

Figure 11.3 Leaf flavonoids from Pelargonium species.

Myricetin and flavone C-glycosides are the most useful flavonoid taxonomic markers
in the genus but the co-occurrence of flavonoids with various other phenolic
constituents i.e. ellagitannins and proanthocyanidins, is more valuable (see below). In
summary, the leaf flavonoid pattern is broadly similar to that encountered in Geranium
(see Chapter 4).
Floral flavonoids
The occurrence of pelargonin (pelargonidin 3,5-diglucoside) (36) Figure 11.4 in flowers of Pelargonium cultivars was established in the 1930s, following the synthesis of this
pigment. Robinson and Robinson (1932) found that the salmon pink petals of zonal

2002 Edited by Taylor & Francis

Table 11.1 The distribution of vacuolar leaf flavonoids* in Pelargonium species


Section/Species/Authority

PELARGONIUM
P. quercifolium
P. graveolens
P. tomentosum
P. cucullatum
P. crispum Whiteknights
c.v. Lady Plymouth
CICONIUM
P. transvaalense
P. acraeum
P. mutans
P. multibracteatum
P. alchemilloides
P. ranunculophyllum
OTIDIA
P. laxum
P. ceratophyllum
P. alternans
P. carnosum
LIGULARIA
P. fulgidum
P. oreophilum
P. pulchellum
SUBSUCCULENTIA
P. karooicum
P. otaviense
P. spinosum
CORTUSINA
P. echinatum
2002 Edited by Taylor & Francis

Flavones

Flavonols
Myricetin (6)

Quercetin (7)

Kaempferol (8)

Isorh (12)

Qu3ME (11)

Lu (9)

C-glycs

(L.f) LHr.
LHr.
Jacq.
(L.) LHr.
(Berg.) LHr.















()

()
()
()




()

()









()

()


()








Knuth
R.A. Dyer
P. Vorster
Hochst.
(L.f.) LHr.
(Eckl. and Zeyh.) Bak.













()



()




















()
()










(Sweet) G. Don
LHr.
Wendl.
(L.) LHr.



()







()









()

()












(L.) LHr.
Schltr.
Sims





()





()

















Compton
Knuth
Willd.





()
()



()










()
()






Curt.



P. magenteum
P. crassicaule
P. cortusifolium
CHORISMA
P. worcesterae
P. tetragonum
P. mollicomum
PERISTERA
P. drummondii
ISOPETALUM
P. cotyledonis
P. cotyledonis 2
P. cotyledonis 3
POLYACTIUM
Caulescentia
P. gibbosum hybrid
POLYACTIUM
P. triste
MAGNISTIPULACEA
P. luridum
SCHIZOPETALA
P. amatymbicum
P. bowkeri
GLAUCOPHYLLUM
P. grandiflorum
CAMPYLIA
P. tricolor
P. ovale ssp. hyalinum
RENIFORMIA
P. abrotanifolium
P. reniforme
P. exstipulatum
P. album
2002 Edited by Taylor & Francis

J.J.A. v.d. Walt


LHr.
LHr.









()



















Knuth
(L.f.) L.Hr.
Fourcade





()















()
()






Turcz.

()



(L.) LHr.
(L.) LHr.
(L.) LHr.









()











()

()





(L.) LHr.



(L.) LHr.





()

(Andr.) Sweet

()



(Eckl. & Zeyh.) Harv.


Harv.

















()




(Andr.) Willd.



()

Curt.
(Burm.f.) LHr.







()
()













(L.f.) Jacq.
Curt.
(Cav.) LHr.
J.J.A. v.d. Walt













()




()
()







()
()
()






Table 11.1 (Continued)


Section/Species/Authority

P. sidoides
P. odoratissimum
HOAREA
P. bubonifolium
P. appendiculatum
P. incrassatum
MYRRHIDIUM
P. surburbanum
P. myrrhifolium
JENKINSONIA
P. antidysentericum
P. trifidum
P. praemorsum
P. griseum
P. senecioides
UNKNOWN
P. rodneyanum
P. quercetorum

Flavones

Flavonols
Myricetin (6)

Quercetin (7)

Kaempferol (8)

Isorh (12)

Qu3ME (11)

Lu (9)

C-glycs

DC.
(L.) LHr.

















()




(Andr.) Pers.
(L.f.) Willd.
(Andr.) Sims





()




()


















Clifford ex Boucher
(L.) LHr.

















()




(Eckl. & Zeyh.) Kostel


Jacq.
(Andr.) Dietr.
Knuth
LHr.







()



()














()


()


()








Mitch.
Agnew




()

















Source: Data from Williams et al. (2000).


Notes
* Flavonoid aglycones identified after acid hydrolysis.
Isorh isorhamnetin; Lu luteolin; Qu3ME quercetin 3-methyl ether; C-glycs flavone C-glycosides.
2002 Edited by Taylor & Francis

Phytochemistry of the genus Pelargonium 107

Pelargonium were pigmented by pure pelargonium 3,5-diglucoside, while the cultivar


Henry Jacoby contained the same pigment together with malvidin 3,5-diglucoside
(37) Figure 11.4. A survey of the three wild species: P. veitchianum, P. bertiana and
P. cucullatum showed that malvidin 3,5-diglucoside was the major pigment in each.
Later investigation of Pelargonium cultivar petals showed that pelargonidin and malvidin
3,5-diglucoside was accompanied by small amounts of the relatively rare peonidin 3,5diglucoside (38) (Harborne, 1961) (Figure 11.4). A further survey of petal pigments in
P.  hortorum showed that all six common anthocyanidins (including delphinidin,
petunidin and cyanidin) could be identified as the 3,5-diglucosides in different colour
forms (Asen and Griesbach, 1983). The 3,5-diglucosides are invariably accompanied by the
corresponding acetates, where an acetyl residue is substituted at the 6-position of the
glucose of C-5 (Mitchell et al., 1998). It may be noted that the acetate of the malvidin
pigment has also been detected in Geranium (see Chapter 4). A range of colourless flavonol

(36) Pelargonidin 3,5-diglucoside

(37) Malvidin 3,5-diglucoside

(38) Peonidin 3,5-diglucoside

Figure 11.4 Anthocyanins found in flowers of Pelargonium species.

2002 Edited by Taylor & Francis

108

Christine Williams and Jeffrey Harborne

glycosides based on kaempferol and quercetin occur with the above anthocyanins in
Pelargonium  hortorum petals. Besides several monoglycosides, the 3-rutinosides and
3-rhamnosylgalactosides of these two flavonols are present (Asen and Griesbach, 1983).
Exudate flavonoids
Many Pelargonium species have glandular hairs on the leaf surface. Besides producing
terpenoid constituents (see under terpenoids), these structures may also yield lipophilic
flavonoids. Such compounds were detected in 35 per cent of the Pelargonium taxa
surveyed by Williams et al. (1997), but mostly only in trace amounts. However, in
P. crispum the simple flavone, chrysin (5,7-dihydroxyflavone) (39) Figure 11.5 is the
major leaf exudate constituent, accompanied by a C-methyl derivative (either 6- or 8-)
of the corresponding 5,7-dihydroxyflavanone. Two unidentified flavanones were detected
in one other species, P. drummondii. Exudate flavones were further found in four taxa:
chrysoeriol (40) Figure 11.5 and acacetin (41) (luteolin 3- and apigenin 4-methyl
ethers, respectively) in P. album and some unidentified apigenin-based flavones in
P. abrotanifolium, P. exstipulatum and P. fulgidum. A variety of flavonol (quercetin and
kaempferol) methyl ethers (see Table 11.2 ) were found in P. fulgidum, P. quercifolium and
Table 11.2 Exudate flavonoids detected in Pelargonium species
Species

Leaf exudate flavonoids


Flavones

Flavanones

Flavonols

Apigenin (33)based, possibly


acylated
Chrysoeriol (40)
Acacetin (41)

P. crispum
(Berg.) LHr.
P. drummondii
Turcz.
P. exstipulatum
(Cav.) LHr.

Chrysin (39)

Apigenin-based

6-or-8-C-methyl
5,7-dihydroxyflavanone
Two unidentified
flavanones


P. fulgidum
(L.) LHr.

Apigenin-based

Qu 3ME (34)
Km MME
Qu 3,7-diME (43)
Km 3,7-diME (42)
Km triME
Qu tetraME

P. quercifolium
(L.f.) LHr.

Qu 3ME
Km 3ME
Qu 3,7-diME
Qu triME

P. tomentosum
Jacq.

Km triME
Qu tetraME

P. abrotanifolium
(L.f.) Jacq.
P. album J.J.A.
v.d. Walt

Notes
Qu quercetin; Km kaempferol; ME methyl ether.

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Phytochemistry of the genus Pelargonium 109

(39) Chrysin

(40) Chrysoeriol

(41) Acacetin

(42) Kaempferol 3,7-dimethyl ether

(43) Quercetin 3,7-dimethyl ether

Figure 11.5 Leaf exudate flavonoids from Pelargonium species.

P. tomentosum. Two typical structures are kaempferol and quercetin 3,7-dimethyl ethers
(42 and 43) (Figure 11.5). Some partially characterised higher methyl ethers of both these
flavonols were also present.
Tannins
The genus Pelargonium, like Geranium is unusual in synthesising both hydrolysable
(ellagitannins) and non-hydrolysable (proanthocyanidins) tannins in abundance in many
of its species. The two types of tannin are produced by different pathways. The proanthocyanidins are formed by condensation of single catechin units (e.g. 44) to form
dimers, trimers, tetramers and higher oligomers (45) (Figure 11.6). The ellagitannins
originate from gallic acid (46), which condenses with glucose to give a digalloyl ester,
which then forms the hexahydroxydiphenoyl ester (47) (Figure 11.6) as a key
intermediate. The proanthocyanidins can be detected by the production of some of the
parent anthocyanidin on treatment with hot acid and the ellagitannins by the release of
ellagic acid (48) (Figure 11.6) on acid hydrolysis. However, some Pelargonium species
produce free ellagic acid in the absence of ellagitannins. In the survey of Williams
et al. (2000) prodelphinidin was found in 53 per cent of the sample, procyanidin in
29 per cent, ellagitannins in 53 per cent and free ellagic acid in 50 per cent of the taxa.
Gallic acid was also recorded from 62 per cent of the species and protocatechuic acid

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110

Christine Williams and Jeffrey Harborne

(44) (+)-Catechin

(46) Gallic acid


(45) Procyanidin C2

(47) Hexahydroxydiphenoyl ester

(48) Ellagic acid

Figure 11.6 Tannins and their precursors in Pelargonium.

from 38 per cent of the sample. In Pelargonium both types of tannin may occur in the
same plant, separately, or both may be absent. Their co-occurrence with flavonoids has
some taxonomic and evolutionary significance. Thus, the presence of myricetin is
correlated with the presence of proanthocyanidins (but not vice versa) and the absence of
ellagitannins. Conversely, the absence of myricetin shows a correlation with the absence
of ellagitannins. On this basis, the various species may be divided into six chemical
groups: i.e. those containing (1) myricetin  proanthocyanidins; (2) myricetin  proanthocyanidins  free ellagic acid; (3) myricetin  proanthocyanidins  ellagitannins 
free ellagic acid; (4) ellagitannins  free ellagic acid but no myricetin; (5) ellagitannins
but no free ellagic acid or myricetin; (6) no tannins or myricetin. There also seems to be
a correlation between flavone C-glycosides and the presence of luteolin in some species.
Bate-Smith (1962) suggested that both ellagitannins and proanthocyanidins are
indicators of primitiveness in the dicotyledons and that they are both associated with
woodiness. He also suggested that there have been two lines of evolution in the dicots
and that in one line ellagitannins were lost before the proanthocyanidins and in the

2002 Edited by Taylor & Francis

Phytochemistry of the genus Pelargonium 111

other the proanthocyanidins were lost first. This was supported by a statistical analysis
of the Bate-Smith data by Sporne (1975), which also indicated that the procyanidins
were lost more quickly than the ellagitannins. These evolutionary trends can be clearly
seen in Pelargonium and are illustrated in Figure 11.7, where the species analysed by
Williams et al. (2000) are grouped in sections according to their tannin constituents and
overlayed with data for the presence of myricetin and glycoflavones.
Detailed chemical investigations of the Pelargonium tannins remain for the future. All
that is known is that the ellagitannin geraniin, which is so widespread in Geranium
species, is apparently not present in the several Pelargonium taxa so far surveyed (Okuda
et al., 1980), which included P. graveolens and P. tomentosum.
MINOR PHENOLIC COMPOUNDS

Coumarins
Four coumarins: the common scopoletin (49), the rare 7-hydroxy-5,6-dimethoxycoumarin (50) and its 7-methyl ether (51) and its 7-glucoside (52) (Figure 11.8) were
identified in roots of Pelargonium reniforme and detected in roots of 11 other species:
P. betulinum, P. capitatum, P. cucullatum, P. hirtum, P. luridum, P.moreanum, P. myrrifolium,
P. radula, P. reniforme, P. salmoneum, P. sidaefolium, P. triste and P. zonale (Wagner and
Bladt, 1975).

ELLAGITANNINS
PROANTHOCYANIDINS

SUBSUCCULENTIA

OTIDIA

P.
P.
P.
PELARGONIUM P.
P. cucculatum *
P. graveolens*
P. quercifolium*
P. tomentosum*

alternans*
carnosum*
ceratophyllum*
laxum *

RENIFORMIA

RENIFORMIA
P. album +

HOAREA

P. bubonifolium
P. crispum *

LIGULARIA

CICONIUM

P. abrotanifolium*

ISOPETALUM
P. cotyledonis2

P. tricolor
P. ovale *

POLYACTIUM
P. amatymbicum

HOAREA

PERISTERA

P. acraeum
P. drummondii
P. transvaalense

RENIFORMIA

CAMPYLIA
P. appendiculatum*

P. mollicomum+
P. tetragonum+

P. ranunculophyllum

P. odoratissimum

P. bowkeri
P. pulchellum
P. gibbosum hybrid*
P. oreophilum
P. luridum +
P. triste *
CORTUSINA
P. echinatum
P. cortusifolium*
P. crassicaule *
P. magentum *

HOAREA

CHORISMA
CICONIUM

PELARGONIUM
POLYACTIUM

P. spinosum +

P. quercetorum+

P. mutans
P. rodneyanum

RENIFORMIA

P. incrassatum*

P. exstipulatum+
P. reniforme +
P. sidoides +

LIGULARIA
P. cotyledonis+

P.
P.
P.
P.
P.

antidysentericum+
griseum +
praemorsum
seneciodes
trifidum +

CHORISMA
P. worcesterae+

SUBSUCCULENTIA

P. fulgidum +

ISOPETALUM

JENKINSONIA

P. otaviense+

GLAUCOPHYLLUM
P. grandiflorum

CICONIUM

P. multibracteatum
P. alchemilloides

Source: Williams et al. (2000)


* Myricetin also present;
+ Flavone C-glycosides also
present

FREE ELLAGIC ACID

SUBSUCCULENTIA
P. karooicum

Figure 11.7 Pelargonium species grouped in sections according to their tannin constituents.

2002 Edited by Taylor & Francis

112

Christine Williams and Jeffrey Harborne

(49) Scopoletin R1=R2=H


(50) 7-hydroxy-5,6-dimethoxycoumarin R1=H, R2=OMe
(51) 5,6,7-trimethoxycoumarin R1=Me, R2=OMe
(52) 7-hydroxy-5,6-dimethoxycoumarin 7-glucoside R1=Glc, R2=OMe

(53) 6-[(Z)-10-Pentadecenyl]salicylic acid

(54) 6-[(Z)-12-Heptadecenyl]salicylic acid

Figure 11.8 Coumarins and salicylic acid derivatives from Pelargonium species.

Salicylic acid derivatives


Plants of Pelargonium  hortorum, (the so-called geraniums sold in garden centres for
summer bedding), were found to be largely resistant to attack by the two-spotted
spider mite, Tetranychus urticae Koch. This resistance was tracked down to the
presence of glandular trichomes on both upper and lower surfaces of the leaves,
which produce a toxic, sticky exudate (Craig et al., 1986). Morphologically similar
trichomes occur in equal number on susceptible plants but they do not produce
any exudate. The two major toxins of the exudate were identified as 6-[(Z)-10pentadecenyl]salicylic acid (53) and 6-[(Z)-12-heptadecenyl]salicylic acid (54)
(Walters et al., 1988) (Figure 11.8). In a study of the relative resistance to the
two-spotted spider mite of seven Pelargonium species, four namely: P. capitatum,
P. australe, P. tomentosum and P. rapaceum were found to be more resistant than the
other three: P. fulgidum, P. odoratissimum and P. graveolens (Snetsinger et al., 1966).
These workers also evaluated the susceptibility of six accessions of P.  hortorum and
found that the three commercial cultivars (two diploids and one tetraploid) were
resistant or moderately resistant to attack and of the other cultivars King Midas
was susceptible and G71 and their hybrid were resistant. The source of the resistance was not investigated. Variation among cultivars of P. peltatum, the ivy-leaved
Geranium, in their resistance to this spider mite has been reported (Potter and
Anderson, 1982) and similar variation has been observed among the tetraploid
cultivars of P.  hortense of European origin (Craig et al., 1986).
Organic acids
Tartaric acid (55) (Figure 11.9) is a characteristic constituent of the genus
Pelargonium. It represents more than 1.5 per cent of the dry weight of the aerial parts
of 23 species and hybrids, 0.751.5 per cent in six other species and hybrids and
less than 0.75 per cent in three further species (Stafford, 1961). Oxalic acid (56)

2002 Edited by Taylor & Francis

Phytochemistry of the genus Pelargonium 113

(55) Tartaric acid

(56) Oxalic acid

(57) Malic acid

(58) Succinic acid

Figure 11.9 Organic acids from Pelargonium species.

(Figure 11.9) has been isolated from P. peltatum. This plant is potentially poisonous
to livestock since oxalic acid is present in a water-soluble form; instead of the more
usual insoluble calcium salt. It occurs together with malic (57), tartaric and succinic
(58) acids in this species (Figure 11.9). The presence of malic acid is expected because
P. peltatum is a Crassulacean acid metabolism CAM plant, and thus accumulates malic
acid in the dark, which disappears during the day.
Alkaloids

Screening studies on Pelargonium species had revealed the presence of alkaloids, especially
in zonal cultivars (Lis-Balchin, 1996, 1997), which had previously only been found in
the Erodium genus of the Geraniaceae (Lis-Balchin and Guittoneau, 1995). The identity of the alkaloids detected was not determined until studies by Lis-Balchin et al. (1996)
on the cultivar Appleblossom. The simple amines tyrosine 1 and tryptamine 2 were first
detected by thin-layer chromatography (TLC) comparison with authentic samples but of
more interest was the isolation of three other, more complex, indole alkaloids. The structures of two of these were determined by spectroscopic methods and they were shown to
be the two isomers elaeocarpidine 3 and isoelaeocarpidine. These alkaloids were found in
all the different types of zonal Pelargonium cultivars, but not in the pure ivy-leaf or regals;
the hybrid ivy-leaf pelargoniums, with the appearance of either ivy-leaf or zonal
Pelargonium also inherited the alkaloids (Lis-Balchin, 1996). These alkaloids only appeared
in half of the section Ciconium, which were originally allocated to the Section and some of
whose genera gave rise to the modern zonals (Lis-Balchin, 1996). The indole alkaloids
appear to have an insect repellent activity against whitefly (Woldemariam et al., 1997)
and concentrate in the darker zonal area of the leaves.
CONCLUSION

The essential oil of Pelargonium (often termed Geranium oil) has already been
intensively investigated. However, in view of its possible medicinal and other useful
properties, it probably deserves continuing studies. There is still much to be learnt
about the volatiles present in those Pelargonium species yet to be cultivated.

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Christine Williams and Jeffrey Harborne

In terms of the polyphenolic pattern, the genus Pelargonium is broadly similar in the
range and type of constituent to the genus Geranium. And yet there are significant
differences. Thus, the characteristic ellagitannin of Geranium is not produced by
Pelargonium species. We know that ellagitannins are abundant in the two genera. What
is formed in Pelargonium to replace the geraniin of Geranium?

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Lis-Balchin, M. (1997) A chemotaxonomic study of the Pelargonium (Geraniaceae) species and
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Structural determination and biosynthetic considerations of anacardic acids of geranium.
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The 135th British Pharmaceutical Conference, Scarborough. Sept. 1518.

2002 Edited by Taylor & Francis

12 Pharmacology of Pelargonium
essential oils and extracts in vitro
and in vivo
Stephen Hart and Maria Lis-Balchin

INTRODUCTION

Pelargonium species originated in southern Africa where a large number were used as
folk medicines with mainly antidysenteric properties (Watt and Breyer-Brandwijk,
1962). A few species were brought over to Europe in the 17th Century and hybridised
over the centuries resulting in thousands of modern cultivars. Commercial Geranium
oil is obtained from the scented leaves of a number of Pelargonium cultivars grown
mainly in Reunion, China, Egypt and Morocco. There are, however, large numbers of
scented species, hybrids and cultivars which are at present unexploited, but exhibit
some potential as odourants for the perfumery and food industry, antimicrobial agents
and insecticides (Lis-Balchin, 1988, 1997; Lis-Balchin et al., 1996b).
FOLK-MEDICINAL USAGE OF PELARGONIUM SPECIES

The Pelargonium species used in South Africa by the local population were also used by
the Boers mainly for antidysenteric purposes e.g. root of P. transvaalense and P. triste and
the leaves of P. bowkeri and P. sidaefolium. Some Pelargonium species were also used to
treat specific maladies e.g. P. cucullatum for nephritis, P. tragacanthoides for neuralgia,
P. luridum and P. transvaalense root for fever; P. minimum, P. reniform and P. grossularioides
for menstrual flow (Pappe, 1868; Watt and Brandwijk, 1962). The last was also used
as an emmanogogue and abortifacient by both Zulus and Boers and has recently been
studied further (Lis-Balchin and Hart, 1994) and shown to have spasmogenic properties on the uterus and smooth muscle preparations in vitro.
All the folk-medicinal attributes have been due to the water-soluble or ethanolic extracts,
as they involved teas and infusions and not volatile essential oils themselves. This differs to
the practice of aromatherapy, where essential oils are used, and furthermore the plant
extracts were not massaged into the skin but mainly used internally. The Pelargonium species
used were often non-scented and the scented ones used were different Pelargonium species to
those utilised in the production of commercial Geranium oil for aromatherapy.
STUDY OF IN VITRO PHARMACOLOGICAL ACTIVITY

The preparation chosen to assess the in vitro pharmacological activity of an essential oil or
its components on smooth muscle must respond to spasmogenic agents i.e. those causing

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117

a contraction and spasmolytic agents which will relax smooth muscle. Preparations of
intestinal smooth muscle are robust and, although spasmogenic and spasmolytic activity
can be identified on those from rabbit and the large intestine of the guinea-pig, the field
stimulated guinea-pig ileum allows quantitative experiments to be performed readily. The
field stimulated guinea-pig ileum also enables a neurogenic response to be distinguished
from a myogenic response and the receptors involved to be elucidated. When the reported
use of the essential oil indicates a targeted organ such as the uterus or lungs then appropriate preparations of these smooth muscles can be studied. For a more complete study of
the in vitro pharmacology it would be necessary to include vascular and cardiac tissues and
to examine activity on skeletal muscle such as the rat phrenic nerve hemi-diaphragm
preparation. It must of course be remembered that essential oils contain many components
and the observed pharmacological action of the oil may be due to several active principles
acting by different mechanisms or, indeed, by opposing mechanisms which may give rise
to biphasic responses. It is also important to verify that the solvent for an essential oil or
its components, in the concentration that will be in contact with the tissue, does not itself
have a spasmogenic or spasmolytic action. Methanol is satisfactory for most smooth muscle
preparations at a dilution of not less than 1:125 but it has been reported that hexane
extracts may give misleading results (Lis-Balchin et al., 1997). It is questionable whether
aqueous emulsions are appropriate but some workers prefer a vehicle such as Arlatone 285
(Reiter and Brandt, 1985) or dimethylsulphoxide, DMSO (Aqel, 1991).
STUDY OF IN VIVO PHARMACOLOGICAL ACTIVITY

There are three appropriate approaches to the study of the effects of Pelargonium in the
whole animal, which differ in the route of administration. The classical approach is the
parenteral administration into the conscious or anaesthetised animal. Results from such
experiments will demonstrate the pharmacology of the compound but may be difficult
to relate to their normal use. Exposure of animals to the aroma of an essential oil, or the
application of the diluted oil to depilated skin, obviously mimics in animals the normal
use of the compounds in humans. The ideal investigation will use human volunteers
and two approaches are possible. In the first, the purpose of the experiment is to determine the pharmacology of the essential oil and a dose-related effect would be expected
whilst in the second, one is interested in whether, at the concentrations normally used,
the oil has any significant effects. The latter experiments require careful design and
this will differ depending on whether the aroma alone, or aroma plus massage plus
absorption across skin, is being investigated.
INVESTIGATIONS OF PELARGONIUM ESSENTIAL OILS

The bioactivity of essential oils has been studied for many years with much of the work
originating from Germany but very little has been published on Pelargonium. Treibs
(1956) and Sticher (1977) have reviewed early work which includes research on some of
the constituents of Pelargonium. Gunn (1921) studied the actions of several volatile oils
(in the form of emulsions) on the activity of intestinal muscle from rabbit, rat and cat
in vitro and in vivo and observed spasmolysis, which appeared to be a direct action on
the muscle, but did not include Pelargonium (or Geranium). A year later Stross (quoted

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Stephen Hart and Maria Lis-Balchin

by Sticher, 1977) reported the spasmolytic activity of several naturally occurring


compounds including geranyl acetate. Imaseki and Kitabatake (1962) report an
antispasmodic action of citronellol, geraniol and linalool on the mouse small intestine.
Buchbauer et al. (1993) have reviewed the biology of essential oils and Tisserand and
Balacs (1995) have described their general activity and safety.
EXPERIMENTS ON IN VITRO GUINEA-PIG ILEUM PREPARATIONS

Method
Segments of ileum (2 cm) from a freshly killed guinea-pig are mounted in an organ
bath (25 ml) containing Krebs solution (composition, mM: NaCl 118.1, KCl 4.7,
NaHCO3 25, Glucose 11.1, MgSO4 1, KH2PO4 1 and CaCl2.2H2O 2.5) maintained at
37 C and gassed continually with 95 per cent oxygen in carbon dioxide. The preparation is placed under a tension of 1 g and contractions recorded through an isometric
force transducer connected to a pen recorder or Mac-Lab. The method of Paton (1954)
is used to stimulate nerves within the wall of the intestine. Two platinum electrodes,
attached to a stimulator, are placed on either side of the intestine and a square wave
(width, 0.5 msec) delivered every 10 sec (0.1 Hz) at an appropriate voltage (about 50 v)
produces a regular and reproducible contraction of the intestine. This contraction is not
affected by the presence of a ganglion blocking agent but is inhibited by atropine
indicating that it is due to the stimulation of post ganglionic parasympathetic nerves
leading to the release of acetylcholine which acts on muscarinic receptors on smooth
muscle. The addition of an extract with spasmogenic activity during field stimulation
is recognised as a rise in the baseline and/or an increase in the size of the electrically
induced contraction. A reduction in the size of the contraction indicates spasmolytic
activity which can be further analysed as described below.
General action on intestinal smooth muscle
Most Pelargonium essential oils and commercial Geranium oils are spasmolytic on
intestinal smooth muscle and reduce the response to electrical stimulation (Figure 12.1).
Geranium oil

Washout
0.1 ml diluted 1000

Figure 12.1 The spasmolytic effect of Geranium oil on the electrically-stimulated guinea-pig ileum
in vitro.

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Pharmacology of Pelargonium essential oils and extracts

119

Reiter and Brandt (1985) and Lis-Balchin and Hart (1997) have shown that citronellol,
citronellal and geraniol have a spasmolytic action on guinea-pig ileum. One exception is
the oil from P. grossularioides which contracts the tissue but on washout, when tone has
returned to normal, inhibits briefly the electrically induced contractions (Lis-Balchin and
Hart, 1994). One of the components of Pelargonium oil, geranyl formate, contracts guineapig ileum (Lis-Balchin et al., 1996b). Alpha- and -pinene are present in very small
amounts and are interesting components because, although they are pure compounds, they
initially contract intestinal smooth muscle and then produce a spasmolytic effect
(Lis-Balchin et al., 1999). The species from which essential oils have been studied, and the
components that have been investigated, by the authors are shown in Tables 12.1 and 12.2.
The concentrations of essential oils which inhibit the electrically induced contraction of the
guinea-pig ileum by 50 per cent range from 6.107 to 4.8.105 (w/v). In all cases the effect
of the essential oil lasts for as long as it is in contact with the ileum but the rate of recovery
of the tissue after washout varies between different species of Pelargonium.

Table 12.1 Summary of investigations of spasmolytic activity of various Pelargonium species and cultivars
on guinea-pig ileum in vitro
Pelargonium

Attar of Roses
Brunswick
Chocolate Peppermint
Clorinda
Copthorne
Geranium oil
Bourbon (rose)
Geranium oil China
Geranium oil Egypt
Lady Plymouth
Madam Nonin
P. citronellum J.J.J. v.d.Walt
P. cucullatum (L.) LHer.
P. filicifolium
P. glutinosum
P. graveolens LHer.
P. grossularioides
P. odoratissimum LHer.
P. quercifolium
P. tomentosum Jacq.
P. viscossimum Sweet
P. vitifolium (L.) LHer.
P.  fragrans
Patons Unique
Purple Unique
Radula
Royal Oak
Sweet Mimosa
Sweet Rosina

Atropine-like

Adrenoceptorinvolvement

No

trq

Yes
No
No
No

Yes

No
No
No

Yes
Yes

cGMPinvolvement
No

No
Yes
No
No

No
No

Yes

No

No

No
No
No

Yes
Yes
No

No
No

No
No

No
No
No

Yes

No
No
No

No

Yes
No

No
Yes

No
No

No
No
No
No
No
No
No
No
No
No
No

No

No
No

Sources: Data from Lis-Balchin et al. (1997, 1998) and Lis-Balchin and Hart (2000).

2002 Edited by Taylor & Francis

cdp

No

No
No
No
No
No

cAMP-involvement

120

Stephen Hart and Maria Lis-Balchin

Table 12.2 Summary of investigations of spasmolytic activity of components of Pelargonium essential oils
on guinea-pig ileum in vitro
Components

Atropine-like

Adrenoceptor-involvement

cAMP-involvement
trq

Citronellal
Citronellol
Citronellyl formate
Damascenone
Geraniol
Geranyl acetate
Geranyl formate
Guaiadiene
Linalool
Linalyl acetate
Linalyl butyate
Menthone
-pinene
-pinene
Rose oxide

No

cGMP-involvement

cdp

No
Yes
No
Yes

Yes

No
No

No
No
No

Sources: Data from Lis-Balchin et al. (1998, 1999) and Lis-Balchin and Hart (2000).

As well as the essential oils obtained from scented Pelargonium leaves, non-scented
pelargoniums were also studied (Table 12.3). These include numerous zonals, regals and
ivy-leaved Pelargoniums, the leaves or roots of which were tested both as methanolic
and water-soluble extracts and all but the P. grossularioides water-soluble and ethanolic
extracts (Figure 12.2) were found to be spasmolytic on guinea-pig ileum.
The alkaloid extracts obtained from the zonals (Lis-Balchin et al., 1996c; Lis-Balchin,
1997) were also all spasmolytic. The methanolic and water-soluble extracts, and
alkaloid fractions of P. luridum (root) and the leaves of P. inquinans and P. cucullatum were
also found to be spasmolytic.
Recently several hydrophilic extracts of numerous Pelargonium species and cultivars
were tested on guinea-pig ileum. Three different hydrophilic extracts were made from
each plant: a cold methanolic extract; a tea, made with boiling water and a hydrosol i.e.
the water remaining after steam/water distillation. And in each case the activity was
compared against the steam/water-distilled essential oils.
Table 12.3 Examples of non-scented leaved Pelargonium cultivars showing a spasmolytic
effect on guinea-pig ileum in vitro: methanolic and water-soluble extracts
Penny
Appleblossom
Frank Headley
Magda
Els
Mr Wren
Mr Henry Cox
Redondo

Golden Harry Hieover


Princess Alexandra
Daydream
Fire Dragon
Lass OGowrie
Occold Shield
Appleblossom
Golden Staph

Note
These samples were stored for many months in the refrigerator prior to pharmacological assays.

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Pharmacology of Pelargonium essential oils and extracts

121

Table 12.4 Evidence for contraction, C and or relaxation, R for extracts and essential oils in guinea-pig
ileum in vitro (electrically stimulated)
Plant

Extract

Tea

Hydrosol

EO

Lady Plymouth
Clorinda
Sweet Mimosa
Attar of Roses
P. tomentosum
Chocolate Tomentosum
P.  fragrans
Madam Nonin
P. odoratissimum
P. graveolens
Orsett
Ardwick Cinnamon
Atomic Snowflake
Patons Unique
Lady Plymouth
Appleblossom
Geranium robertianum

R
C/R
C/R
C/R
C/R
R
C/R
C/R**
R (occasional C)
R/C
C/R
C/R
*C/R
*C/R
C/R
C/R
R

C/R
C/R
CR
*C/R
C/R
R
*C/R
C/R
***C/R
*C/R
*C/R
C/R
*C/R
C/R
C/R
C/R
R

C/R
C/R
C/R
*C/R
C/R
R
*C/R
C/R
C/R (high) R (low)
C/R C (low)
C/R
C/R
C/R
*C/R
C/R (only R, low)
N/T
R

R
R
R
R
R
R
R
R
R
R
R
R
R
R
R
No EO
N/A

Notes
Contraction means an increase in tone, unless stated.
* contraction stronger than relaxation; ** relaxation greater than contraction; *** contraction seems to be very constant
and not dose-related.

The extracts were tested on guinea-pig ileum, with and without electical stimulation
in vitro, using the same conditions as described previously All Pelargonium essential
oils studied to date have again shown a relaxant effect on field-stimulated guinea-pig
ileum as previously shown (Lis-Balchin et al., 1997; Lis-Balchin and Hart, 1998). More
hydrophilic extracts corresponding to most of these scented Pelargoniums, however,
showed a strong initial contractile effect followed in most cases by a relaxation at low
concentrations for the teas and hydrosols as well as the methanolic extracts and showed
a very strong contraction at high concentrations, except for Chocolate Peppermint
extract (Table 12.4).
In contrast, the three extracts of Geranium robertianum all showed a relaxant effect.
Neurogenic or myogenic
A concentration of Pelargonium essential oil which produces a significant inhibition of
the contraction of the field stimulated guinea-pig ileum in vitro, also reduces the size of
the contraction of the smooth muscle induced by exogenous acetylcholine. This shows
that the oil is not affecting nerve conduction (local anaesthetic action) or the release of
acetylcholine (as seen with opioids such as morphine) but is acting directly on the
smooth muscle. All samples studied have a myogenic action.
Atropine-like action
The concentration of Pelargonium oil, which reduces the size of the contraction of
the smooth muscle to acetylcholine, has a similar effect on the contraction due to

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Stephen Hart and Maria Lis-Balchin

exogenous histamine. If the essential oil contains an atropine-like compound the


response to histamine would be unaffected by a concentration of the oil which reduces
the response to acetylcholine: as this did not occur it can be concluded that the oil does
not contain an atropine-like compound and that it is relaxing the smooth muscle by
some other mechanism. None of the extracts studied have been reported to possess
atropine-like activity (Tables 12.1 and 12.2).
Adrenoceptor mediated response
The presence of an adrenoceptor agonist in the essential oil would explain the
relaxation of the intestinal smooth muscle and such activity would be sensitive to
inhibition by a combination of - and -adrenoceptor antagonists. A concentration of
phentolamine and propranolol, which inhibits the spasmolytic action of exogenous
noradrenaline, has no effect on the inhibition of the contraction of the field-stimulated
guinea-pig ileum produced by the Pelargonium oils. The Pelargonium essential oils
do not, therefore, appear to contain a substance which stimulates adrenoceptors
(Tables 12.1 and 12.2).
Geranium oil
0.1 ml diluted 1000

Washout
0.1 ml diluted 1000
Tre Geranium oil

Washout

Figure 12.2 Mode of action of Geranium oil on the guinea-pig ileum in vitro: the enhancement of
spasmolysis following the application of trequensin, a phosphodiesterase inhibitor,
suggesting that cAMP is involved. Tre trequensin addition.

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Pharmacology of Pelargonium essential oils and extracts

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Involvement of cyclic adenosine monophosphate (cAMP)


The relaxation of intestinal smooth muscle, which occurs as a result of adrenoceptor
activation, is mediated by an increase in the level of cAMP as a result of the stimulation
of adenylate cyclase. The duration of action of the cAMP so produced is limited by its
metabolism by phosphodiesterase. It is thus possible that the essential oil contains a
substance which is capable of stimulating adenylate cyclase in which case the spasmolytic
action would be expected to be potentiated by a phosphodiesterase inhibitor.
Several phosphodiesterase inhibitors are available and they may be classified by their
selectivity in inhibiting the seven or so different isoenzymes of phosphodiesterase which
have been identified. Theophylline and trequinsin are non-selective inhibitors whilst
rolipram (Banner et al., 1995) and CDP 840 (Hughes et al., 1996) inhibit the type IV
isoenzyme.
Many of the Pelargonium oils and some of their components appear to mediate a
spasmolytic action on intestinal smooth muscle via a rise in cAMP (Tables 12.1 and 12.2,
Lis-Balchin et al., 1998). Thus a concentration of trequinsin, which potentiates the
response of isoprenaline from 22.6 to 41.8 per cent (per cent inhibition of twitch response
to electrical stimulation), potentiates the spasmolytic activity of Geranium oil from 14.1
to 30.4 (Figure 12.3). Some, such as rose oxide and damascenone, were potentiated by the
phosphodiesterase inhibitor but the potentiation did not reach statistical significance.
Involvement of cyclic guanosine monophosphate (cGMP)
Sodium nitroprusside, and other compounds which lead to the local production of
nitric oxide, produce a spasmolytic action which is mediated by an increase in cGMP
as a result of the stimulation of guanylate cyclase by nitric oxide. A further possible
mechanism of action for the Pelargonium oils is therefore via the stimulation of
guanylate cyclase, a mechanism which is sensitive to inhibition by ODQ (1H-(1,2,4)
oxadia-zolo (4,3-) quinoxalin-1-one) (Garthwaite et al., 1995). A concentration of
ODQ which blocks the spasmolytic action of sodium nitroprusside has no effect on the
activity of Pelargonium essential oils or their components.
Calcium channel blockade
Intestinal smooth muscle contraction involves the influx of calcium ions through
L-type channels and calcium channel blockers, such as verapamil and nifedipine,
which are used therapeutically for their ability to block calcium channels in vascular
and cardiac muscle, have a spasmolytic effect on intestinal smooth muscle. It is
therefore possible that the essential oils contain components capable of blocking calcium channels.
There are several methods by which possible calcium channel blockade can be identified and in each method one uses an accepted calcium channel blocker as a positive
control. Such screening methods have been reviewed by Neuhaus-Carlisle et al. (1997)
and Vuorela et al. (1997) but neither group mention Pelargonium oils.
When normal Krebs solution is replaced by calcium-free Krebs solution the contraction due to field stimulation is lost but returns gradually when the tissue is
returned to normal Krebs solution. The rate of recovery of the twitch is delayed by
the presence of a calcium channel blocking agent, thus in the presence of nifedipine

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Stephen Hart and Maria Lis-Balchin

100

Geranium oil effect on guinea-pig ileum

% Inhibition

80

60

Geranium oil on
FS-GPI

40

Geranium oil on
Ca-Contraction

20
0
0.0

4.6

Log dose

4.3

4.0

Figure 12.3 The effect of Geranium oil on field-stimulated guinea-pig ileum (FS-GPI) under normal
physiological conditions and on calcium induced contractions in depolarising-Krebs
solution. The graph shows that the spasmolytic action of Geranium oil is only partly
explained by calcium channel blockade.

(106 M) recovery of the twitch is delayed from 8.6 1.9 min to 30 5.3 min.
Pelargonium oils, at concentrations which inhibit the twitch and are potentiated
by a phosphodiesterase inhibitor, do not delay the recovery (Lis-Balchin et al.,
1998).
When guinea-pig ileum is bathed with a depolarising-Krebs solution the addition of
calcium chloride solution produces dose-related contractions that are sensitive to
inhibition by calcium channel blockers. Nifedipine (4.105 M) inhibits the calcium

Table 12.5a Evidence for use of Ca channel blocking


Plant

Extract

Ardwick Cinnamon
P. odoratissimum
P. graveolens
G. robertianum

EO
MeOH extract
MeOH extract
Hydrosol

Table 12.5b No evidence for use of Ca channel blocking at normal concentrations
Plant

Extract

Sweet Mimosa
Attar of Roses
Lady Plymouth
P. graveolens
P. odoratissimum
Ardwick Cinnamon

MeOH extract and hydrosol and EO


MeOH extract and hydrosol and EO
MeOH extract and EO
Hydrosol and EO
Hydrosol and EO
Hydrosol and EO

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contraction by 84 per cent whilst Geranium oil, at a concentration which produces a


significant inhibition of the twitch response (8.106 w/v), has no effect. However, at
higher concentrations of Geranium oil there is evidence of calcium block with 2.105
giving 56 per cent inhibition (Figure 12.3) with a complete block occurring at 2.104
(Lis-Balchin and Hart, 2000).
Recent preliminary studies using methanolic and water extracts of various
Pelargonium species and cultivars have shown that there is some evidence for calcium
channel blockage by P. odoratissimum and P. graveolens methanolic extracts as well as the
Ardwick cinnamon essential oil and methanolic extract, whilst the latters hydrosol
did not exhibit this action (Table 12.5a, b). The different extracts tested of Sweet
Mimosa, Attar of Roses, Lady Plymouth, and the hydrosols of P. odoratissimum and
P. graveolens did not show this effect either (Table 12.5b). The essential oils of the last
mentioned pelargoniums had previously all shown that they mediate their activity via
cAMP (Lis-Balchin et al., 1998).

Potassium channel opening


Some drugs which are used therapeutically to relax vascular smooth muscle act by
opening potassium channels and thereby hyperpolarise the cell. Cromokalim is such a
compound and it has a spasmolytic action on intestinal smooth muscle thus emphasising
another possible mode of action for the spasmolytic action of Pelargonium essential oils.
In the presence of a potassium channel opener, guinea-pig ileum will not respond to
a high concentration of potassium (60 mM) with a contraction. If tissue is contracted
with a high concentration of potassium then a relaxation can be obtained with a
calcium channel blocker but not with a potassium channel opener. There is no experimental evidence to suggest that Pelargonium oils contain components capable of opening potassium channels (Lis-Balchin et al., 1998).

SPASMOGENIC ACTION ON GUINEA-PIG ILEUM

The oil of P. grossularioides and some components of Pelargonium oils, namely citronellyl formate, - and -pinene are spasmogenic on guinea-pig ileum. Provisional results
show that -pinene is not acting via muscarinic cholinoceptors or histamine receptors
and that the two enantiomers of -pinene do not have identical pharmacological
activity (Lis-Balchin et al., 1999).
Recent studies on freshly-prepared hydrophilic extracts and methanolic extracts have
shown that many scented Pelargonium species and cultivars have a spasmogenic effect
initially, followed by a relaxation (Table 12.4). This suggests that some of the many
phenolic components may produce this spasmogenic effect. It also appears that there
could be some residual essential oil components present in all these extracts, but even
the unscented Appleblossom cultivar, which in previous experiments had shown only
a spasmolytic effect (Table 12.3) now showed this dual effect; this was probably due to
two reasons, one being that the samples had previously been stored for many months in
a refrigerator and personal experience has indicated that spasmolytic components
disappear quite rapidly under these conditions and secondly the samples were studied
at very low concentrations, where the contraction does not show up.

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EXPERIMENTS ON IN VITRO UTERINE PREPARATIONS

Method
Uterus from a freshly killed rat is mounted in an organ bath containing Krebs solution
maintained at 37 C and gassed continually with 95 per cent oxygen in carbon dioxide.
Activity of the tissue is monitored with an isometric force transducer connected to a
pen recorder. Uterine tissue may be quiescent but usually exhibits regular contractions
and relaxations, after a short period of equilibration, depending upon the oestrus cycle
of the rat. The ability of an essential oil to increase or decrease the overall activity of the
uterus is readily demonstrated but the elucidation of the mode of action is not as
straightforward as with intestinal tissue.
General action on uterus
The essential oil of P. grossularioides stimulates contraction and relaxation of quiescent uterus for as long as it is in contact with the tissue. When added to tissue which
is contracting and relaxing regularly, the oil produces a maintained contraction
followed by an increase in pendular activity after washout (Lis-Balchin and Hart,
1994).
Geranium oil and geraniol both reduce uterine activity at concentrations which are
spasmolytic on intestinal muscle (Lis-Balchin and Hart, 1997) but the mechanism of
action has not been studied (Figure 12.4).

Geranium oil
0.1 ml 100 dilution

Figure 12.4 The effect of Geranium oil on the spontaneously contracting uterus of the rat in vitro,
showing the inhibition of contractions, which at higher Geranium oil concentrations
actually ceased altogether.

EXPERIMENTS ON IN VITRO BRONCHIAL PREPARATIONS

Method
Activity on bronchial muscle is usually studied on guinea-pig tracheal muscle which is
cut transversally to produce rings which are then tied together and mounted in an

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organ bath. An alternative preparation, which reduces the involvement of cartilage, is


favoured by Reiter and Brandt (1985).
General actions on bronchial muscle
Reiter and Brandt (1985) reported the actions of several essential oils and their
components on tracheal and intestinal smooth muscle including some components of
Pelargonium oils but not the oil itself. Citronellal, citronellol, geraniol and linalool are
all spasmolytic with intestinal muscle being more sensitive than tracheal. Linalool is
one of many components of essential oils studied by Brandt (1988) and was found to
be spasmolytic on guinea-pig ileum and trachea. - and -pinene also relax guinea-pig
tracheal muscle (Lis-Balchin and Hart, 2000).
EXPERIMENTS ON IN VITRO CARDIAC PREPARATIONS

Method
A heart from a freshly killed rat or rabbit can be perfused with Krebs solution through
the aortic arch by the method of Langendorf (1895) and the overall activity recorded by
attaching a thread from the ventricles to a transducer. The perfused heart remains viable
for several hours and the effect of essential oils on rate and force can be assessed on
addition to the perfusion fluid and the mode of action investigated by the use of
standard antagonists.
Alternatively, the auricles can be dissected from the heart and set up in an organ bath
in a manner similar to that used for intestinal tissue.
General action on cardiac tissue
The essential oil of P. grossularioides has been reported to reduce the force of contraction
of the spontaneously beating perfused isolated heart (Lis-Balchin and Hart, 1994).
EXPERIMENTS ON IN VITRO SKELETAL MUSCLE PREPARATIONS

Method
It is more difficult to study skeletal muscle than smooth muscle in vitro because preparations of the former are usually thicker and do not remain viable in the organ bath. Two
preparations which are successful are the chick biventer cervices and the rat phrenic
nerve hemi-diaphragm.
The diaphragm with attached phrenic nerves is dissected from a freshly killed rat
and the diaphragm cut in half to give two preparations that are mounted in a 50 ml
organ bath on a support which keeps the diaphragm secure and enables the stimulation of the phrenic nerve (Bulbring, 1946). Stimulation of the phrenic nerve (0.1 Hz,
5 ms, 20 V) causes regular and reproducible contractions of the diaphragm which are
recorded via a transducer and pen recorder. The introduction of an essential oil into
the organ bath during stimulation can raise the tone of the tissue and/or affect the size
of the nerve induced contraction. It is also possible to stimulate the muscle directly

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Stephen Hart and Maria Lis-Balchin

which allows differentiation between compounds acting via the nerve or directly on
the muscle.
General action on skeletal muscle
The essential oil of P. grossularioides increases the tone of the rat diaphragm and reduces
the size of the contraction in response to stimulation of the phrenic nerve and also
when the muscle is stimulated directly (Lis-Balchin and Hart, 1994). Thus the action
is myogenic but the mechanism has not been studied. The commercial Geranium oil,
on the other hand, decreased the tone and did not alter the size of contraction
(Figures 12.5a,b).

Geranium oil
0.2 ml 25 dilution

Figure 12.5a The action of Geranium oil on skeletal muscle using the chick biventer muscle
preparation in vitro. This shows an inhibition of electrically-stimulated contractions
with a rise in the baseline.

Geraniol
0.2 ml 25 dilution

Figure 12.5b The action of geraniol on the skeletal muscle showing a spasmolytic action with no rise
in the baseline at the same concentration as that of Geranium oil.

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RECEPTOR BINDING STUDIES

A precise method of determining whether a compound interacts with a receptor is by


ligand binding studies in which the ability of the compound to displace a radio-labelled
ligand from the receptor is measured. The receptors are present on membranes which
are often prepared from a specific brain region. Such experiments could be performed
with the individual components of an essential oil but not on the oil itself.
Elisabetsky et al. (1995) report that linalool produces a dose-dependent inhibition of
the binding of glutamate (an excitatory neurotransmitter in the brain) to its receptors
on membranes prepared from the cerebral cortex of the rat. The authors propose that
this action is consistent with their observation that linalool is sedative in animals.

EXPERIMENTS IN VIVO

Cardiovascular system
Geranium oil and the components geraniol, linalool and citronellol produce a fall in
blood pressure in experimental animals (Tisserand and Balacs, 1995) but reliable
observations from human experiments are not available.
Central nervous system
Inhalation of vapour from essential oils affects overall activity of mice and although
Pelargonium oils do not appear to have been studied, geraniol, linalyl acetate and
citronellal are sedative (Buchbauer et al., 1993).
In humans, exposure to the vapour of Pelargonium oils affects certain brain waves
(contingent negative variation, CNV) but both depression and stimulation have been
reported (Torii et al., 1988; Manley, 1993).
General activity
Pelargonium oils have not been the subject of well controlled clinical trials for either
the inhalation of the vapour or application through massage.

CONCLUSION

Results from experiments on isolated guinea-pig ileum demonstrate that the majority of
Pelargonium oils, and their components, produce a relaxation of smooth muscle through
a mechanism that involves the enzyme adenylate cyclase and a rise in the concentration
of the second messenger, cAMP. There is some evidence of calcium channel blockade but
only at concentrations higher than those required to produce a significant spasmolytic
effect. This is in contrast to other essential oils, such as peppermint oil, for which there
is good evidence of calcium channel blockade (Hills and Aaronson, 1991). The pharmacology of the central actions of Pelargonium has not been studied sufficiently to reach any
conclusions. Preliminary results using more hydrophilic extracts of Pelargonium species
and cultivars (using methanol and water) indicate that most have a contractile effect

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Stephen Hart and Maria Lis-Balchin

initially which is followed by a relaxation. There is also some evidence that a few
methanolic extracts use calcium channels at normal concentrations, but many have
shown no such activity, in keeping with the mode of action of their equivalent essential oils.
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Brandt, W. (1988) Spasmolytische wirkung atherischer Ole. Zeit. Phytother., 9, 3339.
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Bioactive Volatile compounds from plants, ACS symposium series 525. Washington, DC,
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Bulbring, E. (1946) Observations on the isolated phrenic nerve diaphragm preparation of the
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Elisabetsky, E., Marschner, J. and Souza, D.O. (1995) Effects of linalool on glutamatergic system
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Garthwaite, J., Southam, E., Boulton, C.L., Nielsen, E.B., Schmidt, K. and Mayer, B. (1995)
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Oxadiazolo[4,3-a]quinoxalin-1-one. Mol. Pharmacol., 48, 184188.
Gunn, J.W.C. (1921) The carminative action of volatile oils. J. Pharmacol., 16, 3947.
Hills, J.M. and Aaronson, P.I. (1991) The mechanism of action of peppermint oil on gastrointestinal smooth muscle. An analysis using patch clamp eletrophysiology and isolated tissue
pharmacology in rabbit and guinea pig. Gastroenterol., 101, 5565.
Hughes, B., Howat, D., Lisle, H., Holbrook, M., James, T., Gozzard, N., Blease, K., Highes,
P., Kingaby, R., Warrellow, G., Alexander, R., Head, J., Boyd, E., Eaton, M., Perry,
M., Wales, M., Smith, B., Owens, R., Catterall, C., Lumb, S., Russell, A., Allen, R.,
Merriman, M., Bloxham, D. and Higgs, G. (1996) The inhibition of antigen-induced
eosinophilia and bronchoconstriction by CDP840, a novel stereo-selective inhibitor of
phosphodiesterase type 4. Br. J. Pharmacol., 118, 11831191.
Imaseki, I. and Kitabatake, Y. (1962) Studies on effect of essential oils and their components on
the isolated intestines of mice. J. Pharmaceut. Soc. Jpn., 82, 13261328.
Kitchen, I. (1984) Textbook of in vitro practical pharmacology. Blackwell Scientific
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Langendorff (1895) Pflugers Arch ges Physiol., 190, 280.
Lis-Balchin, M. (1988) The commercial usefulness of the Geraniaceae, including their potential
in the Perfumery, Food manufacture and Pharmacological industries. Proc. Inc. Geraniaceae
Symp., Stellenbosch, South Africa, 2426 Sept., pp. 269277.
Lis-Balchin, M. (1997) A chemotaxonomic study of Pelargonium (Geraniaceae) species and their
modern cultivars, J. Hort. Sci., 72, 791795.
Lis-Balchin, M. and Hart, S. (1994) A pharmacological appraisal of the folk medicinal usage of
Pelargonium grossularioides and Erodium cicutarium (Geraniaceae). J. Herbs, Spices Med. Plants, 2,
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Lis-Balchin, M. and Hart, S. (1997) Pharmacological effect of essential oils on the uterus
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Ch. Franz, A. Math and G. Buchbauer, (eds) Allured Pub. Corp., Carol Stream, Ill. 2932.
Lis-Balchin, M. and Hart, S. (1998) Studies on the mode of action of essential oils of scentedleaf Pelargonium (Geraniaceae). Phytother. Res., 12, 215217.

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Lis-Balchin, M. and Hart, S. (2000) Unpublished observations.


Lis-Balchin, M., Deans, S.G. and Hart, S. (1996a) Bioactivity of Geranium oils from different
commercial sources. J. Essent. Oil Res., 8, 281290.
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Lis-Balchin, M., Houghton, P. and Woldernarian, T. (1996c) Elaeocarpidine alkaloids from
Pelargonium species (Geraniaceae). LAM, 23, 205207.
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scented Pelargoniums (Geraniaceae). Phytother. Res., 11, 583584.
Lis-Balchin, M., Patel, J. and Hart, S. (1998) Studies on the mode of action of essential oils of
scented-leaf Pelargonium (Geraniaceae). Phytother. Res., 12, 215217.
Lis-Balchin, M., Ochocka, R.J., Deans, S.G., Asztemborska, M. and Hart, S. (1999) Differences
in bioactivity between the enantiomers of -pinene. J. Essent. Oil Res., 11, 393397.
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Neuhaus-Carlisle, K., Vierling, W. and Wagner, H. (1997) Screening of plant extracts and plant
constituents for calcium-channel blocking activity. Phytomedicine, 4, 6769.
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Pappe, L. (1868) Florae Capensis Medicae, Prodromus, 3rd ed., Cape Town.
Reiter, M. and Brandt, W. (1985) Relaxant effects on tracheal and ileal smooth muscles of the
guinea-pig. Arzneim. Forsch/Drug Res., 35, 408414.
Sticher, O. (1977 ) Plant mono-, di- and sesquiterpenoids with pharmacological or therapeutical activity. In: H. Wagner and P. Wolf (eds), New natural products and plant drugs with
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Tisserand, R. and Balacs, T. (1995) Essential oil safety. Churchill Livingstone, London.
Torii. S., Fukuda, H., Kanemoto, H., Miyanchio, R., Hamauzu, Y. and Kawasaki, M. (1988)
Contingent negative variation and the psychological effects of odor. In S. Toller and
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Triebs, W. (1956) Die Atherischen Ole, Akademie-Verlag, Berlin.
Vuorela, H., Vuorela, P., Tornquist, K. and Alaranta, S. (1997) Calcium channel blocking
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Ltd, Edinburgh.

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13 Antimicrobial properties of
Pelargonium extracts contrasted
with that of Geranium
Stanley G. Deans

INTRODUCTION

The preservative properties of aromatic and medicinal plant volatile (essential) oils and
extracts have been recognised since Biblical times, while attempts to characterise these
properties in the laboratory date back to the 1900s (Martindale, 1910; Hoffman and
Evans, 1911).
Plant volatile oils
Plant volatile oils are generally isolated from non-woody plant material by steam or
hydrodistillation, and are variable mixtures of principally terpenoids, specifically
monoterpenes (C10) and sesquiterpenes (C15) although diterpenes (C20) may also be
present, and a variety of low molecular weight aliphatic hydrocarbons (linear, ramified,
saturated and unsaturated), acids, alcohols, aldehydes, acyclic esters or lactones and
exceptionally nitrogen- and sulphur-containing compounds, coumarins and homologues
of phenylpropanoids.
Terpenes are amongst the chemicals responsible for the culinary, medicinal and
fragrant uses of aromatic and medicinal plants. Most terpenes are derived from the condensation of branched five-carbon isoprene units and are categorised according to the
number of these units in the carbon skeleton (Dorman, 1999). Traditionally, plants
and their extracts, including geranium (Pelargonium sp.) (Geraniaceae) have been used to
extend the shelf life of foods, beverages and pharmaceutical/cosmetic products through
their antimicrobial and antioxidant properties (Baratta et al., 1998a,b; Cai and Wu,
1996; Gallardo et al., 1987; Janssen et al., 1988; Jay and Rivers, 1984; Plissier et al.,
1994; Shapiro et al., 1994; Shelef, 1984; Ueda et al., 1982; Youdim et al., 1999).
More recently, attempts have been made to identify the component(s) responsible for
such bioactivities (Daferera et al., 2000; Deans and Ritchie, 1987; Deans et al., 1994a,
b; Dorman and Deans, 2000; Jeanfils et al., 1991; Lis-Balchin, 1997; Lis-Balchin and
Deans, 1997; Lis-Balchin et al., 1998a; Vokou et al., 1993). The antimicrobial properties of volatile oils and their constituents from a wide variety of plants have been
assessed and reviewed (Carson et al., 1995, 1996; Garg and Dengre, 1986; Inouye et al.,
1983; Jain and Kar, 1971; Janssen et al., 1987; Larrondo et al., 1995; Nenoff et al.,
1996; Pattnaik et al., 1995, 1996; Rios et al., 1987, 1988; Sherif et al., 1987).
Investigations into the antimicrobial activities, mode of action and potential uses of

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133

plant volatile oils have regained momentum and there appears to be a revival in the use
of traditional approaches to livestock welfare as well as food preservation. The activity
of the oils would be expected to relate and reflect the respective composition of the
volatile oils, the structural configuration of the constituent components and their
functional groups along with potential synergistic interactions between components.
A correlation of the antimicrobial activity of compounds under test in the study by
Dorman and Deans (2000) and their relative percentage composition in the oils, with
their chemical structure, functional groups and configuration suggested a number of
observations on the structurefunction relationship.
Components with phenolic structures, such as carvacrol and thymol, were highly active
against test bacteria, despite their low capacity to dissolve in water. The importance of the
hydroxyl group in the phenolic ring was confirmed in terms of activity when carvacrol
was compared to its methyl ester. The high activity of the phenolic components may be
further explained in terms of the alkyl substitution into the phenolic nucleus, which is
known to enhance the antimicrobial activity of phenols (Pelczar et al., 1988). The
introduction of alkylation has been proposed to alter the distribution ratio between the
aqueous and non-aqueous phases, including bacterial phases, by reducing the surface
tension or altering the species selectivity. Alkyl-substituted phenolic compounds form
phenoxyl radicals which interact with isomeric alkyl substituents (Pauli and Knobloch,
1987). This does not occur with etherified/esterified isomeric molecules, possibly
explaining their relative lack of activity.
The presence of an acetate moiety in the structure appears to increase the activity of
the parent compound as in the case of geraniol where geranyl acetate demonstrated an
increase in activity. Aldehydes, notably formaldehyde and glutaraldehyde, are known to
possess powerful antimicrobial activity. It has been suggested that an aldehyde group
conjugated to a C C is a highly electronegative arrangement which may explain their
activity (Moleyar and Narasimham, 1986), suggesting an increase in electronegativity
increases the antibacterial activity (Kurita et al., 1979, 1981). Such electronegative
compounds may interfere in biological processes involving electron transfer and react with
vital nitrogen components such as proteins and nucleic acids, and therefore inhibit growth
of the microorganisms. The aldehydes cis and trans citral displayed moderate activity
against test bacteria while citronellal was less active. Alcohols are known to possess
bactericidal rather than bacteriostatic activity against vegetative bacterial cells. The
alcohol terpenoids studied did show some activity against test bacteria, acting as
protein denaturing agents, solvents or dehydrating agents.
A number of oil components are ketones, wherein the presence of an oxygen function
in the framework increases the antimicrobial properties of the terpenoids (Naigre et al.,
1996). From this study, and by using the contact method, the bacteriostatic and
fungistatic action of terpenoids was increased when carbonylated. Menthone was shown
to have modest activity with Clostridium sporogenes and Staphylococcus aureus being the
most significantly affected (Dorman and Deans, 2000). An increase in activity
dependant upon the type of alkyl substituent incorporated into a non-phenolic ring
structure appeared to occur in this study. An alkenyl substituent [1-methylethenyl]
resulted in increased antibacterial activity, as seen in limonene [1-methyl-4(1-methylethenyl)-cyclohexene], compared to an alkyl [1-methylethyl] substituent as
in p-cymene [1-methyl-4-(1-methylethyl)-benzene]. The inclusion of a double bond
increased the activity of limonene relative to p-cymene, which demonstrated no activity
against the test bacteria. In addition, the susceptible organisms were principally

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Stanley Deans

Gram-negative, which suggests alkylation influences Gram reaction sensitivity of the


bacteria. The importance of the antimicrobial activity of alkylated phenols in relation
to phenol has been previously reported (Pelczar et al., 1988). Their data suggest that an
allylic side chain seems to enhance the inhibitory effects of a component and chiefly
against Gram-negative organisms.
Furthermore, the stereochemistry has an influence on bioactivity. It was observed
that -isomers are inactive relative to -isomers, for example, -pinene; cis-isomers are
inactive contrary to trans-isomers, for example geraniol and nerol; compounds with
methyl-isopropyl cyclohexane rings are most active; or unsaturation of the cyclohexane
ring further increases the antibacterial activity, for example terpinolene, terpineol and
terpineolene (Hinou et al., 1989).
Investigations into the effects of terpenoids upon isolated bacterial membranes
suggest that their activity is a function of the lipophilic properties of the constituent
terpenes, (Knobloch et al., 1986), the potency of their functional groups and their
aqueous solubility (Knobloch et al., 1988). Their site of action appeared to be at the
phospholipid bilayer, caused by biochemical mechanisms catalysed by these
phosholipid bilayers of the cell. These processes include the inhibition of electron
transport, protein translocation, phosphorylation steps and other enzyme-dependant
reactions (Knobloch et al., 1986). Their activity in whole cells appears more complex
(Knobloch et al., 1988). Although a similar water-soluble tendency is observed,
specific statements on the action of single terpenoids in vivo have to be assessed
singularly, taking into account not only the structure of the terpenoid, but also the
chemical structure of the cell wall (Knobloch et al., 1988). The plant extracts clearly
demonstrate antibacterial properties, although the mechanistic processes are poorly
understood.
Chemotherapeutic agents, used orally or systemically for the treatment of microbial
infections of humans and animals, possess varying degrees of selective toxicity.
Although the principle of selective toxicity is used in agriculture, pharmacology and
diagnostic microbiology, its most dramatic application is the systemic chemotherapy of
infectious diseases. The tested plant products appear to be effective against a wide
spectrum of microorganisms, both pathogenic and non-pathogenic. Administered
orally, these compounds may be able to control a wide range of microbes, but there is
also the possibility that they may cause an imbalance in the gut microflora, allowing
opportunist pathogenic bacteria, such as coliforms, to become established in the
gastrointestinal tract with resultant deleterious effects. Further studies on therapeutic
applications of volatile oils should be undertaken to investigate these issues, especially
when consideration is made of the substantial number of analytical/bioactivity studies
carried out on these natural products.

ANTIMICROBIAL ACTIVITY

Real Geranium species in contrast to Pelargonium species


There is a great difference in the chemical composition and bioactivity between the true
Geranium and Pelargonium species. The commercial Geranium oil is in fact obtained
from a Pelargonium cultivar and there is, therefore, great confusion in the literature
regarding the actual species studied (see General Introduction).

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In the past only Geranium species e.g. G. robertianum not Pelargonium have been studied
and it was reported in various herbals that these Geranium species were useful as an
astringent and tonic, in the treatment of diarrhoea, cholera and chronic dysentery
(Grieve, 1994). The volatile oil of Geranium species has been attributed a number of
biological properties including: antibacterial (Ivancheva et al., 1992; Pattnaik
et al., 1996), antifungal (Pattnaik et al., 1996) and antiviral (Zgorniak-Nowosielska
et al., 1989; Ivancheva et al., 1992; Serkedjieva, 1995) and also some other pharmacological properties (Petkov et al., 1974; Manolov et al., 1977). Recent studies have shown
that root extracts from Geranium pratense exhibited antimicrobial activity against
Streptomyces scabies (Ushiki et al., 1996) and these authors later reported on the isolation
of an antimicrobial substance, geraniin, at approximately 15 per cent root dry weight
based on quantitative analysis by high-performance liquid chromatography (HPLC), and
its antimicrobial activity corresponded to 1.25 per cent of that of streptomycin, based on
the paper-disc assay. These findings suggest that G. pratense has potential agronomic
applications as an organic amendment or companion crop for the control of common scab
of potato (Ushiki et al., 1998).
Polyphenolic complex (PC)

Studies on PC have now shown activity against herpes simplex, vaccinia and HIV-I
in cell cultures. PC has also been shown to inhibit the in vitro growth of Staphylococcus aureus and Candida albicans (Serkedjieva, 1997). High concentrations of PC
( 200 g/mL) exhibited a strong virucidal effect. Although the action was directed
against an early stage of infection (within 3 h of infection), the process affected was not
identified. The selectivity of antiviral action was confirmed by the variation in sensitivity of different influenza viruses to PC and the selection of variants with reduced
drug sensitivity (Serkedjieva and Hay, 1998). The aqueous extract from aerial roots
was the least toxic for cell cultures, yet significantly inhibited the replication of herpes
simplex virus (Serkedjieva and Ivancheva, 1999). Okuda et al. (1992) report on antitumour as well as antiviral activities of numerous polyphenolic compounds isolated
from a number of Asian plants including Geranium thunbergii.
Finally, the antiviral properties of the polyphenol complex (PC) isolated from Geranium
sanguineum have received considerable attention from the Bulgarian Academy of Science
group. Ivancheva et al., 1987 and Serkedjieva and Manolova, 1988 determined the chromatographic characteristics of the complex shown to possess antiviral activity. A later
study was undertaken to investigate the effect of PC on virus-specific protein synthesis in
influenza virus-infected cells, where it was found that the expression of viral glycoproteins
on the surface of chick embryo fibroblasts infected with such viruses was suppressed
(Serkedjieva, 1995). The inhibitory effect was dose-dependant and more pronounced
when PC was applied post-viral infection. The studies have been extended to human and
equine influenza viruses where it was shown that the inhibitory effect was strain-related,
and consistent with a selective antiviral action (Serkedjieva, 1996).
Pelargonium species

In one of the larger studies in this field, Deans and Ritchie (1987) studied 50
commercial volatile oils at four concentrations against a range of 25 bacterial genera. In
the case of Geranium oil, it was found to be most effective against the dairy products

2002 Edited by Taylor & Francis

136

Stanley Deans
Table 13.1 Antibacterial activity of geranium volatile oil against 25 test
bacteria. Inhibition zone diameter in mm, including well diameter
of 4 mm. Each value is the mean of three replicates
Organism

Source*

Inhibition zone

Acinetobacter calcoacetica
Aeromonas hydrophila
Alcaligenes faecalis
Bacillus subtilis
Beneckea natriegens
Brevibacterium linens
Brocothrix thermosphacta
Citrobacter freundii
Clostridium sporogenes
Enterobacter aerogenes
Enterococcus faecalis
Erwinia carotovora
Escherichia coli
Flavobacterium suaveolens
Klebsiella pneumoniae
Lactobacillus plantarum
Leuconostoc cremoris
Micrococcus luteus
Moraxella sp.
Proteus vulgaris
Pseudomonas aeruginosa
Salmonella pullorum
Serratia marcescens
Staphylococcus aureus
Yersinia enterocolitica

NCIB 8250
NCTC 8049
NCIB 8156
NCIB 3610
ATCC 14048
NCIB 8456
Sausage meat
NCIB 11490
NCIB 10696
NCTC 10006
NCTC 775
NCPPB 312
NCIB 8879
NCIB 8992
NCIB 418
NCDO 343
NCDO 543
NCIB 8165
NCIB 10762
NCIB 4175
NCIB 950
NCTC 10704
NCIB 1377
NCIB 6571
NCTC 10460

11.5
9.0
6.0
4.0
6.5
12.0
5.5
9.0
4.0
11.0
4.0
8.5

9.5

7.5
4.0
8.0
10.5
5.0
5.5
6.0
10.0
5.0
13.0

Source: Deans and Ritchie, 1987.


Notes
* NCIB National collection of industrial bacteria; NCTC National collection of
type cultures; ATCC American type culture collection; NCPPB National collection
of plant pathogenic bacteria; NCDO National collection of dairy organisms.
Enhancement of growth.

organism Brevibacterium linens and the toxin-producing Yersinia enterocolitica. With


Klebsiella pneumoniae and Escherichia coli, in contrast, its presence resulted in enhancement of growth (Table 13.1).
Pattnaik et al. (1996) tested Geranium oil for antibacterial activity against 22 bacteria
(Gram-positive cocci and rods, Gram-negative rods) and 12 fungi (three yeast-like, nine
filamentous) by disc diffusion. Only 12 bacterial strains were inhibited by the Geranium
oil, but all the fungi were inhibited.
Differences between samples of Geranium oil

There were significant differences in the chemical composition of a number of


Geranium samples of various geographical origins used as antibacterial agents (LisBalchin et al., 1996c). There was a wide range of citronellol and geraniol levels in
each source category, Reunion, China, Egypt or Morocco, with the ratio of citronellol:geraniol also being very variable, ranging from 1.7 to 10.9. The antibacterial activity

2002 Edited by Taylor & Francis

Antimicrobial properties of pelargoniums

137

against 25 different bacteria also varied between samples of oil, ranging from 8 to 19
inhibited. All samples actively inhibited Clostridium sporogenes, Bacillus subtilis and
Brevibacterium linens, and all but one inhibited Acinetobacter calcoacetica and Staphylococcus
aureus. There were however, differences in the inhibition of all the other organisms which
could not be correlated with the chemical composition of the samples.
The differences in antimicrobial activity reflect those shown for different
Pelargonium species and cultivars. The anti-Listeria action of the Geranium oils was
again very variable, the number of strains affected ranging from 3 to 16 (Lis-Balchin
et al., 1996c). This study highlights the wide variability of biological activity between
commercial samples, which is not directly correlated with the chemical composition.
This can be explained by the following considerations: a high degree of blending,
if not adulteration or the use of synthetics in the commercial oil industry; some of
the samples were diluted when sold; minor components play a substantial part in
biological activities. The study by Lis-Balchin and Deans (1997) indicated
considerable variation in the activity of the same volatile oil, such as that of
Geranium, against different strains of L. monocytogenes, this being in agreement with
the findings of Aureli et al. (1992) and Lis-Balchin et al. (1996a). In the latter
study, 16 Geranium samples were active against 818 of the test bacteria and the
number of active oils against Listeria monocytogenes ranged from 3 to 16 out of a set of
20 bacteria. In the antifungal studies, the Geranium samples varied from 0 to 94 per
cent inhibition of Aspergillus niger, 1295 per cent against A. ochraceus and 4086 per
cent against Fusarium culmorum. This highlights the wide variation within the group
of samples when considering that the samples should be very similar. The adulteration
of volatile oils with synthetic components may give rise to a different proportion of
enantiomers for a large number of components than in a pure botanical sample: this
can greatly influence the bioactivity of the subsequent material (Lis-Balchin
et al., 1996b; 1998a).
These conclusions were in agreement with the results of an earlier study (Lis-Balchin
et al., 1995) wherein 24 cultivars were tested for antimicrobial activity against 25 test
bacteria and Aspergillus niger. Of these test bacteria, the most sensitive bacteria were
Alcaligenes faecalis, Bacillus subtilis, Brevibacterium linens, Brocothrix thermosphactum,
Clostridium sporogenes, Flavobacterium suaveolens and Staphylococcus aureus, a group of
predominantly Gram-positive organisms, whilst the least sensitive organisms were
Aeromonas hydrophila, Beneckea natriegens, Escherichia coli, Klebsiella pneumoniae, Leuconostoc
cremoris and Pseudomonas aeruginosa, a group of predominantly Gram-negative organisms. The inhibition against A. niger ranged from 3 to 98 per cent with two extracts
causing growth enhancement. The activity in some cultivars was attributed to the level
of monoterpenes present.
Synergistic antibacterial agents

In a study into the potential usage of mixtures of plant volatile oils as synergistic
antibacterial agents in foods, Lis-Balchin and Deans (1998) included Geranium oil in
a mixture with nutmeg and bergamot oils. In the case of Bacillus subtilis, the mixture
was more active than Geranium on its own whilst Enterobacter aerogenes was less affected by the mixture compared with Geranium alone. The activity of the mixture was
marginally improved in the case of seven bacteria and lessened in five bacteria with
Serratia marcescens being unchanged (Table 13.2). These results indicate that mixing

2002 Edited by Taylor & Francis

138

Stanley Deans

Table 13.2 Antibacterial activity of geranium volatile oil alone and in combination with nutmeg and
bergamot volatile oils against test bacteria. Inhibition zone diameter in mm, including well
diameter of 4 mm. Each value is the mean of three replicates. Bacterial sources as in Table 13.1
Organism

Geranium

Nutmeg

Bergamot

Mean

Mixture

Aeromonas hydrophila
Bacillus subtilis
Brocothrix thermosphacta
Enterobacter aerogenes
Enterococcus faecalis
Escherichia coli
Lactobacillus plantarum
Leuconostoc cremoris
Micrococcus luteus
Salmonella pullorum
Serratia marcescens
Staphylococcus aureus
Yersinia enterocolitica

7.0
7.3
8.8
5.4
5.6
8.5
5.5
6.2
5.6
4.0
4.0
9.0
6.7

8.6
6.3
8.7
5.7
4.0
6.0
6.3
4.0
4.0
4.0
6.3
4.0
4.0

9.2
11.4
4.0
4.0
17.0
14.1
8.2
5.2
8.2
6.4
6.0
16.4
9.1

8.3
8.3
7.2
5.0
8.9
9.5
6.7
5.1
5.9
4.8
5.4
9.8
6.6

7.6
10.5
7.1
4.0
7.5
5.8
6.8
8.4
5.8
5.6
4.0
7.4
5.7

Source: Lis-Balchin and Deans, 1998.

three oils did not have any real synergistic effect. The chemical components of the
individual oils were diluted by a third in the 1:1:1 mixture and the most active oil
therefore became less potent compared with its solo use. Although there was clearly no
real synergistic antibacterial activity, it may still be reasonable to use mixtures of
volatile oils to lower the individual odour potential when used in processed foodstuffs
as at least some of the mixtures referred to showed a similar net effect compared with
the mean of the individual effects.
Antimicrobial activity of Pelargonium oil components
A number of individual oil components were tested for antibacterial activity (Dorman
and Deans, 2000). In the case of Geranium oil constituents, the ranking order of
activity was linalool (mean inhibition zone diameter of 12.5 mm) geranyl acetate
(9.4 mm) nerol (8 mm) geraniol (7 mm) menthone (6.8 mm) -pinene
(6.3 mm) limonene (6.1 mm) -pinene (5.8 mm). Compared with more phenolic
compounds, these activities are relatively modest. The bacteria showing the greatest
level of inhibition were Clostridium sporogenes (11.5 mm) Lactobacillus plantarum (10.5
mm) Citrobacter freundii (9.9 mm) Escherichia coli (9.6 mm) Flavobacterium
suaveolens (9 mm): all remaining bacteria had mean inhibition zone diameters of
9 mm (Table 13.3).
Antifungal properties of different Pelargonium species and cultivars

In addition to antibacterial activities, Geranium oil also possesses antifungal properties.


Pelargonium  hortorum leaves were reported as being most active against Candida
albicans, Trichophyton rubrum and Streptococcus mutans, organisms causing common
dermal, mucosal or oral infections in humans (Heisey and Gorham, 1992). The action
of 16 samples of Geranium oil against three filamentous fungi was investigated and
revealed a wide range of activities. In the presence of 1 l of Geranium oil per ml of

2002 Edited by Taylor & Francis

Antimicrobial properties of pelargoniums

139

Table 13.3 Antibacterial activity of geranium methanolic extracts against 25 test bacteria. Inhibition zone
diameter in mm, including well diameter of 4 mm. Each value is the mean of three replicates.
Bacterial sources as in Table 13.1
Organism

A*

Acinetobacter calcoacetica
Aeromonas hydrophila
Alcaligenes faecalis
Bacillus subtilis
Beneckea natriegens
Brevibacterium linens
Brocothrix thermosphacta
Citrobacter freundii
Clostridium sporogenes
Enterobacter aerogenes
Enterococcus faecalis
Erwinia carotovora
Escherichia coli
Flavobacterium suaveolens
Klebsiella pneumoniae
Lactobacillus plantarum
Leuconostoc cremoris
Micrococcus luteus
Moraxella sp.
Proteus vulgaris
Pseudomonas aeruginosa
Salmonella pullorum
Serratia marcescens
Staphylococcus aureus
Yersinia enterocolitica

12
19
17
19
10
18
9
11
24
11
15
16
12
20
16
16
17
18
12
16
16
11
20
9
23

11
17
15
17
6
18
13
10
24
10
12
13
9
15
15
14
14
17
10
13
16
10
16
8
20

6
4
6
6
4
7
6
5
5
6
6
6
6
5
4
5
6
6
6
6
5
6
7
6
6

17
13
15
20
4
23
14
13
24
4
18
14
14
15
11
17
14
21
4
26
15
11
20
12
22

11
11
15
16
4
17
10
7
20
4
16
15
8
15
14
13
12
17
4
15
15
12
17
8
20

12
10
15
16
4
17
11
17
18
4
14
16
8
16
15
12
13
17
4
16
15
9
17
9
18

12
8
14
10
6
14
12
4
4
4
13
13
4
15
13
11
11
15
12
8
13
10
16
4
17

10
4
11
7
9
8
8
4
18
4
13
4
4
15
9
5
11
10
8
6
9
4
10
4
9

Source: Lis-Balchin and Deans, 1996.


Notes
* Key to Pelargonium: A P. zonale; B P. inquinans; C P. capitatum; D P. acraem; E White Boar; F P. scandens;
G P. hybridum; H P. cucullatum.

YES broth, Aspergillus niger was inhibited by 094 per cent, A. ochraceus by 1295 per
cent and Fusarium culmorum by 4086 per cent. Correlation between chemical composition and antimycotic activity is not always clear. The test organisms, A. niger,
A. ochraceus and Fusarium culmorum reacted differently to the oils, with the plant pathogenic F. culmorum being less affected, with two exceptions, than the two Aspergilli. The
spoilage organism A. niger was more inhibited in its growth, again with two exceptions,
than the mycotoxigenic A. ochraceus whilst antifungal action was poor with 40 per
cent inhibition. The antioxidant properties of the Pelargonium oils is also given for
these eight methanolic extracts (Table 13.4).
Antioxidant properties of Pelargonium species

Pelargonium species, including the commercial Geranium oil have been shown to have
antioxidative properties (Dorman et al., 2000; Fukaya et al., 1988; Youdim et al., 1999),
though these properties had very variable activities in different commercial samples of
Geranium oil (Lis-Balchin et al., 1996c). Various pharmacological properties have also

2002 Edited by Taylor & Francis

Table 13.4 Antibacterial activity of Pelargonium volatile oils, petroleum ether and methanol extracts
against four bacteria. Inhibition zone diameter in mm, including well of 4 mm. Each value is
the mean of three replicates
Pelargonium type

Extract type

Attar of Roses

Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol

Lady Plymouth
Pink Little Gem
Radula
Robers Lemon Rose
Sweet Mimosa
P. tomentosum
Chocolate Tomentosum
Lemon Fancy
Crispum variegatum
Clorinda
Copthorne
Oak cultivar
Village Hill Oak
P. denticulatum
P.  fragrans

2002 Edited by Taylor & Francis

A*

B*

C*

D*

17
10
4
ND
7
11
ND
13
13
10
4
13
7
7
17
ND
11
12
ND
8
9
ND
13
9
18
8
10
8
7
7
ND
16
11
7
8
17
ND
11
ND
9
4
11
8
4
4
ND
19
16

11
12
8
11
4
12
11
11
16
7
4
13
4
4
20
10
10
17
4
10
10
8
11
12
13
8
11
4
9
10
10
13
11
4
8
16
8
9
ND
8
8
11
7
7
8
9
10
23

12
11
9
7
4
12
8
8
14
8
6
13
4
7
18
7
8
14
6
12
10
8
10
8
9
19
12
4
9
14
11
16
9
4
8
16
11
9
ND
8
8
9
8
8
8
10
17
28

8
10
13
4
4
11
4
4
15
8
4
18
8
4
20
4
4
18
4
11
10
8
8
10
12
8
8
7
8
4
4
11
9
10
9
18
4
6
ND
8
8
12
7
7
7
8
14
19

Antimicrobial properties of pelargoniums

P. odoratissimum
Orsett

Steam distill
Pet ether
Methanol
Steam distill
Pet ether
Methanol

8
ND
ND
ND
12
12

8
ND
ND
10
9
15

8
ND
ND
9
9
11

141

7
ND
ND
4
8
13

Source: Lis-Balchin et al., 1998b.


Notes
* Key to bacteria and their source: A Bacillus cereus NCIMB 6349; B Proteus vulgaris ATCC 13315;
C Staphylococcus aureus ATCC 9144; D Staphylococcus epidermidis ATCC 12228.

been determined for Pelargonium essential oils (Lis-Balchin et al., 1995), which were not
found to be related to the antimicrobial activity to any great extent.
METHANOLIC EXTRACTS OF PELARGONIUM

Bioactivity of methanolic extracts of Pelargonium against


25 species of bacteria
Methanolic extracts of representative species and cultivars of Pelargonium were
assessed for bioactivity against the set of 25 test bacteria (listed in Table 13.1). The
antibacterial of all the extracts was very pronounced (Lis-Balchin and Deans, 1996).
The ranking order of the greatest inhibition of growth was Clostridium sporogenes
(mean inhibition zone diameter of 17.1 mm) Yersinia enterocolitica (16.9 mm)
Serratia marcescens (15.4 mm) Micrococcus luteus (15.1 mm) Flavobacterium
suaveolens (14.5 mm) Bacillus subtilis (13.9 mm) Alcaligenes faecalis (13.5 mm)
Enterococcus faecalis (13.3 mm) ~ Proteus vulgaris (13.3 mm) Pseudomonas aeruginosa (13 mm): all remaining bacteria had mean inhibition zone diameters of
 13 mm. The individual extracts were ranked by activity as P. zonale (15.5 mm)
P. acraem (15.2 mm) P. inquinans (13.7 mm) P. scandens (12.9 mm) White
Boar (12.6 mm) P. hybridum (10.5 mm) P. cucullatum (8.2 mm) P. capitatum
(5.6 mm) (Table 13.5).
Comparison of antibacterial activity between different
extractives of the same Pelargonium
In a similar study, the volatile oil, petroleum spirits and methanol extracts from 18
Pelargonium cultivars were assayed against four bacteria, Bacillus cereus, Proteus vulgaris,
Staphylococcus aureus and Staphylococcus epidermidis. There was considerable variation in
the activity both between the cultivars themselves and the different extraction techniques (Table 13.6) (Lis Balchin et al., 1998b).
In summary, the genus Pelargonium is a rich source of bioactive compounds having
applications as antibacterial, antifungal, and antioxidant agents in addition to their
contribution to the food/beverage, cosmetic and pharmaceutical sectors (Lis-Balchin
et al., 1995; Dorman and Deans, 2000; Pattnaik et al., 1996), whilst Geranium species
are apparently more active as antiviral agents (Serkedjieva, 1996).

2002 Edited by Taylor & Francis

Table 13.5 Antibacterial activity of Geranium oil constituents against 25 test bacteria. Inhibition zone
diameter in mm, including well diameter of 4 mm. Each value is the mean of three replicates.
Bacterial sources as in Table 13.1
Organism

A*

Acinetobacter calcoacetica
Aeromonas hydrophila
Alcaligenes faecalis
Bacillus subtilis
Beneckea natriegens
Brevibacterium linens
Brocothrix thermosphacta
Citrobacter freundii
Clostridium sporogenes
Enterobacter aerogenes
Enterococcus faecalis
Erwinia carotovora
Escherichia coli
Flavobacterium suaveolens
Klebsiella pneumoniae
Lactobacillus plantarum
Leuconostoc cremoris
Micrococcus luteus
Moraxella sp.
Proteus vulgaris
Pseudomonas aeruginosa
Salmonella pullorum
Serratia marcescens
Staphylococcus aureus
Yersinia enterocolitica

6.1
6.4
7.0
6.4
6.2
7.3
7.4
9.2
12.9
6.4
12.9
8.1
9.7
7.0
4.0
6.2
4.0
6.1
6.1
5.6
5.7
6.3
5.7
5.2
8.0

10.3
9.0
10.5
10.8
10.8
12.5
9.2
6.8
20.4
7.6
7.5
8.7
11.0
11.0
7.8
12.9
4.0
8.0
9.0
9.8
6.5
8.7
6.8
6.6
8.2

4.0
4.0
4.0
4.0
4.0
4.0
4.0
7.8
10.3
7.1
4.0
7.4
11.2
10.6
7.0
4.0
4.0
4.0
7.9
7.4
4.0
11.2
6.5
4.0
7.1

9.3
11.5
12.1
14.0
11.4
12.5
8.1
27.5
20.3
9.7
16.7
12.3
13.8
15.7
12.6
25.3
4.0
13.4
10.3
12.2
4.0
7.5
8.8
9.0
9.5

9.7
7.0
6.2
7.1
5.9
4.0
6.8
7.8
10.7
6.3
4.0
6.5
6.6
5.8
5.9
8.8
4.0
7.1
6.9
6.2
4.0
6.2
7.1
10.2
8.0

11.4
7.7
7.1
12.4
11.3
11.7
9.0
7.8
4.0
7.2
4.0
7.7
7.6
7.0
4.0
19.1
4.0
7.4
4.0
4.0
13.6
4.0
8.5
9.4
7.1

4.0
4.0
4.0
4.0
4.0
4.0
4.0
6.0
5.7
4.0
9.2
8.7
8.9
6.5
8.1
4.0
4.0
7.6
6.2
7.5
4.0
7.9
4.0
8.3
6.6

11.2
7.1
7.8
4.0
6.5
4.0
5.9
5.9
7.5
4.0
7.8
4.0
7.8
8.4
7.9
4.0
4.0
6.3
4.8
6.6
6.5
6.0
5.4
7.4
5.8

Source: Dorman and Deans, 2000.


Notes
* Key to compounds: A geraniol; B geranyl acetate; C limonene; D linalool; E menthone; F nerol;
 -pinene;  -pinene.

Table 13.6 Bioactivity of geranium methanolic extracts: antimycotic action against Aspergillus niger at
10 L mL1 YES broth; antioxidant activity expressed as zone of colour retention in mm,
including well diameter of 4 mm, followed by indication of intensity of colour retention on
scale  mild,  moderate,  intense
Pelargonium

Antimycotic inhibition (%*)

Antioxidant activity/intensity

P. zonale
P. inquinans
P. capitatum
P. acraem
White Boar
P. scandens
P. hybridum
P. cucullatum

31
28
36
27
25
38
35
20

16.6
19.5
12.6
18.6
18.3
18.5
21.4
15.4










Source: Lis-Balchin and Deans, 1996.


Note
* Fungal Inhibition Index calculated as (C-T)/C  100 where C is the weight of mycelium from control flasks and
T is the weight of mycelium from test flasks.

2002 Edited by Taylor & Francis

Antimicrobial properties of pelargoniums

143

ACKNOWLEDGEMENTS

SAC received financial support from the Scottish Executive and Executive Rural Affairs
Department.

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14 Essential oils from different


Pelargonium species and cultivars:
their chemical composition (using
GC, GC/MS) and appearance of
trichomes (under EM)
Maria Lis-Balchin

INTRODUCTION

Commercial Geranium oil is obtained from various Pelargonium cultivars (derived


mainly from P. graveolens, P. capitatum and P. radens) growing mainly in Reunion, China
and Egypt. The chemical composition of the oils is variable due to the difference in
cultivars used, the climate (including sunlight, rainfall and temperature), the time of
the harvest, fertilizers applied etc). Geranium oil is used mainly in perfumery, but also
has potent antimicrobial potential (Lis-Balchin et al., 1996). It also has relaxant
pharmacological properties on smooth muscle e.g. guinea-pig ileum and the rat uterus
(Lis-Balchin and Hart, 1997a) as well as striated muscle (Lis-Balchin and Hart, 1997b).
The mode of action of commercial Geranium oil appears to act through cAMP (cyclic
adenosine monophosphate) as the secondary messenger (Lis-Balchin and Hart, 1999).
Other scented Pelargonium species, hybrids and cultivars yield essential oils of many
different chemical compositions, many of which also have antimicrobial potential
(Lis-Balchin, 1991a; Lis-Balchin et al., 1998) and some, with floral scents also act in a
similar pharmacological way to that of commercial Geranium oil (Lis-Balchin and
Hart,1997b, 1999). Others, with camphoric, mentholic or more medicinal scents did
not show this mechanism of action (Lis-Balchin, 1991b; Lis-Balchin and Hart, 1999).
ODOUR CLASSIFICATION

Pelargonium essential oils, with their many distinctive odours, can be grouped in many
different ways. One of the problems is that the odour can change dramatically during
flowering e.g. P. graveolens becomes rosy during flowering, whilst minty at other times
leading up to this; similarly the cultivars, Attar of Roses and others. An example of
a particular arbitrary grouping is shown together with the chemical composition of
different Pelargonium species and cultivars, as assessed using gas chromatography (GC)
with or without mass spectrometry (MS) in Tables 14.114.5. All samples were run on
an OV 101 column or equivalent.

2002 Edited by Taylor & Francis

Table 14.1 The chemical composition of Rosy pelargoniums


Component

KI

0.147.5
05.5
00.7
00.1
01.4
00.7
00.7
00.5
0.210.7
0.12.8
0.136.8
0.19.8
00.9
00.3
0.99.1
0.215.0
0.314.3

929
980
1020
1082
1097
1107
1142
1159
1216
1233
1255
1279
1333
1359
1408
1431
1467

1.310
00.7
2.77.8
17.843.4
7.442.8
2.611.2
1.1
0.23.1
4.310.6

1086
1101
1168
1211
1236
1259
1283
1434
1451

P. capitatum

-Pinene
Myrcene
Limonene
Linalool
cis-Rose oxide
trans-Rose oxide
Menthone
Isomenthone
Citronellol
Geraniol
Citronellyl formate
Geranyl formate
Citronellyl acetate
Geranyl acetate
-Caryophyllene
Gauia-6,9-diene
Germacrene D
Source: Demarne (1989).

Attar of Roses
Linalool
cis-Rose oxide
Isomenthone
Citronellol
Geraniol
Citronellyl formate
Geranyl formate
-Caryophyllene
Guaia-6,9-diene
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

P. cv. Rose
Linalool
cis-Rose oxide
Menthone
Isomenthone
Citronellol
Geraniol
Citronellyl formate
Geranyl formate
-Caryophyllene
Guaia-6,9-diene
Geranyl propionate
Germacrene D

2002 Edited by Taylor & Francis

4.6
0.2
0.4
7.8
19.0
21.5
8.5
9.5
0.8
7.2
1.6
2.1

1086
1101
1129
1168
1208
1233
1259
1279
1408
1432
1450
1467

Citronellyl butyrate  XX
Geranyl butyrate
Phenylethyl tiglate
Geranyl tiglate
 many sesquiterpenes unidentified

1.1
1.2
0.7
1.4

1507
1537
1547
1673

0.10.4
0.23.7
0.31.1
0.20.7
0.61.7
0.30.9
0.83.2
00.4
0.34.3
32.881.8
0.253.7

928
976
1002
1017
1022
1082
1097
1107
1142
1159
1216

1.212.8
0.24.5
7.081.5
017.6
19.141.9
11.2
6.0
0.74.2
04.0

1090
1145
1155
1208
1237
1259
1450
1539
1626

0.2
0.2

1176
1178

1.512.8
1.7
0.7
5.88.1
19.156.9
4.39.8
3.112.6
025.8
02.7

1087
1102
1126
1170
1212
1238
1260
1434
1448

Source: Demarne, 1989.

P. radens

-Pinene
Myrcene
-Phellandrene
p-Cymene
Limonene
Linalool
cis-Rose oxide
trans-Rose oxide
Menthone
Isomenthone
Citronellol
Source:Lis-Balchin (Masters Thesis Supervisor).

P. graveolens
Linalool
Menthone
Isomenthone
Citronellol
Geraniol
Citronellyl formate
Guaia-6,9-diene
Geranyl formate
10-Epi-eudesmol
 many sesquiterpenes unidentified
Unusual components identified by GC/MS
Hexyl butyrate
Hexenyl butyrate
Source: Lis-Balchin (Masters Thesis Supervisor).

Robers Lemon Rose


Linalool
cis-Rose oxide
trans-Rose oxide
Isomenthone
Citronellol
Geraniol
Citronellyl formate
-Caryophyllene
Guaia-6,9-diene
 many sesquiterpenes unidentified
Source: Lis-Balchin, 1988.

2002 Edited by Taylor & Francis

Table 14.2 The chemical composition of Minty pelargoniums


Component

KI

0.4
0.6
2.2
2.2
45.6
46.6
0.9

942
991
1014
1038
1155
1165
1174

1.0
1.0
tr
1.4
2.8
0.2
3.9
0.5
0.3
0.1
25.1
60.8
0.1
0.1
0.8
0.1
0.1
0.3
0.1
0.2

921
931
973
983
1011
1013
1022
1026
1037
1085
1134
1148
1161
1210
1224
1235
1257
1414
1447
1472

P. tomentosum

-Pinene
-Pinene/myrcene
p-Cymene
Limonene
Menthone
Isomenthone
Terpinen-4-ol
Lis-Balchin (Masters Thesis Supervisor).

P. tomentosum (2)
Tricyclene
-Pinene
-Pinene
Myrcene
-Phellandrene
p-Cymene
Limonene  X
cis-Ocimene
trans-Ocimene
Linalool  X
Menthone
Isomenthone
Menthol
Citronellol
Piperitone
Geraniol
Citronellyl formate
-Caryophyllene
-Humulene
Germacrene D
Source: Demarne et al., 1986.

Chocolate tomentosum

-Pinene
-Pinene
Myrcene
-phellandrene
p-Cymene
Linalool
Menthone
Isomenthone
n-Hexyl isobutyrate
Citronellol
Geraniol
Citronellyl formate
Citronellyl acetate
-Caryophyllene
Guaia-6,9-diene
 numerous sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

2002 Edited by Taylor & Francis

07.7
0.12.9
00.7
2.517.5
1.44.7
0.9
0.139.1
0.422.1
0.65.5
05.0
00.8
02.9
0.30.7
1.33.1
05.6

941
989
989
1005
1019
1083
1147
1156
1153
1206
1233
1256
1334
1431
1446

Lady Plymouth

-Pinene
Myrcene
-Phellandrene
-Terpinene
p-Cymene
Limonene
Linalool
Isomenthone
-Terpineol
Octyl acetate
Citronellol
Geraniol
 sesquiterpenes unidentified

0.61.8
0.20.6
0.40.9
0.40.8
0.41.0
0.51.9
0.20.3
71.981.9
00.4
0.2
0.20.5
0.20.6

942
984
1008
1022
1022
1032
1087
1158
1181
1185
1206
1241

Source: Lis-Balchin (Masters Thesis Supervisor).

Table 14.3a Chemical composition of Peppery-pungent pelargoniums


Component

KI

00.9
00.7
00.2
0.11.5
00.2
0.10.4
0.20.9
0.30.6
2.66.3
00.1
76.983.9
0.40.9
00.1

997
1011
1019
1024
1035
1083
1129
1139
1208
1233
1318
1408
1432

P. vitifolium

-Phellandrene
p-Cymene
Limonene
cis-Ocimene
trans-Ocimene
Linalool
Menthone
Isomenthone
Citronellol
Geraniol
Citronellic acid
-Caryophyllene
Guaia-6,9-diene
 many sesquiterpenes unidentified
Source: Demarne, 1989.

Table 14.3b Comparison of the main components of P. papilionaceum and Sweet Rosina
Component

Citronellic acid
Citronellol
Geranic acid
Isomenthone
Source: Lis-Balchin and Roth, 1999.

2002 Edited by Taylor & Francis

P. papilionaceum

Sweet Rosina

85.989.3
0.21.6
0.15.0
0.10.4

27.843.1
14.543.1
10.312.5
15.224.8

Table 14.4 The chemical composition of Citrusy pelargoniums


Component

KI

0.5
0.2
0.1
3.7
0.9
30.5
2.6
0.1
42.6

987
1018
1054
1084
1161
1221
1224
1235
1240

P. citronellum
Myrcene
p-Cymene
-Terpinene
Linalool
Isomenthone
Citronellol
Neral
Geraniol
Geranial
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

P. crispum variegatum

-Pinene
Limonene
-Terpinene
Fenchone
Citronellal
Isomenthone
Hexyl butyrate
Citronellol
Neral
Geranial
Sesquiterpene
 many sesquiterpenes unidentified

0.4
2.1
0.7
2.2
2.5
00.6
02.8
21.632.9
2.5
27.948.7
55.3

939
1028
1053
1078
1134
1170
1174
1223
1236
1247
1551

0.51.7
0.91.3
0.31.3
0.21.5
0.41.1
013.9
55.718.1
1.45.0
0.13.9
32.544.6
055.3

987
1018
1054
1084
1161
1173
1221
1224
1237
1256
1551

1.3
0.5
2.8
1.1
2.5

1018
1054
1084
1161
1221

Source: Lis-Balchin (Masters Thesis Supervisor).

P. scabrum
Myrcene
p-Cymene
-Terpinene
Linalool
Isomenthone
Terpinen-4-ol
Citronellol
Neral
Geraniol
Geranial
Sesquiterpene
 many sesquiterpenes unidentified
Lis-Balchin (Masters Thesis Supervisor).

Lemon Fancy
p-Cymene
-Terpinene
Linalool
Isomenthone
Citronellol

2002 Edited by Taylor & Francis

Neral
Geraniol
Geranial
Sesquiterpene
 many sesquiterpenes unidentified

28.8
3.9
38.2
55.3

1224
1237
1252
1551

Source: Lis-Balchin (Masters Thesis Supervisor).

Table 14.5 The chemical composition of Camphoraceous-pungent pelargoniums


Component

KI

1.13.7
2.016.4
16.023.0
2.813.4
0.14.0
8.315.2
0.84.3
23.525.0
20.726.4

985
1008
1026
1033
1170
1176
1224
1450
1613

9.7
19.7
6.0
1.5
7.5
8.4
0.7
10.2
2.6

928
940
982
1017
1028
1079
1106
1373
1431

1.2
0.3
3.5
1.34.3
2.59.3
1.0
4.619.4
1.48.7
31.779.8
1.52.2

944
985
1021
1030
1081
1144
1155
1238
1373
1432

P. glutinosum
Myrcene
-Phellandrene
p-Cymene
Limonene
Hexyl butyrate
Hexenyl butyrate
Citronellol
Sesquiterpene
Sesquiterpene
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

P.  fragrans

-Thujene
-Pinene
-Pinene
p-Cymene
Limonene
Fenchone
-Fenchyl alcohol
Methyl eugenol
-Caryophyllene
Source: Lis-Balchin and Roth, 2000.

P. odoratissimum

-Pinene
-Pinene
p-Cymene
Limonene
Fenchone
Menthone
Isomenthone
Piperitone
Methyl eugenol
-Caryophyllene
 many sesquiterpenes unidentified
Source: Lis-Balchin and Roth, 2000.

2002 Edited by Taylor & Francis

Table 14.5 (Continued)


Component

KI

25.0
12.3
4.3
0.5
2.7
18.5
0.3
4.5
0.2
4.3
0.2
0.6
3.7
0.5
0.9
0.2
10.3

921
931
949
968
978
1029
1053
1078
1083
1134
1146
1150
1170
1174
1179
1500
1577

0.2
0.6
19.2
0.1
5.1
0.2
1.6
0.8
30.5
1.1
1.7
3.8

933
941
982
1005
1025
1030
1046
1159
1166
1217
1221
1365

1.0
15.9
9.6
3.1
2.7
4.0
3.1

940
980
1004
1018
1029
1084
1189

4.5
1.8

931
940

P. exstipulatum

-Thujene
-Pinene
Benzaldehyde
Sabinene
Myrcene
Limonene
-Terpinene
Fenchone
Linalool
Camphor
Menthone
Isomenthone
Terpinen-4-ol
Hexyl butyrate
-Terpineol
Sesquiterpene
Sesquiterpene
 many sesquiterpenes unidentified
Source: Lis-Balchin and Roth, 2000.

P. quercifolium

-Thujene
-Pinene
-Pinene
-Phellandrene
p-Cymene
Limonene
trans-Ocimene
Isomenthone
-Terpineol
Nerol
Neral
Unknown
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

Clorinda

-Pinene
-Pinene
-Phellandrene
p-Cymene
Limonene
Fenchone
Linalool
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

Copthorne

-Thujene
-Pinene

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-Pinene
p-Cymene
Limonene
-Terpinene
Fenchone
-Caryophyllene
Sesquiterpene
 many sesquiterpenes unidentified

5.5
1.7
2.5
1.1
4.0
9.2
5.1

980
1017
1027
1053
1082
1482
1445

0.5
0.6
0.8
5.0
25.4
2.9
1.8
2.3
11.0
15.3

931
940
997
1004
1022
1030
1054
1085
1174
1226

8.0
2.8
16.0
5.5
1.8
2.6
0.6
7.3

939
948
988
1011
1025
1035
1090
1159

Source: Lis-Balchin (Masters Thesis Supervisor).

Village Hill Oak

-Thujene
-Pinene
-Pinene/myrcene
-Phellandrene
p-Cymene
Limonene
-Terpinene
Fenchone/linalool
Terpinen-4-ol
Nerol/citronellol
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

Sweet Mimosa

-Thujene
-Pinene
-Pinene/myrcene
-Phellandrene
p-Cymene
Limonene
Linalool
Isomenthone
 many sesquiterpenes unidentified
Source: Lis-Balchin (Masters Thesis Supervisor).

P. grossularioides
Myrcene
p-Cymene
Limonene
Fenchone
Linalool
Menthone
Isomenthone
-Terpineol
Citronellol
Neral
Geraniol
Geranial
Phenylethylisobutyrate
Methyl eugenol
-Caryophyllene
Guaia-6,9-diene
Geranyl propionate
Geranyl butyrate

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1.8
3.0
1.0
8.2
4.6
1.8
12.8
0.7
11.6
1.2
15.9
3.7
0.5
11.2
0.0
0.0
0.0
0.7

156

Maria Lis-Balchin

Table 14.5 (Continued)


Component

Phenylethyl tiglate
Caryophyllene oxide
Geranyl tiglate

0.8
1.8
1.1

KI

Source: Lis-Balchin, (1991b).

Odour classification
1 Rosy
2 Minty
3 Peppery-pungent
4 Citrusy
5 Camphoraceous-pungent

Rosy: In the rosy group (Table 14.1) there is P. capitatum L., found on the coastline of
the Cape in South Africa, with many different varieties occurring from the point of view
of appearance and odour (Demarne, 1989). Attar of Roses is an old cultivar, which is
probably the same as Otto of Roses, a form of P. capitatum mentioned and illustrated
by Andrews (1805). This is the common form of the rose-scented Pelargonium in cultivation and is almost identical to the cultivar Ros grown on the Island of Reunion for
its essential oil known as Geranium Bourbon. There are many cultivars of this type
from hybridizations between P. capitatum and P. radens H.E. Moore (Demarne and
van der Walt, 1990) which produce essential oils of different odour and chemical
composition (Demarne, 1989). P. graveolens LHerit., is quoted most often as the species
producing commercial Geranium oil and could be considered the parent of some of the
Egyptian and Moroccan Geranium oils due to its content of 10-epi-eudemol. A
common hybrid is Robers Lemon Rose, with rather jagged, irregular leaves and a distinctive rose-like odour with a hint of lemon. The parentage is said to involve P. graveolens (Abbott, 1994). P. radens, also known as as the cultivar Radula could be placed in
this group or the minty group, (similarly to P. graveolens) depending on the time the
sample is taken: if the plant is in flower, then the rosy odour is superior to the mintiness
of the essential oils at other times.
Minty: The minty group (Table 14.2) includes P. tomentosum Jacq. with over 90 per cent
of menthone and isomenthone and also one of its hybrids (with P. quercifolium
(L.f ) LHerit.) giving the more pungent Chocolate tomentosum. A cultivar with a
preponderance of isomenthone is Lady Plymouth, but it also sometimes has a rosy
odour. It was said to be the Geranium capitatum variegatum (Abbott, 1994) illustrated
and described by Andrews (18051806).
Peppery-pungent: The peppery-pungent group (Table 14.3) includes P. vitifolium (L.)
LHerit., P. papilionaceum (L.) LHerit. and the cultivar Sweet Rosina whose parent
was stated by the hybridiser to be P. graveolens (Lis-Balchin and Roth, 1999). All
three contain a very distinctive, pungent and lasting component called citronellic
acid, which has also beeen found in one essential oil sample from P. filicifolium
(Lis-Balchin et al., 1999).

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Essential oils from different Pelargonium species and cultivars

157

Citrusy: The citrusy group (Table 14.4) include P. scabrum (Burm.f.) LHerit.,
P. citronellum J.J.A. v.d.Walt and P. crispum Berg with a variegated form being often
commercially available. The Pelargonium species differ in the size and leaf shape but
have a uniquely similar citrus odour. The main components are geranial and citronellol. P. scabrum has very rough, large tri-lobed leaves and forms a bush sometimes
reaching over a metre in height; P. citronellum has five-lobed leaves, smaller than
previously and P. crispum has very tiny leaves on a woody, short bush which can be
grown upright in various shapes by professionals. A common cultivar is Lemon fancy,
which was raised by Helen Bowie in 1974 from Prince of Orange and Mabel Grey
(Abbott, 1994), the latter being regarded as synonymous with P. scabrum.
Camphoraceous-pungent: The camphoraceous-pungent pelargoniums (Table 14.5) include
P. exstipulatum (Cav.) LHerit., P. odoratissimum (L.) LHerit. and P.  fragrans Willd. The
latter is said to be a hybridization product of the first two species (Sweet, 1826) and the
chemical composition seems to add weight to this proposal (Lis-Balchin and Roth, 2000,
2002). P. quercifolium (L.f.) LHerit. and its various hybrids from Village Hill Oak to
Clorinda and Copthorne (which included also Regals in the hybridization) are put into
this hotch-potch group of pungent odouriferous Pelargonium, many of which have similarities with Vicks ointment and which also includes P. glutinosum Jacq. The cultivar Sweet
Mimosa derived from P. graveolens is included. The very unusual P. grossularioides L. is also
included, as it has a pungent, lemony smell; this is a tiny-leaved species which sprawls
across the ground and is the only Pelargonium essential oil found to have a spasmogenic
action on smooth muscle and the uterus (Lis-Balchin and Hart, 1994) and was used as an
abortifacient by Zulus and Boers. The main components in this group include monoterpenes, with methyl eugenol and fenchone in P. odoratissimum and P.  fragrans as well as
P. grossularioides, and, p-cymene featuring in P. quercifolium and the Oaks (its hybrids).

TRICHOMES IN PELARGONIUM SPECIES AND CULTIVARS

As the essential oils are stored in trichomes on the leaves of the scented pelargoniums,
there was a strong possibility that the shape, size and density of trichomes could be
indicative of the resultant odour of each Pelargonium and a simple means of classification both of odour and also inherent biological properties.
A study of 133 species and subspecies of Pelargonium trichomes by Oosthuizen (1983)
using a dissecting microscope showed numerous classes of indumentum, density and
trichome types. The author described the indumentum as ciliated (thin hairs of equal
size), glabrous (without trichomes), glandular (covered with glandular hairs), hirsute
(covered with stiff, long, straight hairs), pubescent (short, thin, soft hairs) and other
intermediate categories. The density varied from sparse to very dense. Eleven types of
trichomes were described and illustrated by drawings. Both non-glandular and glandular trichomes were described. Oosthuizen (1983) stated that the glandular hairs had
a uniserial stalk, of various lengths, and a unicellular head of various shapes. The heads
were either globular, bulb-shaped or pear-shaped. Some of the non-glandular trichomes
had a short, straight, stiff hair with or without a basal podium, while others were
described as soft, with/without podium etc.
Oosthuizen (1983) stated that in the Hoarea Section, the petioles and laminae are
mainly strigose (covered with stiff hairs with a sharp point, the hairs being compressed to

2002 Edited by Taylor & Francis

158

Maria Lis-Balchin

the surface and orientated in a distal or proximal direction). In Pelargonium, Glaucophyllum


and Eumorpha, it was hispid to setose and in Cortusina it was pilose, whilst in Otidia it was
sericeous. The author stated that long glandular hairs occurred especially in the sections
Hoarea, Ciconium, Pelargonium and Polyactium and were lacking in Seymouria, Otidia (except
P. carnosum), Myrrhidium, Peristera (except P. harveyanum), Dibrachya and Glaucophyllum.
Glandular hairs with pear-shaped heads occurred in sections Ligularia, Jenkinsonia and
Myrrrhidium. Glandular hairs were said to be absent from P. laevigatum, P. lanceolatum,
P. grandiflorum, P. lateripes. In some species in the section Polyactium, Peristera and
Glaucophyllum, non-glandular hairs are completely absent with only glandular ones
appearing. Oosthuizen (1983) concluded that there was some degree of classification
possible using the trichomes. However, looking at the individual results of trichomes for
each species in each section, some significant discrepancies occur and generalizations can
only really be made regarding a few species in each section. No clear correlation could be
made between the actual general odour of the plant and the actual trichomes present. In
particular, the non-odourific leaves of e.g. Hoarea still contained glandular hairs, which
would presumably have indicated the storage of scented exudates.
A study by van der Walt and Demarne (1988) on the origins of the Geranium oil
producing cultivars included a comparison of the leaves of P. graveolens and P. radens
using the scanning electron microscope. The leaves were dehydrated in a graded series
of ethanol, critical point dried with liquid CO2 and sputter-coated with gold. The
authors showed slight differences in the size and shape of two types of glandular hairs
in the two species, and also that one type only of non-glandular hairs occurring in
P. graveolens, whilst two types were present in P. radens. Oosthuizen (1983) had
described three types of non-glandular hairs in P. radens, with two types of glandular
hairs but had not studied P. graveolens.
One of the problems of studying trichomes in Pelargonium is that changes seemingly
occur in the morphology of glandular hairs during development and that in P. scabrum
the different morphological types represent different developmental stages of a single
glandular hair type (Oosthuizen and Coetzee, 1983). Their studies, using scanning
electron microscopy and transmission electron microscopy. The results therefore throw
into disarray, the results obtained by Oosthuizen (1983) regarding classification of the
numerous trichomes in the different sections.
Oosthuizen and Coetzee (1983) also showed that the secretion of essential oil from
the young trichome occurs repeatedly as a new cuticle develops each time beneath the
ruptured one. Glandular hairs are initiated throughout the different stages of leaf
development, whilst the non-glandular hairs are only initiated in the young leaf
(Oosthuizen and Coetzee, 1983). Because the rate of glandular hair initiation is lower
than that of epidermal cell differentiation and enlargement, the indumentum becomes
less dense with leaf expansion and therefore age (Oosthuizen and Coetzee, 1984). This
again makes comparison between petioles difficult, even within the same species, let
alone between different sections as slight changes in development in leaves would give
substantial variations in trichome density as well as appearance.
Personal studies of over 500 species and cultivars of Pelargonium using the scanning
electron microscope, after processing the leaves in glutaraldehyde (to prevent any
distortion) and sputter-coating with gold, indicated no precise segregation of pelargoniums based on their trichomes. Both scented and unscented Pelargonium leaves
contained both glandular and non-glandular hairs (Figures 14.114.12). These varied
largely during development of the leaf, more so than differences in different species.

2002 Edited by Taylor & Francis

Figure 14.1 P. abrotanifolium scented. Both glandular and non-glandular trichomes are illustrated.

Figure 14.2 P. ribifolium scented. Both glandular and non-glandular trichomes are illustrated.

2002 Edited by Taylor & Francis

Figure 14.3 P. tetragonum scented. Both glandular and non-glandular trichomes are illustrated.

Figure 14.4 P. graveolens scented. Both glandular and non-glandular trichomes are illustrated.

2002 Edited by Taylor & Francis

Figure 14.5 Robers Lemon Rose scented. Both glandular and non-glandular trichomes are
illustrated.

Figure 14.6 P. barklyi unscented. Both glandular and non-glandular trichomes are illustrated where
only the glandular hair is shown on the micrograph, although non-glandular hairs were
also present.

2002 Edited by Taylor & Francis

Figure 14.7 P. triste unscented. Both glandular and non-glandular trichomes are illustrated.

Figure 14.8 P. tongaense unscented. Both glandular and non-glandular trichomes are illustrated.

2002 Edited by Taylor & Francis

Figure 14.9 P. rapaceum unscented. Both glandular and non-glandular trichomes are illustrated
where only the glandular hair is shown on the micrograph, although non-glandular hairs
were also present.

Figure 14.10 P. grossularioides scented. Both glandular and non-glandular trichomes are illustrated
where only the glandular hair is shown on the micrograph, although non-glandular
hairs were also present.

2002 Edited by Taylor & Francis

Figure 14.11 P. echinatum unscented. Both glandular and non-glandular trichomes are illustrated.

Figure 14.12 P. praemorsum unscented. Both glandular and non-glandular trichomes are illustrated.

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Essential oils from different Pelargonium species and cultivars

165

REFERENCES
Abbott, P. (1994) A guide to Scented Geraniaceae. Hill Publicity Services, West Sussex.
Andrews, H.C. (18051806) Geraniums, vol. 1 & 2, London.
Demarne, F. (1989) LAmelioration varietale du Geranium rosat (Pelargonium sp.). Contribution
systematique, caryologique et biochimique. Thesis: Doctor of Science. Universite de Paris-Sud,
Centre DOrsay.
Demarne, F., Garnero, J. and Mondon, J.-M. (1986) LHuile essentielle de Pelargonium tomentosum Jacquin (Geraniaceae). Parf. Cos. Aromes., 70, AugSept., 5760.
Demarne, F. and van der Walt, J.J.A. (1990) Origin of the rose-scented Pelargonium cultivar
grown on Reunion Island. S. Afr. J. Bot., 55, 184191.
Lis-Balchin, M. (1991a) Essential oil profiles and their possible use in Hybridization of some
common scented Geraniums. J. Essent. Oil Res., 3, 99195.
Lis-Balchin, M. (1991b) The essential oil of Pelargonium grossularioides and Erodium cicutarium
(Geraniaceae). J. Essent. Oil Res., 5, 317318.
Lis-Balchin, M. and Hart, S. (1994) A pharmacological appraisal of the folk medicinal usage of
Pelargonium grossularioides and Erodium cicutarium (Geraniaceae). Herbs, Spices Med. Plants,
2, 4148.
Lis-Balchin, M., Deans, S.G. and Hart, S. (1996) Bioactivity of commercial Geranium oil from
different sources. J. Essent. Oil Res., 8, 281290.
Lis-Balchin, M. and Hart, S. (1997a) Pharmacological effect of esssential oils on the uterus compared to that on other different tisue types. In: Ch. Franz, A. Math and G. Buchbauer (eds),
Proc. 27th Int. Symp. Ess. Oils, Vienna, Austria, 811 Sept., 1996.
Lis-Balchin, M. and Hart, S. (1997b) A preliminary study of the effect of essential oils on skeletal and smooth muscle in vitro. J. Ethnopharmacol., 58, 183187. Allured Pub. Corp., Carol
Stream, III., pp. 2428.
Lis-Balchin, M., Hirtenlehner, T. and Resch, M. (1998) Antimicrobial activity of novel
Pelargonium essential oils added to a quiche filling as a model food system. LAM, 27,
207210.
Lis-Balchin, M. and Hart, S. (1999) Studies on the mode of action of the essential oils of scentedleaf Pelargonium (Geraniaceae). Phytother. Res., 12, 215217.
Lis-Balchin, M. and Roth, G. (1999) Citronellic acid: a major component in two Pelargonium
species (Geraniaceae). J. Essent. Oil Res., 11, 8385.
Lis-Balchin, M., Hart, S. and Roth, G. (1999) The pharmacological activity of the essential oils
of scented Pelargonium (Geraniaceae). Phytother. Res., 11(8), 83840.
Lis-Balchin, M. and Roth, G. (2000) Composition of the essential oils of P. odoratissimum,
P. exstipulatum and P.  fragrans (Geraniaceae). Flav. Fragr. J., 15, 391.
Lis-Balchin, M. and Roth, G. (2002) The chemical composition of selected Pelargonium essential
oils with reference to their pharmacological action. Flav. Fragr. J., To be published.
Lis-Balchin, M. Masters Thesis Supervisor (Magister der Pharmazie) Pharmacy Department,
University of Vienna, Austria [Gerhild, Roth (July, 1997), Ribisch, K. (September, 1998a),
Wenger, M.-T. (September, 1998b), Brandstetter, A. (September, 2001), Groiss, S. (January,
2002)].
Oosthuizen, L.-D. (1983) The taxonomic value of Trichomes in Pelargonium LHerit.
(Geraniaceae). J. S. Afr. Bot., 49, 221242.
Oosthuizen, L.-D. and Coetzee, J. (1983) Morphogenesis of trichomes of Pelargonium scabrum.
S. Afr. J. Bot., 2, 305310.
Oosthuizen, L.-D. and Coetzee, J. (1984) Trichome initiation during leaf growth in Pelargonium
scabrum. S. Afr. J. Bot., 3, 5054.
Sweet, R. (18201830) Geraniaceae, vol. 15, London.
van der Walt, J.J.A. and Demarne, F. (1988) Pelargonium graveolens and P. radens: A comparison
of their morphology and essential oils. S. Afr. J. Bot., 54, 617622.

2002 Edited by Taylor & Francis

15

Chemotaxonomy of Pelargonium
based on alkaloids and
essential oils
Peter Houghton and Maria Lis-Balchin

INTRODUCTION

There have been few chemotaxonomic studies of the genus Pelargonium and the results
of studies on tannins and flavonoids (Asen and Grisbach, 1983; Bate-Smith, 1973,
1981; Marszewski, 1990) and unidentified phenolic compounds (Harney, 1966, 1976)
were of limited value in the allocation of species into sections. Other components
studied included tartaric acid (Stafford, 1961), which proved to be unsatisfactory as
chemotaxonomic indices. Essential oils were studied in Pelargonium species and
cultivars by Demarne and van der Walt (1989), Lis-Balchin (1991), Lis-Balchin et al.
(1998a,b) and Lis-Balchin and Roth (1999) and proved of value in classification,
but only according to odour. The detection of alkaloids in some Pelargonium species
suggested that this criterion could be used as a chemotaxonomic marker (Lis-Balchin,
1993, 1996). Prior to the latter work, alkaloids had only been detected in some Erodium
species (Medina et al., 1977; Mossa et al., 1983; Lis-Balchin and Guittonneau, 1995).
Alkaloid Chemotaxonomy
The Geraniaceae is not known as an alkaloid-producing family although alkaloids have
been detected in phytochemical screening of Erodium glaucophyllum from Saudia Arabia
(Mossa et al., 1983) and E. malacoides from Argentina (Medina et al., 1977). Traces of
caffeine and choline had previously been found in the aerial parts of Erodium cicutarium
(van Eijk, 1952a), a herb used by the Sotho in South Africa as a uterine tonic but
caffeine was not detected in Geranium molle (van Eijk, 1952b).
Lis-Balchin and Guittoneau (1995) screened the leaves of 38 species of Erodium for
the presence of alkaloids and found different alkaloidal thin-layer chromatography
(TLC) profiles for the sections recognised within the genus. A single major compound
was detected in the section Malacoidea although no alkaloids were observed in extracts
from the subsection Gruina. The pattern in other sections was more variable and no
clear correlations could be established.
Similar screening studies on Pelargonium species had revealed the presence of alkaloids,
especially in zonal cultivars. The identity of the alkaloids detected was not determined
until studies by Lis-Balchin et al. (1996) on the cultivar Appleblossom. The simple
amines tyrosine 1 and tryptamine 2 were detected by TLC comparison with authentic
samples but of more interest was the isolation of three other, more complex, indole

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Chemotaxonomy of Pelargonium 167

alkaloids. The structures of two of these were determined by spectroscopic methods and
they were shown to be the two isomers elaeocarpidine 3 and isoelaeocarpidine 4.
These were known compounds which had previously been isolated from Elaeocarpus
(Elaeocarpaceae) (Johns and Lamberton, 1973) and Tarenna vanprukii (Rubiaceae)
(Takayama et al., 1992). Neither of these two families are considered to be closely
related to the Geraniaceae in classical systematic botany so the presence of these
alkaloids is likely to be the product of some process of convergent evolution.
Method of extraction and detection
The method used involved: extraction of the fresh leaves with boiling water, extracting
the initial acidic chloroform extract and subsequently after basifying with saturated
sodium carbonate solution to pH 10, extracting the alkaline chloroform fraction. The
extracts were separated on silica gel plates using two solvent systems; and sprayed with
Dragendorfs reagent or iodoplatinate reagent. Three to four major spots were obtained,
which were very stable, remaining bright yellow for months on the plates; other spots
were less stable. The general pattern proved consistent for all the species which
contained the alkaloids.
Chemotaxonomy of the genus Pelargonium
The study of representative species of all Sections of the genus Pelargonium indicated
that there was a main chemotaxonomic division in the genus. (Table 15.1), based on the
presence or absence of the alkaloids (Lis-Balchin, 1993). The latter were found in just
a few of the 44 species studied from all the sections: many of the species in the
Ciconium Section but otherwise only in the root of P. antidysentericum ssp. inerme, Section
Jenkinsonia, root of P. radulifolium, Section Polyactium and leaves of P. fulgidum,
Section Ligularia.
COOH
NH2
N
H
OH
(1) Tyrosine

(2) Tryptamine

N
H

H
20

(3) 20-H -Elaeocarpidine


(4) 20-H -Epielaeocarpidine

Figure 15.1 The structure of elaeocarpidine and related compounds.

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168

Peter Houghton and Maria Lis-Balchin

Table 15.1 A survey of the presence of alkaloids in representative species in different sections of Pelargonium
Section

Species

Campylia (Sweet) D.C.


Ciconium (Sweet) Harv.

P. elegans (Andr.) Willd


P. acetosum (L.) LHrit. 
P. alchemilloides (L.) LHrit. sensu lato
P. inquinans (L.) LHrit. 
P. tongaense Vorster
P. transvaalense Knuth
P. zonale (L.) LHrit. 
P. odoratissimum (L.) LHrit.
P. reniforme Curt. sensu lato
P. peltatum (L.) LHrit.
P. grandiflorum (Andr.) Willd
P. lanceolatum (Cav.) Kern
P. appendiculatum (L.f.) Willd
P. punctatum (Andr.) Willd
P. cotyledonis (L.) LHrit.
P. antidysentericum ssp. inerme  (root)
(Eckl. and Zeyh.) Costel P. antidysentericum
ssp. antidysentericum (root) (Eckl. and
Zeyh.) Costel P. tetragonum (L.f.) LHrit.
P. fulgidum (L.) LHrit. 
P. pulchellum SimsP. mollicomum Fourcade
P. multicaule Jacq.
P. carnosum (L.) LHrit. sensu lato
P. dasyphyllum E. Mey. ex Knuth
P. betulinum (L.) LHrit.
P. capitatum (L.) LHrit.
P. citronellum J.J.A.v.d. Walt
P. cucullatum subsp. tabulare (L.) LHrit.
P. denticulatum Jacq.
P. graveolens LHrit.
P. hispidum (L.f.) Willd
P. tomentosum Jacq.
P. vitifolium (L.) LHrit.
P. viscossimum
P. filicifolium
P. australe Willd
P. grossularioides (L.) LHrit. sensu lato
P. luridum (Andr.) Sweet sensu latoP. radulifolium (root) (Eckl. and Zeyh.) Steud. 
P. triste (L.) LHrit.

Cortusina D.C.
Dibrachya (L.) LHrit.
Glaucophyllum Harv.
Hoarea D.C.
Isopetalum (Sweet) D.C.
Jenkinsonia (Sweet) Harv.

Ligularia (Sweet) Harv.

Myrrhidium D.C.
Otidia (Sweet) G. Don
Pelargonium (D.C.) Harvey

Peristera D.C.
Polyactium (Eckl. and Zeyh.) D.C.

Chemotaxonomic revision of the Ciconium Section


Studies on the Section Ciconium species (Lis-Balchin, 1996) showed a 50 per cent
division in the presence of alkaloids (Table 15.2). The results strongly suggested that
species which were recently re-allocated from other sections into Ciconium do not

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Chemotaxonomy of Pelargonium 169


Table 15.2 The presence of alkaloids in Section Ciconium
Alkaloid-positive species

Alkaloid-negative species

P. zonale
P. acraeum
P. scandens
P. frutetorum
P. salmoneum
P. ranunculophyllum

P. alchemilloides
P. elongatum
P. transvaalense
P. multibracteum
P. quinquelobatum
P. caylae
P. mutans
P. tongaense

comply with the chemotaxonomy of the original Ciconium (Sweet) Harv., members.
These include P. alchemilloides, P. elongatum and P. transvaalense (all lately in Eumorpha);
P. multibracteum, P. quinquelobatum, P. caylae, P. mutans and P. tongaense also did not
comply. The remaining species with true Ciconium characteristics (and containing
alkaloids) are: P. zonale, P. inquinans, P. acraeum, P. scandens, P. frutetorum, P. salmoneum
and P. ranunculophyllum. The fact that P. zonale, P. inquinans and P. frutetorum were
alkaloid-positive is consistent with their use in the development of P.  hortorum
cultivars which are all alkaloid-positive.
The chemotaxonomic separation of P. alchemilloides from P. ranunculophyllum supports
the morphological findings and cytological differences observed (Gibby, 1989). The
alkaloid-negative species have a wider distribution than the alkaloid-positive species,
which are found in the Cape area, e.g. P. caylae is found as far as Madagascar. The chemotaxonomic division found is supported by recent botanical studies (Vorster, 1993). The
presence of alkaloids suggests a more evolved characteristic, possibly in response to the
presence of non-beneficial insects or other predators, as alkaloids are largely unpalatable.
Chemotaxonomy of modern cultivars
The modern cultivars, known as geraniums (Table 15.3) showed the presence of the
alkaloids in P.  hortorum Bailey cultivars (zonals), but absent from P.  domesticum
Bailey (regals) and P.  peltatum LHeritier (ivy-leaf). The zonal  ivy-leaf hybrids also
contained the alkaloids in their leaves regardless of whether they had an ivy-leaf
appearance (e.g. Millfield Rose, Jack of Hearts, Elsi) or zonal appearance (e.g. Deacons),
indicating a dominant trait (Lis-Balchin, 1997).
All zonals showed a similar alkaloid pattern regardless of the leaf colouration etc.
including the various golden-leaf cultivars, bronze-leaf cultivars, dark-leaf stellar
cultivars, the Deacons and Highfield cultivars, the mesh-leaf cultivar Wantirna, the
Boar, Magic Lantern, Red Kewense and the white-stemmed Freak of Nature and
shiny-leaf Skellys Pride.
The results support the theory that P.  domesticum cultivars and P.  hortorum
cultivars arose from different species. The lack of alkaloids in the P.  domesticum
cultivars supports the theory that P. cucullatum and P. capitatum were the probable
parents, together with a large number of other possible parents from a number of
sections e.g. P. fulgidum (Ligularia).

2002 Edited by Taylor & Francis

Table 15.3 Modern Pelargonium cultivars assessed for presence of alkaloids


P.  hortorum cultivars (all ve)
(Zonals)
Highfields Symphony
Highfields Delight
Highfields Perfection
Penny (Irene)
Christopher Lee
Burgenland Girl
Mr Wren
Magic Lantern (P. frutetorum cultivar)
White Boar (P. frutetorum cultivar)
Crystal Place gem (ornamental)
Distinction (ornamental)
Bridesmaid (golden-leaf )
Dovedale (golden-leaf )
Appleblossom (Rosebuds)
Skellys Pride (shiny-leaf )
Wantirna (mesh-leaf )
Bird Dancer (steller)
Redondo (dwarf, dark-leaf )
Fire Dragon (cactus-flower)
Els (stellar)
Red Star (stellar)
P.  domesticum cultivars (all ve)
(Regals)
Judith Thorpe
Fringed Aztec
Mosaic Belle Notte
Noche
P. peltatum cultivars (all ve)
(Ivy-leaved)
Crocketta
Madame Crousse
Feuerriesse
Sugar Baby
Hybrid ivy-leaf (all ve)
Ivy-leaf appearance
Millfield rose
Jack of Hearts
Elsi
Auden Ken an Emil Eschbach
Zonal appearance
Deacon Moonlight
Deacon Birthday
Deacon Ragatta
Deacon Regalia

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Chemotaxonomy of Pelargonium 171

The parents of P.  hortorum cultivars were obviously derived from the alkaloidpositive members of the Ciconium Section e.g. P. acraeum, P. inquinans and P. zonale.
These all originate from South Africa, mainly from the Cape, and had presumably
evolved the ability to synthesise alkaloids in response to either the original geographical
location or more likely to a biological effect. A local infestation by predators for
example could have provoked the synthesis of phytoalexins: in this case alkaloids. With
time, alkaloids could have become a regular secondary metabolite and therefore the
information was incorporated into the DNA. It is known that the earliest species of
Ciconium exported from the Cape was P. zonale and this was presumably one of the
major hybridisation parents of P.  hortorum cultivars.
The ability to synthesise alkaloids is apparently a strong characteristic as illustrated by
the inheritance of alkaloids from the P.  hortorum parent in the hybrid ivy-leaf
pelargoniums both those with a zonal appearance and those with an ivy-leaf appearance.
Possible insecticidal function of alkaloids
The presence of these alkaloids, identified as elaeocarpidine alkaloids (Lis-Balchin et al.,
1996) in zonal Pelargonium suggested an insecticidal action, as the latter are more
resistant to whitefly than the regals and the alkaloids were distributed at the zones,
associated with tannins, and whitefly appeared to desist from staying on these areas
(Woldemariam et al., 1997).
Citronellic acid
This unusual component has been found so far in just two Pelargonium species,
P. papilionaceum L. LHerit. and P. vitifolium L. LHerit. and one cultivar, P. Sweet
Rosina (Lis-Balchin and Roth, 1999). Both the species and the cultivar have a very
acrid, persistent odour, mildly reminiscent of the he-goat or Rambossie, which is
the vernacular name given to P. papilionaceum in South Africa. The cultivar is said to
be a cross between P. capitatum and P. graveolens: (Keys, 2000) both of which are
implicated in the parentage of the rose-like Geranium oil of commerce (Dermarne
and van der Walt, 1989).
P. papilionaceum is related both to P. vitifolium and P. capitatum (van der Walt and
Vorster, 1988). The former was used as a tobacco substitute in South Africa and
smoked, possibly for medicinal purposes, as well (Watt and Breyer-Brandwijk, 1962).
The percentage of citronellic found in P. vitifolium and P. papilionaceum essential oils was
about 7986 per cent. This component was also obtained in similar quantities by
solvent extractions of the species using hexane or petroleum spirits, therefore it was
shown not to be an artefact of steam distillation (Lis-Balchin and Roth, 1999). The
percentage in Sweet Rosina was 2843 per cent depending on extraction technique.
Citronellic acid was also identified in considerable quantities in one sample of
steam-distilled P. filicifolium, but this remained unconfirmed in other extractions
(Lis-Balchin personal research).
Citronellol and geranic acid

Citronellol was found at about 1 per cent in P. vitifolium and P. papilionaceum, but was
between 15 and 43 per cent in the cultivar. Geranic acid was found at 05 per cent in
P. papilionaceum, it was higher in the cultivar (1013 per cent), and absent in P. vitifolium.

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172

Peter Houghton and Maria Lis-Balchin

The results offer strong support for the implication of P. papilionaceum and P. vitifolium
as a parent of the cultivar, although the actual breeder was adamant that only P. capitatum
(the rose-scented parent of commercial Geranium oil) and P. graveolens (another possible
parent of a different cultivar for Geranium oil production) was involved in the cross. It is
noteworthy that many Pelargonium crosses bear no resemblance to either parent.
The citronellic containing Pelargonium species and cultivars could possibly be used to
produce a very strong fixative for perfumery, as other possibilities of use, including
antimicrobial and pharmacological investigations have not shown any other attributes
to date.
Further differences in the essential oil composition of scented Pelargonium species and
cultivars are found in Chapter 14.

REFERENCES
Asen, S. and Grisbach, R. (1983) High pressure liquid chromatographic analysis of flavonoids in
geranium florets as an adjunct for cultivar identification, J. Am. Soc. Hort. Sci., 108, 845850.
Bate-Smith, E.C. (1973) Chemotaxonomy of Geranium. Bot. J. Linn. Soc., 67, 347359.
Bate-Smith, E.C. (1981) Astringent tannins of the leaves of Geranium species. Phytochem., 20,
211216.
Demarne, F. and van der Walt, J.J.A. (1989) Origin of the rose-scented Pelargonium cultivar
grown on Reunion Island, S. Afr. J. Bot., 55, 184191.
Gibby, M. (1989) Pelargonium ranunculophyllum (Geraniaceae) in Southern Africa. S. Afr. J. Bot.,
55, 539542.
Harney, P.M. (1966) A chromatographic study of species presumed ancestral to
Pelargonium  hortorum Bailey. Canad. J. Genet. Cytol., 8, 780787.
Harney, P.M. (1976) The origin, Cytogenetics and Reproductive Morphology of the zonal
Geranium: A Review. Hort. Sci., 11, 189194.
Johns, S.R. and Lamberton, J.A. (1973) Elaeocarpus alkaloids. Alkaloids, 14, 325346.
Keys, H. (2000) National Pelargonium Collection, Fibrex Nurseries, Pebworth, Warwickshire.
Personal communication.
Lis-Balchin, M. (1991) Essential oil profiles and their possible use in hybridisation of some common scented Geraniums. J.Essent. Oil Res., 3, 99105.
Lis-Balchin, M. (1993) A chemotaxonomic study of the Pelargonium (Geraniaceae) species and
their modern cultivars. J. Hort. Sci., 72, 791795.
Lis-Balchin, M. (1996) A chemotaxonomic reappraisal of the Section Ciconium Pelargonium
(Geraniaceae). S. Afr. J. Bot., 62, 277279.
Lis-Balchin, M. and Guittonneau, G.-G. (1995) Preliminary investigations on the presence of
alkaloids in the genus Erodium LHerit. (Geraniaceae). Acta Bot. Gallica, 141, 3135.
Lis-Balchin, M. and Roth, G. (1999) Citronellic acid: a major compound in two Pelargonium
species (Geraniaceae) and a cultivar. J. Essent. Oil Res., 11, 8385.
Lis-Balchin, M., Houghton, P. and Woldermariam, T. (1996) Elaeocarpidine alkaloids from
Pelargonium (Geraniaceae). Nat. Prod. Lett., 8, 105112.
Lis-Balchin, M., Buchbauer, G., Hirtenlehner, T. and Resch, M. (1998a) Antimicrobial activity
of novel Pelargonium essential oils and solvent extracts, Lett. Appl. Microbiol., 27, 135141.
Lis-Balchin, M., Buchbauer, G., Hirtenlehner, T. and Resch, M. (1998b) Antimicrobial
activity of novel Pelargonium essential oils added to a quiche filling as a model food system.
Lett. Microbiol., 27, 207210.
Marszewski, D.E. (1990) Chemotaxonomy of Pelargonium, Proceedings of the International Geraniaceae
Symposium, Stellenbosch University, South Africa 2426 Sept., (Vorster, P. ed.), pp. 211214.

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Chemotaxonomy of Pelargonium 173


Medina, J.E., Rondina, R.V.D. and Coussio, J.D. (1977) Phytochemical screening of Argentine
plants with potential pharmacological activity (Part VII). Planta Med., 31, 136140.
Mossa, J.S., Al-Yahya, M.A., Al-Meshal, I.A. and Tariq, M. (1983) Phytochemical and biological screening of Saudi medicinal plants Part 5 Fitoterapia, 54, 147152.
Stafford, H.A. (1961). Distribution of tartaric acid in the Geraniaceae, Am. J. Bot., 48, 699701.
Takayama, H., Katsura, M., Seki, N., Kitajima, M., Aimi, N., Sakai, S., Santiarworn, D. and
Liawruangrath, B. (1992). Elaeocarpidine, A Naturally Occurring Racemate From Tarenna
vanprukii. Planta Med., 58, 289290.
van Eijk, J.L. (1952a) Pharm., Weekblad, 87, 425 (cited in Hegnauer, R. (1966) Chemotaxonomie
der Pflanzen, Vol. 4. Birkhauser, Basle, p. 200).
van der Walt, J.J.A. and Vorster, P.J. (1988) Pelargoniums of Southern Africa, National Botanic
Gardens, Kirstenbosch, S.Africa.
van Eijk, J.L. (1952b) Pharm. Weekblad, 87, 70 (cited in Hegnauer, R. (1966) Chemotaxonomie der
Pflanzen, Vol. 4. Birkhauser, Basle, p. 200).
Vorster, P.J. (1994) Taxonomy of Pelargonium, Austrian Pelargonium Soc. Symposium,
Burgenland, Aug. 1214.
Watt, J.M. and Breyer-Brandwijk, M.G. (1962) The Medicinal Plants of Southern Africa.
Livingston Ltd, Edinburgh.
Woldermariam, T., Houghton, P.J., Lis-Balchin, M. and Simmonds, M.S.J. (1997) Alkaloid and
tannin distribution in the leaves of Pelargonium zonale with reference to insect behaviour.
Pharmaceut. J., 259, 481.

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16 Phylogenetical relationship within


the genus Pelargonium based on
the RAPD-PCR method of DNA
analysis correlated with the
essential oil composition
J. Renata Ochocka, Adam Bogdan,
Arkadiusz Piotrowski and Maria Lis-Balchin

INTRODUCTION

DNA markers have recently been extensively used for genetic studies and plant
identification. With the introduction of new techniques such as polymerase chain
reaction (PCR), restriction fragment length polymorphism (RFLP) or sequencing of
DNA molecule, taxonomy based on DNA is one of the most developed approaches to
identification of biodiversity (Schierwater et al., 1997; Demeke and Adams, 1994,
Caetano-Annoles, 1996; Hadrys and Schierwater, 1992). Such studies were also carried
out on the Pelargonium genus, and also other genera of the Geraniaceae family (Erodium,
Geranium, Monsonia, Sarcocaulon) as well. Price and Palmer (1993) examined chloroplast gen rbcL in order to assess kinship within the Geraniaceae family and likewise
among other families from the Geraniales. The same approach was employed by Pax et
al. (1997) in the analysis of relatedness among endemic Hawaiian geraniums. Apart
from chloroplast DNA (fragment between trnL and trnF), internal transcribed spacer
ITS sequences from rDNA, was the basis for work by Bakker et al. (1998) to analyse
the phylogenetics of the Peristera section of Pelargonium.
One of the approaches used during the last few years is PCR-based amplification of
arbitrary DNA sequences (Schierwater et al., 1997). A technique derived from this is
randomly amplified polymorphic DNA RAPD which was used in this study (Demeke
and Adams, 1994; Hadrys and Schierwater, 1992; Caetano-Annoles, 1996). The main
advantage of RAPD is that no prior knowledge of the genome subjected to analysis is
required. The reaction can also be done with nanogram amounts of total genomic
DNA. In standard PCR protocols, one pair (two different) primers (one stranded,
oligonucleotide fragment of DNA) is used. After shifting the temperature of the assay
to that above the denaturation temperature of template DNA and subsequently reducing to an annealing temperature, primers are attached to the template but only at sites
whose sequences are complementary to that in the primers. If primers are situated in an
inverted direction, after elevating the temperature to about 72 C, new fragments of

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Phylogenetical relationship within the genus Pelargonium 175

DNA, the same as between sites of annealing primers, are amplified in an exponential
fashion. In contrast to standard PCR protocol, researchers do not have to know what
the sequences flanking the amplified fragment are in order to construct appropriate
primers. The RAPD amplification protocol differs from standard protocols in that only
a single primer is employed. Using short (i.e. 10 nucleotides in length) primers, there
is a high probability that genomic, template DNA contains several sites close to
one another, complementary to the sequence of the primer. The amplification products
are resolved according to length by means of gel electrophoresis, stained, and then the
visible bands are scored. Bands on the electrophoretic gel are marked as 0 (absence) in
some positions, and 1 (present) in others, i.e. converted the data to the binary form. To
explain genetic relationships, about ten primers, yielding a total of 100 bands are needed.
The data are subsequently subjected to numerical analysis with one of the selected
algorithms and plotted as a tree. RAPD analysis provides the knowledge about events
studied at various taxonomical levels. Despite limitation regarding reproducibility and
sometimes scoring of bands, RAPD is often used because of its simplicity.
Plant material used in the study
The material used was dried leaf tissue of representative species of Pelargonium:
P. filicifolium, P. tomentosum, P. scabrum, P. Lady Plymouth, P. glutinosum, P. Chocolate
Peppermint, P. Atomic Snowflake, P. graveolens, P. cucullatum, P. quercifolium and P. trifidum
which are shown in the table below with their appropriate numbers.
Name
P. filicifolium var. of P. denticulatum Jacq.
P. tomentosum Jacq.
P. scabrum LHerit.
P. Lady Plymouth
P. glutinosum ( Jacq.) LHerit.
P. Chocolate Peppermint
P. Atomic Snowflake
P. graveolens LHerit.
P. cucullatum subsp. tabulare LHerit.
P. quercifolium LHerit.
P. trifidum Jacq.

No.
1
5
6
7
10
11
12
13
15
16
18

All the species bar P. trifidum belong to the Section Pelargonium, the latter is in the
Section Ligularia.
Essential Oil analysis, Genomic DNA Isolation and PCR protocol
Essential Oil analysis by GC and MS was carried out on all the essential oil samples and
the total Genomic DNA Isolation was isolated according to the CTAB method
(Palmarczyk et al., 1995) from eleven samples as described in the table above. The
PCR protocol using the following sequences of primers: RA07-GAAACGGGTG,
RA09-GGGTAACGCC, RA17-GACCGCTTGT, RA18-AGGTGGACCGT, RA20GTTGCGATCC, RN01-CTCACGTTGG resulted in 220 of the total bands.

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Renata Ochocka et al.

Gel electrophoresis and data analysing


After the PCR reaction, products were resolved in agarose gel and their positions
formed the basis in constructing a matrix consisting of one (when the band was present)
or zero (when there was no band, but if it existed at the same position along any of
tracks of the other samples). The original data were converted to dissimilarity matrices
according to algorithms contained in RAPDistance Package Version 1.04. using
various algorithms (given below):
1 2*n11/((2*n11)  n01  n10) Dice (Czekanowski, 1913; Dice, 1945; Nei and
Li, 1979; Sorensen, 1948).
2 n11/(n n00) Jaccard (1901, 1908).
3 n11/(n01  n10) Kulczynski 1 (Kulczynski, 1927).
4 0.5*((n11/(n11  n01))  (n11/(n11  n10))) Kulczynski 2 (Kulczynski, 1927).
5 (n11*n00)  (n01*n10)/sqrt((n11  n01)*(n01  n00)*(n11  n10)*(n10 
n00)) the Phi coefficient or Pearsons Phi coefficient (Sokal and Sneath, 1963).
6 n11/n Russell and Rao (1940).
7 n11/(n11  2*(n10  n01)) Sokal and Sneath 1 or Anderberg (Sokal and
Sneath, 1963).
8 0.25*((n11/(n11  n10))  (n11/(n11  n01))  (n00/(n00  n10)) 
(n00/(n00  n01))) Sokal and Sneath 2 (Sokal and Sneath, 1963).
9 n11/sqrt((n11  n10)*(n11  n01)) Ochiai (1957).
10 n11*n00/sqrt((n11  n10)*(n11  n01)*(n00  n10)*(n00  n01)) Sokal and
Sneath 3 (1963).
11 ((n11*n00)(n10*n01))/((n11*n00)  (n10*n01) Yule and Kendall (1950).
12 0.5*(sqrt((F*F)  (8*F))F))**(1/n), where F 2*n11/(nx  ny) Upholt (1977).
13 Evolutionary distance estimate (K) (Li and Graur, 1991).
14 (n11  n00)/n Simple Matching (or Apostol) (Apostol et al., 1993).
15 n*(1  (n11/n)) Excoffie (Excoffier et al., 1992).
16 (n11  n00)/(n11  2*(n10  n01)  n00) Rogers and Tanimoto (1960).
17 (n11  n00)/(n11  0.5)*(n10  n01)  n00 Sokal and Sneath (1963).
18 (n11  (n10  n01)  n00)/n Hamman (Spath, 1980).
where: n the number of band positions
nx the number of bands present in the track with bands from one sample
ny the number of bands present in the track with bands from compared sample
n11 the number of positions where x 1 AND y 1
n00 the number of positions where x 0 AND y 0
n01 the number of positions where x 0 AND y 1
n10 the number of positions where x 1 AND y 0.
Trees reflecting relationships of analysed samples were drawn according to the neighbour joining method. Validity of trees was tested by means of permutation tail probability (PTP) test. Unweighted pair-group method using arithmetic averages (UPGMA)
was used with the average distance between all pairs of objects in the two different
clusters according to Sneath and Sokal (1973) and also weighted pair-group method
using arithmetic averages (WPGMA) with the size of the respective clusters used as a
weight (Sneath and Sokal, 1973).

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Phylogenetical relationship within the genus Pelargonium 177

The results were compared to the results of factor analysis by means of principal
components analysis (PCA) (Dunteman, 1989; StatSoft, Inc., 1995), presented on a 3D
plot (unrotated) using the first three principal components that were chosen using the
Kaiser criterion (Kaiser, 1960) as well as the scree test (Cattell, 1966).
COMPARISON OF RESULTS OF GENETIC ANALYSIS
AND PHYTOCHEMICAL ANALYSES

With algorithms included in the RAPDistance program two kinds of trees were
obtained. Algorithms from 1 to 13 (without No. 6) gave similar trees; the length
of branches of particular trees were variable, but the positions of the branches were
the same. An example of such a tree is shown in Figure 16.1a, drawn according
to algorithm 4. Algorithms from 14 to 18 resulted in another group of trees; Figure
16.1b represents the tree based on algorithm 14.
P. filicifolium, P. glutinosum, P. Chocolate Peppermint and P. quercifolium are clustered
in all trees so their reciprocal positions seem to be convincing. The same conclusion
is drawn as to P. Atomic Snowflake and P. graveolens with P. scabrum and P. cucullatum
as well. High values of the PTP test was observed both with the first group of algorithms
(113) or the second (1418) so none of the plots were preferable. The tree was therefore also drawn using the original set of data (0;1) by the UPGMA method (Fig. 16.2a),
calculating the dissimilarity matrix, by the WPGMA method (Fig. 16.2b) and the PCA
method (Fig. 16.3). The results obtained with the UPGMA and PCA method were more
consistent than with those obtained using the neighbour-joining method based on algorithms from 1 to 13. Taking into account these facts a model of genetic relationships
from Figure 16.1a is therefore proposed.
When analysing the contents of 51 compounds in Pelargonium essential oils with the
application of the PCA method (Fig. 16.4), it is possible to point out a clustering of
samples into three subgroups. In one cluster there are: P. filicifolium (P1), P. glutinosum
(P10) and P. quercifolium (P16); in the second and the third there are: P. scabrum (P6), P.
cucullatum (P15) and then P. tomentosum (P5), P. Lady Plymouth (P7), P. Chocolate
Peppermint (P11) and P. graveolens (P13) respectively (Table 16.1).
The genetic results presented in the PCA diagram (Fig. 16.3) also point out the clustering of the samples investigated. Similarity of the genetic and phytochemical profiles
can be seen for samples P6 (P. scabrum) and P15 (P. cucullatum).
The results obtained initially for Pelargonium, indicate that the RAPDPCR method
may be very useful for comparison of genetic changes with chemical composition of plants.
COMPARISON OF RESULTS WITH THE PHYLOGENY
OF PELARGONIUM USED

There was a consistent clustering of P. Atomic Snowflake and P. graveolens on all the
cladograms. This indicates the close genetic relationship, as the former is a hybrid of
P. graveolens. The chemical analysis of P. Atomic Snowflake was not available, but the
odour partly resembles the mintiness and rosyness of P. graveolens with an extra
persistent acrid odour which resembles that of P. papilionaceum containing citronellic
acid (Lis-Balchin et al., 1999).

2002 Edited by Taylor & Francis

(a)

P. Lady Plymouth (7)


P. trifidum (18)
P. scabrum (6)
P. cucullatum (6)
P. tomentosum (5)
P. filicifolium (1)
P. quercifolium (16)
P. glutinosum (10)
P. Chocolate Peppermint (11)
P. Atomic Snowflake (12)
P. graveolens (13)

(b)

P. filicifolium (1)
P. glutinosum (10)
P. Chocolate Peppermint (11)
P. quercifolium (16)
P. Atomic Snowflake (12)
P. graveolens (13)
P. Lady Plymouthp (7)
P. tomentosum (5)
P. trifidum (18)
P. scabrum (6)
P. cucullatum (15)

Figure 16.1 a,b The tree diagram obtained by the neighbour joining method for RAPD
dataset: (a) using algorithm 4 included in the RAPDistance program
(b) using algorithm 14 included in the RAPDistance program.

2002 Edited by Taylor & Francis

Table 16.1 Concentration of Essential oil components in various Pelargonium species


Compounds
cis-3-Hexanol
-Thujene
-Pinene
-Pinene
Benzaldehyde
Sabinene
Myrcene
-Phellandrene
Hexyl acetate
1,4-Cineole
-Terpinene
p-Cymene
Limonene
Ocimene
-Terpinene
()-Fenchone
Linalool
Camphor
Menthone
Isopulegol
Isoborneol
p-Cymene-8-ol
Isomethone
Terpinen-4-ol
-Terpineol
Hexyl butyrate
Hexenyl butyrate
Octyl acetate
trans-Carveol
Citronellol
Nerol
Neral
Geraniol
Citronellyl formate
n.i.
Geranial
Cuminyl alcohol
n.i.
Citronellyl acetate
2-Propenyl benzene
-Caryophyllene
Guaia-6,9-diene
Geranyl butyrate
Citronellyl ester
10-Epi-eudesmol
Geranyl tiglate

Essential oils concentration (%)


1
0
0
0
0
0.70
0.12
0.07
0.58
0
1.89
0.39
0.23
0
0
0
0.15
0
0.14
0
0.36
0
31.29
0
0
0
0
0
0
0.30
0.14
0
0
0
0
1.18
0
0
47.47
0
0.53
0
0
0
0
0
0

5
0
0
0.4
0.6
0
0
0
0
0
0
0
2.2
2.2
0
0
0
0
0
45.6
0
0
0
46.6
0.9
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0

6
1.7
0
0
0
0
0
0.26
0
0
0
1.16
0
0
0
0.27
0
1.53
0
0
0
0.28
0
0.44
13.85
0.68
0
0
0
0
2.60
17.96
4.95
32.48
0
0
0.70
2.29
0
0
0
0.38
0
0
2.20
0
0

7
0
0
6.00
0.6
0
0
0
0.7
0
0
0
2.2
2.5
0
0
0
0
0
0
0
0
0
73.4
0
0
0
0
0
0
17.6
0
0
0
0
0
0
0
0
0
0
0
0.2
0
0
0
0

10
0
0
0
0
0
0
1.1
2.0
0
0
0
23.7
2.8
0
0
0
0
0
0
0
0
0
0
0
0
1.0
8.3
0
0
0.9
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0

11
0
0
7.7
0.1
0
0
0
0
0
0
0
0
0
0
0
0
0.9
0
0
0
0
0
0.4
0
0
0
0
0
0
5.0
0
0
0.8
2.9
0
0
0
0
0
0
0
5.6
24.0
0
0
0

13
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
12.8
0
0.2
0
0
0
7.0
0
0
0.2
0
0
0
17.6
0
0
41.9
11.2
0
0
0
0
0
0
0
6.0
0.7
0
4.0
2.7

15
0.63
0
0
0
0
0
0
0
0
0
0
0
0.30
0
0
0
0
0
0
0
0
0
0
0
0
0
0
18.55
0
0
0
0
0
0
0
0
0
0
0
0
0.99
0
0
0
0
0

16
0.37
0.17
0
0
0.62
3.16
0
0.10
17.32
19.19
0.81
5.01
0.24
1.56
0
0
0
0
0.81
0
0
0
30.50
0
0
0
0
0
0
0.21
0
0
0
0
0
0
0
0
0.87
0
0
0
0
0
0
0

Notes
(1) P. filicifolium, (5) P. tomentosum, (6) P. scarbum, (7) P. Lady Plymouth, (10) P. glutinosum, (11) P. Chocolate
Peppermint, (13) P. graveolens, (15) P. cucullatum, (16) P. quercifolium.

2002 Edited by Taylor & Francis

180

Renata Ochocka et al.


(a)

P. filicifolium (1)
P. tomentosum (5)
P. glutinosum (10)
P. quercifolium (16)
P. Chocolate Peppermint (16)
P. scabrum (16)
P. Atomic Snowflake (12)
P. graveolens (13)
P. Lady Plymouth (7)
P. trifidum (18)
P. cucullatum (15)

9.0

8.5

8.0

7.5

7.0

6.5

6.0

Linkage distance
(b)

P. filicifolium (1)
P. tomentosum (5)
P. glutinosum (10)
P. quercifolium (16)
P. Chocolate Peppermint (16)
P. scabrum (16)
P. Atomic Snowflake (12)
P. graveolens (13)
P. Lady Plymouth (7)
P. trifidum (18)
P. cucullatum (15)

9.5 9.0

8.5

8.0

7.5

7.0

6.5

6.0

Linkage distance

Figure 16.2 a,b The tree diagram obtained for the RAPD dataset (a) by the UPGMA
method (b) by the WPGMA method.

The linking together of P. filicifolium, P. glutinosum, P. quercifolium, P. Chocolate


Peppermint and P. tomentosum can be explained almost entirely on the basis of their
odour, although there are some verifications also from the genetic point of view as
P. tomentosum is the parent of the hybrid, P. Chocolate Peppermint and the other parent is derived initially from P. quercifolium.

2002 Edited by Taylor & Francis

P15
P6

0.6
0.4

P16
P10

P13

0.0

P11
P12

0.2
0.4

P5
P1

0.2

0.4

Factor 3

P7
P18

0.2

r1

to

c
Fa

.6
0
.8

.4

.2

Factor
2

.6

0.0

.4

0.2

0.4

.2

0.6

0.0

0.6

Figure 16.3 Genetic results: The 3D plot obtained by the PCA method for RAPD dataset.

Factor 3

0.8
0.6
0.4
0.2
0.0
0.2
0.4
0.6
0.8

0.8

P1
P7
P16

P10
P13 P11

P5

P15
P6

0.6

0.4

0.2

Fa
c

tor

0.0

0 .2

0.4

0.6

0.
0.8 0.4

0.0

0.2

0.4

0.6

0.8

1.0

r1

to
Fac

Figure 16.4 Phytochemical results: The 3D plot obtained by PCA method for phytochemical dataset.

2002 Edited by Taylor & Francis

182

Renata Ochocka et al.

GC data for P. trifidum indicates that it contains a substantial percentage of menthone,


some isomenthone, and monoterpenes including camphene, myrcene, -terpinene,
limonene (MLB personal analysis). This explains the clustering with P. Lady Plymouth
(Figures 16.1a, 16.2a, b); with P. tomentosum (Figure 16.1b). Unfortunately the analytical results were not available for the essential oil correlations in Figure 16.4. The results
also support the hypothesis that the DNA profiles obtained by the RAPD-PCR method
correlates with the chemical composition rather than with the genetic angles, as P. trifidum is in a completely different section to that of the other two Pelargonium with which
it is clustered.
The clustering of P. cucullatum with P. scabrum in Figure 16.1a and 16.1b can only be
explained on the basis of similarity in their chemical composition as the two species are
very different in most botanical parameters.

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2002 Edited by Taylor & Francis

17 Geranium essential oil:


standardisation, ISO; adulteration
and its detection using GC,
enantiomeric columns, toxicity
and bioactivity
Maria Lis-Balchin

INTRODUCTION

Definition of Geranium oil and specification


The International Organisation for Standardization or ISO, defines Geranium oil as
The oil obtained by steam distillation of the fresh or slightly withered herbaceous parts
of Pelargonium graveolens LHeritier ex Aiton, Pelargonium roseum Willdenow and other
undefined hybrids which have given rise to differing ecotypes in the various geographical areas (International standard 4731: 1972). The colour is various shades of amberyellow to greenish-yellow. The odour is given as characteristic of the origin, rose-like
with a varying minty note.
The specification does not include the Bulgarian Geranium oil distilled from
Geranium macrorrhizum, known as Zdravetz oil, containing mainly sesquiterpenes of
which half is apparently germacrone (Ognyanov, 1985).
ISO 4731 has set the concentration for citronellol content at a minimum 42 per
cent/maximum 55 per cent for Bourbon Geranium oil; 35/58 for Moroccan; 40/58 for
Egyptian and 40/58 per cent for Chinese oils . Other physico-chemical values are given
in Table 17.1.

ORIGIN AND NOMENCLATURE OF GERANIUM OIL

There are numerous misnomers given for the origin of Geranium oil in both scientific books (Fenaroli, 1997) and most aromatherapy books. The worst are: Geranium
maculatum, G. robertianum and other Geranium species, as the medicinal properties of
Geranium oil were mistakenly taken from Herbals (Culpeper, 1653; Grieve, 1937).
Some of the other misnomers most frequently used are: Pelargonium odoratissimum,
P. graveolens, P. asperum and P. roseum Willd. However, the main source of the commercial oil is from a cultivar known as P. cv. rose giving the Geranium oil, Bourbon from
Reunion and also lately from China. The Rose cultivar has been found to be, most
probably, a hybrid between P. capitatum  P. radens (Demarne and van der Walt, 1989).
The cultivars used for the production of Geranium oil in many parts of the world

2002 Edited by Taylor & Francis

Geranium essential oil: standardisation, ISO; adulteration

185

Table 17.1 Physico-chemical characteristics of Geranium oil Bourbon and from other sources

Relative density at 20 C
Refractive Index at 20 C
Optical rotation at 20 C
Acid value maximum
Ester value
Ester value after Acetylation
Carbonyl value Expressed as iso-menthone
Apparent citronellol (rhodinol) content

Bourbon

Morocco

Egypt

0.8840.892
1.4621.468
8 to 14
10
5278
205230
58
4255

0.8830.900
1.4641.472
8 to 13
10
3580
192230
58
3558

0.8870.892
1.4661.470
8 to 12
6
4258
210235
Not given
4058

remain confused; in some papers originating in India, the cultivar is stated to be that
obtained as a cutting from the cultivar Rose from Reunion, however, many papers
state that their Geranium oil source is from P. graveolens.
PRESENT SOURCE

Numerous parts of the world have produced Geranium oil in the past (Weiss, 1997) but
even in the country of origin of Pelargonium i.e. South Africa, this has proven to be noneconomical. Small amounts, for own country consumption is produced in India,
Morocco and Algeria. In Kenya it is known as Mawah oil, and is stated to be from
P. fischeri (Weiss, 1997). Nowadays, there is no production of Geranium oil in Grasse,
which simply acts as a market base for imported oil from all over the world and where
some adjustments are made to the oil, demanded for its various uses. African Geranium
oil usually refers to the Egyptian oil but also to that of Morocco and Algeria where the
same or similar Pelargonium cultivar is used.
China produced a type of Bourbon oil, but Weiss (1997) refers to it as an Morocco-style
oil, which makes it more like the Egyptian type. The area of Yunnan, Binchuan, Shiping
and Yuxi Provinces are gradually being decreased in favour of other essential oil crops.
The descriptions of the unique but different odour qualities found in the essential oil
bible by Arctander (1960) probably no longer apply to the modern produce. The different chemical compositions of Geranium oils from different geographical areas
(Lawrence, 1992, 1994; Weiss, 1997) are also not found to conform to norm in practice,
as adulteration of commercial oils is profuse (Lis-Balchin et al., 1996).
GERANIUM CONCRETE AND ABSOLUTE

Geranium concrete and absolute are made in small amounts for certain perfumes and
are produced mainly in Egypt. The concrete, extracted with petroleum spirits or hexane
is dark green or brownish-green with a foliage-like odour and great tenacity. The geranium absolute, made from the concrete by dissolving in absolute alcohol and then chilling to precipitate the insoluble components, followed by evaporation of the solvent, is
also greenish with a somewhat leaf-earthy and powerful odour (Arctander, 1960).
Terpeneless Geranium oil can be produced from the Geranium oil and the absolutes, by

2002 Edited by Taylor & Francis

186

Maria Lis-Balchin

vacuum distillation; this makes the oil more soluble in diluted alcohol and is useful in
foods as well as cosmetics.
The name geranium rose oil was formerly used to indicate a special French
Geranium oil produced in Grasse, which was distilled over rose petals. Nowadays the
Geranium rose refers to the Geranium c.v. Rose cultivated in Reunion as the Bourbon
Geranium oil.
One of the main products of Geranium oil and absolutes in the past was rhodinol,
which is composed mainly of the citronellol fraction. This was used extensively in the
poor-mans rose perfumes and cosmetics, including soaps, creams, etc. (Arctander,
1960). Nowadays, rhodinol is produced synthetically, as the price of geranium has
soared.

ADULTERATION

Geranium oil contains mainly citronellol and geraniol and their esters, therefore can
be easily concocted from cheaper essential oils and adjusted to the recommended ISO
standards. The antimicrobial activity of such essential oils is much greater than that
of some authentic oils but has a similar pharmacological effect on smooth muscle
(spasmolytic) and the actual odour can be even more appreciated by perfumers than
the real essential oil. The essential oil composition of this Geranium oil differs
completely from that of a true G. robertianum oil (Pedro et al., 1992) or that of
G. maccrorhizum (Ognyanov, 1985).
The most expensive Geranium oil was always the Bourbon, but over the years this
has inexplicably increased in tonnage (which is surprising for a small volcanic island
with relatively limited Pelargonium-growing areas) as well as value; this could be partly due to the increase in Geranium oil production in China, which being very similar
to that of Bourbon would often get accepted as such (Verlet, 1992).
Recent Geranium oil production in China is restricted to the region of Binchuan 450
km from Kunming (Cu, 1996) and there are two harvests, a summer one which yields
an oil which is relatively similar to Bourbon and the winter harvest which gives a lowgrade oil with only 4 per cent geraniol, compared to the summer 7 per cent and the
Bourbon with 14 per cent. The citronellol content is however much greater than that
of Bourbon geranium and is virtually doubled. The characteristic sesquiterpene is
guaia-6,9-diene as in Bourbon oil.
Adulteration of Geranium oil is perhaps encouraged by the ISO requirements themselves and the comparatively low price of synthetics. The yield of Geranium oil is less
than 0.3 per cent, and is usually 0.2 per cent. There are excellent recipes for a synthetic
Geranium oil, one of which is shown in Table 17.2, which was given to the author by
a perfumer 15 years ago.
Adulteration of all essential oils occurs to a considerable extent with diluents like
propylene glycol, triacetin, triethyl citrate or benzyl alcohol, ethyl alcohol and in the
case of aromatherapy oils with fixed oils like almond oil, which are added in excessive
amounts. Adulteration also implies giving the wrong source on the labelling e.g.
Bourbon, if it came from another country or was synthetic, or even when Body Shop
had a Geranium oil leaflet stating that it originated from G. maculatum (which is not
only the wrong species but has no odour).

2002 Edited by Taylor & Francis

Geranium essential oil: standardisation, ISO; adulteration

187

Table 17.2 Recipe for a synthetic Geranium oil


Component/chemical

Parts

Dimethylsulphoxide (DMSO) 0.1%


Citral
Citronellol
Citronellyl formate
Geraniol
Geranyl formate
Geranyl propionate
Geranyl tiglate
guaia-6,9-diene
iso-menthone
menthone
L-rose oxide
Linalool
Diluent

10
200
2800
1000
1500
800
150
150
500
500
150
150
1000
1090
100%

DETECTION OF ADULTERATION

Carrier or fixed oil or solvents


Geranium oil Bourbon is frequently adulterated and the real or preferred oil can only
be detected by experienced noses and stringent chemical analysis, unless solvents are
used in any quantity, where simple gas chromatography (GC) can detect adulteration,
if one knows where to look for it. Adulteration with carrier oils (fixed oils like almond
oil) is easily detected by putting a drop of the sample on blotting paper or a piece
of cloth and looking for signs of a halo of grease remaining after a few hours (as pure
essential oils would evaporate completely, leaving no residual mark.
Chiral or enantiomeric columns
However, ordinary GC, with or without mass spectrometry (MS) or other identification
facilities, like Infra-red (IR) etc. are not sophisticated enough to find most adulterations
when fractions of other oils or synthetic components are used. The determination of
such adulteration of essential oils was perfected by the use of special enantiomeric or
chiral columns, mainly composed of an -cyclodextrin phase (Ravid et al., 1992; LisBalchin et al., 1999). One of the major components, citronellol occurs in the ()-form
in geranium and rose oils and has a finer rose odour than the () enantiomer, and a
sweet, peach-like flavour. The ()-citronellol enantiomer has been found in citronella
oils from Ceylon and Java, Cymbopogon winterianus, Boronia citridora, Eucalyptus citriodora,
Spanish verbena and other essential oils.
The two enantiomers are starting materials for numerous chiral pheromones and
flavours (Ravid et al., 1992) and are prepared commercially by partial or total synthesis,
sometimes involving particular yeast strains. This abundance of the citronellol lends
itself to adulteration on a grand scale. Initial analyses of commercial Egyptian Geranium
oil yielded almost a racemic mixture of citronellol enantiomers, whilst a true Bourbon
oil gave a highly concentrated S()-citronellol (Ravid et al., 1992); Further analyses

2002 Edited by Taylor & Francis

188

Maria Lis-Balchin

using chiral columns showed that some cultivars of Egyptian type geranium leaves
(distilled in the laboratory) had an almost racemic mixture, while others had more of the
() enantiomer. Bourbon Geranium oil distilled in the laboratory had in contrast a
predominance of the () enantiomer of 7378 per cent, whilst commercial samples had
a more racemic content, as did Eucalyptus citriodora and Lemon mint oil. Citronella had
only 26 per cent of the () enantiomer. The rose-like quality of the ()-citronellol
determines the odourific value of the Geranium oil and synthetic rose compounds and
therefore addition of synthetic citronellol or extracts from plant oils with a low content
of ()-citronellol would be detrimental to the odour and quality of the product.
Recent studies on Australian Geranium oils grown from specific Pelargonium clones
showed that using 10 key chiral components, and calculating a so-called chiral excess,
it was possible to distinguish geographically different and seasonally different essential
oils and also adulteration (Doimo et al., 1999).
It is worth noting that chiral columns can also be used by synthetic chemists and
those involved in adultering esential oils, as the same type of column can be used to
separate out the enantiomers, which could then be added in the correct proportion for
a given essential oil, i.e. for Geranium oil Bourbon, the proportion of the ()-citronellol could be adjusted to 75 per cent for maximum odour quality and authenticity. It
is always difficult to keep up with forgers, let alone be a step ahead of them!
Like Geranium oil itself, Rhodinol ex Geranium is often adulterated with synthetic
rhodinol, fractions of citronella or palmarosa oils and synthetic components.
G. macrorrhizum (Zdravetz oil), produced almost solely in Bulgaria, has been used
for adulterating Geranium oil (Guenther, 1950; Pedro et al., 1992). The essential oil
composition of this Geranium oil differs completely from that of a true G. robertianum
oil or that of commercial Geranium oil from Pelargonium cultivars.
G. robertianum contains mainly -terpinene, linalool, -terpineol and an assortment
of monoterpenes in contrast to commercial Geranium oil with citronellol and geraniol
as its main components (Pedro et al., 1992).
The percentage of linalool in G. robertianum is considerably higher than that in commercial Geranium oil, which is about 310 per cent (Lis-Balchin, 1995; Lis-Balchin
et al., 1996), which was based on the actual analytical data of over 40 commercial
Geranium oils from different geographical sources (as on labels) bought from many
different commercial outlets). Adulteration with G. robertianum oil would therefore be
easily detected using conventional GC as well as simply by its smell.
Geographical source and chemical composition of commercial
Geranium oil
The apparent geographical source had on the whole no correlation with the chemical
composition of commercial Geranium oil (Lis-Balchin et al., 1996) except for the
presence or absence of the relevant sesquiterpene: i.e. 10-epi-g-eudesmol in
Egyptian oils (37 per cent) and guaia-6,9-diene (17 per cent) in the Bourbon and
China oils; a Moroccan oil contained both these sesquiterpenes. The proportion of
the main components i.e. citronellol, geraniol, linalool, iso-menthone, citronellyl
formate and geranyl formate was not consistent for any geographical source. The
bioactivity, as determined by the action of the oils against 25 different bacterial
species, 20 different Listeria monocytogenes cultivars, three different fungi and also
their anti-oxidant action was not correlated with either the geographical source of

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the Geranium oil specimens or their chemical composition. The activity of the main
components, citronellol and geraniol, was assessed against all the bioactivity
parameters either singly or in combination, in the percentages listed by the ISO for
different Geranium oils. The bioactivity was very potent for both the components,
and the mixtures. However, a sample of Australian oil extracted using fielddistillation and obtained directly from its source, was comparatively inactive,
suggesting possible adulteration of commercial oils with synthetic components
(Lis-Balchin et al., 1996).
The effects of different samples of Geranium oil was also investigated pharmacologically using guinea-pig ileum in vitro (Lis-Balchin et al., 1996). There was again a
variation in the bioactivity as shown by the relaxation produced in the smooth
muscle. There was insufficient variation to warrant this to be a sensitive method for
geranium, but other work using enantiomers (Lis-Balchin et al., 1996, 1999) have
indicated that there is scope for seeing differences in activity due to individual
enantiomers which react differently in different tissues.
In conclusion, due to the high sensitivity, biological evaluation using several
different parameters, can be a useful tool in evaluating essential oils and checking for
their adulteration, as it is more sensitive than ordinary GC.

PRICE OF GERANIUM OIL

The price of Geranium Bourbon has recently rocketed due to poor crops (through
cyclones and other calamities) and therefore scarcity of oil production. Although, it is
almost impossible to find out the production of pure Geranium oil, the imports into
USA from 1992, 1993, 1994 was increasing, showing about 53,000 kg, 64,000 kg,
82,000 kg respectively and in the last year having a market value of $57 per kg, having increased from $37 per kg from 1992.
The price/kg in 19992000 has reached between $160 for Chinese P. graveolens
oil to $360 for Geranium Rose Maroc (CH-Imports Ltd., Greensboro, USA
catalogue). Other sources of the oil are therefore eagerly sought, as China
has decreased production (from 80 ton in 1990 to 9.4 ton in 1991, (Quinhua,
1993)), and this is still falling; India may perhaps be able, in future, to bridge the
production gap.

TOXICITY OF PELARGONIUM SPECIES

Toxicology of the essential oil


Status

Geranium oil Bourbon, Algerian, Moroccan were granted generally recognised as safe
(GRAS) status by Flavoring Extract Manufacturers Association (FEMA) (1965) and
approved by the Food and Drug Administration (FDA) for food use. The Council of
Europe (1970) included Geranium oil in the list of spices, seasonings, etc., deemed
admissible for use with a possible limitation of the active principle in the final
product.

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Biological toxicity studies


Acute toxicity

Oral LD50 in rats, 5 g/kg; dermal in rabbits, 2.5 g/kg (Moreno, 1973). Irritation:
applied undiluted to abraded or intact rabbit skin for 24 h under occlusion was found
to be moderately irritant (Moreno, 1973), but applied to backs of hair-less mice, it was
not irritating (Urbach and Forbes, 1972). Human patch test (closed) to 10 per cent
Geranium oil in petrolatum produced no irritation after 48 h (Kligman, 1966).
Sensitisation

a maximisation test on 25 volunteers, using 10 per cent in petrolatum produced no


sensitisation (Kligman, 1966).
Phototoxicity

Was not found for Geranium oil (Urbach and Forbes, 1972).
Toxicity of Pelargonium species

Toxicity of Pelargonium is usually found under the heading of geranium toxicity. There
are very few, scattered, references to any toxicity, and all references are due to contact
dermatitis and sensitisation. Most of the references are to the Geranium oil and the
main components geraniol (Lovell, 1993).
Toxicity of Geranium oil Components
Patch tests to geraniol proved negative but dermatitis to perfumes containing
Geranium oil has been shown in a few cases (Klarmann, 1958). Ointments containing
geraniol e.g. Blastoestimulina were reported to cause sensitisation when used in the
treatment of chronic leg ulcers (Romaguera et al., 1986, Guerra et al., 1987), although
the patients were also sensitive to other ointments which contained no essential oils.
Blastoestimula contained:
Conc.
Glyco-D-116-F
as is
Corn oil
as is
Neomycin sulphate
20 per cent pet.
Geraniol
2 per cent pet.
Propylene glycol
10 per cent aq.
Centella asiatica extract
1 per cent o.o.
Lavender
2 per cent pet.
The patients were obviously sensitised prior to this by other chemicals. Sensitisation to
geraniol using a maximisation test proved negative (Opdyke, 1975), but the allergen
may be geraniol as cross-reactions often occurred with citronella (Keil, 1947), however,
the main sensitiser in citronella is citronellal, with citronellol less reactive; geraniol was
even weaker, as was citral. A patient who had used citronella oil to smear over his windows against mosquitoes developed a skin reaction and four other patients were found
with sensitivity to citronella. In two cases, strong reactions were obtained with 1 per cent

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solutions of citronellal and weaker ones with citronellol, geraniol, geranyl acetate. In
23/23 cases no response was found using lemon oil, therefore suggesting specificity
of the response. However, sensitisation to geraniol using a maximisation test proved
negative (Opdyke, 1975). In a lemon oil sensitisation case, -pinene gave a greater
response than -pinene: this is due to the close similarity between limonene and
-pinene (due to an exposed methylene radical).
Latest reports from Japanese studies, using patients with ordinary cosmetic dermatitis and pigmented cosmetic dermatitis, who showed a positive allergic responses to
a wide range of fragrances (Nakayama, 1998), gave a list of Class A fragrances which
were termed common cosmetic sensitisers and primary sensitisers. This Class included
Geranium oil, geraniol, sandalwood oil, artificial sandalwood, musk ambrette, jasmine
absolute, hydtroxycitronellal, Ylang ylang oil, cinnamic alcohol, cinnamaldehyde,
eugenol, balsam of Peru and lavender oil.
Geraniol was found to give a positive patch test in over 1.2 per cent cases when used
at 1 per cent in white petrolatum with 5 per cent sorbitan sesquioleate (Frosch, 1998).
Toxicity of Pelargonium plants
A vesicular hand dermatitis in a young man who removed dead leaves from an unknown
Pelargonium was reported (Anderson, 1923). This was not identified, and the paper
mentions it could have been one of hundreds of varieties. The patient had been suffering from tuberculosis, therefore his immunity was very low. The dermatitis was
successfully treated with black mercurial lotion!
Both zonals and forms of the scented rose geranium have caused sensitisation in a few
cases (Rook, 1961; Hjorth, 1969).

REFERENCES
Anderson, J.W. (1923) Geranium dermatitis. Archives Dermatol. Syphilology, 7, 510511.
Arctander, S. (1960) Perfume and Flavor Materials of Natural Origin, Elizabeth, New Jersey, USA.
Cu, J.-Q. (1996) Geranium oil from Yunnan, China. Perf. Flav., 21, 2324.
Culpeper, N. (1653) The English Physitian Enlarged, George Sawbridge, London.
Demarne, F.E. and van der Walt, J.J.A. (1989) Origin of rose-scented Pelargonium cultivar grown
on Reunion Island. S. Afr. J. Bot., 55, 184191.
Doimo, L., Fletcher, R.J. and DArcy, B.R. (1999) Chiral excess: measuring the chirality of geographically and seasonally different Geranium oils. J. Essent. Oil Res., 11, 291299.
FEMA (Flavoring Extract Manufacturers Association) (1965) Survey of flavoring ingredient
usage levels. No. 2508. Food Technol. Champaign, 19, part 2, 155.
Frosch, P.J. (1998) Are major components of fragrances a problem? In: P.J. Frosch, J.D.
Johansen, and I.R. White, (eds), Fragrances: Beneficial and Adverse Affects, Springer Verlag,
Berlin pp. 9299.
Fenaroli, G. (1997) Handbook of Flavour Ingredients. 3rd ed. CRC Press, London. Vol.1.
Grieve, M. (1937) A Modern Herbal. Reprinted 1992. Tiger books International London.
Guerra, P., Aguilar, A., Urbina, F., Cristobal, M.C. and Garcia-Perez, A. (1987) Contact dermatitis to geraniol in a leg ulcer. Contact Dermat., 16, 298299.
Guenther, E. (1950) The Essential Oils, Vol. 4, van Nostrand Co., New York.
Hjorth, N. (1969) Plant dermatitis. Contact Dermat, Newsletter, 6, p. 126.
Keil, H. (1947) Contact dermatitis due to oil of Citronella. J. Investig. Dermatol., 8, 327334.
Klarmann, E.G. (1958) Perfume dermatitis. Ann. Allergy, 16, 425434.

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Kligman, A.M. (1966) Report to RIFM, 31 October.


Lawrence, B.M. (1992) Progress in Essential Oils. Perf. Flav., 17(2), 4649; (6), 5960.
Lawrence, B.M. (1994) Progress in Essential Oils. Perf. Flav., 19(1), 4042.
Lis-Balchin, M. (1995) Aroma Science: The chemistry and activity of Essential Oils, Amberwood Pub.
Ltd., Surrey.
Lis-Balchin, M., Deans, S.G. and Hart, S. (1996) Bioactivity of commercial Geranium oil from
different sources. J. Essent. Oil Res., 8, 281290.
Lis-Balchin, M., Ochocka, R.J., Deans, S.G. and Hart, S. (1999) Differences in bioactivity
between the enantiomers of -pinene. J. Essent. Oil Res., 11, 393397.
Lovell, C.R. (1993) Plants and the skin, Blackwell Scientific. Publ., Oxford.
Moreno, O.M. (1973) Report to RIFM, 25 July.
Nakayama, H. (1998) Fragrance Hypersensitivity and its control. In: P.J. Frosch, J.D. Johansen,
and I.R. White (Eds) Fragrances: Beneficial and Adverse Affects, White, Springer Verlag, Berlin
pp. 8391.
Ognyanov, I. (1985) Bulgarian Zdravetz oil. Perf. Flav., 10(6), 3844.
Opdyke, D.L.T. (1975) Monographs on fragrance raw materials. Food Cosmet. Toxicol., 13, 451.
Pedro, L.G., Pais, M.S.S. and Scheffer, J.J.C. (1992) Composition of the essential oil of Geranium
robertianum L. Flav. Fragr. J., 7, 223226.
Quinhua, Z. (1993) Chinas perfumery industry picks up. Perf. Flav., 18, 4748.
Ravid, U., Putievsky, E., Katzir, I., Ikan, R. and Weinstein, V. (1992) Determination of the
enantiomeric composition of citronellol in essential oils by chiral GC analysis on a modified
-cyclodextrin phase. Flav. Fragr. J., 7, 235238.
Romaguera, C., Grimalt, F. and Vilaplana, J. (1986) Geraniol dermatitis. Contact Dermat., 14,
185186.
Rook, A. (1961) Plant dermatitis-botanical aspects. Trans. St. Johns Dermatol. Soc., 46, 4147.
Urbach, F. and Forbes, P.D. (1972) Report to RIFM, 22 September.
Verlet, N. (1992) Geranium Bourbon: quel avenir? Parf Cosmet. Aromes, 108, 4951.
Weiss, E.A. (1997) Essential Oil Crops, CAB International, Oxon.

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18

Rose-scented geranium a Pelargonium


grown for the perfume industry
Frdric-Emmanuel Demarne

INTRODUCTION

The interest shown in growing scented-leaf geranium dates from the mid nineteenth
century. At that time, the real Rose of the Levant, Rosa damascena Mill. (Rosaceae),
became rare and its essential oil reached excessive levels of price in Paris (Hricart De
Thury, 1845). This situation forced the perfumers to look for new essential oils with a
rose scent and they remembered the distillation trials of rose geranium carried out by
Rochez in Lyon (France) in 1819. In 1844, Demarson established the first plantations
in the sunshine of Provence, near Grasse (France).
But, from a physiological point of view, the geranium cultivation requires generous sunshine and well-drained soils, rich in organic matter. The crop dreads frost and temperatures
below 2 C as they are harmful to the growth and even to the survival of the plant.
And, from an agro-economic point of view, the traditional cultural practices are very
labour consuming: preparation of cuttings for plantation, muck-spreading, hoeing for
weed control, manual harvesting and firewood duty for distillation are costly operations.
Furthermore, in the countries with pronounced winter season, the risk of frost leads to
an annual crop management and needs to shelter the cuttings till the next plantation.
For these reasons and because of the lack of mechanised solutions, the production of
rose Geranium oil did not take a long time to abandon the South of France and to move
to more merciful skies, where an abundant and cheap labour existed. From 1850, the
French colonies of northern Africa and Indian Ocean seem predestined for growing
geranium. The crop is introduced to Algeria in 1847 and developed on an industrial
scale by Lon Chiris and Monk towards 1865 (Naves, 1934; Igolen, 1941). In 1880 the
plant is introduced to Reunion Island where it will be distilled for the first time in
1882. After the turn of the twentieth century, the crop was attempted in Corsica, Italy,
Morocco, Tunisia, Egypt, Southern Russia, Congo, Kenya, Tanganyika, Madagascar,
India, Spain, Portugal, Brazil, Comoro Islands . . . The most recent development was
in the Peoples Republic of China in the fifties.
TAXONOMY AND GENETICS

Since the beginning, and as pointed out by Guenther (1951), the taxonomy of the plants
which are cultivated in various parts of the world for the production of commercial
Geranium oil has been a matter of much controversy and has given rise to considerable

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Frdric-Emmanuel Demarne

confusion. Basically, the name geranium itself is incorrect, since the species involved in
the production of rose Geranium oil are all Pelargonium, not Geranium. All these plants
belong to the Geraniaceae family, but Geranium and Pelargonium form two different
genera, beside three other which are Erodium, Monsonia and Sarcocaulon.
In the same way, the cultivars which, by a great misnomer, are referred to as P. capitatum or P. graveolens or P. radens are not natural species. According to the revision of
the genus Pelargonium, carried out since 1977 under the supervision of J.J.A. van der
Walt at the University of Stellenbosch (Republic of South Africa) (van der Walt, 1985),
we now know that the true P. radens H.E. Moore (Moore, 1955) and P. graveolens LHrit.
(LHritier Dom De Brutelle, 1789) are mint-scented species (van der Walt and
Demarne, 1988) with 88 chromosomes (Albers and van der Walt, 1984), while
P. capitatum (L.) LHrit. is a 66 chromosomes species very poor in essential oil and
with a very faint rose scent (Demarne et al., 1993; Viljoen et al., 1995). All these
natural species have originated from Southern Africa.
According to past and recent researches in genetics (Ducellier, 1933; Kuchuloriya,
1964, 1968; Demarne, 1989; Demarne and van der Walt, 1989), we also know that all
the cultivars grown worldwide for rose Geranium oil production are interspecific
hybrids between P. capitatum, on one hand, and P. graveolens or/and P. radens, on the
other hand. Most of these cultivars have 77 chromosomes (Tamai et al., 1958, 1963;
Payet, 1981; Demarne, 1989) and their main features (chromosome number, habit, leaf
and flower shape, essential oil yield and composition . . . ) are in-between those of their
natural parents. The oil composition in particular depends on the P. capitatum parent
which transmits the ability to synthesise geraniol and citronellol rather than isomenthone. Furthermore, the presence of 6,9-guaiadiene and/or 10-epi--eudesmol, which
usually distinguishes between the African type and Bourbon type oils (Vernin and
Metzger, 1983), is also inherited from the P. capitatum parent.
Thus, the cultivars of rose-scented geranium should be named Pelargonium hybrids of
P. capitatum  P. radens or Pelargonium hybrids of P. capitatum  P. graveolens. The choice
of the proper variety, when establishing a new production anywhere in the world, is
fundamental: it will directly influence the yield and the quality of the oil.
CULTIVATION

Growing rose geranium for essential oil production is not easy. For a profitable crop, this
fragile bush must be cultivated as a perennial on a 35 year basis, and every harvest can
question its survival. This is especially true when the plantations are established in tropical countries, where fungal and bacterial diseases are numerous and particularly virulent.
Probably because of that fragility, rose geranium is usually grown on small plots of
about 12 ha, sometimes less. Most of the cultural practices are done by hand, making
the cultivation resemble horticulture and keeping the farmer busy throughout the year.
Propagation
All the cultivars of rose geranium are heterozygotic and highly polyploid (x 11;
2n 7x 77 chromosomes). Due to their hybrid character and their unusual
chromosome number, the plants are usually male-sterile and do not set seed (Ducellier,
1933; Tokumasu, 1970). Their agronomic performances and the quality of their essen-

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tial oils depend on complex genetic balances. Therefore, asexual propagation is the rule
and the cultivars are usually propagated by terminal stem cuttings.
Rooting of the cuttings is influenced by the nutritional state (carbohydrates/nitrogen
ratio), the sanitary state and the age of the mother-plants (Bricheteau et al., 1980;
Dartigues and Lemaire, 1980; Vidalie, 1980), by wilting and application of rootpromoting hormones and fungicides (Michellon, 1975, 1976; Demarne, 1981, 1992c;
Rajeswara Rao et al., 1993), and by water supply, temperature and growing medium.
From a common experience, the best rooting is obtained from herbaceous terminal stem
cuttings of 1220 cm long (710 nodes) with 45 terminal leaves, grown in nursery under
partial shade and mist irrigation. Day/night temperature should be 2127/1217 C and
the growing medium should provide a sufficient porosity as well as a good water-holding
capacity to allow good aeration and good water supply. Treating the base of the cuttings
with a mixture of indolebutyric acid (IBA/0.10.2 per cent) and captane (10 per cent)
in talcum powder is also recommended. Under those conditions, the cuttings quickly
develop a profuse root system and are ready for transplanting after 4060 days.
However, beside these ideal conditions of propagation, a traditional method is still
in use in most of the producing countries. It consists of planting unrooted woody
cuttings, 3040 cm long, directly into the field, just after the rainy season, but
unfortunately, the mortality rate after planting is usually high.
Planting and cropping system
The profitability of a geranium crop is directly correlated to the number of plants per
hectare. Depending on soil and climatic conditions, plant spacing varies between
80  30 cm and 100  60 cm; the optimum being of about 35,000 plants/ha. Rose
geranium is generally cultivated as a pure crop installed on a cleared land. Cuttings are
planted in holes or furrows dug manually, at the bottom of which the farmer usually
puts a handful of manure (farm manure or composted distillation residues) and sometimes, some fertilizer, lime, and a slow-released insecticide to prevent the young roots
from white grubs and other soil insect attacks.
During the first 6 months, geranium grow quite slowly, leaving large portions of the
inter-row uncovered. Intercroping geranium with short duration legumes or maize
allows a profitable use of this space and an efficient weed control (Lougnon, 1924;
Prakasa Rao et al., 1984a, 1986; Narayana et al., 1986; Garin, 1987).
In the traditional cropping systems, rose geranium is thus a perennial weeded crop, and
in the tropical countries, rainfall combined with hoeing for weed control causes severe
erosion. Fields on a slope must be arranged in bench terraces with swathes, and new concepts of sustainable agriculture, based on planting geranium into a controlled cover crop,
are now developed. These techniques favour the microbiological activity of the soil and
lead to a better preservation of soil fertility and a better water management (Michellon
et al., 1994a,b, 1996; Perret et al., 1996). The foliage production and the life span of the
crop are thus improved, but the drawback is that this agriculture is more technical,
especially in keeping the cover crop under control, without damaging the rose geranium.
Fertilization
In traditional cultivation, the fertilization of rose geranium usually combines chemical
fertilization, restitution of organic matter and sometimes liming (Garin, 1987).

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Frdric-Emmanuel Demarne

Because of their relatively high costs, the chemical fertilizers are sparingly used
(Chabalier, 1992). The composted residues of distillation and/or an organic manure
bring back to the field some fertilizer elements, but the time of application and the
placement of these residues mainly benefit the intercrops. Generally speaking, the
fertilization level is low and the traditional system is not stable.
Chemical fertilization
The first fertilization trials on rose geranium date from 1894. According to Fritz (1976),
a high yield crop can produce 7 tons of dry matter/ha/year, which correspond to average
exportations of 100 kg N, 32 kg P2O5, 165 kg K2O, 250 kg CaO, 28 kg MgO, 15 kg
Na and 10 kg S. The dry matter is about 1820 per cent of the total biomass. These
figures obtained on Reunion Island have been confirmed in India (Prakasa Rao et al.,
1988).
It is now well known that rose geranium responds to nitrogen applications but on
the condition that balanced fertilization is used and other elements are not limited,
especially phosphorus (Chabalier, 1992). On Reunion Island, Fritz has observed linear
increases of herb yield with nitrogen applications up to 150 kg/ha/year (Fritz, 1976).
Similar results were obtained in India with doses up to 225 kg/ha/year (Prakasa Rao
et al., 1986, 1988).
Rose geranium also responds to phosphate applications. Fritz (1976) observed that
the essential oil yield is linked to the P content of the plant and, as far back as 1899,
Dantes (1899) reported that massive applications of superphosphate (2 t/ha) doubled
the herb yield. Weiss (1967) reported similar results in Kenya and advised the renewal
of the application of 200 kg/ha of P2O5 after the fifth harvest of a geranium crop. Other
hints are given by Chabalier (1992) to grow rose geranium in andic1 soils and to
prevent phosphorus deficiencies when this element is made unavailable by the absorbing complex of the soil.
Rose geranium can withstand low levels of potassium before displaying deficiency
symptoms. Those symptoms and a yield drop appear when the K content of the plant
drops down 0.3 per cent of the dry matter (Chabalier, 1992).
Lastly, spraying miconutrients (B, Cu, Zn, Mo . . .) is sometimes recommended
(Ladaria, 1968; Arumugam and Kumar, 1979; Dhakshinamoorthy et al., 1980; Prakasa
Rao et al., 1984b). Under certain conditions, those trace elements can favour the oil
production.
In practice, the type of chemical fertilizer will depend on the soil conditions and on
the cropping system; the doses and the applications timetable will depend on the
possible level of intensification. For an intensive crop, the theoretical fertilization,
based on the restoration of the exported nutrients and on the normal losses is 150200
kg N/ 6080 kg P2O5/150200 kg K2O.
N, P and K can be combined by using a complete fertilizer at the time of planting
and then once a year at the end of the rainy season. In intensive cultivation N (urea or
calcium ammonium nitrate) can be applied in 24 split doses. In any case, when the
fertilizer is put in the hole at the time of planting, it is important to avoid the contact
between the cutting and the fertilizer to prevent burning.

1 Dark soil of volcanic origin, with particular physical and chemical properties.

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Lime and organic manure


When rose geranium is traditionally grown without a cover crop, its erosive character
often requires incorporated applications of lime and organic matter for restoring the soil
fertility. In Reunion Island, an additional practice consists in a several years growth of
bush fallow of Acacia decurrens before planting.
In all cases, the use of organic manure in combination with fertilizers at the time
of planting is advocated. The beneficial impact of organic matter to the microbial activity
and soil structure is well known. Michellon (1987) observed that application of
510 tons of distillation residues on a geranium intercropped with legumes leads to a
better root development and a two-fold increase of essential oil yield compared with
geranium grown as a sole crop. Further to that observation, Chabalier (1992) gave the
composition of different sources of organic matter suitable for rose geranium cultivation.
Irrigation
Rose geranium is rather drought resistant and dreads excess of water. Irrigation is
usually left to nature and when a waterlogging risk exists, the cuttings are planted
on ridges for insuring a good drainage, as in the Nile valley in Egypt.
But, attempts made to grow geranium in harsh weather conditions in Egypt (Koriesh
and Atta, 1986), in Israel (Sanderovich et al., 1983) or in India (Singh et al., 1996;
Sabina Aiyanna et al., 1998; Singh, 1999), demonstrated that rose geranium can take
advantage of different techniques of irrigation and fertigation to increase both its herb
and essential oil yields per hectare. However, a negative correlation is often found
between plant water content and the essential oil content, as a result of irrigation
treatment (Sanderovich et al., 1983).
In intensive cropping systems, both plasticulture and cover crops allow the reduction
of the water needs of the crop.
Weed control
Weed control is important in geranium cultivation. Under tropical and sub-tropical
climates, weeds grow very quickly and tend to invade the fields, competing with the crop
for space, light, water and nutrients. When left uncontrolled, the weeds smother the young
cuttings which become etiolated; they limit growth and branching leading to poor yields
(Trmel, 1992; Rajeswara Rao and Bhattacharya, 1997). Moreover, some odouriferous
weeds can be harvested and distilled with the crop and will affect the quality of the oil.
In most producing countries, manual weeding is practised. This operation is very labourconsuming and requires from 60 to 125 days of labourer/ha/year. Even when herbicides are
used in the inter-row, weeding the row is always done manually. In practice, weed control
is a combination of manual hoeing, herbicide application, cultural tricks (mulching,
plasticulture . . . ) and suitable rotations or co-cultivation with soil-cover plants.
In all cases, man must keep in mind that hoeing tends to deconstruct and to dry the
soil, increasing the erosion. On the other hand, pre-emergence, systemic or contact herbicides can be used but they must be checked against their ability to be traced later in the
essential oil. Different active ingredients have been tested on numerous weeds in geranium
cultivation (atrazine, diuron, glyphosate, paraquat, metribuzine, nitrophen, alachlor. . . );
their selectivity and the way to use them is available in the literature (Gravaud et al.,
1976; Srinivasan et al., 1979; Didelot et al., 1985; Garin, 1987; Trmel, 1992).

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Pest and diseases


Rose geranium in cultivation is subject to attacks of insects, nematodes, fungi and
bacteria. Pests and diseases are so numerous that it seems inconceivable to give the
chemicals a miss and to produce organic Geranium oil in profitable conditions.
A little information is available on pests in Egypt and China, but in Reunion Island,
a general survey (Quilici et al., 1992) of the harmful insects revealed that geranium is
attacked by at least 14 different species belonging to the Hemiptera (six species), Coleoptera
(three species), and Lepidoptera (five species). Among the most important pests are the
white grubs of Hoplochelus marginalis Fairmaire (Coleoptera, Fam. Scarabaeidae), the
cockchafers Cratopus humeralis Boh., and C. angustatus Boh. (Coleoptera, Fam. Curculionidae),
the whitefly Trialeurodes vaporariorum Westwood (Hemiptera, Fam. Aleyrodidae), the scale
insect Pseudaulacaspis pentagona Targioni-Tozzetti (Hemiptera, Fam. Diaspididae) and the
defoliating caterpillar of Lobesia vanillana (Lepidoptera, Fam. Tortricidae). An efficient integrated control of these insects exists as a combination of light trapping, agronomic
controls (minimum tillage, cover-crop . . .), chemical controls (insecticides spraying,
chemical trapping . . .) and biological controls (with insects and fungi which parasitize the
larva) (Quilici et al., 1992).
Nematodes have also been reported as important pests, especially in India. According
to Rajeswara Rao (personal communication) several species of Criconemoides,
Helicotylenchus, Meloidogyne, Pratylenchus, Scutellonema and Xiphenema damage the crop
and inflict yield losses up to 75.8 per cent (Doraswamy et al., 1979; Kumar and
Nanjan, 1985; Anita and Vadivelu, 1997). Chemical control seems possible as well as
biological control with a nematophagous fungus and/or companion cropping with
nematicidal plants (periwinkle, marigold . . . ) (Anita and Vadivelu, 1997).
Fungal and bacterial diseases are also numerous and very virulent, and considerable literature is available on these subjects. Several lists were established by different plant
pathologists who have studied and referenced the pathogens in the producing countries
(Bouriquet, 1946; Sinaretty and Trmel, 1992) (Rajeswara Rao) personal communication).
Wilt, dieback, leaf blight, leaf spot, root and stem rot, anthracnose, are common and can
be ascribed to several species of fungus (Colletotrichum, Botrytis, Septoria, Cercospora,
Armillaria, Rosellinia, Phomopsis, Pythium, Fusarium. . .) and bacteria (Pseudomonas
solanacaerum). Certain of those pathogens cause severe damages leading sometimes to the
total destruction of the crop and the impossibility of growing geranium again on the same
plot (e.g. wilt caused by Pseudomonas solanacearum). Generally speaking, the suggested control measures of these pathogens are only partially satisfactory, even if anthracnose and
botrytis can be controlled by spraying specific fungicides. Despite the need for resistant
varieties, a genetic improvement program does not seem reasonable or economically viable
regarding the economic importance of the crop in the individual oil-producing countries.
HARVESTING

The Geranium oil is contained in glandular trichomes (Demarne and van der Walt, 1989)
which are mainly located on both surfaces of the young leaves, on the young stems, on the
buds and on different parts of the inflorescences. Oil is thus obtained from the top
young parts of the plant and, because of the perennial character of the crop, harvesting
geranium must fulfil two opposing objectives: the maximum production of herb and
the preservation of the subsequent shoot development ability (Demarne, 1992d).

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Therefore, the performance of a particular harvesting technique depends on the


actual herb and essential oil yields, but also on the re-growth of the plants and the rate
of mortality. The quality of the shoot development will govern the frequency and the
yield of the subsequent harvests on individual plants, while the rate of mortality will
drastically influence the number of plant per hectare, the time spent to fill in the gaps
and hence the survival and the medium-term profitability of the crop.
From that point of view, manual harvesting with secateurs, knives or sickles is the best
way for harvesting geranium as it prioritizes an individual approach of the plant architecture and tends to optimize both the herb yield and the re-growth ability. On the contrary, mechanical harvesting carries out an intermediate trimming of the whole field and
only optimizes the labour productivity. Whatever principles they are based on (Korezawa
et al., 1967; Boyko, 1977; Paillat, 1987; Ducreux, 1993), the mechanical harvesters
developed up till now partly solve the question of plant re-growth in cutting the utmost
top of plants only (Demarne, 1992a) and in the different trials conducted mainly in
Reunion, the loss of earnings was offset in increasing the harvesting frequency. Details on
the way to prune rose geranium in different conditions are available in the literature
(Doraswamy and Sundaram, 1982; Demarne, 1992d).
For all these reasons, geranium is still largely harvested by hand. The crop is ready for
the first harvest 68 months after planting. Subsequent harvests are made at 35 months
intervals, depending on plant development, weather conditions, crop management,
labour availability. . . In all cases, harvests must be performed on clear and sunny days.
The plant material is usually left one day on the inter-row to wilt. It is then transported
to the distillery. At that time, heaping up or chopping the plant material is inadvisable
to avoid fermentation, and distillation must be done quickly.
DISTILLATION

Distillation is the ultimate step of geranium cultivation. Because the essential oil is
located in secretory sacs at the end of glandular hairs, its extraction is easy. Therefore,
all the techniques of distillation and organic solvent or supercritical fluid extraction
(SFE) give results; the differences being only in the yield and the quality of the
products. In practice, there is only a market for water-distilled essential oil. Only Egypt
produces and markets on request small quantities of geranium concrete and/or absolute.
Different kinds of distillery can be found in the producing countries, which correspond to different technical, economical and social situations. The numerous direct-fired
stills of about 1000 l capacity operating in the countryside in Reunion Island, in China,
in Egypt or in India have nothing in common with the batteries of 3000 l stills
equipped with a separate boiler and encountered in certain factories, in Egypt or in
Reunion Island.
However, the major part of the world production of Geranium oil is distilled in small
units, belonging to small holders or to village communities. Processing 300350 kg of
plant material in a 1000 l direct-fired equipment lasts 90150 min and gives a 0.10.2
per cent yield of oil. A complete description of the traditional equipment, including
the limiting factors, the possible improvements and the detailed field distillation procedure is available in the literature (Demarne, 1992b). However it is interesting to
point out that under such conditions, the distillation of 1 ha can take 40100 days/year,
without counting the time necessary for firewood or charcoal duty.

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ESSENTIAL OIL PRODUCTION

World production
After more than one century of attempts, the so-called rose Geranium oil is now produced mainly in the Peoples Republic of China, Egypt, Reunion Island and India.
A few kilos are also exported from Madagascar and smaller quantities are sometimes
produced in Algeria, Morocco and Russia.
China is now by far the biggest producer of Geranium oil. The cultivation is concentrated in the Yunnan Province, in the district of Binchuan. From an agricultural
point of view, geranium is grown as a perennial (3 years) and makes the best of the horticultural techniques of the Chinese agriculture; the fields can be harvested four times
a year, and the average oil yield is pretty good ( 45 kg/ha). An accurate assessment of
the Chinese production and domestic consumption is precluded by the lack of reliable
statistical data. Nevertheless and for several years, the annual production seems to be
about 80110 t, of which 2030 t are used on the Chinese domestic fragrance market
and 6080 t are exported.
Egypt is the second biggest producer. Major areas of production are primarily in
upper Egypt, mainly Bani Sweif and Fayoum. In this country the crop is annual, with
two harvests a year. The oil is of the African type, as it contains substantial quantities
of 10-epi--eudesmol. According to different sources, the production in the past
10 years has averaged 5055 t per year, with important year to year fluctuations.
On Reunion Island, despite big efforts made by the French government and the local
authorities to support the production through research and development programs, and
the remarkable results obtained by the agronomists, the production of rose Geranium
oil has drastically declined over the years. The unequalled quality of the real Bourbon
oil, universally recognised in high class perfumery, has not been sufficient to maintain
the price at levels that can balance the increasing standard of living of the population
and nowadays, the annual production is about 6 t, all of which is exported.
India has a small production ( 2 t) in south hills and plains (Nilgiri hills, Pulney
hills) which is used for its internal market.
International trade and demand
The main importers of Geranium oil are France and USA. However, whereas the bulk
of US imports are consumed domestically, there is a big re-export trade from France.
The French exports consist, on one hand, in pure Geranium oil and, on the other hand,
in a proportion of oil that has been re-processed and blended to users specifications. In
most cases these oils are of very high quality.
The international trade appears to be relatively stable and it is very likely that the USA
and France will continue to dominate the import trade for the foreseeable future
(Robbins, 1984). The average annual imports of Geranium oil into the USA are about
6065 t, and into France about 9095 t. Japan imports about 15 t and the remainder of
the European Community an other additional 30 t. Other appreciable markets include
Brazil, India and a few others, but the trade statistics often fail to show Geranium oil separately, and it is difficult to gauge the extent of these trade flows in the majority of cases.
For all these markets combined, the total need is about 220 t, when trade between
the USA and European Community, and within the European Community, is excluded.

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All in all, the supply no longer fits the demand, and despite a production adjustment
between the main sources, there is still an extra demand for 2025 t of a very high
quality Geranium oil to replace the Bourbon type.
Geranium oil is purchased and assessed mainly on the basis of its odour character and,
in a lesser extent on its suitability for the preparation of rhodinol. For many years, it
was traded almost exclusively on the basis of samples and this procedure still applies,
even if, for certain origins (Bourbon and certain Yunnan oils), it is possible to buy on
the basis of product description only.
In the importing countries, Geranium oil is traditionally marketed through
a comprehensive network of intermediaries of various types including import merchants, dealers, commissioned brokers, agents and the processing and compounding
houses. Geranium oil prices vary widely depending on the quality, the origin and also
unforeseen supply fluctuations. Bourbon oil from Reunion Island traditionally
commanded a price premium over oils from other sources, but the shortage of this
quality in the recent years has caused switches to oils from alternative sources, causing
the price of the latter oils to rise sharply.
OIL COMPOSITION AND QUALITY

Geranium oil is one of the most important raw materials used in perfume and soap
industries. This product is rather well known and has been studied for the end of the
nineteenth century. Its physical properties and its chemical composition have given rise
to a great number of publication, as the analytical techniques progressed.
The works of Naves (Naves, 1934, 1944, 1951, 1957; Naves et al., 1935, 1961, 1963;
Melera and Naves, 1961; Naves and Tullen, 1961; Naves and Ochsner, 1962; Benesova
et al., 1964; Romanuk et al., 1964; Krepinsky 1966), Teisseire (Teisseire and Corbier, 1964;
Pesnelle et al., 1969, 1971), Giannotti (Giannotti, 1966; Giannotti and Schwang, 1968a, b),
Wolff et al. (1963), Klein (Klein and Rojahn, 1977; Rojahn and Klein, 1977), have been
amongst the important contributions to the knowledge of the chemical composition of the
Geranium oil. Since 1960, the development of gas-chromatography (GC) and associated
identification techniques (GC-MS, GC-FTIR...) have sped up this acquisition of knowledge
with the works of Garnro et al. (Garnro and Buil, 1969; Garnro, 1974; Garnro et al.,
1980), Peyron (Peyron, 1962a, b), Teisseire (Corbier and Teisseire, 1966; Pesnelle et al.,
1969), Kaptanidis (Heuss et al., 1969), Timmer (Timmer et al., 1971; Ter-Heide et al.,
1975), Kami (Kami et al., 1969), Kaiser (Kaiser, 1984), Demarne (Gurre and Demarne,
1985; Demarne, 1989), Vrin (Vrin et al., 1998), and others. More recently, techniques of
multidimensional chiral gas chromatography coupled with mass spectrometry (enantioMDGC/MS) (Ravid et al., 1992; Kreis and Mosandl, 1993; Casabianca et al., 1996; Wst and
Mosandl, 1998, 1999; Wst et al., 1996, 1998a,b, 1999; Allemant, 1998; Doimo et al.,
1999) has led to a better knowledge of the enantiomeric distribution of chiral compounds in
the oils of different origins and, in a certain extent, could be used as criteria for authenticity
assessment.
Based on this mass of academic information, applied research programs were carried
out on the variation in the quality of the oil and to determine the influence of different
internal, external and management factors influencing this (Gailleton, 1959; Korezawa
and Tanida, 1969; Naragund and Divakar, 1983; Obaladze and Kuchuloriya, 1986;
Angadi and Vasantha Kumar, 1989; Demarne and van der Walt, 1989; Zobenko and

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Arinshtein, 1989; Kulkarni et al., 1997), the climate and the soil (Charapov, 1968;
Kalix, 1968; Michellon, 1980; Sun Handong et al., 1985; Rajeswara Rao et al., 1990,
1996; Bhattacharya et al., 1993; Yan Dongwei et al., 1994; Southwell et al., 1995;
Chakib, 1998), the plant part (Pieribattesti, 1982; Mallavarapu et al., 1997), the crop
age (Kaul et al., 1998), the shade (Kaul et al., 1997b), the fertilization (Korezawa, 1961),
the presence of weeds and diseases (Rajeswara Rao and Bhattacharya, 1997; Rajeswara
Rao et al., 1999a), the irrigation (Singh, 1999), the time of harvesting and the technique
used (Yoshida et al., 1968; Mani and Sampath, 1981; Ravid and Putievsky, 1983;
Tiberghien, 1989; Baret, 1991; Prakasa Rao et al., 1995; Rajeswara Rao et al., 1996), the
post-harvest treatments (Mani et al., 1981; Rajeswara Rao, et al., 1992, 1999b), the distillation (Gurre et al., 1985), the conditions and duration of storage (Mani et al., 1981;
Mahmoud et al., 1983; Kaul, et al., 1997a).
All these studies would tend to confirm that as far as the production scale is concerned, the three main important factors influencing the oil quality are the variety, the
soil and climate conditions and also the distillation procedure. The quality variations
of the oil mainly concern the relative concentrations of eight important compounds
which are (E)- and (Z)-rose oxides, linalool, geraniol, citronellol, isomenthone,
guaia-6,9-diene and 10-epi--eudesmol.
Chemical composition of the oil
Several reviews were published by Lawrence (Lawrence, 1976, 1978, 1984, 1985, 1986,
1988, 1992, 1994, 1996, 1999) during the last years, which amalgamated the information published in the scientific literature on the composition of different Geranium
oils from different geographical origins, but also on the identification of new components of the oil and on the enantiomeric ratios of some chiral compounds
( -terpineol, rose oxides, linalool, citronellol, menthone, isomenthone). Rose
Geranium oil is a very complex product that contains hundreds of compounds, some
being hydrocarbons (aliphatic, aromatic, monoterpenic, sesquiterpenic with different
skeletons), and the others being oxygenated with alcohol, phenol, oxide, aldehyde,
ketone, acid, ester and ether functional groups.
Only 30 compounds are regularly and individually present at more than 0.3 per cent
of the oil; together they represent about 90 per cent of the essential oil and are sufficient to form the basis of the essential oil quality. The other components appear as
traces, the correct identification of which is sometimes difficult, especially when
sesquiterpenic hydrocarbons are concerned.
Quality
So, the quality of rose Geranium oil used in the fragrance industries depend on several
criteria, from analytical determinations to compliance with international standards.
The standards classify the Geranium oils into three types, according to their origins:
the Chinese type is applicable to the essential from the Peoples Republic of China, the
African type is for the oils from Algeria, Morocco and Egypt, and the Bourbon type
for the essential oil from Reunion Island. The other oils are produced in too small
quantities to be the subject of particular standards; when they appear on the international market, they are bought on the basis of their similarities with one of the three
above-mentioned types.

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According to the standards (Anonymous, 1996), the Geranium oils are easily characterised by their physical properties (specific gravity, optical rotation, refractive index,
flash point, solubility in ethanol and colour), chemical properties (acid value, ester
value, carbonyl value) and above all by their organoleptic properties (aspect, colour,
odour) and their GCs profiles. The rose Geranium oils are liquid, limpid and less dense
than water (0.88220d200.892). Their colour vary from amber-yellow (Egypt) to
yellowish-green, brownish-green or green (Bourbon). They all have a strong rose
scent with a more or less pronounced mint note depending on their origin.
Capillary GC using polar or non-polar phases reveals that the major components of
the oils are the monoterpenic alcohols (citronellol, geraniol, nerol, linalool, -terpineol)
and their esters (citronellyl formate, citronellyl butyrate, citronellyl propionate,
citronellyl tiglate, geranyl formate, geranyl butyrate, geranyl propionate, geranyl
tiglate, neryl formate), the monoterpenic ketones (menthone, ()-isomenthone), the
monoterpenic aldehydes (neral, geranial), the monoterpenic oxides ((E)- and (Z)-rose
oxides), monoterpenic hydrocarbons (-pinene, myrcene, limonene . . .), an aromatic
ester (phenylethyl tiglate), several sesquiterpenic hydrocarbons (guaia-6,9-diene,
germacrene D, -bourbonene, -caryophyllene), two sesquiterpenic ketones (furopelargones A and B) and a sesquiterpenic alcohol (10-epi--eudesmol).
Among these components, geraniol, citronellol, linalool, isomenthone, geranyl formate, citronellyl formate, guaia-6,9-diene and 10-epi--eudesmol play a particular
role, as they allow to distinguish between oils of different origins and different varieties
of rose geranium. The Bourbon type oil from Reunion Island contains large quantities
(ca. 57 per cent) of guaia-6,9-diene but does not contain 10-epi--eudesmol. Chinese
geranium does not contain 10-epi--eudesmol as well. On the contrary, the African
types contain 10-epi--eudesmol (ca. 45 per cent) but do not contain guaia-6,9-diene
(Pesnelle et al., 1969, 1971). However, when the varieties and the growing conditions
are not fixed for long, both guaia-6,9-diene and 10-epi--eudesmol can be found
together, as in some Indian oils (Kaul et al., 1997b), but on the international market
this lead to suspicions of blending between oils of different origins.
Linalool is a good indicator of the extraction process as it seems to be formed from
geraniol during steam water distillation. When the herb is extracted with solvent, the
concrete thus obtained contains only small quantities of linalool (0.5 per cent). But
when the herb is distilled for more than 2 h in a traditional field equipment, the oil
contains 510 per cent of linalool; the sum (linalool  geraniol) being constant in both
the solvent extract and the water-distilled oil (Gurre et al., 1985). In the industrial
process, because of a limited contact between the herb and hot water, the linalool
percentage is in-between those limits (ca. 45 per cent).
Geraniol, linalool and citronellol together also typify the different qualities.
Citronellol is usually higher in Chinese oil (3840 per cent) and Egyptian oil (3133
per cent) than in Bourbon oil (1921 per cent). On the contrary, geraniol and consequently linalool are higher in Bourbon oil (1619 per cent/710 per cent) than in
Egyptian oil (1315/56 per cent) and Chinese oil (710/23 per cent); the ratio
(linalool  geraniol)/citronellol varies from 0.3 (Chinese oil) to 0.6 (Egyptian oil) and
1.4 (Bourbon oil). The amount of geranyl formate and citronellyl formate are proportional to the corresponding alcohol in the oils; isomenthone is slightly higher in
Bourbon oil (89 per cent) than in the others oils (ca. 6 per cent).
As far as the Indian oils are concerned, these figures vary depending on the variety
under cultivation. The oil of certain cultivars even contain more geraniol than citronellol.

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Wst, M., Beck, T., Dietrich, A. and Mosandl, A. (1996) On the biogenesis of rose oxide in
Pelargonium graveolens LHritier and Pelargonium radens H.E. Moore. Enantiomer, 1, 167176.
Wst, M. and Mosandl, A. (1998) On the biogenesis of rose oxide in Pelargonium graveolens
(Geraniaceae). In 29th International Symposium on Essential Oils, Frankfurt am Main
(Germany), September 69.
Wst, M. and Mosandl, A. (1999) Important chiral monoterpenoid ethers in flavours and essential oils enantioselective analysis and biogenesis. Eur. Food Res. Tech., 209(1), 311.
Wst, M., Reindl, J., Fuchs, S., Beck, T., and Mosandl, A. (1999) Structure elucidation, enantioselective analysis, and biogenesis of nerol oxide in Pelargonium species. J. Agric. Food
Chem., 47(8), 31453150.
Wst, M., Rexroth, A., Beck, T., and Mosandl, A. (1998a) Mechanistic aspects of the biogenesis of rose oxide in Pelargonium graveolens LHritier. Chirality, 10(3), 229237.
Wst, M., Rexroth, A., Beck, T., and Mosandl, A. (1998) Structure elucidation of cis- and transrose oxyde ketone and its enantioselective analysis in Geranium oils. In 29th International
Symposium on Essential Oils, Frankfurt am Main (Germany), September 69.
Yan Dongwei, Zhang Zhengju, and Ouyang Ning (1994) Analysis of the chemical compositions of essential oils from scented leaves of Pelargonium hybrids acclimated in Yunnan
province. Fruits, 49(1), 22.
Yoshida, T., Ikawa, S. and Morisada, S. (1968) Seasonal variation of both the percentage yield
of essential oil and the chemical composition in Pelargonium species. Proc. Crop Sci. Soc. of Jpn.,
37(4), 565569.
Zobenko, L.P. and Arinshtein, A.I. (1989) Results and problems of breeding essential oil crops.
Selektsiya i Semenovodstvo, Moscou(1), 1012.

2002 Edited by Taylor & Francis

19 Cultivation and distillation


of Geranium oil from Pelargonium
species in India
B.R. Rajeswara Rao

INTRODUCTION

Rose-scented geraniums are grown in various parts of India, from the plains to high
altitudes, and in spite of some differences in the major components of the oils, the oils
are accepted on the domestic market in India.

LOCATIONS

The experimental crops have been grown in the South Indian State of Andhra Pradesh
in Hyderabad; in the State of Karnataka in Bangalore; in the State of Tamil Nadu in
the Pulney Hills, the Nilgiri Hills and in the North Indian State of Uttar Pradesh in
Gaza, Kanatal, Lucknow, Pantnagar, Ranichauri. The altitude varies from: 120 m in
Lucknow, 540 m in Hyderabad, 900 m in Bangalore, to 15002400 m in Pulney Hills
and Nilgiri Hills.The climate is equally variable from semi-arid, sub-tropical in
Lucknow to cool, sub-tropical in the Hills.The temperature variation is commensurate
with the locality and can rise as high as 40 C and as low as 5 C; there is a wide range
of temperatures in each area itself.

GENOTYPES

Two main genotypes are commercially cultivated in India: the Algerian or Tunisian
type and the Bourbon or Reunion type, whilst a third, Kelkar or Egyptian is grown in
limited areas. These are shown in Figures 19.119.3, and illustrate the similarity
between the leaves of the three cultivars. The only way to distinguish between the cutivars is through their odour and therefore their chemical composition. The main distinguishing sesquiterpenes for Bourbon and Egyptian oils, 6,9-guaiadiene and
10-epi--eudesmol respectively are sometimes both present in the Bourbon, Algerian
and Egyptian types of oil grown in India; the Egyptian type however has a higher ratio
of 10-epi--eudesmol to 6,9-guaiadiene and the Bourbon a higher ratio of 6,9-guaiadiene to 10-epi--eudesmol. (Kaul et al., 1997; Ram et al., 1997). The Kelkar oil abounds
in geraniol, from 34 to 44 per cent with a low citronellol content, from 8 to 11 per cent.
The physico-chemical characteristics of two Indian Geranium oil are shown in Table
19.1. To avoid confusion with the International names, the two main types have been

2002 Edited by Taylor & Francis

Figure 19.1 Close-up of cultivar Algerian. Courtesy: Dr K.P. Sastry, CIMAP Field Station, Kodaikanal,
India.

Figure 19.2 Close-up of cultivar Bourbon. Courtesy: Dr K.P. Sastry, CIMAP Field Station, Kodaikanal,
India.

2002 Edited by Taylor & Francis

214

Rajeswara Rao

Figure 19.3 Close-up of cultivar Kelkar. Courtesy: Dr K.P. Sastry, CIMAP Field Station, Kodaikanal,
India.
Table 19.1 Physico-chemical characteristics of Geranium oil Reunion type and Indian type
Physico-chemical Characteristics

Reunion

Relative density at 30 C
Refractive index at 30 C
Optical rotation at 30 C
Acid value maximum
Ester value
Ester value after acetylation
Carbonyl value expressed as
iso-menthone % by weight, maximum

0.8790.891
1.4601.464
11 to 13
5
6575
217227
13

Indian
0.8840.899
1.4641.474
7 to 11
10
5076
205230
16

Source: (Bureau of Indian Standards Specification, IS: 5871965)

renamed: Hemanti (Algerian or Tunisian), Bipuli (Bourbon or Reunion) and Kunti


(Kelkar or Egyptian).
The composition of the two main genotypes varies somewhat when the plants are
grown in different sites (Rajeswara Rao et al., 1990; Singh et al., 1996), but they
are more acceptable on the market than the Kelkar.
Ambiguity prevails over the botanical nomenclature adopted in India for all these
genotypes, which are referred to either as Pelargonium species or as Pelargonium graveolens
LHerit. ex Aiton (Rajeswara Rao, 1999).
Attempts have been made to develop new strains using Gamma irradiation (Cobalt
60, dose: 1 KR) (Angadi and Vasantha Kumar, 1995), leaf cuttings (Kulkarni et al.,

2002 Edited by Taylor & Francis

Geranium oil production in India

215

1998), tissue culture (Anonymous, 1997, 1999) and by crossing genotypes in the
normal way.
New Algerian-type strains, have resulted in e.g. a higher content of geraniol than
normal, equal to that of the Bourbon (strains IIHR-2, PG-7, Rn Pb). Another clone
(64) is identical to that of the Australian genotype (Kulkarni et al., 1997). However,
some strains contain substantial quantities of iso-menthone.
PROPAGATION, GROWTH CONDITIONS, DISEASE AND
AGE OF PLANTS FOR HARVESTING

Plants are propagated from stem cuttings, which are either terminal i.e. soft stem, or
hard stem cuttings: both produce similar essential oil (EO). Changes in the EO composition has been shown to occur for a number of reasons: fully expanded old leaves,
petioles and tender stems contain small amounts of EO, whilst the young, expanding
leaves have a greater density of oil glands than the old. Planting dates make a substantial difference to the oils eventually produced; there are different changes in the concentration of citronellol or geraniol in different cultivars, depending on the month they
are planted out. The effect of plant growth regulators have been studied and found to
contribute to the quality of EO produced: Triacontanol and Mixatalol, NAA, Ethrel
and Mepiquat chloride had some enhancing effect on linalool, iso-menthone, citronellol and geraniol (Rajeswara Rao, 1999).
Diseases like wilt, caused by fungi or Little leaf disease caused by phytoplasma, cause
not only plant losses but also loss of quality of the EO produced (Rajeswara Rao, 1999).
This is possibly through a direct effect of the organism or an indirect effect through
reduced photosynthesis etc. Geraniums grown in hilly areas are often infested with nematodes: Criconemoides sp., Helicotylenchus dihystera, Meloidogyne incognita, Meloidogyne hapla,
Pratylenchus sp., Scutellonema conicephalum and Xiphenema sp. damage the crop and can
inflict losses of up to 76 per cent (Anita and Vadivelu, 1997). A number of other diseases
occur including: root rot (Fusarium sp., Pythium sp., Phytophora sp.,), tip rot or tip burn
(Gleosporium sp.), stem rot (Rhizoctonia solani); rust (Puccinia sp.), root galls (Agrobacterium
tumifaciens). Control measures using various pesticides are used to control these.
Changes in temperature, humidity, rainfall, have a great effect on EO production,
especially regarding their composition. Hot months favour accumulation of citronellol,
whilst cool months with that of geraniol and its esters. Harvesting at different times of
the day even on the same day influences the EO composition. The same was true of the
height of the plants when harvested.
In general, the crop is harvested at flowering at high altitudes and during full growth
elsewhere. In hilly areas, the crop is ready for harvesting with well-developed foliage
within 78 months of planting and in plains, 46 months after planting (Doraswamy
and Sundaram, 1982; Rajeswara Rao, 1999) Subsequent harvests are at 35 month
intervals, depending on weather conditions and crop management. Plants are harvested
using a sickle on sunny days and not when raining. In the hills, three to four harvests
are made per year and the plants give a good yield for 810 years after wards, but in
South Indian plains, plants last only for 24 years; in North Central Indian plains, the
geranium plants are cultivated solely as an annual crop (Ram et al., 1997). Only the top
1520 cm length of shoot is harvested, leaving enough biomass for re-growth, in areas
where multiple harvests are obtained.

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Rajeswara Rao

DISTILLATION

The leaves, stems and flowers collected are allowed to wilt or wither to reduce their volume, as this allows a greater biomass to be distilled at any one time and cuts down on
the cost of distillation etc. Wilting even for a day increased the per cent citronellol and
geraniol in the EO in an Algerian cultivar. Usually, the harvested biomass is wilted for
a few hours, but in the hot climates of the plains, there is a loss in the yield of EO after
just few hours. Comminution enhances oil yield and also has a significant effect on the
composition (Rajeswara Rao, 1999). The method of distillation again has a considerable influence. Hydrodistillation or steam distillation will affect different cultivars in
a distinct manner.
The oil is then filtered through cotton, muslin or filter paper to exclude extraneous
matter and then treated with anhydrous sodium chloride or sulphate, allowed to stand
for a few hours for absorption of free and dissolved water, and then refiltered, filled up
to the brim in airtight containers, capped tightly and stored in a cool, dry place.
Quality can remain high for many years.
Occasionally, the oil is coloured red due to reacting with the metal (mild steel) of the
distillation vessel. Tartaric acid usually restores the proper colour. If the red colour
persists, then the oil is re-distilled. For shorter periods of storage, glass or hard plastic
cans and galvanised iron drums are used; longer storage requires aluminium drums or
amber-coloured bottles.
REFERENCES
Angadi, S.P. and Vasantha Kumar, Y. (1995) Geranium. In: K.L. Chadha, and R. Gupta (eds)
Advances in Horticulture, vol. 11, Malhotra Publishing House, New Delhi, India, pp. 667687.
Anita, B. and Vadivelu, S. (1997, 1999) Management of root knot nematode, Meloidogyne hapla
on scented geranium, Pelargonium graveolens L. Indian J. Nematol., 27, 123125.
Anonymous (1997, 1999) Annual Reports, 19961997, 19981999, Central Institute of
Medicinal and Aromatic Plants, Lucknow, India, pp. 5760; pp. 1087.
Doraswamy, K. and Sundaram, M. (1982) Geranium cultivation in South India, In: C.K. Atal,
and B.M. Kapur (eds) Cultivation and Utilization of Aromatic Plants, Regional Res. Lab.,
Jammu Tawi, pp. 573577.
Kaul, P.N., Rajeswara Rao, B.R., Bhattacharya, A.K., Mallavarapu, G.R. and Ramesh, S. (1997)
Changes in the chemical composition of rose-scented geranium (Pelargonium sp.) oil during
storage. J. Essent. Oil Res., 9, 115117.
Kulkarni, R.N., Baskaran, K., Ramesh, S. and Kumar, S. (1997) Intra-clonal variation for essential oil content and composition in plants derived from leaf cutings of rose-scented geranium
(Pelargonium sp.) Ind. Crops Products, 6, 107112.
Kulkarni, R.N., Mallavarapu, G.R., Baskaran, K., Ramesh, S. and Kumar, S. (1998) Composition
of the essential oils of two iso-menthone-rich variants of geranium (Pelargonium sp.) Flav. Fragr.
J., 13, 389392.
Mallavarapu, G.R., Prakasa Rao, E.V.S., Ramesh, S. and Narayana, M.R. (1993) Chemical
and agronomical investigations of a new chemotype of geranium, J. Essent. Oil Res., 5,
433438.
Rajeswara Rao, B.R. (1999) Rose-scented geranium (Pelargonium species): Indian perspective.
Paper: National Seminar on the Research and Development in Aromatic Plants: Trends in
Biology, Uses, Production and Marketing of Essential Oils, Central Institute of Medicinal and
Aromatic Plants, Lucknow, India, July 3031.

2002 Edited by Taylor & Francis

Geranium oil production in India

217

Ram, M., Singh, R., Naqvi, A.A. and Kumar, S. (1997) Effect of planting time on the yield and
quality of essential oil in geranium Pelargonium graveolens, J. Hort. Sci., 72, 807810.
Rajeswara Rao, B.R., Sastry, K.P., Prakasa Rao, E.V.S. and Ramesh, S. (1990) Variation in yields
and quality of geranium (Pelargonium graveolens L, Her. ex Aiton) under varied climatic and
fertility conditions, J. Essent. Oil Res., 2, 7379.
Singh, A.K., Bisht, P.S., Singh, K., Kumar, D. and Naqvi, A.A. (1996) Introduction of
geranium Pelargonium graveolens in Uttar Pradesh hills in India, J. Med. Arom. Plant Sci.,
18, 2225.

2002 Edited by Taylor & Francis

20 Micropropagation and biotechnological


approaches to tissue culture of
Pelargonium species and production
of essential oils of scenteds
Barry V. Charlwood and Maria Lis-Balchin

MICROPROPAGATION OF COMMERCIAL GERANIUMS

Micropropagation of commercial glasshouse geraniums was reviewed by Cassells (1992a)


who pointed out that propagation of Pelargonium for commercial purposes has always been
a problem due to poor seed production and disease. Also, in many commercial
Pelargonium, there is cytological diversity, exemplified by the fact that different cultivars
in the same group can exhibit euploidy, auto and allopolyploidy and aneuploidy. Due also
to the selection of chimeral groups, the crop is largely vegetatively propagated from stock
plants; this involves considerable cost due to labour, space and disease control. Of the
numerous diseases of Pelargonium including fungal, bacterial and viral vascular pathogens,
the most serious are bacterial blight caused by Xanthomonas pelargonii and tomato spot
virus. Both reduce the vigour of stock plants, and often cause their early death.

MERISTEM CULTURE AND THE PRODUCTION OF


VIRUS-FREE PLANTS

The introduction of meristem culture resulted in the production of virus-free plants


(Pillae and Hildebrandt, 1968) and Xanthomonas-free plants (Hamdorf, 1976; Theiler,
1977; Reuther, 1983). Numerous plants could be produced from meristem tip culture
by cloning, and this also facilitated the production of culture-virus-indexed (CVI)
plants without the need for heat treatment (Cassells, 1982, 1986, 1988).
Protocol
The micropropagation protocol for commercial geraniums favoured by Cassells (1992a)
consisted of Stage 1 which involved genetic selection, whereby chimeras, beneficiallyinfected varieties (Cassells et al., 1982) and unstable genotypes were rejected (including
some beautiful chimeras e.g. Mr Wren and the ivy-leaf LElegante, as well as beneficiallyinfected varieties like picotee-flowered varieties of ivy-leaf Mexicana and the unstable
Speckles). The next stage was screening for disease and contaminants which produced

2002 Edited by Taylor & Francis

Micropropagation and tissue culture

219

axenic stock; this involves using enzyme-linked immunosorbant assay (ELISA) or DNA
probes for known pathogens and culture indexing using a range of common bacterial and
fungal media (Schaad, 1979) and identification of contaminants (Cassells, 1991, 1992b).
Then the cloning strategy followed, which involved meristem or nodal culture,
adventitious regeneration and somatic embryogenesis: this would be monitored for
genetic stability. The final stage involved rooting procedure and transfer to the environment: either in vivo rooting in clumps or individual transplanting, then weaning by
misting or fogging, or in vitro self-rooting or induced rooting followed by biopackaging.
Virus-screening
Meristem culture does not eliminate all known viruses, therefore screening the donor plant
is imperative (Cassells, 1992 a,b); the problem also arises when using a nodal or explant
culture. Virus contamination may not be expressed in vitro, as a high salt concentration
favours masking; clonal loss can therefore result after establishment or subculturing in
low-salt media (Cassells et al., 1982). Symptomless donors are usually selected and these are
then culture-indexed for Xanthomonas etc. and tested for tomato ringspot using serology. If
tests are positive for viruses, then heat therapy is applied; if bacterial contamination is
found the plants are grown under hard conditions or treated with antibiotics. Whitefly and
aphids should be eliminated from growth areas as cross-contamination is possible.
Conditions favouring meristem culture
Meristem culture is favoured by dark conditions of the donor plant, culture at low
temperature, and dark incubation of cultures and auxin apparently influences meristem
establishment (Menard et al., 1985; Cassells, 1992a).
Establishment of culture was achieved in about 2 weeks, by using MS (Murashige and
Skoog, 1962) basal medium, supplemented by 0.825 g/L ammonium nitrate, 0.15 g/L
sodium dihydrogen phosphate 1 g/L casein hydrolysate, 30 g/L sucrose, 2 mg/L IAA,
1 mg/L GA3, 4 mg/L kinetin, 50 mg/L adenine sulphate, 100 mg/L mesoinositol, with
6 g/L agar at pH 5.8. Subculturing was done every 46 weeks, depending on variety.
Shoots were allowed to develop and then rooting was achieved in vitro by placing the
implant with 1 cm length shoots onto half-strength MS basal medium containing 15 g/L
sucrose, 0.01 mg/L kinetin and 0.1 mg/L IAA with 6 g/L agar pH 5.8. Rooting in vivo
was allowed by placing the shoot culture onto seed compost in a special chamber
(Cassells, 1992a).
Other methods were used by different workers: Menard et al. (1985) used 500 mg/L
polyvinylpyrrolidone in their culture establishing media, which also included
250 mg/L of casein hydrolysate, 250 mg/L yeast extract and 30 g/L sucrose and 8 g/L
agar pH 5.8. Zeatin and triiodobenzoic acid was used in the differentialtion medium
and half-strength MS with 0.1 mg/L NAA for rooting.

IN VITRO PROPAGATION OF REPRESENTATIVE SPECIES


OF ALL SECTIONS OF PELARGONIUM (GERANIACEAE)

As there is a wide diversity of Pelargonium species, but a shortage of specimens available


for ornamental purposes, due to difficulties in finding their location (e.g. elusive

2002 Edited by Taylor & Francis

220

Barry Charlwood and Maria Lis-Balchin

geophytes, spending most of the year underground), their inherent scarcity and also
difficulties in exporting from South Africa, and also the difficulty of mass propagation
from the few stock plants available, the possibility of micropropagating members of the
genus was examined (Lis-Balchin, 1996). Few different Pelargonium species had been
micropropagated apart from some scented-leaf ones (Skirvin and Janick, 1976) as the
main concern was to mass-produce the main crop geraniums and in particular to keep
them virus-free (Debergh and Maene, 1977; Menard et al., 1985; Horn, 1988; Cassells,
1992a,b). Most micropropagation was from meristems except for Pillai and
Hildebrandt (1968), Stefaniak and Zenkteler (1982) who used petioles.
Micropropagation conditions used
Petioles were used as these were available in suitable numbers on all species, in contrast
to meristems. Sections of petioles from a wide range of representative species of all
sections of Pelargonium were taken from mature plants in summer, grown in a greenhouse under normal light conditions at a minimum temperature of 20 C in soil-free
compost with added grit. Plants in England were identified according to van der Walt
(1977), van der Walt and Vorster (1981, 1988) or by van der Walt and Voster on site
in South Africa.
The petioles were sterilised for 10 min in 10 per cent Domestos (sodium
hypochlorite with added wetting agents) mixed with a few drops/100 mL of household
washing-up liquid. For hirsute plants, a pre-wash of a 10 sec dip in methylated spirits
was made. The explant was then rinsed three times in sterile water and 0.5 to 1 cm
lengths were cut and inserted into the prepared MS solid medium in glass pots 10 cm
tall and 2 cm wide with white plastic screw tops containing the appropriate hormones
in the same direction as in the original plant (from stem base up to tip). The pots were
incubated under fluorescent lamps at 25 C in an 18 h photocycle of light to 6 h
darkness. The callus or developing plantlets were subcultured every 6 weeks. Plantlets
with shoots and roots were transferred to soil-less compost after washing off the agar
mixture thoroughly under running water.
The best hormonal conditions were determined in preliminary experiments using
13 different mixtures in the basic MS agar mixture containing 0.8 per cent agar and
3 per cent sucrose. (Table 20.1). At least five cuttings were used for each determination.
A range of different callus-inducing media were substituted for possible shoot-inducing
media as soon as the callus was established. The root-inducing medium (k), or other
media were substituted when the roots did not form for 2 weeks after the shoots were
visibly evident and also green.
Micropropagation results for different species
Callus formation

The mean time taken for the initiation of callus in the different species (using the most
active media composition as shown in Table 20.2) was found to vary for different species
and was not correlated with any particular section. The shortest average time for callus
formation was 13 days for e.g. P. patulum and P. ranunculophyllum: however, some species
e.g. P. abrotanifolium and P. trifidum took 58 days. An individual species within a particular section could take 19 days (P. exstipulatum) to 58 days (P. abrotanifolium). Callus

2002 Edited by Taylor & Francis

Table 20.1 Comparison of the hormone mixtures used to initiate callus formation, shoots and roots in
different species
Section

Species

Callus

Shoot

Root

Campylia (Sweet) D.C.


Ciconium (Sweet) Harvey

P. oenothera
P. acetosum
P. acraem
P. caylae
P. inquinans
P. monstrum
P. ranunculophyllum
P. stenopatalum

Dibrachya (Sweet) Harvey


Glaucophyllum Harvey

P. dichondrifolium
P. echinatum
P. mollicomum
P. odoratissimum
P. reniforme
P. sidoides
P. peltatum
P. glaucum

Harvey

P. patulum

a,b,c,f,j

e
a,h
e
a,d,e,f
a,d,e,f
a,d,e,I,j
a,e
c,d,f
ve
e,j
h
a,c,h,j
a,c,d
a,c,d
a,j,e
a
ve

k
k
k
k
k
k
k
k

Cortusina D.C.

a,b,c,f,j
a,h,j
a,b,c,d,f
a,b,c,d,f
a,b,c,d,f
a,b,c,d,I,j
a,b,c,f,h,j
c,d,f
ve
a,b,c,I,j
a,b,c,f,I,j
a,b,c
a,c,d
a,b,c,d
a,j
a,b,c,d,f

Hoarea D.C.

P. appendiculatum
P. punctatum
P. rapaceum
P. cotyledonis

a,b,c,f,j
a,b,c,j
a,b,c,f,j
ve

e,j
a,c,e,h,I,j
e
ve

j,k
I,k
k
ve

P. antidysentericum
P. endlicheraianum
P. tetragonum

a,j
c,j
I,j

ve
ve

ve
ve

g,h

Ligularia (Sweet) Harvey

P. abrotanifolium
P. barklyi
P. dolomiticum
P. exstipulatum
P. fulgidum
P. griseum
P. hirtm
P. hystrix
P. pulchellum
P. trifidum

a,b,c,d,h
a,b,c,I,j
a,b,c,f,j
a,b,c
h,I
a,b,c,d
a,b,c,g
a,b,c
a,b,c,f,j
a,b,c

a,e
e,j
e
a,d
h,I
a,c,d
a,c,g
f,I
e
a

k
k
k
k
k
k
k
k
k
k

Myrrhidium D.C.

P. multicaule

b,f,h

f,h

Otidia (Sweet) G. Don

P. alternans
P. carnosum
P. ceratophyllum
P. dasyphyllum

a,b,c,f,j
f,g,h
a,b,c,h,j
I

a,j
f,g,h
e
I,j

k
k
k
k

Pelargonium (D.C.) Harvey

P. capitatum
P. graveolens
P. papilionaceum
P. tomentosum

a,b,c,f,j
a,b,c,f,j
a,b,c,f,j
a,b,c,I,j

a,e
e,f
a,e
a,e,h

c,e,k
c,e,k
k
a,j,k

Peristera D.C.

P. album
P. australe

a,b,c,d,h
a,b,c,I,j

a,c,d,h
a,I,j

k
a,k,l

Polyactium (Eckl. and Zeyh.) D.C.

P. triste

a,b,c,I,j

a,e

e,k,l

Isopetalum (Sweet) D.C.


Jenkinsonia (Sweet) Harvey

2002 Edited by Taylor & Francis

ve

k
k
k
k
k
k
k
ve

222

Barry Charlwood and Maria Lis-Balchin

Table 20.1 (Continued)


Hormones and proportions used (mg/L):
a
b
c
d
e
k

BA:NAA
BA:NAA
BA:NAA
BA:IAA
BA:IAA
NAA alone

5:1
5:5
1:5
5:5
10:1

f
g
h
i
j

KIN:IAA
KIN:NAA
KIN:IAA
KIN:NAA
KIN:NAA

5:5
5:5
5:1
1:5
5:1

Notes
BA (benzyladenine); NAA (naphthylene-acetic acid; IAA (indoleacetic acid); K (kinetin).

Table 20.2 Average number of days to initiate callus in different


Pelargonium species
Days

Species

Section

13

P. patulum
P. ranunculophyllum
P. dolomiticum
P. rapaceum
P. triste
P. caylae
P. exstipulatum
P. echinatum
P. glaucum
P. papilionaceum
P. capitatum
P. hirtum
P. mollicomum
P. tomentosum
P. australe
P. appendiculatum
P. ceratophyllum
P. graveolens
P. hystrix
P. oenothera
P. monstrum
P. album
P. reniforme
P. stenopetalum
P. inquinans
P. barklyi
P. alternans
P. pulchellum
P. abrotanifolium
P. trifidum

Glaucophyllum
Ciconium
Ligularia
Hoarea
Polyactium
Ciconium
Ligularia
Cortusina
Pelargonium
Pelargonium
Pelargonium
Ciconium
Cortusins
Pelargonium
Peristera
Hoarea
Otidia
Pelargonium
Ligularia
Campylia
Ciconium
Peristera
Cortusina
Ciconium
Ciconium
Ligularia
Otidia
Ligularia
Ligularia
Ligularia

19

26

28
29
30
34

37
43
58

formation was possible in most species using BA:NAA ratios of 5:1 and 1:5; kinetin
could replace BA in any auxin combination; IAA and NAA were also interchangeable.
One of the main problems with the Section Ciconium, which also gives rise to
P.  hortorum cultivars (the household geraniums), is the exudation of phenolics from

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the cut surfaces; this has been remarked on by Hildebrand and Harney (1988) and is
best treated by more numerous washing of the cut petioles with sterile water; experiments were also conducted whereby the cut petioles were kept in sterile water for 30
min to 24 h with no greater success.
Callus formation proved impossible under all possible conditions for P. cotyledonis,
a very high-phenolic containing species, which is endemic to the island of St. Helena
and differs in many ways with the rest of the Pelargonium species. However, the high
phenolic concentration alone was probably not the reason for this lack of success, as
P. antidysentericum, (the underground root of which is used for treating dysentery by
locals in South Africa) has a very high phenolic concentration, but proved amenable to
formation of callus although further transformations were not possible.
Callus formation times for P. australe, P. echinatum and P. tomentosum were similar to
those reported by Brown and Charlwood (1986). The majority of other species had not
been micropropagated before, except for some of the geophytic and xerophytic species
(De Marie, 1991), whose callus formation times were not reported, although the shootstage was reached.
Shoot formation

The time taken for shoots to appear (Table 20.3) was also variable for different species
and again there was no observable correlation with different sections. P. rapaceum and
P. exstipulatum took 4 weeks; whilst P. tetragonum took 12 weeks. Shoot formation in
P. echinatum was initiated within 6 weeks, in contrast to the negative results of Brown
and Charlwood (1986). The geophytes , P. appendiculatum, P. punctatum and P. rapaceum
(Hoarea) formed shoots within 45 weeks. The xerophytic P. hystrix also formed
shoots, though after 7 weeks, in contrast to the negative results of De Marie (1991).
Table 20.3 Average number of weeks to produce shoots in different
Pelargonium species
Weeks

Species

Section

P. rapaceum
P. exstipulatum
P. triste
P. papilionaceum
P. dolomiticum
P. australe
P. appendiculatum
P. barklyi
P. echinatum
P. album
P. capitatum
P. ceratophyllum
P. graveolens
P. hystrix
P. oenothera
P. trifidum
P. abrotanifolium
P. tetragonum

Hoarea
Ligularia
Polyactium
Pelargonium
Ligularia
Peristera
Hoarea
Ligularia
Cortusina
Peristera
Pelargonium
Otidia
Pelargonium
Ligularia
Campylia
Ligularia
Ligularia
Jenkinsonia

10
11
12

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In the present studies, however, shoot formation did not occur in P. patulum,
P. antidysentericum and P. endlicherianum calluses under all possible hormonal conditions,
even after 4 months.
Root initiation

Root initiation was very prompt in most species when the shoot-forming callus was
transferred to a hormone-free MS medium or sometimes a high auxin:cytokinin
medium (Table 20.1). There were a few exceptions, including P. tetragonum, which
formed roots in a lower kinetin: even lower NAA (0.5:0.05) than used for the rest of
the species; P. tomentosum formed roots in a high NAA alone medium (10 ppm) or BA
alone (10 ppm); P. triste, P. capitatum and P. graveolens formed roots on almost any type
of hormone concentration or mixture used.
The ease of micropropagating the bulk of different Pelargonium species was in
contrast to some of the earlier difficulties associated with micropropagation of
Pelargonium cultivars (so-called Geraniums, or zonals), which were hybridised mainly
from the Ciconium section.
The resulting plants appeared to be identical with their parent plants, but not
enough experiments were conducted to state categorically that genetic modifications
would not occur as often found when using petioles (Skirvin and Janick, 1976).
In conclusion, most of the species, from all sections, could be micropropagated
successfully.
BIOTECHNOLOGICAL APPROACH

Apart from the capability to produce large amounts of biomass of clonal lines of the
commercially important pelargoniums as outlined above, plant biotechnology has
application in more general terms for plant improvement and for essential oil
production.
SECONDARY PLANT METABOLITES

During the 1980s there emerged a significant interest in the potential use of cultured plant cells (callus and suspension) for the production of secondary compounds
of importance to the pharmaceutical, food processing and cosmetic industries.
Because of the wide range of monoterpene classes to be found in the many scentedleaf variants of Pelargonium, and the ease with which these variants may be taken into
culture (Charlwood and Charlwood, 1983), this genus provided an important model
system through which much valuable information was derived concerning the accumulation of lower isoprenoids in undifferentiated cultures (Charlwood and
Charlwood, 1991).
Essential oil accumulation in calluses
Table 20.4 shows the partial results of one such study (Brown and Charlwood,
1986a; Brown, 1988; Charlwood et al., 1989) in which calluses, derived from stem

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Table 20.4 The oil content, callus characteristics and regeneration capacities of scented-leaf variants
of Pelargoniuma
Scented-leaf variant b
P. Miss Australia
P. nervosum Sweet
P. Mabel Grey
P. australe Willd.
P. Lillian Pottinger
P. quercifolium (a)
P. tomentosum (a)
P. quercifolium (b)
P. radula LHer
P. tomentosum (b)
P. Royal Oak
P. fragrans Willd.
P. tomentosum (c)

Days to
form callus c,d
8
7
18
13
18
13
10
13
7
10
11
7
8

Callus
morphology d,e

Oil content
(g/g fresh weight) f

Weeks to
formShoots d,g

White/pink, friable
White, friable
Pigmented, hard
White, friable
Pigmented, friable
Pigmented, friable
Green, friable/hard
Pigmented, friable
Pigmented, friable/hard
Green, friable/hard
White, friable
Pigmented, friable
Green, friable/hard

31.0
21.7
15.8
13.5
9.2
8.8
4.2
2.7
0.81
0.06
0.06
0.06
0.006

8
4
14
3
46
11
14
13
18
3
26
15
3

Notes
a Data derived from Brown (1988).
b Letters in parenthesis indicate different cell lines of the same variant.
c Callus initiation medium: Charlwood and Charlwood (1983) medium (pH 5.5) containing 30 g/L sucrose, 10 g/L
agar, 0.2 mg/L kinetin and 1 mg/L 2,4-D.
d Incubations were at 26 C under either continuous light (3 E/m2s) or a 16 h light/8 h dark photoperiod.
e Callus maintenance medium: Murashige and Skoog (1962) medium (pH 5.5) containing 30 g/L sucrose, 10 g/L agar,
5 mg/L BAP and 1 mg/L NAA.
f Average oil content of intact plant was 620 g/g fresh weight.
g Shoot regeneration medium: Murashige and Skoog (1962) medium (pH 5.5) containing 30 g/L sucrose, 10 g/L agar,
0.5 mg/l BAP and 0.05 mg/L NAA.

material of around 30 different scented-leaf pelargoniums, were studied with respect


to morphology, growth rate, ability to regenerate shoots and capacity for
accumulation of essential oil. The monoterpene accumulation in nearly all of the
callus lines investigated was very low, typically only about 0.1 per cent of that
accumulated by the parent plant, although in rare cases accumulations of up to 5 per
cent of the oil of the parent plant could be detected (e.g. P. nervosum and P. Miss
Australia). Throughout this study, no clear correlation between the level of oil
accumulation and either the growth characteristics or the morphological nature of
the callus material ever emerged.
Typical low levels of oil accumulation were further maintained when finely
divided suspension cultures were produced from the parent callus lines. Thus for
P.  fragrans, a callus line which accumulated between 0.060.09 g oil/g
fresh weight gave rise to a suspension culture which accumulated 1.3 g oil/g fresh
weight when grown under subdued light, although this accumulation could be
increased to 11.5 g oil/g fresh weight when the culture was incubated under
photoperiod conditions (Brown and Charlwood, 1986b). Despite exhaustive
attempts to augment this low level accumulation in undifferentiated cells by, for
example, supplementation of the medium with plant growth regulators (PGRs),
biotic and abiotic inhibitors, organic acids etc. (Charlwood et al., 1988), the
maximum accumulation that could ever be achieved was only 35 g oil/g fresh
weight, and this was obtained using a highly aggregated suspension culture.

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Differentiation of calluses
Calluses of most scented-leaf pelargoniums which had been sub-cultured at two-weekly
intervals on maintenance medium (see Table 20.4) for periods of up to 1 year could be
induced to differentiate through transfer to Murashige and Skoog (1962) solid medium
(MS) containing low levels of BAP and NAA (0.5 and 0.05 mg/L, respectively).
Typically, shoot formation occurred within 414 weeks following transfer to regeneration medium (Table 20.1; Brown and Charlwood, 1986a), although for some varieties
(e.g. P. Lillian Pottinger and P. Robers Lemon Rose) prolonged culture of up to
1 year on regeneration medium was required. A few scented-leaf pelargoniums (e.g.
P. echinatum and P. glutinosum) appeared not to be competent for regeneration under
these conditions.

ESSENTIAL OIL ACCUMULATION IN


DIFFERENTIATED/UNDIFFERENTIATED PELARGONIUMS

Relationship between storage site (trichomes) and


essential oil accumulation oil
Accumulations in shoot cultures were an order of magnitude greater than those
determined in undifferentiated cultures, although qualitatively the oils differed from
those found in the respective parent plants, being composed almost exclusively of
monoterpene hydrocarbons with only small amounts of oxygenated species.
Interestingly, stable, submerged shoot-proliferation cultures could also be formed from
a number of pelargoniums, in particular for P.  fragrans, P. tomentosum (Charlwood and
Moustou, 1988) and P. graveolens (Katagi et al., 1986), and oil accumulation in this type
of culture approached 50 per cent of that associated with the intact parent plant grown
under greenhouse conditions. The reduced proportion of oxygenated monoterpenes
within such shoot proliferation cultures was still observed although, unusually, for
P. tomentosum the major components of the oil were menthone and isomenthone (in
roughly equal amounts) corresponding identically with those of the parent plant. In
these cultures, the density of the glandular hairs (the storage sites for the EOs) present
on the surface of the shoot tissue varied both with the concentrations of PGRs present
in the medium and following treatment with various herbicides (i.e. Metflurazon,
Amitrol, desmethyl-norflurazon, 5C cycocel and AMO 1618): a direct correlation
between glandular hair density and the accumulation of oil could be established
(Charlwood et al., 1989).
It would thus appear that the capacity of scented-leaf Pelargonium cultures to
accumulate essential oils is closely associated with the availability of suitable storage
sites (Charlwood, 1993). Clearly if a cell culture is to be able to accumulate product,
then the product itself must not be deleterious to the producing cell, and the rate of
synthesis of the product must be greater than its rate of breakdown.
Toxicity of essential oils produced to the cells
Mono- and sesqui-terpenes are actually toxic to plant cells causing an inhibition
of photosynthesis and respiration and giving rise to a significant reduction in the
number of mitochondria and golgi bodies. The treatment of suspension cultures of

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P.  fragrans with a range of monoterpenes, all of which naturally occur in scentedleaf pelargoniums, resulted in a 90 per cent loss of cell viability at concentrations of
additive in excess of 100 mg oil/L medium (Brown et al., 1987). Surprisingly,
cultured cells showed no increased resistance to those monoterpenes present in
the oil accumulated by the individual parent plant. Autotoxicity of the product to
the cell line thus sets an upper limit on the amount of monoterpene that a culture
could be expected to accumulate under conditions where the product remains in
contact with the producing cells.
Metabolism of terpenes produced
However, there is a further possible cause of product loss from undifferentiated cell
cultures, and this is associated with the breakdown of the terpenes so formed. There
have been many reports (Charlwood, 1993) concerning the rapid metabolism of
monoterpenes which had been added to plant cells in culture, and numerous salvage
enzymes have been identified through which the carbon skeletons of such compounds
can be returned to the pool of acetyl CoA (Berger et al., 1990). In some instances the
rate of breakdown of product can exceed the rate of synthesis by several orders of
magnitude in which case, of course, no product can ever accumulate. Clearly this is not
the case for cultures of scented-leaf pelargoniums as some product, albeit in small
amount, is often observed. Theoretically then it should be possible to increase oil
accumulation by simply removing the product immediately formed by the cultured
cells, and sequestering the oil at some remote location.
Immobilised cells
This can most readily be performed by immobilising suspension cells through
entrapment within the pores of reticulate polyurethane foam and passing medium continuously over the immobilised cells in order to wash the product away. Using such
a system, a yield of oil equivalent to 110 mg oil/g fresh weight could be obtained from
a suspension culture of P.  fragrans that originally accumulated 100-fold less
(Charlwood and Charlwood, 1991). Alternatively, an artificial storage site, in the form
of a non-toxic lipophilic oil, may be added to the finely divided suspension culture as
a second phase in order preferentially to absorb any monoterpene product formed.
When suspension cultures of P.  fragrans were treated in this way a minimum of
a 10-fold increase in essential oil accumulation was observed (Charlwood and Brown,
1988), but under optimal incubation conditions an increase in oil accumulation of some
500-fold was attainable.
Retention of individual characteristics
Although, in general, cultures of scented-leaf pelargoniums seem not to retain their
ability to accumulate the monoterpenes associated with the parent plant, this capacity
returns following morphological regeneration. Thus when calliclones of a number of
scented-leaf pelargoniums were grown under greenhouse conditions for 3 months after
rooting, their essential oils were similar both qualitatively and quantitatively to those
of the parent plants (Brown, 1998). It should be noted that environmental conditions
play a significant role in determining the yield and composition of the essential oil of

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Barry Charlwood and Maria Lis-Balchin

pelargoniums, and hence it is essential that both the parent plant and the resulting
calliclones be subjected to identical growing environments if comparisons of oil
product are to be made. Skirvin and Janick (1976) carried out similar studies with 166
first-generation calliclones of the variant Robers Lemon Rose and found that only
one line showed an essential oil significantly different from that of the parent plant
even though a number of lines showed aberrant leaf morphologies. The frequency of
somaclonal variation of a specific trait is generally estimated to be between 0.2 and
3 per cent.
Production of variation in plants
Passage through tissue culture can hence provide an element of variation in the
regenerated plants, thus increasing the range of genetic diversity currently available in
the natural germplasm. Such a strategy has been employed in the search for
commercial pelargoniums showing resistance to bacterial blight caused by
Xanthomonas campestris pv. pelargonii (Dunbar and Stephens, 1989). In this study, calluses with shoot primordia were induced either from shoot tips and hypocotyls of germinated seeds, or from leaves excised from sterile plants, incubated on MS medium
(pH 5.8) containing 20 g/L sucrose, 9 g/L agar and 2 mg/L each of either IAA and
trans-zeatin for seed-derived material, or NAA and BAP for leaf explants. Shoots were
developed during 30 days on similar medium containing no auxin and one-tenth of
the cytokinin concentration, and well-developed shoots were eventually rooted on
Hoaglands solution containing 7 g/L agar. Thirty-day-old calliclones were assayed for
resistance to blight by rubbing the upper surface of their leaves with a sterile cotton
swab that had been moistened with bacterial suspension, and the level of infection was
monitored 23 weeks later. It was found that regenerated plantlets of P. grandiflorum,
a P.  domesticum c.v., P. hispidum, P. betulinum, P. scabrum and P. multicaule were much
more resistant to blight than were a P.  hortorum c.v. and P. denticulatum (Dunbar and
Stephens, 1989).

Use of Agrobacterium rhizogenes for production of variety


The selection of calliclones with appropriate characteristics has also been attempted in
order to improve the ornamental quality of scented-leaf pelargoniums. However, an
alternative strategy has been used by Pellegrineschi and Davolio-Mariani (1996) who
treated microcuttings of P.  fragrans, P. odoratissimum and P. quercifolium with a suspension culture of Agrobacterium rhizogenes (strain HRi) for 30 min and then co-cultivated
the infected explants on MS medium (with one-fifth macronutrients) containing agar
for 2 days, followed by further incubation on the same medium supplemented with 200
mg/l cefotaxime (to eliminate the contaminating bacteria) for up to 40 days. Hairy roots
(which first appeared after 10 days from the basal ends of the microcuttings) were
removed and tips were subcultured onto the same medium to produce spontaneous shoots
within 2 months. Such transformed shoots were rooted and grown-on in the greenhouse
to give plants that showed 23 times the number of branches compared to nontransformed plants. The leaves of the transformed plants were darker green than those of
the controls, and were more numerous per plant (although the leaf number per branch
was unchanged).

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The same group (Pellegrineschi et al., 1994) also transformed sterilised petioles of
P. Lemon Geranium with A. rhizogenes (strains A4RSII, LBA9402 and 15834) using
a similar technique and, following spontaneous shoot formation, obtained
regenerated transformed plants which had shorter internodal distances with increased
leaf and branch formation giving a more rounded appearance. The transformants
also showed accelerated rooting of cuttings yielding a shorter and more highly
branched root system, whilst the leaves themselves did not yellow as rapidly as the
controls.
Use of Agrobacterium rhizogenes for improving production
of essential oil
Interestingly, the oil content of the transformants had also changed in that they
accumulated up to 4.4 times more geraniol, 2.8 times more linalool, and 13 times more
1,8-cineole compared with their non-transformed counterparts, although the content of
citronellol decreased slightly (Pellegrineschi et al., 1994). The authors suggest that
hairy-root transformation may have application in producing pelargoniums with
a favourable globosus aspect to the plant canopy as well as increased oil yield (by up
to 10 fold in view of the increased leaf production).
Disadvantages of using A. rhizogenes
The transformation of plant material using A. rhizogenes is a relatively facile technology
since each transformation event occurring at a single cell gives rise to a separate,
putatively-transformed root, the tip of which may be excised and cultured to produce
a non-chimeric line. However, the major disadvantages of this technique are that
transformed roots of many plant species are not able to produce shoots spontaneously,
and regenerated plants that have been transformed using the Ri plasmid may show
altered leaf morphology, inhibition of flowering, and low fertility.
Use of A. tumefaciens for gene transfer
The more common method for gene transfer involves infection with A. tumefaciens,
typically employing a disarmed strain in which the natural transfer-DNA (t-DNA) has
been removed from the Ti plasmid so as not to produce crown galls upon plant
infection. The gene to be transferred to the target plant is typically inserted into a small
plasmid (the so-called binary vector) which is designed to permit DNA transfer to the
plant and subsequent expression both of the gene required and of a selectable marker
gene (normally one which confers resistance to a phytotoxin in transformed plant cells).
This second plasmid is then incorporated into the disarmed A. tumefaciens using the
process of triparental mating. Upon infection, no transformed cells can be chosen based
on morphological attributes (as they can following infection with A. rhizogenes), but
such cells are selected by growth of the infected explant on medium containing levels
of the phytotoxin which are just sufficient to kill those cells which do not express the
marker gene.
A number of A. tumefaciens-based transformation systems have been developed for
use with pelargoniums. One of the earliest (Robichon et al., 1995) involved infection of
cut segments of cotyledons and hypocotyls, which had been removed aseptically from

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Barry Charlwood and Maria Lis-Balchin

8-day-old seedlings of P.  hortorum, with disarmed A. tumefaciens (strain EHA 101)


containing a binary vector carrying hygromycin and kanamycin resistance genes and
a -glucuronidase reporter gene. Following a 20 min infection with an Agrobacterium
suspension, the treated explants were incubated on a shoot induction medium (containing
cefotaxime) for 15 days before being transferred to a regeneration medium which also
contained 20 g/ml of the selective agent hygromycin. It appears that P.  hortorum
is naturally resistant to kanamycin at levels up to 400 g/ml and hence this antibiotic could not be employed as a selective agent. The authors claimed that the transformation protocol was 20 per cent efficient, and that the resulting transformed plants possessed
one or two copies of the t-DNA although most copies were not full length.
An alternative transformation strategy was described by Boase et al. (1996, 1998),
involving infection of cut segments of leaf explants of in vitro grown plantlets of
P.  domesticum Dubonnet with A. tumefaciens (strain LBA 4404 with a kanamycin
resistance gene and, in some experiments, a plasmid bearing a phytochrome A gene
from oat) followed by co-cultivation for 2 days in the presence of 19.6 mg/L
acetosyringone. Regeneration of transformed cells took place on a selection medium
containing 50 mg/L kanamycin, as well as timentin (to eliminate the remaining
Agrobacterium). Regenerated shoots were rooted on a medium containing 200 mg/L
kanamycin to ensure that there were no escapes (regenerants that were non-transformed
but naturally resistant to lower levels of the phytotoxin). From 150 explants that were
inoculated, the authors reported obtaining 58 kanamycin resistant shoots from which
29 rooted plantlets were recovered, 24 of which expressed the phytochrome A gene
a transformation efficiency of 16 per cent.
In order to avoid the formation of chimeric transformants, KrishnaRaj et al. (1997)
developed a transformation strategy for P. Frensham via somatic embryogenesis.
Surface sterilised leaf petioles were soaked in a suspension of A. tumefaciens for 10 min
and co-cultivated for 2 days on an embryo induction medium (MS containing 30 g/L
sucrose, 8 g/L agar, 3.4 mg/L BAP and 0.9 mg/L NAA). After this time the tissues were
transferred to new induction medium supplemented with 500 mg/L cefataxime and
100 mg/L kanamycin (for selection of transformants): 45 weeks later the cultures were
moved to an embryo development medium (MS containing 30 g/L sucrose, 8 g/L agar,
2.8 mg/L NAA and 500 mg/L cefataxime). The authors claim that on average each segment (1 cm long) of leaf petiole produced 45 embryos within 4 weeks, and more than
80 per cent of these embryos converted into plantlets: the transformation efficiency was
around 14 per cent.
Future genetic modifications
Genetic modification, using the techniques outlined above, may be employed to extend
the genetic variation presently available for traditional plant breeding, and may be
applied to the alteration of flowering characteristics, leaf colour and zonation, disease
resistance, and oil quality and yield. One of the most pressing problems associated with
the commercial production of pelargoniums is associated with the susceptibility of the
plants to a variety of pathogens. In greenhouse grown plants, one particular problem is
gray mould (or Botrytis blight) caused by Botrytis cinerea Pers.:Fr which attacks plants
growing under wet, humid conditions and is presently combated by the use of chemical fungicides. However, some plants, including radish, barley and onion, produce a
number of small, cysteine-rich antimicrobial proteins (AMPs) which have recently been

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shown to play significant roles in plant defence. The AMP from onion (Ace-AMP1) has
a wide spectrum of antimicrobial activity in vitro and has been shown to be active even
in the presence of cations at physiological ionic strength. Bi et al. (1999) transformed
P. Frensham with A. tumefaciens containing a binary vector which carried the signal
peptide, the mature protein and the carboxyl-terminal propeptide domains
of Ace-AMP1 cDNA driven by a CaMV 35S promoter with duplicated enhancers, using
the somatic embryogenesis strategy of KrishnaRaj et al. (1997). Seven transformed
plants were obtained following selection on kanamycin and all showed expression of the
Ace-AMP1 protein. Using an assay method which involved infecting a 10 mm leaf disc
with spores of B. cinerea and incubating the plant tissue under humid conditions on agar
containing paraquat (to kill the plant tissue and hence speed up the sporulation of the
fungus), the three transformants which were further tested all showed significantly
lower sporulation densities after 6 days. Furthermore, there was a significant correlation
between resistance and the level of Ace-AMP1 protein in the transformant.
Since culture-derived (somaclonal) variation has had only a small impact on
increasing the genetic diversity available for breeding ornamental plants, it seems that
direct gene transfer strategies (using Agrobacterium vectors or through biolistic
techniques) are likely to be the method of choice for the introduction of desired traits
into Pelargonium lines in the next decade. Despite the current low level of public
acceptance of this technology, a number of laboratories are presently developing new
variants of pelargoniums altered with respect to leaf and petal colour, oil quality and
quantity and enhanced disease resistance.
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21 Geranium oil and its use in


aromatherapy
Maria Lis-Balchin

INTRODUCTION

Aromatherapy is broadly defined as treatment with odours, the inhalation of which


can have beneficial effects on clients through their action on the limbic system in
the brain (Buchbauer, 1992; Warren and Warrenburg, 1993; Lis-Balchin, 1997).
However, in England it involves the application of a very diluted essential oil (EO) or
mixture of EO(s) (12 per cent) in a carrier oil like almond oil, which is massaged into
the skin; either on hands, feet, head or the total body. Aromatherapy can also mean the
addition of drops of EO to the bath or a basin of hot water, or the volatilization of the
EO(s) using various burners. It usually involves counselling about diet, exercise,
lifestyle etc. by the aromatherapist, who may have absolutely no qualifications to offer
such advice.
In France, Germany and other parts of Europe, aromatherapy takes on a different
meaning as it involves the internal usage of EO(s) as medicines, and is practised by
medically qualified doctors (Lis-Balchin, 1997). This includes oral, rectal and vaginal
introduction of EO(s) into the body, treatment of wounds, as well as massage using
more concentrated EO(s). This clinical aromatherapy has also spread to England
and the USA, where totally unqualified people practise internal usage of various EO(s)
after making their diagnosis of the clients medical condition. Other herbs, novel
medicinal plant extracts, hydrolats, herbal oils, phytols, infusions, etc. are often
included in the aromatherapy treatment (Buckle, 1997), although the herbal
knowledge of the aromatherapists may be lacking (Lis-Balchin, 1999).
Looking through aromatherapy books (Tisserand, 1985; Westwood, 1991;
Worwood, 1991), the definition and application of aromatherapy is found to be a
mixture of the esoteric (if not paranormal aspects of plant essences and their
energetics) and the medical and scientific aspects of the EO(s) as chemicals.
It remains to be seen whether aromatherapy has any actual medicinal benefits,
other than stress-alleviating, through massage, and whether these are attributable
only to massage with the true EO(s), especially as there is a wide difference in
the actual percentage chemical composition of EO(s) obtained from different geographical sources and also different samples from plants grown in various countries
where differences in hybridization has occurred and even the same plants grown
under different climatic conditions etc. show differences. These differences can be
further accentuated in commercial oils due to blending, deterpenation, addition of
other essential oils fractions or synthetic components and also often dilution with
solvents.

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Geranium oil and its use in aromatherapy 235


AROMATHERAPY BASICS

Aromatherapy applications include:


1
2

3
4

6
7

A diffuser, which can be powered by electricity, giving out a fine mist of the essential oil (EO).
A burner, with water added to the fragrance to prevent burning of the EO: about
14 drops of EO is added to 10 ml water. The burner can be warmed by candles
or electricity. The latter would be safer in a hospital/childrens room/ and even a
bedroom.
Ceramic or metal rings placed on an electric light bulb with a drop or two of EO.
This results in a rapid burnout of the oil and also lasts for a very short time due to
the rapid volatalization of the EO in the heat.
A warm bath with drops of EO added. This results in the slow volatalization of the
EO, and not in absorption of the EO through the skin as stated in aromatherapy
books, as the EO does not mix with water. Pouring in an EO mixed with milk
serves no useful purpose as the EO will still not mix with water; the pre-mixing of
the EO in a carrier oil, as for massage, results in a nasty oily scum around the bath.
A bowl of hot water with drops of EO, usually used for soaking feet or used as a
bidet. Again, the EO will not mix with the water. This is useful for respiratory
conditions and colds, where the EO can be breathed in when the head is over the
container and a towel placed over the head. This is an old way of treatment and has
been used successfully with Vicks, Obas oil, Eucalyptus oils for numerous years.
Compresses using EO drops on a wet cloth, either hot or cold, to relieve inflammation, treat wounds, etc. Again, the EO is not able to mix with the water and can
be concentrated in one or two areas.
Massage of body, hands, feet, back or all over using 24 drops of EO (single EO or
mixture) diluted in 10 ml carrier oil (fixed, oily) e.g. almond oil or jojoba, grapeseed, wheatgerm oils, etc.

The last is the most common method used by aromatherapists.


Another method uses medicinal properties of the EO after oral intake. This is not
to be condoned, unless effected under a medically qualified aromatherapist.
EO drops are mixed in a tumbler of hot water or presented on a sugar cube or
mixed with a teaspoonful of honey and taken internally. This is not true aromatherapy,
as almost all the rest of the methods are based on EO volatalization and therefore largely
the effect of the EO on the central nervous system via the nose and thence the limbic
system which can cause a secondary effect on other parts of the body. Direct effects on the
skin can also occur e.g. antiseptic action of the EO or counterirritant effect which can
cause reddening of the skin and an increased blood flow to the area and could presumably
ease pain and swelling. The latter could only be effected by a few EOs e.g. thyme, clove,
oregano. Many EOs can be effective antiseptics, but this may not be the outcome when
used as a 12 per cent dilution in a carrier oil.
Massage
The massage applied is usually gentle effleurage with some petrissage (kneading) with
some shiatsu, lymph drainage in some cases and sometimes more vigorous massage,

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according to the aromatherapists skills. The massage should be relaxing, but also able
to increase the circulation of the blood and lymphatic system in order to release toxins,
break down tension in muscles and tone weak muscles (Price, 1993).
EO blending
The actual blending of EOs is considered an art form, but is basically simple: to 10 ml
of carrier oil, in a brown bottle, 1 4 drops of the same or different EO are added and the
bottle stopperred. The contents are then gently mixed without shaking the bottle too
much and creating air-bubbles. Some Aromatherapists swear that different people can
create a different mixture simply by their own energetic, but scientifically, it may simply
be a question of slight changes in the volume of EO applied by different people.
GERANIUM OIL: MISINTERPRETATION OF ITS
BOTANICAL SOURCE

The wrong genus


Although Geranium oil is one of the most widely-used EOs, there is apparently great
confusion regarding its botanical source and therefore its functions. Geranium oil, sold
as an aromatherapy oil or included in perfumes and some food products, is extracted
from the scented leaves of some Pelargonium species and cultivars and has therefore
nothing to do with the genus Geranium. However, this is not apparent when reviewing
the origin of Geranium oil in aromatherapy books and aromatherapy journals, as these
often implicate Geranium maculatum, G. robertianum and other Geranium species. Even
Body Shop referred to Geranium maculatum as source of their Geranium oil. This arose
due to the unfortunate mistake by some of the original aromatherapy book authors,
who looked up the medicinal properties of geranium from the many Herbals
(Culpeper, 1653; Grieve, 1937) thinking it was the same species.
There are amazing botanical concoctions e.g. The oil is extracted from the species
Pelargonium, Geranium Robert or lemon plant (Worwood, 1991). Tisserand (1985)
informs us that: Pelargonium odorantissimum graveolens is found on wasteland and was
used by the ancients as a remedy for wounds and tumours. He is undoubtedly referring to G. robertianum (Culpeper, 1653) as the quote is partly extracted from this
source.
Lawless (1995) informs us that the British plant herb Robert (Geranium robertianum)
and the American cranesbill, (G. maculatum) are the most widely-used types in herbal
medicine today, but seemingly does not realise that this has nothing to do with
Pelargonium.
Moreover, geranium species are usually used as a tea or alcoholic extract, which is
taken orally (Culpeper, 1653; Grieve, 1937) and volatile EOs are not mentioned. The
use of G. maccrorhizum EO is one exception, however this is produced mainly for its use
in perfumery as Zdravetz oil and is mainly confined to Bulgaria.
The wrong species
Frequent misnomers for the origin of Geranium oil include: Pelargonium odorantissimum, which is often misspelt as P. odorantissimum (Lawless, 1992; Valnet, 1982) and

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Geranium oil and its use in aromatherapy 237

also another version: Pelargonium odorantissium (Westwood, 1991), which is an actual


species with apple-scented leaves (van der Walt, 1977).
Other misnomers include: P. asperum, P. roseum Willd. and P. graveolens. The latter
species may have contributed to the parentage of some Geranium oil originating in
Africa, but the species itself has a more distinctive peppermint aroma (Demarne and
van der Walt, 1989; Lis-Balchin, 1991). The cultivar known as P. cv. Ros which gives
rise to the commercial Geranium oil, Bourbon is, most probably, a hybrid between
P capitatum  P. radens (Demarne and van der Walt, 1989).
Geranium oil contains mainly citronellol and geraniol and their esters and differs
completely from that of a true Geranium oil e.g. Geranium robertianum oil (Pedro et al.,
1992) or that of G. maccrorhizum (Ognyanov, 1985).
A further misconception is that of the name Geranium Rose, which has been
interpreted by some aromatherapists as meaning that geranium was distilled over rose
(Price, 1993). This would be rather difficult as geranium leaves would smother the rose
petals!
MISCONCEPTIONS ABOUT THE FUNCTION
OF GERANIUM EXTRACTS AND GERANIUM OIL

Genus Geranium usage and Geranium oil


The actual usages of the geranium extracts mentioned in old herbals are associated with
their tannin content and other water-soluble chemicals e.g. flavonoids, in the leaves or
roots. Essential oils, on the other hand, are steam-distilled volatiles and do not contain
these components.
Valnet (1980) gave Geranium oils major attributes as its vulnerary powers (according to Ancients) and its power to mend fractures and eliminate cancers; he then
provided the following list of properties: internal use as astringent, tonic, antiseptic,
antidiabetic, anticancer; external use as cicatrising agent, antiseptic, analgesic,
parasiticide, insect repellent for mosquitos and gnats. The indications for use vary with
usage i.e. internal use: adrenal cortex deficiency, gastroenteritis, uterine haemorrhage,
sterility, jaundice, urinary stones, gastric ulcer, cancer; external use is indicated by:
engorgement of breasts, sore, burns, cancers, tonsillitis, ophthalmia, facial neuralgia,
gastric and lumbar pain, oedema of legs, herpes, shingles, scurf, lice, etc. The directions
for oral use are given as for Herb Robert, including infusions of the fresh or dried leaves!
The same botanical mistakes have been made by Tisserand (1985) who quotes
directly from Culpepers herbal (1653) about Herb Robert. Tisserand (1985 ) also lists
properties of Geranium oil as: analgesic, antidepressant, antiseptic, cicatrisant,
diuretic, haemostatic, sedative, stimulant of adrenal cortex, tonic and vulnerary. Its
uses are for: aphthae, burns, cancer (uterine), depression, dermatitis, diabetes, diarrhoea, eczema, engorgement of breasts, gastralgia, glossitis, haemorrhage, jaundice,
kidney stones, nervous tension, neuralgia, pediculosis, ringworm, shingles, skin care,
sterility, stomatitis, throat infections, ulvers (ulcers?), and wounds.
Further attributes of Geranium oil
The myth is perpetuated by other authors e.g. Worwood (1991) who says that
Geranium oil is advocated for: depression, menstrual problems, diarrhoea,

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diabetes, sores, neuralgia, bleeding, circulatory problems, eczema, sore throats, nervous
tension, kidney stones. The following home uses are advocated by Lawless
(1992): acne, bruises, broken capillaries, burns, congested skin, cuts, dermatitis, eczema, haemorrhoids, lice, oily complexion, mature skin, mosquito repellent,
ringworm, ulcers, wounds, cellulitis, engorgement of breasts, oedema, poor
circulation, tonsillitis, adrenocortical glands and menopausal problems, nervous tension
and stress-related conditions. Other attributes include having a stimulating effect on
the lymphatic system and a tendency to balance extremes on both the physical and
emotional levels (Westwood, 1991). The same author lists the following as indications
for use: abrasiveness, excessive attachment, lack of balance, emotional extremes, lack of
harmony, lack of moderation, mood swings, overpowering, excessive talkativeness, lack
of tolerance and workaholic. The Geranium oil has also yin qualities and its ruling
planet is Venus (Tisserand, 1985).
It seems, therefore, that Geranium oil is effective for just about every malady. Some
of the remarks in aromatherapy books are even more incredulous e.g. It (Geranium oil)
is reputed to help in cases of uterine and breast cancer and if nothing else, would
certainly help the patient to relax and cope with the pain (Worwood, 1991).
But, where is the proof for all these different functions?
FACTUAL EVIDENCE FOR GERANIUM OIL EFFECTS

The only factual evidence for Pelargonium activity must be taken from the folkmedicinal usage of the plants in their native country (southern Africa), as they were not
available in Europe in any quantity till the eighteenth century and even then were
used solely as ornamentals.
Folk-medicinal usage of Pelargonium species
Pelargonium species were used in South Africa by the local population and also by the
Boers (Pappe, 1868; Watt and Brandwjik, 1962). Several Pelargonium species were used
for antidysenteric purposes, and the more tannin-containing root was used for syphilis.
Wooden articles made for sale were sprinkled with a decoction of some scented
Pelargonium species to ensure a quick sale. Some of the folk-medicinal properties of
Pelargonium species include:
Antidysenteric/antidiarrhoea/anticolic action
P. antidysentericum root
P. reniforme root
P. bowkeri leaf
P. sidaefolium
P. cucullatum root and leaves
P. transvaalense root
P. flabellifolium (syn. P. luridum) root
P. triste root
P. pulveratum root
Antihelmintic
P. triste root

Neuralgia
P. ramosissimum (syn. P. tragacanthoides)

Antiseptic
P. peltatum

Haemorrhoids
P. pulveratum leaves

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Geranium oil and its use in aromatherapy 239

Nephritis
P. cucullatum

Syphilis/gonorrhoea
P. sidaefolium

Fever
P. luridum root
P. alchemilloides
P. transvaalense root

Menstrual flow initiator


fumarioides (syn. P. minimum)
P. grossularioides
P. reniforme

Wounds/abcesses
P. alchemilloides
P. cucullatum leaves
P. reniforme leaves

Astringent
P. antidysentericum
P. peltatum leaf
P. reniforme root
P. luridum root

Colds
P. ramosissimum (syn P. tragacanthoides)
Abortifacient
P. grossularioides

Liver complaints in animals


P. reniforme

Emmanogogue
P. grossularioides
Unfortunately, all these attributes have been due to:
(a) different Pelargonium species to those used in the production of Geranium oil.
(b) they implicate mostly the water-soluble components, as they involved teas and
infusions and not volatile EO.
(c) the plant extracts are mainly used internally and not massaged into the skin.
The pharmacological activity of the water-soluble extracts of the two genera (Geranium
and Pelargonium) are, however, not very different, as Geranium incanum tea was used by
indigenous South Africans as an antihelmintic, but the Europeans used it as an infusion
for venereal diseases; the Southern Sotho tribes in South Africa used Geranium canescens
as a remedy for colic, diarrhoea, dysenteries and fevers (Pappe, 1868; Watt and
Brandwjik, 1962). But this still does not account for the volatile EO functions of
Pelargonium-derived Geranium oil quoted in most aromatherapy books, as virtually no
scientific literature was available at the time.
Pharmacological action of Pelargonium oils
The lipophylic essential oils of Pelargonium species have mainly a spasmolytic effect on
smooth muscle, except for P. grossularioides, which was used as an abortifacient in
Southern African folk medicine (Watt and Breyer-Brandwijk, 1962) and has been
shown to have a spasmogenic action on smooth and uterine muscle in vitro (Lis-Balchin
and Hart, 1994).
Pelargonium EOs from leaves of the many different species and cultivars (other than
those grown to produce commercial Geranium oil) have very different odours and
chemical compositions, but most of the floral-smelling ones act through cyclic AMP as

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Maria Lis-Balchin

the secondary messenger; others with odours which are more pine or menthol-like have
a different mode of action (Lis-Balchin and Hart, 1998). There is therefore some
correlation between their mode of action and their odour and chemical composition.
Furthermore, there was a distinct correlation between the following three criteria:
1
2
3

the chemical composition;


the predicted effect of the oil on smooth muscle in vitro (relaxation, contraction or
both); and
the actual effect on man (either relaxation, stimulation or a mixture of both) as
predicted by aromatherapists (Lis-Balchin and Hart, 1997a).

This indicated that effects shown on the isolated guinea-pig ileum would mimic the
effect on the whole body.
Exploitation of the medicinal properties of Pelargonium
One of the more successful modern medicines derived from the original folk medicinal
usage is Umckaloabo, which is extracted from P. reniforme and P. sidoides tubers
(Kolodziej et al., 1995; Kolodziej and Kaiser, 1997) and used to treat respiratory
conditions. However, this involves internal oral usage of the water-soluble (rather than
volatile) components of the drug and is therefore not true aroma therapy.
Scientific proof of antimicrobial EO efficacy in vitro
Many plant EOs are extremely potent antimicrobials in vitro and can have a substantial effect on many bacteria (Maruzella and Henry, 1958; Deans and Ritchie,
1987) e.g. thyme or oregano oils, which inhibited 25 out of 25 different bacteria
(Lis-Balchin, 1995; Lis-Balchin et al., 1996, 1998). Geranium oil was one of the
most potent antimicrobials after these two oils, but there was a large variation in the
activity of different commercial geranium oils from different sources (Bourbon,
Egyptian, Chinese) or supplier (Lis-Balchin et al., 1996). The actual chemical
composition of the oils was also variable and there was no correlation between
the composition and the bioactivity, suggesting that there was some degree of
adulteration.
CLINICAL AROMATHERAPY TRIALS

Virtually no trials have been conducted using Geranium oil, as lavender oil has almost
always been the choice EO.
Use in childbirth
Studies of the use of aromatherapy in childbirth (Burns and Blaney, 1994) were not very
conclusive, mainly because a large number of different EOs were used at different times
and in different ways and there was a bias towards the use of a few oils e.g. lavender and
clary sage, the latter having a probably undeserved (and unproven) status of being
oestrogenic.

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Geranium oil and its use in aromatherapy 241

High dose chemotherapy


A study at the London clinic into the use of EOs for the treatment of chemotherapyinduced side effects in a group of patients undergoing high dose chemotherapy, with
stem cell rescue for breast cancer (Gravett et al., 1995) was reported at an Aromatherapy
conference but no scientific publications followed. Groups of patients were not randomly allocated, and no-double blinding was attempted.
Treatment for mucositis (damage to mouth lining due to chemotherapy), where
mouth washes often give burning sensation was changed to: one drop Tea tree: one drop
bergamot: one drop geranium in half a tumbler of boiled warm water 5 times a day.
Gargling with swallowing was allowed! This is therefore internal medicine, rather than
aromatherapy. No statistically significant difference was found, but the actual experiment can be severely criticised, as EOs are not soluble in water and the un-dispersed
globules of the oil could have caused even further damage to the mucosa. Another
group suffering from diarrhoea, which was normally treated with codeine phosphate
were treated with Buscopan and aromatherapy, consisting of geranium 15 drops,
German chamomile 10 drops, patchouli 1 drop, turmeric phytol 10 drops mixed in
50 ml of sweet almond oil (i.e. a 5 per cent dilution) which was initially applied by
abdominal massage twice a day, but due to nausea and diarrhoea oral administration in
small doses in an alcoholic vehicle, usually sherry was substituted. The justification for
using geranium was that Geranium is a traditional remedy for gastroenteritis and
stomatitis, which refers to the true geranium and its water-soluble tea and not a
lipophylic, volatile EO from a different genus! No significant differences between
groups, was again found, but the one good outcome was that patients taking this
mixture had a fragrant diarrhoea.
Lack of statistically-significant difference between
massage with and without essential oils
There are few clinical studies and none of them show a statistically-significant difference
between massage with and without EOs (Vickers, 1996); there are no studies using
Geranium oil specifically. Studies involving lavender oil have shown no difference
between three treatments involving aromatherapy massage, massage alone and giving the
patients 30 min of rest in an intensive care unit (Dunn et al., 1995). Another study using
massage, with and without various EOs, on children with atopic eczema showed no
differences after several weeks of treatment, however, a continuation of the study using
EO massage showed a possible sensitization effect, as the symptoms became worse after
subsequent massages following a three-month period of rest (Anderson et al., 2000).
Use in depression
Studies in Italy and France, have offered very little in the way of scientific evidence on
the efficacy of EOs and perfumes on patients and have been reported mainly in Trade
Journals (Rovesti and Colombo, 1973). There was apparently some success in the
treatment of depressed patients, but there is little data supplied as to the precise
diagnosis of the patients, their symptoms, which of these symptoms were relieved, the
number of patients involved and the statistical significance or otherwise of the results.
Under such circumstances, the evidence is at best anecdotal. Most of the recent work

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has not been published in peer-reviewed journals and has consisted of single case studies
of various treatments e.g. Franchomme and Penoel (1990), which largely involve
internal use of EOs.
Use as anti-ageing products
Some EOs are strong antioxidant agents e.g. thyme and clove oils, and have recently
been shown to counteract ageing in animals, as measured by the changes in the lipid
composition of tissue membranes (Dorman et al., 1995). However, the antioxidant
values for 18 commercial geranium samples studied (Lis-Balchin et al., 1996) showed
inconsistencies and suggested that antioxidants may have been added to some of the oils
and not to others.
Psychological and physiological effects of Geranium oil
Many fragrances have been shown to have an effect on mood and in general, pleasant
odours generate happy memories, more positive feelings and a general sense of wellbeing (Warren and Warrenburg, 1993). Much of this type of research has been
conducted by perfumery companies ( Jellinek, 1956) to boost sales and some EOs have
also been used in hospitals in the USA to create a more happy and positive atmosphere
and also in offices and factories in Japan to enhance productivity.
Many EO vapours have been shown to depress contingent negative variation (CNV)
brain waves in human volunteers (Table 21.1) and these are considered to be sedative.
Others increase CNV and are considered stimulant. The effects of inhaling different EOs
on the CNV is compared to the effect on mouse motility and the direct effect of the EO
on smooth muscle in vitro (Table 21.1). Although there is a great difference in the application of the oils and the measurement of their effect, there is surprisingly, frequent
agreement. However, in the case of Geranium oil, both a sedative and stimulant effect is
shown for CNV studies, unlike that for lavender and sandalwood which show sedative
effects throughout. However, even valerian, a well-known sedative showed some stimulant effects in CNV studies. This suggests that either there is a different effect through
concentration or it depends on the individuals liking/disliking of a given smell.
There is some evidence that certain EOs can lower blood pressure, if it is elevated e.g.
nutmeg (Warren and Warrenburg, 1993), but Geranium oil has not been tested for this
specific function.
Table 21.1 Sedative and stimulant EOs
Essential oil

Sedative

Stimulant

Geranium
Rose
Jasmine
Lavender
Sandalwood
Valerian

2,3,5
5
5
1,2,4,5
1,2,3,4,5
1,3,5

2,3
2,3
1,2,4
3

Sources: Kubota et al. (1992): CNV studies in man; Torii et al. (1988):
CNV studies in man; Manley (1993): CNV studies in man; Buchbauer
et al. (1991, 1993): Jager et al. (1992): motility of mice; Lis-Balchin et al.
(1997a,b): smooth muscle in vitro.

2002 Edited by Taylor & Francis

Geranium oil and its use in aromatherapy 243

Direct effect on tissues after skin absorption?


There is no scientific evidence, as yet, regarding the direct action of EOs, applied
through massaging of the skin, on specific internal organs. This is despite some
evidence that certain EO components can be absorbed either through the skin or lungs
( Buchbauer et al., 1992; Jager et al., 1992). Furthermore, although many EOs are very
active on many different animal tissues in vitro ( Lis-Balchin and Hart, 1997b), we have
no idea as yet whether their activity in minute amounts (as used in aromatherapy massage) can benefit the patient through direct action on target organs or tissues (Vickers,
1996) rather than through the odour pathway leading into the mid-brains limbic system and thence through the normal sympathetic and parasympathetic pathways. There
is also no proof that synergism occurs when mixtures of EOs are used (Lis-Balchin
et al., 1998).
Future clinical application of aromatherapy
What could be achieved by using aromatherapy as an adjunct to clinical medicine
especially in hospitals and general practice? So far there have been many successes in
various areas, notably hospices. There are no miracle cures, but an alleviation of suffering and possibly pain, mainly through relaxation due to gentle massage, a nice odour
like Geranium oil, and the presence of someone who cares and listens to the patient.
This is probably also the case in geriatric wards, in general wards, in the treatment
of severely physically and mentally-challenged children and adults etc. There is a need
for this kind of healing contact and the added power of odour, and aromatherapy fits
this niche.
Nurses and other healthcare professionals have the wish to learn and train in the use
of aromatherapy in favour of all the other alternative therapies (Trevelyan, 1996). The
medical profession is also turning towards any branch of alternative medicine, which is
useful in the treatment of patients whose symptoms are largely based on stress and who
do not respond to conventional medicine.
Possible toxicity of Geranium oil
From the toxicological aspect, there is, however, the danger of causing dermatitis in
sensitive people (Rudzki et al., 1976). Geranium oil has only been implicated rarely and
all references are due to contact dermatitis and sensitization. Most of the references are
to one of the main components geraniol (Lovell, 1993). Patch tests to geraniol proved
negative but dermatitis to perfumes containing Geranium oil has been shown in a few
cases (Klarmann, 1958). Sensitization to geraniol using a maximization test proved
negative (Opdyke, 1975). Latest reports from Japanese studies, using patients with
ordinary cosmetic dermatitis and pigmented cosmetic dermatitis, who showed a
positive allergic responses to a wide range of fragrances (Nakayama, 1998), gave a list
of Class A fragrances which were termed common cosmetic sensitizers and primary
sensitizers. This Class included Geranium oil, geraniol, sandalwood oil, artificial
sandalwood, musk ambrette, jasmine absolute, hydroxycitronellal, Ylang ylang oil,
cinnamic alcohol, cinnamaldehyde, eugenol, balsam of Peru and lavender oil.
There is also the danger of airborne contact allergic dermatitis through overuse of
EOs and their continued storage in the home (Schaller and Korting, 1995). There may

2002 Edited by Taylor & Francis

244

Maria Lis-Balchin

also be danger in the overuse of EOs during pregnancy and childbirth. Studies during
childbirth in particular should take into account the babys health, as there is always
the danger of over-sedation of the infant and the subsequent lack of the breathing reflex
after birth.

CONCLUSION

The numerous aromatherapeutic uses for Geranium oil are yet to be scientifically
validated, although there is every reason to accept the scientific evidence that inhalation
of a pleasant aroma and its action through the limbic system has a relaxing effect, as has
massage; theoretically, the two used together could relieve many stress-related conditions like dermatitis, asthma, intestinal problems and headaches could be alleviated.

REFERENCES
Anderson, C., Lis-Balchin, M. and Kirk-Smith, M. (2000) Evaluation of massage with essential
oils on Childhood Atopic Eczema. Phytother. Res., 14, 452456.
Buckle, J. (1997) Clinical Aromatherapy in Nursing. Arnold, London.
Buchbauer, G., Jirovetz, L., Jager, W., Dietrich, H., Plank, C. and Karamat, E. (1991)
Aromatherapy: evidence for the sedative effects of the essential oils of lavender after inhalation. Z. Naturforsch., 46, 10671072.
Buchbauer, G. (1992) Biological effects of fragrances and essential oils. Perf. Flav., 18, 1924.
Buchbauer, G., Jager, W., Jirovetz, l., Ilmberger, J. and Dietrich, H. (1993) Therapeutic properties of essential oils and fragrances. In: R. Teramishu, R.G. Buttery and H. Sugisawa (eds),
Bioactive Volatile Compounds from Plants, 159165. ACS symposium series 525. Washington,
DC: American Chemical Society.
Burns, E. and Blaney, C. (1994) Using Aromatherapy in childbirth. Nurs. Times, 90, 5458.
Culpeper, N. (1653) The English Physitian Enlarged, George Sawbridge, London.
Deans, S.G. and Ritchie, G. (1987) The antibacterial properties of Plant Essential Oils. Int. J.
Food Microbiol., 5, 165180.
Demarne, F. and van der Walt, J.J.A. (1989) Origin of the rose-scented Pelargonium grown on
Reunion Island. S. Afr. J. Bot., 55, 184191.
Dorman, H.J.D., youdim, K.A., Deans, S.G. and Lis-Balchin, M. (1995) Antioxidant-rich plant
volatile oils: in vitro assessment of activity. 26th Int. Symp. Essential Oils, Hamburg,
Germany, Sept., 1013.
Dunn, C., Sleep, J. and Collett, D. (1995) Sensing an improvement: an experimental study to
evaluate the use of aromatherapy, massage and periods of rest in an intensive care unit. J. Adv.
Nursing, 21, 3440.
Franchomme, P. and Penoel, D. (1990) Aromatherapie exactement. Paris. Roger Jollois.
Gravett, P.J., Finn, M. and Hallasey, S. (1995) An investigation of the use of essential oils for
the treatment of chemotherapy-induced side-effects in a group of patients undergoing high
dose chemotherapy, with stem cell rescue for breast cancer. Paper given at Aromatherapy
Conference, AROMA 95, UK.
Grieve, M. (1937) A Modern Herbal. Reprinted 1992. Tiger Books International, London.
Jager, W., Buchbauer, G., Jirovetz, L. and Fritzer, M. (1992) Percutaneous absorption of
lavender oil from a massage oil. J. Soc. Cosmet. Chem., 43, 4954.
Jellinek, P. (1956) Die Psychologischen Grndlagen der Parfumerie. Alfred Hutig Verlag, Heidelberg.
Klarmann, E.G. (1958) Perfume dermatitis. Ann. Allergy, 16, 425434.

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Geranium oil and its use in aromatherapy 245


Kolodziej, H. and Kaiser, O. (1997) Pelargonium sidoides DC. Neuste Erkenntnisse zum
Verstandnis des Phytotherapeutikums Umckaloabo. Z. Phytother., 19, 141151.
Kolodziej, H., Kaiser, O. and Gutman, M. (1995) Arzneilich verwendete Pelargonien aus
Sudafrika. Disch. Apotheker Ztg., 135, 853864.
Kubota, M., Ikemoto, T., Komaki, R. and Inui, M. (1992) Odor and emotion-effects of essential oils on contingent negative variation. Proc. 12th Int. Congress on Flavours, Fragrances and
Essential oils, Vienna, Austria, Oct. 48. pp. 456461.
Lawless, J. (1992) The Encyclopaedia of Essential Oils. Element, Dorset.
Lis-Balchin, M. (1991) Essential oil profiles and their possible use in hybridization of some
common scented geraniums. J. Essent. Oil Res., 3, 99195.
Lis-Balchin, M. and Hart, S. (1994) A pharmacological appraisal of the folk medicinal usage of
Pelargonium grossularioides and Erodium cicutarium (Geraniaceae). J. Herbs, Spices, Med. Plants, 2,
4148.
Lis-Balchin, M. (1995) The Chemistry and Bioactivity of Essential Oils. Amberwood Publishing
Ltd. Surrey.
Lis-Balchin, M., Deans, S.G. and Hart, S. (1996) Bioactivity of commercial Geranium oil from
different sources. J. Essent. Oil Res., 8, 281290.
Lis-Balchin, M. (1997) Essential oils and Aromatherapy: their modern role in healing. J. Roy.
Soc. Health, 117, 324329.
Lis-Balchin, M. and Hart, S. (1997a) Correlation of the chemical profiles of essential oil mixes
with their relaxant or stimulant properties in man and smooth muscle preparations in vitro.
Proc. 27th Int. Symp. Ess. Oils, Vienna, Austria, 811 Sept. 1996. Ch. Franz, A. Mathe and
G. Buchbauer (eds), Allured Pub. Corp., Carol Stream, III. pp. 2428.
Lis-Balchin, M. and Hart, S. (1997b) Pharmacological effect of essential oils on the uterus compared to that on other tissue types. Proc. 27th Int. Symp. Ess. Oils, Vienna, Austria, 811 Sept.
1996. C.H. Franz, A. Mathe and G. Buchbauer (eds), Allured Pub. Corp., Carol Stream, III.
pp. 2932.
Lis-Balchin, M., Deans, S.G. and Hart, S. (1997a) A study of the changes in the bioactivity of
essential oils used singly and as mixtures in aromatherapy. J. Alt. Complement. Med., 3,
249255.
Lis-Balchin, M., Hart, S., Deans, S.D. and Eaglesham, E. (1997b) Comparison of the pharmacological and antimicrobial action of commercial plant essential oils. J. Herbs, Spices, Med.
Plants, 4, 6986.
Lis-Balchin, M. and Hart, S. (1998) Studies on the mode of action of scented-leaf Pelargonium
(Geraniaceae). Phytother. Res., 12, 215217.
Lis-Balchin, M., Deans, S.G. and Eaglesham, E. (1998) Relationship between the bioactivity
and chemical composition of commercial plant essential oils. Flav. Fragr. J., 13, 98104.
Lis-Balchin, M. (1999) Possible Health and Safety Problems in the use of Novel Plant essential
oils and extracts in Aromatherapy. J. Roy. Soc. Prom. Health, 119, 240243.
Lovell, C.R. (1993) Plants and the skin, Blackwell Scientific. Publ., Oxford.
Manley, C.H. (1993) Psychophysiological effect of odor. Crit. Rev. Food Sci. Nutr., 33, 5762.
Maruzella, J.C. and Henry, A. (1958) The in vitro antibacterial activity of essential oils and oil
combinations. J. Am. Pharmaceut. Assoc., 47, 294296.
Nakayama, H. (1998) Fragrance Hypersensitivity and its control. In: P.J. Frosch, J.D. Johansen
and I.R. White (eds), Fragrances: Beneficial and Adverse Affects, Springer Verlag, Berlin.
pp. 8391.
Ognyanov, I. (1985) Bulgarian Zdravetz oil. Perf. Flav., 10(6), 3844.
Opdyke, D.L.T. (1975) Monographs on fragrance raw materials. Food Cosmet. Toxicol., 13, 451.
Pappe, L. (1868) Florae Capensis Medicae, Prodromus; 3rd ed. Cape Town.
Pedro, L.G., Pais, M.S.S. and Scheffer, J.J.C. (1992) Composition of the Essential oil of Geranium
robertianum L. Flav. Fragr. J., 7, 223226.
Price, S. (1993) Aromatherapy Workbook, Thorsons, London.

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Rovesti, P. and Colombo, E. (1973) Aromatherapy and aerosols. Soap. Perfumery and Cosmetics, 46,
475477.
Rudzki, E., Grzywa, Z. and Bruo, W.S. (1976) Sensitivity to 35 essential oils. Contact Derm., 2,
196200.
Schaller, M. and Korting, H.C. (1995) Allergic airborne contact dermatitis from essential oils
used in aromatherapy. Clin. Exp. Dermatol., 20, 143145.
Tisserand, R. (1985) The Art of Aromatherapy, Revised ed. C.W. Daniel Co. Ltd, Saffron Walden,
pp. 231, 232.
Torii, S., Fukuda, H., Kanemoto, H., Miyanchio, R., Hamauzu, Y. and Kawasaki, M. (1988)
Contingent negative variation and the psychological effects of odor. In: S. Toller and G.H.
Dodds (eds), Perfumery: The Psychology and Biology of Fragrance. Chapman & Hall, New York.
Trevelyan, J. (1996) A true complement. Nurs. Times, 92, 4243.
Valnet, J. (1982) The Practice of Aromatherapy. C.W. Daniels Co. Ltd, Saffron Walden.
Vickers, A. (1996) Massage and Aromatherapy. A Guide for Health Professionals. Chapman & Hall,
London.
Warren, C. and Warrenburg, S. (1993). Mood Benefits of Fragrance. Perf. Flavorist, 18, 915.
Watt, J.M. and Breyer-Brandwijk, M.G. (1962) The Medicinal Plants of Southern Africa.
Livingstone Ltd, Edinburgh.
Westwood, C. (1991) Aromatherapy. Stress Management: A Guide for Home Use. Amberwood
Publishing Ltd, Dorset.
Worwood, V.A. (1991) The Fragrant Pharmacy. Bantam Books, London. p. 25.

2002 Edited by Taylor & Francis

22 Perfumery and cosmetic products


utilising Geranium oil
Rhona Wells and Maria Lis-Balchin

ORIGINS OF COMMERCIAL GERANIUM OIL

Geranium oil, included in perfumes and cosmetic products is extracted from the
scented leaves of several Pelargonium species and cultivars which originated from
southern Africa. John Tradescant obtained the first species in 1631 for the UK and
other species were introduced over the next 300 years and subsequently hybridized.
The origin of Geranium oil is very confused as it is frequently referred to as
Pelargonium odoratissimum. This is an apple-scented species and the misnomer probably
arose from a particular P. graveolens variety which was very odouriferous. The name
P. odoratissimum was then used by early writers of Essential Oil books (Guenther, 1951)
as well as the trade distributors.
Other names used are P. asperum and P. graveolens. The latter may be a parent of some
Geranium oils originating in Africa, but the main source of the oil is from a cultivar
known as P. cv. Ros which gives rise to the commercial Geranium oil, Bourbon and
originated from hybridizations in England, in the eighteenth century; the cultivar was
then exported to the South of France and Reunion and also lately to China. The Ros
cultivar is most probably, a hybrid between P. capitatum  P. radens (Demarne and van
der Walt, 1989).
The first plants grown for the French perfumery industry were planted in Algeria in
1847; in the 1880s extensive plantings were set out in Reunion Island. Nowadays the
main sites are China, Egypt and Reunion, although the latter is decreasing its production. Geranium plants were also extensively grown in the provence region of France,
but due to the high costs of production, they are no longer grown there.
THE POOR MANS ROSE OIL

Geranium oil and concoctions using Geranium oil components have long been used in
making artificial rose oil. Examples of rose extenders and various rose formulations
abound, based on either the essential oil of geranium and its fractions (Table 22.1) or
synthetic components (Table 22.2). Other Rose bases and enhancers are provided by
Curtis and Williams (1994).
Geranium oil mixes well with artificial musk, vanillin, bergamot oils, patchouli,
clove and heliotropin. Geranium oil Bourbon is frequently adulterated and the real
or preferred oil can only be detected by the perfumery Noses and stringent chemical
analysis. Geranium oil is frequently made entirely from synthetic components.

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Rhona Wells and Maria Lis-Balchin


Table 22.1 Rose extender
Constituent
Geraniol ex Palmarosa
Oil of Grasse geranium
Phenylethyl alcohol
Linalool ex bois de rose
Rhodinol ex African geranium
l-Citronellol
Nerol
Farnesol
Total

Part by weight
1.5
0.5
2.5
1.2
1.2
3.0
0.07
0.03
10.00

Table 22.2 Rose perfume


Constituent
Rhodinol
Phenylethyl alcohol
Cinnamic alcohol
Geraniol
Citronellol
Linalool
Hydroxycitronellol
Linalyl acetate
Eugenol
Rose de Grasse absolute
Geranium (African) oil
Phenylethyl acetate
Total

Part by weight
10
20
6
20
10
6
5
4
4
4
10
1
100

Rhodinol ex Geranium is used with hydroxycitronellol, linalool, geraniol, dimethyl


benzyl carbide, cinnamic alcohol, phenyl ethyl alcohol, geranyl and linalyl esters in modern
perfumery and cosmetic products. This rhodinol is often adulterated with synthetic
rhodinol, fractions of citronella or palmarosa oils and other synthetic compounds.
Some of the geranium oils produced are not suitable for perfumery due to a earthy,
potato-like, sulphide top notes often found. This depends partly on the method of
production, especially the use of old, iron stills, and more so on the actual cultivar of
Pelargonium used and the conditions under which it grows. Modern, massive, stainless
steel stills ensure a better and more consistent product.
Geranium oil is still used in high quality perfumes and to a lesser extent the food
processing industry. Its herbal character also lends itself to some toiletries where a
delicate herbal note is required to reinforce the natural concept. It is also well loved
by aromatherapists, who use it as a sedative essential oil.
FAMOUS PERFUMES CONTAINING GERANIUM OIL

Geranium oil displays green herbal, fresh yet earthy characterisitics and is frequently used
in masculine fragrances especially as a heart note. Geranium is seldom found as a top note,

2002 Edited by Taylor & Francis

Perfumery and cosmetic products utilizing Geranium oil 249


Table 22.3 Perfumes containing Geranium in conjunction
with Lavender
Compound

Parts

Fougere-type perfume
Lavender oil, French
Bergamot oil, FCF
Coumarin
Rose base
Jasmine base
Oakmoss absolute
Patchouli oil, light
Vetivert oil, Bourbon
Geranium oil, Bourbon
Iso-amyl salicylate

14
8
12
5
4
6
2
10
2
3

Source: Curtis and Williams, 1994.

Modern Lavender water


Lavender oil, French
Bergamot oil, FCF
Lemon oil, Sicilian
Neroli oil, reconstituted
Musk ketone
Sweet orange oil
Geranium oil, Reunion
Benzoin resinoid

45
25
6
4
3
3
4
4

Source: Curtis and Williams, 1996.

as it tends to be long-lasting and add body to a fragrance. It is frequently used in conjunction with lavender in the true mens lavender scents such as Moustache (Rochas) or
Pino Silvestre, and also the classical fougre blends (Table 22.3), where the top notes are
primarily lavender linked and the heart lends itself well to the dry floral aspects of geranium. It also adds floral aspects to green fragrances such as Grey Flannel and Monsieur
Lanvin.
Although geranium is more predominant in mens classical fragrances, it also appears
in womens fragrances, in green florals, as in a heart note in Ivoire, Balmain (1980) as
well as featuring in heart notes of classical chypres such as Cabochard, Gres (1958). The
original Chypre was that of Coty (1917), a bouquet of orange, geranium, spices and
oakmoss and a fragrance so individual that it inspired a whole family of chypres.
Giorgio, Armani (1981) is a combination of mandarin and geranium to give touch of
freshness to the top note.
Jean-Francois Laporte designed perfumes after the countries he had visited e.g. geranium was a perfume inspired by his visit to Egypt, reminding him of the heady fragrance of sun-drenched geraniums stacked on a wooden cart (Barille and Laroze, 1995).
Paris, Yves St. Laurent (1983) contained geranium as one of the top notes, with
mimosa, bergamot, mayflower, hawthorn and juniper. The middle notes were from
Damascus rose, may-rose and violet and the base notes were provided by sandalwood,
iris and amber (Edwards, 1997).

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Rhona Wells and Maria Lis-Balchin

REFERENCES
Barille, E. and Laroze, C. (1995) The Book of Perfume, Flammarion, Paris.
Curtis, T. and Williams, D.G. (1994) Introduction to Perfumery, Part, III, Ellis Horwood, London.
Demarne, F. and van der Walt, J.J.A. (1989) Origin of the rose-scented Pelargonium grown on
Reunion Island, S. Afr. J. Bot., 55, 184191.
Edwards, M. (1997) Perfume Legends, HM Editions, Paris.
Guenther, E. (1951) The Essential oils, vol. 3, van Nostrand Co., New York.

Other general references for perfumery


Arctander, S. (1960) Perfume and Flavor Materials of Natural Origin, Elizabeth, N.J., USA.
Haarman and Reimer (1989) The Book of Perfume, 5 vols., R. Gloss & Co., Germany.
Irvine, S. (1995) Perfume, Aurum Book, Haldane Mason Ltd., London.
Lamparsky, D. ed. (1991) Perfumes, Art, Science and Technology, Elsevier Science, New York.
Lefkowith, C.M. (1994) The Art of Perfume, Thames and Hudson, London.
Morris, E.T. (1984) Fragrance. The Story of Perfume from Cleopatra to Chanel, Charles Scribners
Sons, New York.
Pavia, F. (1995) The World of Perfume, Knickerbocker Press, New York.
Piesse, S. (1890) Histoire des parfums, J.B. Baillire et fils, Paris.
Poucher, W.A. (1994) The Production, Manufacture and Application of Perfumes. Chapman & Hall,
New York.
Trueman, J. (1975) The Romantic Story of Scent, Aldus/Jupiter.
Wells, F.V. and Billot, M. (1988) Perfumery Technology, Ellis Harwood Ltd., Chichester, 2nd Ed.

2002 Edited by Taylor & Francis

23 New research: possible uses


of various Pelargonium leaf oils
and extracts as food preservatives
Maria Lis-Balchin

INTRODUCTION

Conventional food preservatives are falling into disrepute as more data accumulates
regarding the toxicity of the chemicals used. Butylated hydroxytoluene (BHT) and
butylated hydroxyanisole (BHA) are particularly suspect, but there are no available substitutes as they have such a wide usage in foods. Many herbs, containing essential oils
(EOs), have been used as preservatives in foods for centuries, but the most biocidal of these
are very odourous e.g. thyme, oreganum, clove and therefore have a restricted value.
Pelargonium EOs obtained from different species, and having a wide spectrum of
chemical compositions, have shown considerable potential as antimicrobial agents
(Lis-Balchin et al., 1995); Pelargonium solvent extracts have shown a similar property
(Lis-Balchin et al., 1998a), including the more hydrophylic extracts (Lis-Balchin
and Deans, 1996). Commercial geranium oil, obtained from different sources and
commercial outlets, showed considerable variation in bioactivity against 25 different
bacterial species, 20 different variants of Listeria monocytogenes and three fungi, which
was not correlated with the chemical composition or the stated country of origin
(Lis-Balchin et al., 1996a). The bioactivity against microorganisms was very potent for
the main synthetic components citronellol and geraniol, but low for authentic Geranium
oil, suggesting that differences in adulteration were responsible for the main differences
in bioactivity. These results were also in line with former studies of commercial EOs
(Lis-Balchin et al., 1998b), where differences in bioactivity between EOs, which were
similarly-labelled, proved to have different bioactivities.
The possibility of detecting adulteration was further supported by bioactivity measurements using two enantiomers of limonene (Lis-Balchin et al., 1996b) and -pinene
(Lis-Balchin et al., 1999), which suggested that the individual bioactivity of each
enantiomer varied against different parameters, and that adulteration of commercial
oils with synthetic components could possibly be proven.
ANTIBACTERIAL ACTIVITY OF ESSENTIAL OILS AND SOLVENT
EXTRACTS OF PELARGONIUM SPECIES AND CULTIVARS

The bioactivity of 18 Pelargonium species and cultivars (extracted with solvents and
by steam distillation) was studied against four bacteria, namely: Staphylococcus aureus

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Maria Lis-Balchin

Table 23.1 Antimicrobial activity of plant extracts against four bacteria


Plant

Attar of Roses
SD
MeOH
Radula
SD
MeOH
Sweet Mimosa
SD
MeOH
P. tomentosum
SD
MeOH
Chocolate tomentosum
SD
MeOH
Lemon Fancy
SD
MeOH
Crispum variegatum
SD
MeOH
P.  fragrans
SD
MeOH
Geranium oil (Commores)
SD undiluted
SD dil 10
SD dil 100

Zones of inhibition, mm
Staphylococcus aureus Proteus vulgaris

Bacillus cereus Staphylococcus epidermidis

12
9

11
8

17

8
13

8
13

7
13

10
13

8
18

7
14

10
17

n/a
12

18

6
10

10

n/a
9

10

8
8

8
12

n/a
9

8
10

9
8

13
11

18
10

12
8

14

10

8
7

10
28

9
23

n/a
16

8
19

10
8

10
7

9
6
6

9
8

Notes
SD steam distilled extract; MeOH methanolic extract.

(ATCC 9144); S. epidermidis (ATCC 12228); Proteus vulgaris (ATCC 13315) and Bacillus
cereus (NCIMB 6349).
The solvent extracts were made using fresh Pelargonium leaves, which were sequentially, but not exhaustively extracted with petroleum spirits followed by methanol. The
solvent extracts were all reduced in a rotary evaporator (at temperatures under 40 C).
Essential oils were obtained using a Clavenger-type apparatus, from fresh leaves after
2 h of distillation.
Bioactivity and chemical composition
The bioactivity of Attar of Roses was similar to the published activities of commercial
geranium oils, which themselves showed a considerable span (Figure 23.1). This was not
surprising as the source of commercial Geranium oil is from a cultivar very similar to
that of the latter. The bioactivity of different Pelargonium EOs were largely correlated
with their chemical composition: the rose-like geranium oils were potent antibacterials,

2002 Edited by Taylor & Francis

Zone of inhibition

Uses of various Pelargonium oils and extracts as food preservatives 253


20
18
16
14
12
10
8
6
4
2
0

Staph aureus
Proteus
Bacillus
Staph epid.

9 10 11 12 13 14 15 16 17 18 19 20
Pelargoniums

Figure 23.1 Antibacterial effect of Pelargonium extracts (steam distilled). 1 Attar of Roses, 2 Lady
Plymouth, 3 Pink Little Gem, 4 Radula, 5 Robers Lemon Rose, 6 Sweet
Mimosa, 7 P. tomentosum, 8 Chocolate tomentosum, 9 Lemon Fancy, 10 P. crispum
variegatum, 11 Clorinda, 12 Copthorne, 13 Oak cv., 14 Village Hill Oak,
15 P. denticultum, 16 P.  fragrans, 17 P. odoratissimum, 18 Orsett, 19 Geranium
oil (commercial), 20 Cinnamon oil (commercial)
Table 23.2 Chemical composition of Pelargonium oils
Pelargonium

Main components

Attar of Roses
Robers lemon Rose

Citronellol, geraniol
Citronellol, citronellyl formate, isomenthone, linalool,
sesquiterpenenes;

-Cymene, hexenyl butyrate, limonene, sesquiterpenes;


-Pinene, methyl eugenol, fenchone, limonene;
-Pinene, -phellandrene,
-cymene, sesquiterpenes;
Neral, geranial, sesquiterpenes;
Neral, geranial, sesquiterpenes;
Citronellol, geraniol, citronellyl formate, isomenthone.

P. denticulatum
P.  fragrans
Clorinda
Lemon Fancy
Crispum variegatum
Geranium oil (Commercial)

as were their main components: citronellol and geraniol, confirming previous results
(Lis-Balchin et al., 1996a,b).
The minty and the commercial Vicks ointment-like species showed very different
low antibacterial effects. P. tomentosum which is largely composed of the two components
menthone and isomenthone, showed the lowest bactericidal activity; however, the
Chocolate tomentosum or Chocolate Peppermint which is a cultivar of P. tomentosum,
was more active, the activity being a reflection of the high concentration of monoterpenes and sesquiterpenes in its composition.
Lemon Fancy, containing neral and geraniol i.e. citral, as its main components, had
the most potent activity against B. cereus and P. vulgaris, a reflection of synthetic citral
itself. However, Crispum variegatum with a similar composition, did not have the same
activity as Lemon Fancy, suggesting that other components also play a part.
The camphoraceus, Vicks-like group: Clorinda, Copthorne, Oak-cultivars,
Orsett, P. denticulatum, P.  fragrans, and the apple-scented P. odoratissimum, had a similar antibacterial action. However, their chemical composition was very different.

2002 Edited by Taylor & Francis

254

Maria Lis-Balchin
20
18

Zone of inhibition

16
14
12

Staph aur.
Proteus
Bacillus
Staph. epid

10
8
6
4
2
0
1

10 11 12 13 14 15 16 17 18

Pelargoniums

Figure 23.2 Antibacterial effect of Pelargonium extracts (petroleum ether). 1 Attar of Roses, 2 Lady
Plymouth, 3 Pink Little Gem, 4 Radula, 5 Robers Lemon Rose, 6 Sweet
Mimosa, 7 P. tomentosum, 8 Chocolate tomentosum, 9 Lemon Fancy, 10 P. crispum
variegatum, 11 Clorinda, 12 Copthorne, 13 Oak cv., 14Village Hill Oak,
15 P. denticultum, 16 P.  fragrans, 17 P. odoratissimum, 18 Orsett.

Pelargonium oils with a high level of limonene, a component of citrus oils, e.g. Sweet
Mimosa, Copthorne, and the Oak cultivars, had a low biological activity, similar to
that of citrus oils like lemon (Lis-Balchin et al., 1998b).
Hydrophobic extracts
The petroleum spirit extracts, which resemble the steam distilled samples, except for
the additional extraction of various other components, shared many similarities
with the latter and had activities in the same range, but due to the dilution factors
involved, the antibacterial activities were in fact much higher (Figure 23.2).
Hydrophylic extracts
The hydrophylic extracts in the series, proved to have more potent antibacterial activity than the EOs (Figure 23.3): this suggests that the flavonoids, tannins and other
phenolics are the effective antimicrobial agents in the whole plant (Lis-Balchin and
Deans, 1996; Lis-Balchin et al., 1998c).
ESSENTIAL OILS OF PELARGONIUM SPECIES AND CULTIVARS:
USE AS PRESERVATIVES IN FOOD PROCESSING

Using a Quiche filling as a model food system


Using a quiche filling as a model food system, the antimicrobial activity of
Pelargonium EOs was investigated against Salmonella enteriditis (PT4 WT 132344),

2002 Edited by Taylor & Francis

Uses of various Pelargonium oils and extracts as food preservatives 255


30

Zone of inhibition

25
20
Staph aur.
Proteus
Bacillus
Staph. epid

15
10
5
0
1

10 11 12 13 14 15 16 17 18

Pelargoniums

Figure 23.3 Antibacterial effect of Pelargonium extracts (methanol). 1 Attar of Roses, 2 Lady
Plymouth, 3 Pink Little Gem, 4 Radula, 5 Robers Lemon Rose, 6 Sweet
Mimosa, 7 P. tomentosum, 8 Chocolate tomentosum, 9 Lemon Fancy, 10 P.
crispum variegatum, 11 Clorinda, 12 Copthorne, 13 Oak cv., 14 Village Hill
Oak, 15 P. denticultum, 16 P.  fragrans, 17 P. odoratissimum, 18 Orsett.

Listeria innocua (NCTC 10528), Saccharomyces ludwigii (a cider isolate), and


Zygosaccharomyces bailii (NCTC 1766). The EOs were in concentrations ranging from
250 to 500 ppm (Lis-Balchin et al., 1998b). The quiche filling was composed of two
medium eggs, mixed with 200 ml milk and 750 g of mixed frozen vegetables which
were previously boiled till soft and mashed up; the mixture was autoclaved prior to
inoculation, and EOs were added at 250, 500 and 1000 ppm to different portions.
At 250 ppm, Attar of Roses, P. filicifolium, Patons Unique, Sweet Mimosa, and
P. glutinosum showed considerable antimicrobial activity, compared with commercial
cinnamon, clove, thyme and coriander (Figure 23.4). The most active against Z. bailii
was thyme oil and Sweet Mimosa; the activity of EOs was lower against the bacteria,
with Patons Unique having the most potent activity against S. enteriditis. The log
cfu/g1 reduction was around 0.1 (for Salmonella enteriditis and Listeria innocua) to 2.6
(for Salmonella ludwigii and Zygosaccharomyces bailii).
At 500 ppm, thyme oil was most inhibitory against S. ludwigii, followed by Madam
Nonin and P. glutinosum and was considerably more active than cinnamon, clove, and
coriander oils (Figures 23.5a,b). Thyme, Madam Nonin, Patons Unique and Sweet
Mimosa were all equally active against Z. bailii. Coriander, followed by P. glutinosum,
Patons Unique, Geranium oil (commercial) and Sweet Mimosa were strongly active
against S. enteriditis and L. innocua. Clorinda, P. filicifolium and Lady Plymouth, were
almost equally good. The log cfu/g1 reduction was around 1.4 (for Salmonella enteriditis) to 4.3 (for Salmonella ludwigii).
The comparatively low dosages of Pelargonium EOs showing antimicrobial activity, used
in this study, was more beneficial than higher doses of mint oil used by Tassou et al.
(1995), who also used a lower inoculum in their model food. This strongly suggests that

2002 Edited by Taylor & Francis

256

Maria Lis-Balchin
3.5

SL
ZB
SE
LI

log cfu/g reduction

3
2.5
2
1.5
1
0.5
0

GER

THY

ATTAR

PU

SM

PF

EO added

Figure 23.4 Antimicrobial activiy of essential oils (at 250 ppm) against Saccharomyces ludwigii (SL),
Zygosaccharomyces bailii (ZB), Salmonella enteriditis (SE) and Listeria innocua (LI) respectively.
GER Commercial Geranium oil, THY Commercial thyme oil, ATTAR Attar of
Roses, PU Patons Unique, SM Sweet Mimosa, PF P. filicifolium.

Table 23.3 Pelargonium essential oils and hydrophilic


extracts useful as antimicrobial agents
P. filicifolium
P.  fragrans
P. exstipulatum
P. Lady Plymouth
P. scabrum
P. tomentosum
P. Chocolate Peppermint
P. vitifolium
P. glutinosum
P. odoratissimum
P. graveolens
P. Rose/Attar of Roses
P. quercifolium
P. cucullatum
P. citronellum
P. papilionaceum
P. Clorinda
P. Purple Unique

Pelargonium EOs have a great potential as antimicrobial agents in foods, as they are nontoxic and have a more pleasant and not over-bearing odour potential than the strong
antimicrobial EOs. The probability of their commercial usage in foods, when mixed with
other natural antimicrobials ( Lis-Balchin and Deans, 1997), is under investigation.

2002 Edited by Taylor & Francis

5
4.5
4

log cfu/g reduction

3.5
SL
ZB
SE
LI

3
2.5
2
1.5
1
0.5
0

GER

THY

ATTAR

PU

SM

PF

Pelargoniums

Figure 23.5a Antimicrobial activiy of essential oils (at 500 ppm) against Saccharomyces ludwigii (SL),
Zygosaccharomyces bailii (ZB), Salmonella enteriditis (SE) and Listeria innocua (LI) respectively.
GER Commercial Geranium oil, THY Commercial thyme oil, ATTAR Attar of
Roses, PU Patons Unique, SM Sweet Mimosa, PF P. filicifolium.

4.5
SL
ZB
SE
LI

log cfu/g reduction

3.5
3
2.5
2
1.5
1
0.5
0

CIN

CLOVE

COR

LP
EO added

MN

CLOR

PG

Figure 23.5b Antimicrobial activiy of essential oils (at 500 ppm) against Saccharomyces ludwigii (SL),
Zygosaccharomyces bailii (ZB), Salmonella enteriditis (SE) and Listeria innocua (LI) respectively.
CIN Commercial cinnamon oil, CLOVE Commercial clove oil, COR Commercial coriander oil, LP Lady Plymouth, MN Madam Nonin, CLOR Clorinda,
PG P. glutinosum.

2002 Edited by Taylor & Francis

258

Maria Lis-Balchin

COMPARATIVE ANTIMICROBIAL ACTIVITY OF


PELARGONIUM AND SELECTED PLANT ESSENTIAL OILS AND
THEIR RESPECTIVE HYDROSOLS IN A MODEL FOOD SYSTEM

Steam/water distillation of EOs inevitably results in the production of a hydrosol as


well as leaving the residual plant material. This hydrosol residue is often not utilized,
except for a few floral products like rose-water. It seemed that there is therefore a
possible loss of opportunity for salvaging the hydrosols if they proved to have some
commercially feasible bioactivity like, for example, antimicrobial activity.
Preliminary studies using the more water-soluble extracts of various Pelargonium
plants indicated that these had indeed considerable antimicrobial activity. These studies
were carried out using the in vitro agar well test (Lis-Balchin and Deans, 1996). The
idea, which in theory seemed plausible, seemed therefore worthwhile to be studied in
a model food system.
Plant EOs were obtained by distillation using a glass Clavenger-type laboratory still,
from fresh leaves of Pelargonium Attar of Roses. Other, potentially very active antimicrobial plants were also tested. These comprised: dried leaves of meadowsweet
(Filipendula ulmaria), dried cinnamon bark (Cinnamomum verum), dried bay leaves
(Laurus nobilis), clove buds (Eugenia caryophyllus) (Lis-Balchin et al., 2000). The hydrosol
remaining, after the distillation of the EO in each case, was reduced by a hundred-fold
using a rotary evaporator at 50 C.
A Model Food System, consisting of 250 g Porridge oats, 200 ml whole milk
and 300 g of mixed vegetables (Tesco frozen vegetables) was mixed well together
with (Maximum recovery diluent, 1:1) (MRD), and then 10 g portions were
inoculated with a 24 h subculture of either Staphylococcus aureus (gram-positive) or
Escherichia coli (gram-negative) at 104 cfu/ml and incubated with or without a plant
EO or its hydrosol (at 1000 ppm) for 24 h at 37 C for E. coli and 30 C for
S. aureus. The log cfu g1 reduction in the bacterial numbers (estimated using the
pour-plate technique, after incubation at 25 C  48 h) was then compared against
controls.

log cfu/g reduction

7
6
5
4
EO
Hydrosol

3
2
1
0

Pel

Cin

Clove

Bay

Mead

EO or hydrosols

Figure 23.6 Antimicrobial action of essential oils and hydrosols against Staphylococcus aureus
in porridge.

2002 Edited by Taylor & Francis

Uses of various Pelargonium oils and extracts as food preservatives 259

log cfu/g reduction

7
6
5
4

EO
Hydrosol

3
2
1
0
Pel

Cin

Clove

Bay

Mead

EO or hydrosol

Figure 23.7 Antimicrobial action of essential oils and hydrosols against Staphylococcus aureus in MRD.

Activity against Staphylococcus aureus in the porridge system


The results indicated that meadowsweet oil (at 1000 ppm) was totally effective against
both S. aureus and E. coli, but its hydrosol was only slightly effective against S. aureus
in the porridge system (Figure 23.6); the oil was totally effective from 250 ppm. The
clove, cinnamon and Pelargonium oils were very effective against S. aureus, with bay oil
slightly so; however there was only slight antibacterial effect using cinnamon and
bay hydrosols and the rest of the hydrosols were ineffective. The effect against this
bacterium in MRD was very potent (Figure 23.7).
Activity against E. coli in the porridge system
Meadowsweet oil had a very strong effect against E. coli in porridge, and there was a
decreasing effect with cinnamon, clove and Pelargonium oils respectively; there was no
significant effect against E. coli by any plant hydrosol (Figure 23.8).
Activity in MRD
Antimicrobial effectiveness of all plant EOs against both the bacteria in the MRD was
greatly enhanced (Figure 23.7), suggesting that the porridge-based food system was
sequestering the oils or the bacteria or simply inhibiting the effect of EOs; the
effectiveness of hydrosols from meadowsweet, Pelargonium, clove and to a lesser extent
cinnamon and bay in MRD, again showed the difficulties of the practical application of
potential antimicrobial agents in some foods.
The results using hydrosols, i.e. the hydrophylic extracts in actual food systems were
therefore disappointing, as the results in an in vitro assay had shown great promise.
Possible explanation for poor antimicrobial results of hydrosols
in a food system
The fact that all hydrosols were effective against S. aureus in the liquid MRD, and the
lack of action of the hydrosols, compared to the potent action of the corresponding EOs

2002 Edited by Taylor & Francis

260

Maria Lis-Balchin

against E. coli, suggested that the difference in composition of the food system and
MRD and the difference in the water-solubility of the extracts was largely responsible
for this difference in bioactivity.
Taking first the divergent activity of the EO and its corresponding hydrosol against
S. aureus in the food system compared to that in MRD, one can see that hydrosols seem
to be effective in an aqueous medium, but not in a medium containing fat, protein and
carbohydrate. The main problematic food component seems to be the fat content. This
theory was suggested by preliminary results using a bechamel sauce as the food system.
This high-fat system (Table 23.4) proved to be completely detrimental in attaining any
positive antimicrobial results at all using hydrosols. Reducing the fat content (Table
23.4) in the porridge system had a positive effect on the antimicrobial action of the
hydrosols. The probable reason for this is that the fat-soluble EOs are probably
sequestered in the fatty components whilst the bacteria are to be located mainly in the
watery component and therefore unavailable to the EO. Therefore the more fat there is,
the greater sequestering of the EOs occur.
The difference in fat solubility between the hydrosols and their corresponding EOs
probably accounts for their difference in antimicrobial activity in the food system.
9
8

log cfu/g reduction

7
6
5
4

EO
Hydrosol

3
2
1
0
Pel

Cin

Clove

Bay

Mead

EO or hydrosol

Figure 23.8 Antimicrobial action of essentials oils and hydrosols against E. coli in Porridge.

Table 23.4 Nutritional composition of model food systems


Food component
Porridge
Protein
Fat
Carbohydrate
Bechamel sauce
Protein
Fat
Carbohydrate

Per 10 g (g)
0.33
0.22
0.92
0.33
0.73
0.77

Notes
Composition of Bechamel sauce: 10 g butter; 10 g flour; 200 ml milk.

2002 Edited by Taylor & Francis

Uses of various Pelargonium oils and extracts as food preservatives 261

However, the very reasons given above could not be used as an argument for the lower
antimicrobial activity shown by the hydrosols compared with that of the EOs. If we
consider the fact that both the bacteria and the hydrosols have a preference for the aqueous phase of the medium, this would suggest that the hydrophylic hydrosols would be
more active. However, the reverse is apparent (Figure 23.7). There is therefore a much
more complex explanation for this differential effect.
CONCLUSION

The potential usefulness of Pelargonium EOs and more hydrophylic extracts is only
beginning to emerge. The main Pelargonium EOs so far studied and shown to be strongly
antimicrobial are shown in Table 23.4. As there is a strong indication that the
hydrophylic extracts are even more potent as antimicrobials, there remain more than
240 species and thousands of cultivars to study in order to ascertain which are the most
active antimicrobial agents and which could be used commercially in food processing
and in household products like cleaners and air-fresheners and even the great range of
cosmetics.
REFERENCES
Lis-Balchin, M., Hart, S., Deans, S.G. and Eaglesham, E. (1995) Potential agrochemical and
medicinal usage of essential oils of Pelargonium species. Herbs, Spices Med. Plants, 3, 1122.
Lis-Balchin, M. and Deans, S.G. (1996) Antimicrobial effects of hydrophylic extracts of
Pelargonium species (Geraniaceae). Letts. Appl. Microbiol., 23, 205207.
Lis-Balchin, M. and Deans, S.G. (1997) Studies on the potential usage of mixtures of plant
essential oils as synergistic antibacterial agents in foods. Phytother. Res., 12, 14.
Lis-Balchin, M., hart, S., Deans, S.G. and Eaglesham, E. (1996a) Comparison of the pharmacological and Antimicrobial action of commercial plant Essential Oils. J. Herbs, Spices & Med. Plants,
4, 6986.
Lis-Balchin, M., Deans, S.G. and Hart, S. (1996b) Bioactivity of commercial Geranium oil from
different sources. J. Essent. Oil Res., 8, 281290.
Lis-Balchin, M., Buchbauer, G., Hirtenlehner, T. and Resch, M. (1998a) Antimicrobial activity
of novel Pelargonium essential oils added to a quiche filling as a model food system. Lett. Appl.
Microbiol., 27, 207210.
Lis-Balchin, M., Deans, S.G. and Eaglesham, E. (1998b) Relationship between the bioactivity
and chemical composition of commercial plant essential oils. Flav. Fragr. J., 13, 98104.
Lis-Balchin, M., Buchbauer, G., Ribisch, K. and Wenger, M.-T. (1998c) Comparative antibacterial effects of novel Pelargonium essential oils and solvent extracts. Lett. Appl. Microbiol., 27,
135141.
Lis-Balchin, M., O chocka, R.J., Deans, S.G. and Hart, S. (1999) Differences in bioactivity
between the enantiomers of -pinene. J. Essent. Oil Res., 11, 393397.
Lis-Balchin, M., Buchbauer, G., Astrid Brandstetter, A. and Andrea Bauer, A. (2000) Comparative
antimicrobial activity of Pelargonium and other selected plant essential oils and their respective
hydrosols in a model food system. Paper presented at: Int. Ess. Oil. Symp., Hamburg, Sept.
1013. To be published.
Tassou, C.C., Drosinos, E.H. and Nychas, G.J.E. (1995) Effects of essential oil from mint (mentha piperita) on Salmonella enteriditis and Listeria monocytogenes in modal food systems at 40 C
and 100 C. J. Appl. Bacterial., 78, 593600.

2002 Edited by Taylor & Francis

24 Pelargonium reniforme and


Pelargonium sidoides: their botany,
chemistry and medicinal use
Herbert Kolodziej

INTRODUCTION

Traditionally, the plant kingdom has been recognised as an inestimably rich source of
potentially active metabolites not only as drugs, but also as unique leads that could serve
as a starting point for the synthesis of new chemical analogues. This is best documented
by the very great extent to which current medicines have their origins in plants. For
example, artemisinin, codeine, digoxin, morphine, quinine, and taxol represent plant
constituents of considerable therapeutic value, while salicin and khellin promoted the
development of non-steroidal antiinflammatory agents and that of the antiasthmatic
agent cromoglycinic acid, respectively. Thus, a successful modus operandi for finding
promising agents involves the exploration of plants of traditional medical systems.
Pelargonium species indigenous to areas of southern Africa are highly valued by
traditional healers and the native population for their curative properties. Among those
traditional herbal medicines is umckaloabo, which originates from Pelargonium sidoides
DC (De Candolle), and Pelargonium reniforme Curt (Curtis). Whereas Pelargonium species
are well known for the beauty of their flowers, representing very popular ornamental
plants in Europe, little is known of the medical practice with pelargoniums in folk
medicine in areas of southern Africa.
Our interest in umckaloabo is explained by the therapeutic use amongst the local
native population of southern Africa and its present utilisation in modern phytomedicine in Europe (Umckaloabo, ISO-Arzneimittel, Ettlingen, Germany). The hitherto
limited information on the chemical constituents of P. sidoides and P. reniforme and the
underlying biologically active principle(s) prompted a more detailed chemical and
pharmacological study on this plant medicine. This report represents a summary of the
latest botanical facets, structural studies and recent pharmacological investigations of
the titled Pelargonium species mainly carried out in our research group, and provides an
overview of the clinical studies on the herbal medicinal product Umckaloabo giving
credence to its efficacy and safety in the claimed clinical indications.
PELARGONIUM RENIFORME CURT.

Botany
Species of Pelargonium are all very similar and have been much confused in the past. For
example, the existence of gradual variation between P. reniforme and P. sidoides adds to

2002 Edited by Taylor & Francis

Pelargonium reniforme and Pelargonium sidoides

263

general problems of taxonomic classification, as reflected in the past by numerous


revisions in the framework of the Linneaen taxonomic system (van der Walt and
Vorster, 1988; Dreyer et al., 1992). In this context, a brief illustration of the taxonomic
variations of both Pelargonium species may be justified. Following the first description
of the Geraniaceae by Burmann (1738), LHeritier de Brutelle (1788) outlined a
number of genera including Pelargonium in his fundamental edition Geraniologia. At
the turn of the century, the botanical names Pelargonium reniforme Curt (Curtius, 1800)
and Geranium sidaefolium Thunb. (Thunberg, 1794), the latter being subsequently
changed into the present taxon Pelargonium sidoides DC. (De Candolle, 1824), have been
given to two newly discovered species. However, in his revision of the Geraniaceae,
Harvey and Sonder (1859) considered P. sidoides as a variety of P. reniforme and turned it
to P. reniforme Curt. var. sidaefolium. Adopting de Brutelles earlier taxonomic treatment
of Pelargonium, these authors divided the genus into 15 sections and placed the titled
Pelargonium species in section Cortusina. A sixteenth section was later recognised by
Dreyer et al. (1992). Treatment by Knuth (1912) of the Geraniaceae resulted in the
re-naming of P. reniforme var. sidaefolium at the species level to P. sidaefolium (Thunb.)
R. Knuth. Wettsteins revision to P. sidoides DC., rewards De Candolle as first author of
this species (Wettstein, 1935). Based on geographical, chemical, karyotypic, anatomical
and morphological criteria, Dreyer et al. (1992) replaced the Section Cortusina s. l. by
the Sections Cortusina (DC.) Harv. s. str., and Reniformia (Knuth) Dreyer, comb. nova. In
the most recent treatment of the species P. reniforme, Dreyer et al. (1995) reported on the
existence of the ssp. reniforme Curt., and ssp. velutinum (Eckl. and Zeyh.) Dreyer stat. nov.
et comb. nov. The present taxonomic classification of P. reniforme and P. sidoides with
reference to the essential textbook Strasburger Lehrbuch der Botanik (Sitte et al.,
1998) is shown in Table 24.1.
The pink-flowered P. reniforme (Figure 24.1) is an attractive erect shrublet of up to 1 m
in height, developing from a tuberous rootstock. The zygomorphous flower heads are
borne on tall slender stalks; each flower has five lanceolate petals, with two distinctive

Table 24.1 Taxonomic classification of P. reniforme and P. sidoides


Taxon

Taxonomic category

Kingdom
Subkingdom
Division
Subdivision
Class
Subclass
Superorder
Order
Family
Tribe
Genus
Section
Species
Subspecies

Euca
Cormophyta
Spermatophyta
Magnoliophytina
Rosopsida
Rosidae s. lat.
Rosanae
Geraniales
Geraniaceae
Geraniae
Pelargonium
Reniformia (Knuth) Dreyer, comb. nova
P. reniforme Curt.
P. reniforme ssp. reniforme Curt.

2002 Edited by Taylor & Francis

P. sidoides DC.
P. reniforme ssp. velutinum
(Eckl. and Zeyh.) Dreyer stat. nov. et
comb. nov.

264

Herbert Kolodziej

Reniform leaves (reniforme)

Flower head with distinctive stripes and dots

Morphology of Pelargonium reniforme ssp. reniforme

Figure 24.1 P. reniforme CURT. (See Colour plate 14)

stripes on the upper two petals. The reniform leaves with crenate or finely lobed margins are a characteristic feature of this species that is reflected in its botanical name
reniforme. Most leaves have a velvety texture and greyish-green colour due to the presence of matted hairs (van der Walt and Vorster, 1983, 1988). The triporate pollen is
ovoid and distinctly white, at least in terms of the ssp. reniforme; the non-availability of
ssp. velutinum material excluded a similar microscopic inspection of its pollen.
Noteworthy is that the two subspecies of P. reniforme not only differ morphologically,
but also in area of distribution (Dreyer et al., 1995). Pelargonium reniforme ssp. reniforme
is confined to the region at Port Elizabeth where it is fairly widespread at low altitudes.
All the material extending in the coastal districts further north and south and in inland
areas is represented by the ssp. velutinum (Figure 24.2). The only notably morphological
difference between the two subspecies lies in the shape and arrangement of leaves and
in the length of petioles; ssp. velutinum shows reniform to predominantly cordate leaves
and conspicuously longer petioles, reminiscent of those of P. sidoides (vide infra).
Chemical constituents
Although Pelargoniums have a long tradition, limited chemical sampling of members of this
genus produced mainly common organic acids, derivatives of cinnamic acid, flavonoids, and
phytosterols (Hegnauer, 1966, 1989). With the exception of the detection of the unique
alkaloids (epi)elaeocarpidin in hybrids (Lis-Balchin et al., 1996a,b), all recent papers deal
with these types of secondary products. Owing to the persistent interest in perfumery,
reflected by numerous papers on Geranium oil (P. graveolens, hybrids and other Pelargonium
species) (van der Walt and Vorster, 1981; Kaiser, 1984; van der Walt and Demarne, 1988;
Southwell and Stiff, 1995), essential oils (EOs) of distinct Pelargonium species have been the
subject of detailed studies (Demarne and van der Walt, 1990, 1992, 1993a; Demarne et al.,

2002 Edited by Taylor & Francis

Pelargonium reniforme and Pelargonium sidoides

Ora

SOUTH AFRICA

NORTHERN
PROVINCE

je

Pretoria

DURBAN

LESOTHO

Pletersburg

Mmabatho

Mpumalanga

Johanneshurg

ATLANTISCHER
OZEAN

265

MIDDELBURG

UMTATA

INDISCHER
OZEAN

NORTH WEST

GRAHAMSTOWN
KWA-ZULU
NATAL

Upington
Kimberley

CAPE TOWN

KNYSNA

EAST LONDON
PORT ELIZABETH

NORTHERN CAPE
Durban

Stellenbosch

WESTERN
CAPE

East London

Cape Town

P. reniforme ssp. reniforme


P. reniforme ssp. velutinum

Port Elizabeth

P. sidoides

P. reniforme
Geographical distribution of P. reniforme and P. sidoides

Figure 24.2 Geographical distribution of P. reniforme and P. sidoides ssp.

1993b). Reports on the metabolites of P. reniforme are hitherto limited and have revealed the
occurrence of coumarins, tannins, flavonoids, carbohydrates and hydroxycinnamic acids
(Wagner and Bladt, 1975). However, it should be stressed that chemical studies have not
been carried out on distinct plant extracts of either Pelargonium species. Current evidence
points also to erroneous identification of the plant material claimed to be P. reniforme in the
earlier investigation. For example, the coumarin pattern and here the striking presence of
7-hydroxy-5,6-dimethoxycoumarin (umckalin) (71), typical of P. sidoides, in the previous
paper on alleged P. reniforme conflicts with current information (vide infra). Independent
support for this conjecture is also provided by the geographical origin of the former plant
material, i.e. Grahamstown, an area where the ssp. velutinum commonly occurs. Thus, it
would be of great interest to extend our studies to this subspecies. With botanically defined
plant materials available through cultivation, studies on the individual patterns of
constituents of each Pelargonium species were permitted for the first time. It should be noted
that the plant material studied conformed with ssp. reniforme.

Root material
Structural examination of root metabolites of P. reniforme ssp. reniforme led to the
characterisation of a total of 19 various metabolites including five simple phenolic acids
(1, 2, 57), three hydroxycinnamic acid derivatives (8, 9, 12), six coumarins (2227),
four flavonoids (2831), and one phytosterol (63) (Table 24.2). The majority of these
metabolites has been encountered in relatively low yields. Noteworthy, however, is the
presence of gallic acid (1) and its methyl ester (2) in fairly high amounts.
Monomeric flavan-3-ols, which apparently represent the precursors of associated
condensed tannins (proanthocyanidins), were only detectable in traces. A substantial

2002 Edited by Taylor & Francis

Table 24.2 Constituents of P. reniforme ssp. reniforme


No.
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
44
45
46
47
48
49

Compound
Phenolic acids, Phenylpropanoids and Derivatives
Gallic acid
Gallic acid methyl ester
Gallic acid ethyl ester
Gallic acid butyl ester
p-Hydroxybenzoic acid
Protocatechuic acid
Vanillic acid
Caffeic acid
Ferulic acid
p-Coumaric acid
p-Coumaroyl-4-O--D-glucopyranoside
p-Coumaraldehyde
Shikimic acid 3-O-allate
Shikimic acid 3,5-di-O-gallate
p-Hydroxyphenylethanol
p- Hydroxyphenyl acetic acid
p-Hydroxybenzyl alcohol
Glycerol-1-gallate
Glucogallin
(,)-3,4-Di-O-galloylglucopyranoside
Salidroside-6-O-gallate
Coumarins
7-Hydroxy-6-methoxycoumarin (Scopoletin)
6,7,8-Trihydroxycoumarin
8-Hydroxy-6,7-dimethoxycoumarin (Fraxidin)
6-Hydroxy-5,7-dimethoxycoumarin (Fraxinol)
5,6-Dihydroxy-7-methoxycoumarin (Isofraxetin)
8-Hydroxy-5,6,7-trimethoxycoumarin
Flavonoids
Kaempferol 3-O--D-glucoside
Kaempferol 3-O--D-galactoside
Quercetin 3-O--D-glucoside
Myricetin 3-O--D-glucoside
Kaempferol 7-O--D-glucoside
Kaempferol 3-O--D-rutinoside
Quercetin 7-O--D-glucoside
Quercetin 3-O--D-rutinoside
Naringenin 7-O--D-glucoside
Dihydrokaempferol
Dihydroquercetin (Taxifolin)
Taxifolin 7-O--D-glucoside
Luteolin 7-O--D-glucoside
Vitexin
Vitexin 2-O-gallate
Orientin
Orientin 2-O-gallate
Isovitexin
Isovitexin 2-O-gallate
Isoorientin
Isoorientin 2-O-gallate
Hydrolysable Tannins
Brevifolin carboxyclic acid

2002 Edited by Taylor & Francis

Roots

Herb

Flowers



































































Pelargonium reniforme and Pelargonium sidoides

50
51
52
53
54
55
56
57
58
59












Phyllantusiin E
Phyllantusiin E O-methyl ester
Strictinin
Isostrictinin
Corilagin
Phyllantusiin C
Pelargoniin A
Pelargoniin B
Pelargoniin C
Pelargoniin D
Miscellaneous
()-cyclolariciresinol-2--D-glucoside
Stereoisomer of 60
4,6-dihydroxyacetophenone 2-O--D-glucoside
-sitosterol

60
61
62
63

267









proportion of the proanthocyanidins present in the roots is represented by oligomeric


and polymeric forms, with catechin and gallocatechin entities as dominating extender
units. A plausible interpretation is that precursors, when available at low concentration
in the presence of an excess of competitive nucleophiles are immediately and
quantitatively converted into high-molecular weight products. An illustrative general
structure of these complex molecules is presented as depicted in formula (69).
Other characteristic constituents of P. reniforme included a remarkable series of simple
coumarins as regards the high degree of aromatic functionalisation including hydroxyl
and methoxyl groups. Such oxygenation patterns are very rarely found in the plant kingPhenolic acids, Phenylpropanoids and Derivatives

COOR4

R3

R1
R2

(1) R1 = R2 = R3 = OH; R4 = H
(2) R1 = R2 = R3 = OH; R4 = CH3
(3) R1 = R2 = R3 = OH;R4 = C2H5
(4) R1 = R2 = R3 = OH; R4 = C4H9
(5) R1 = R3 = R4 = H; R2 = OH
(6) R1 = R4 = H; R2 = R3 = OH
(7) R1 = R4 = H; R2 = OH; R3=OCH3

COOR3
(8) R1 = OH; R2 = OH; R3 = H
(9) R1 = OH; R2 = OCH3; R3 = H
(10) R1 = OH; R2 = H; R3 = H
(11) R1 = glucosyl; R2 = R3 = H
R2
R1

CHO

CH2OH

COOH
CH2OH

COOH
(13) R1 = galloyl; R2 = H
(14) R1 = R2 = galloyl
R2O

OR1
HO
(15)

OH

OH
(12)

CH2OR4
HO

galloyl

HO (34)

R3O

O
OR1

R2O
OH

2002 Edited by Taylor & Francis

HO
(16)

HO
(17)

(19) R1 = galloyl; R2 = R3 = R4 = H
(20) R1 = R4 = H; R2 = R3 = galloyl
(21) R1 = (4-hydroxyphenyl)ethyl;
R2 = R3 = H; R4 = galloyl

268

Herbert Kolodziej
Coumarins
R4
8

R3

7
R2

(22) R1=R4=H; R2=OCH3; R3=OH


(23) R1=H; R2=R3=R4=OH
(24) R1=H; R2=R3=OCH3; R4=O
(25) R1=R3=OCH3; R2=OH; R4=H
(26) R1=R2=OH; R3=OCH3; R4=H
(27) R1=R2=R3=OCH3; R4=OH

R1

dom, but apparently typical for the genus Pelargonium. Apart from the widely distributed
di-substituted scopoletin (22), all the coumarins possess tri- and tetra-substituted
oxygenation patterns on the aromatic nucleus. Amongst these, 6,7,8-trihydroxycoumarin
(23) and 8-hydroxy-5,6,7-trimethoxycoumarin (27) represent novel metabolites of the
above class of secondary products.
Aerial parts
In contrast to the roots, the aerial parts of P. reniforme have not been the subject of
chemical studies, which may be attributed, at least in part, to less relevant therapeutic
uses. The results of our systematic examination of the metabolites present in the aerial
parts of P. reniforme are included in Table 24.2.
Hydroxylated benzoic and cinnamic acids, gallic acid derivatives, flavonoids and tannins
are the principal phenolic substances found in the aerial parts of P. reniforme. As regards
flavonoids, the parent methanol extract afforded a complex mixture of flavonols (3235),
flavanones (36), dihydroflavonols (3739) and flavones (4048) (Table 24.2). Noteworthy
is the presence of a series of CC linked -D-glucopyranosides (4148) based on the
flavones apigenin and luteolin. Although the C-6-glucopyranosylflavones, isovitexin (45)
and isoorientin (47), and their C-8 regiomers, vitexin (41) and orientin (43), exhibit a wide
taxonomic distribution (Jay, 1994), their occurrence in this natural source is of some
chemotaxonomic significance in that C-glycosyl-flavonoids are considered to be poorly
represented or generally lacking in the Geraniaceae (Jay, 1994; Hegnauer, 1989). These
metabolites are accompanied by a unique series of 2-galloyl analogues (42, 44, 46,
46), representing the first O-galloyl derivatives of C-glucosylflavones (Latt et al., 2002).
In addition to the aforementioned flavonoids, the ethyl acetate and n-butanol phases
of P. reniforme afforded a unique series of O-galloylated metabolites, including simple
galloyl esters (24), shikimic acid 3-(13) and 3,5-di-gallate (14), glycerol-1-gallate
(18), glucogallin (19), salidroside-6-gallate (21), and (,)-3,4-di-O-galloylglucopyranoside (20) (Table 24.2) (Latt and Kolodziej, 1999). The majority of the identified isolates represents new or rarely found secondary products. For example, the occurrence of
glycerol-1-gallate (18) has hitherto been demonstrated only in Mallotus japonicus
(Euphorbiaceae) (Saijo et al., 1990) and in a Rheum species (Polygonaceae) (Nonaka and
Nishioka, 1983), while that of (,)-3,4-di-O-galloylglucopyranoside (20) is confined
to Macaranga tamarius (Euphorbiaceae) (Lin et al., 1990) and that of salidroside-6-gallate (21) to Quercus phillyraeoides (Fagaceae) (Nonaka et al., 1989) and Q. stenophylla
(Nonaka et al., 1982). On the other hand, gallic acid butyl ester (4) represents a new
natural product. The remarkable broad range of O-galloylated compounds present in

2002 Edited by Taylor & Francis

Pelargonium reniforme and Pelargonium sidoides

269

Flavonoids
R1
OH
O

R4O

R2
OR3

OH

R1
OH
O

R3O

(28) R1 = R2 = R4 = H; R3 = glucosyl
(29) R1 = R2 = R4 = H; R3 = galactosyl
(30) R1 = OH; R2 = R4 = H; R3 =glucosyl
(31) R1 = R2 = OH; R3 = glucosyl; R4 = H
(32) R1 = R2 = R3 = H; R4=glucosyl
(33) R1 = R2 = R4 = H; R3 = rutinosyl
(34) R1 = OH; R2 = R3 = H; R4 = glucosyl
(35) R1 = OH; R2 = R4 = H; R3 = rutinosyl

(36) R1 = OH; R2 = H; R3 = glucosyl


(37) R1 = R3 = H; R2 = OH
(38) R1 = R2 =OH; R3 = H
(39) R1 = R2 = OH; R3 = glucosyl

R2
OH

R1
OH

R4
O

R3O
R2
OH

(40) R1 = OH; R2 = R4 = H; R3 = glucosyl


(41) R1 = R2 = R3=H; R4 = glucosyl
(42) R1 = R2 = R3 = H; R4 = (2-galloyl)glucosyl
(43) R1 = OH; R2 = R3 = H; R4 = glucosyl
(44) R1 = OH; R2 = R3 = H; R4 = (2-galloyl)glucosyl
(45) R1 = R3 = R4 = H; R2 = glucosyl
(46) R1 = R3 = R4 = H; R2 =(2-galloyl)glucosyl
(47) R1 = OH; R2 = glucosyl; R3 = R4 = H
(48) R1 = OH; R2 = (2-galloyl)glucosyl; R3 = R4 = H

P. renifome suggests galloylation of secondary products to be a putative chemotaxonomic


marker for the genus Pelargonium. Although this conjecture is supported by similar
observations made for the morphologically closely related species P. sidoides, further
studies are required to place this hypothesis beyond doubts.
A major group of the metabolic pool of the aerial parts of P. reniforme is represented by
a wealth of tannins. Here, polymeric proanthocyanidins are associated with ellagitannins,
which are conspicuously absent from the root material. Their occurrence explains the
traditional use of the aerial parts as wound healing agent, which may be attributed, at
least in part, to their astringent action. Ellagitannins, receiving currently increasing interest, display a remarkable array of biochemical and pharmacological actions, including
antiviral, antimicrobial and antitumoral properties (Okuda et al., 1995).
Identified members included strictinin (52) and isostrictinin (53), composed of a central glucose core, adopting the 4C1 conformation, a -linked galloyl
group at C-1 and a hexahydroydiphenoic (HHDP) moiety, formed by oxidative CC
coupling of two adjacent galloyl groups. In the case of strictinin (52) the HHDP
group bridges the 4,6-position, while isostrictinin (53) represents the isomeric
2,3-coupled analogue.
Noteworthy is the co-occurrence of a series of structural variants in P. reniforme,
similarly based on a 1-O-galloyl--D-glucopyranose precursor which itself adopts the

2002 Edited by Taylor & Francis

270

Herbert Kolodziej
Hydrolyzable tannins
HO

(50) R = H
(51) R = CH3

OH

HO

ROOC

HOOC

O
O
O

HO

(49)

HOH2C

OH
HO

OH

HO
O
C-C-H2

HO

O=C

HO

O-C
O HO

HO

OR
OH

OH
(52) R = galloyl

OR
O

O
C=O

HO

OH
HO HO OH

OH

(53) R = galloyl

less favourable 1C4 conformation. However, the galloyl ester groups at C-3 and C-6 are
ideally aligned in a axial position for the feasible coupling in this energetically
unfavourable chair conformation. These metabolites included corilagin (54) and a
series of corilagin-based ellagitannins such as the rarely found phyllantusiin C (55)
(Yoshida et al., 1992b; Liu et al., 1999; Amakura et al., 1999) and four structurally
related unique ellagitannins (5659), designated as pelargoniins A, B, C, and D (Latt
and Kolodziej, 2000). A remarkable common structural feature of these analogues is
the presence of an oxidized DHHDP entity, bridging the 2,3-position. From their
close structural relationship to geraniin, a biogenetic relationship may be postulated,
though geraniin itself appears to be conspicuously absent from members of the genus
Pelargonium.
Generally oxidative coupling of galloyl ester groups via the 4 C 1 form of the
glucopyranose precursor is much more widely encountered in plants than that via the
alternative 1C4 conformation (Haslam, 1998). According to present evidence plants
appear to specialise in just one of these two distinctive forms of oxidative metabolism
of the precursor (Haslam, 1988). This is the first example of the co-occurrence of
ellagitannins with 4C1 and 1C4 glucose cores demonstrated for plants belonging
to Geraniaceae. Up to now, only a few plants of the Euphorbiaceae (Saijo et al., 1989a,b),
Melastomataceae (Yoshida et al., 1992a) and Onagraceae (Haddock et al., 1982) have
been shown to contain both forms of metabolites.
Our detailed chemical study on P. reniforme has also led to the isolation of two
structurally closely related lignan glucosides (Table 24.2), the first members of this
group of secondary products to be reported for the Geraniaceae and characterised by
means of spectroscopic methods as ()-isolariciresinol-2--glucopyranoside (60) and
an isomer of undefined stereochemistry (61) due to limited sample quantity. To date, the
natural occurrence of ()-isolariciresinol-2--glucopyranoside (60) is hitherto limited
to Populus nigra (Thieme and Benecke, 1969) and Stemmadenia minima (Achenbach
et al., 1992). Noteworthy is also the detection of 4,6-dihydroxyacetophenone

2002 Edited by Taylor & Francis

Ellagitannins based on a C4-glucose precursor

HO C

H
(55) R1, R2 =

OH
HO

HO

HO HO

HO

OH

HO

OH

OH

HO C

(56) R1, R2 =

H
O

OH

H 2C

HO

O-Galloyl
O

OH

OH

R 1O

(57) R1, R2 =

R 2O

H
HOOC

(54) R1 = R2 = H
O
HO C
(58) R1, R2 =

OH

O
(59) R2 =

OH

OH
HO

HOOC
HO

OHC

OH

OH
O

Lignans
H3CO
HO

Acetophenone
H

CH3

OH
OGluc
H

Phytosterols

C O
OGluc

HO

H
H

OCH3
OH
(60)

2002 Edited by Taylor & Francis

RO
OH
(62)

(63) R = H
(76) R = glucosyl

272

Herbert Kolodziej

2-O- - D -glucopyranoside (62) in that acetophenones being reported to occur only in a


limited number of plant families (Singh et al., 1997).
Essential Oil
Many Pelargonium species have a characteristic scent, based on the content of EOs, which
provides for their utilisation in perfumery, cosmetic and food applications (Gildemeister
and Hoffmann, 1959). Also worthy of mention is the observation that a trichome
exudate, comprising a mixture of anacardic acids and tetrahydropyrans (Walters et al.,
1989 and 1990), is a potent chemical defence against small pest species, but also that
some Pelargonium species are effectively repellent to insects and, hence, are widely
employed in southern Africa by the native population in this respect. Although
Pelargonium EOs, sporadically incorrectly declared as Geranium oils, have a long tradition, detailed studies on the chemical composition of EO of distinct Pelargonium species
are rare (Demarne and van der Walt, 1990, 1992, 1993a; Demarne et al., 1993b).
The details of the composition of the volatile fraction of P. reniforme are presented
elsewhere (Kayser et al., 1998). Therefore, only a brief summary will be presented here
with an informative table of the chemical composition of the EOs of both Pelargonium
species in terms of chemical classes (Table 24.3). Hydrodistillation of dried aerial parts
produced a strongly aromatic-scented EO in 0.71 per cent yields related to the dry
weight. About 230 components were detected of which 81 were unambiguously identified, accounting for about 49 per cent of the total peak area. The majority of the
unknown compounds were represented by sesquiterpenes, as concluded from their mass
spectral data and their retention times. The leaf oil consists of a complex mixture of different substances, with sesquiterpenes (ca. 60 per cent, inclusive of the unknowns) as
the dominating components. Noteworthy is the relatively high level of sesquiterpene
hydrocarbons (19.4 per cent) including -muurolene, - and -selinene, cyclosativene
and calamene. The monoterpenes comprised 4.7 per cent of the EO, with oxygenated
components as the most abundant group (3.8 per cent).
Table 24.3 Composition of the essential oils of P. reniforme and P. sidoides
Class

Hydrocarbons/Oxyg. Terpenoids
Monoterpenes
Hydrocarbons
Alcohols
Aldehydes
Esters
Ketones
Oxides
Sesquiterpenes
Hydrocarbons
Oxyg.
Diterpenes
Phenylpropanoids
Fatty Acids

2002 Edited by Taylor & Francis

P. reniforme
Number of
components

(%)

4
 26
10
7

0.4
 4.7
0.9
2.5

7
2
 30
18
12
1

1.2
0.1
 36.9
19.4
17.5
0.5

4.5

P. sidoides
Number of
components

(%)

12
 41
11
18
1
4
6
1
 37
23
16
2
5
7

4.1
 16.3
0.9
8.4
0.2
3.0
3.7
0.1
 32.9
8.1
24.8
0.8
8.5
4.7

Pelargonium reniforme and Pelargonium sidoides

273

Detection of anacardic acids (Walters et al., 1990) via the characteristic salicylic
fragment m/z 138 and the presence of constituents with reputed repellent properties such
as -pinene, limonene, carvone and -myrcene in the EO provide for a rational explanation for reported insect deterrency by Pelargonium species (Thorsell et al., 1998). Also, the
furan-type constituents identified (2-pentylfuran, perillene) and naphthalene derivatives
(naphthalene, 1,2-dihydro-1,1,6-trimethylnaphthalene) are suggested to contribute significantly to plant protection against insects (Rodriguez-Saona et al., 1999).
PELARGONIUM SIDOIDES DC

Botany
As the following botanical description may lead to the impression of a clear distinction between P. reniforme and P. sidoides, it is appropriate to recall the existence
of gradual variations (vide supra). In its unadulterated form, this species (Figure 24.3)
can be distinguished by the shape of the leaves and the colour of the flowers (van der
Walt and Vorster, 1988). Dark red, but commonly almost black flowers are borne on
long, slender stalks, spreading outwards from a woody base. The rosette-like plant
has crowded, velvety, cordate, long-stalked leaves with short glandular trichomes
sparsely interspersed. The triporate pollen is globose in shape and yellowish,
but apparently not orange as indicated by van der Walt and Vorster (1988);
accordingly, the various pollen characters do represent a diagnostic feature for the
discrimination of the two Pelargonium species (vide supra). This species is predominantly found over large parts of the interior of southern Africa, but also occurs
in coastal mountain ranges up to 2300 m (van der Walt and Vorster, 1983 and
1988) (Refer also to Figure 24.2).

Cordate leaves
Morphology of Pelargonium sidoides

Figure 24.3 P. sidoides DC. (See Colour plate 15)

2002 Edited by Taylor & Francis

Flower head

274

Herbert Kolodziej

Table 24.4 Constituents of P. sidoides


No.
1
2
13
19
49
54
47
64
65
66
67
68
22
23
70
71
72
73
74
75
76

Compound
Phenols
Gallic acid
Gallic acid methyl ester
Shikimic acid 3-O-gallate
Glucogallin
Hydrolysable Tannins
Brevifolin carboxyclic acid
Corilagin
Flavonoids
Isoorientin
Quercetin
Taxifolin 3-O--glucoside
Flavan-3-ols
()-Afzelechin
()-Catechin
()-Gallocatechin
Coumarins
7-Hydroxy-6-methoxycoumarin (Scopoletin)
6,7,8-Trihydroxycoumarin
6,8-Dihydroxy-7-methoxycoumarin
7-Hydroxy-5,6-dimethoxycoumarin (Umckalin)
7-Acetoxy-5,6-dimethoxycoumarin
5,6,7-Trimethoxycoumarin
6,8-Dihydroxy-5,7-dimethoxycoumarin
5,6,7,8-Tetramethoxycoumarin (Artelin)
Phytosterols
Sitosterol-3-O--D-glucoside

Roots

Herb































Chemical constituents
A similar picture of a broad metabolic profile is also visible for P. sidoides based on our
current data, though this study is not completed yet. Here, only the characteristic constituents of the roots and the aerial parts are briefly dealt with. Additional compounds
unambiguously characterised are included in Table 24.4.
Root material
Compositional studies provided similar proof of the occurrence of oligomeric and polymeric flavan-3-ols in significant amounts. Here, the putative precursors ()-afzelechin
(66), ()-catechin (67) and ()-gallocatechin (68) could be successfully isolated from
this source. One can conclude that the high-molecular weight tannins produced by
P. sidoides, but also other Pelargonium species in its root tissues ultimately provide a
significant barrier to invading microorganisms and other pests.
In addition to the high content of proanthocyanidins with their presumed ecological
function, the root extract of P. sidoides also contained a wealth of highly oxygenated
simple coumarins, unique in its composition (Table 24.4). For example, 6,8-dihydroxy5,7-dimethoxycoumarin (74), 5,6,7-trimethoxycoumarin (73), 6,8-dihydroxy-7-

2002 Edited by Taylor & Francis

Pelargonium reniforme and Pelargonium sidoides

275

OH
OH
HO

Flavan-3-ols

R1

OH
OH

HO

R2

OH

HO

OH
OH

(66) R1 = H; R2 = H
(67) R1 = OH; R2 = H
(68) R1 = OH; R2 = OH

OH

OH

R
OH

OH

OH

OH

HO

R
OH

OH
(69) R = H or OH

methoxy-coumarin (70), and 7-acetoxy-5,6-dimethoxy-coumarin (72) represent new


natural products; the latter being the first natural compound known hitherto within
this group possessing an acetoxy function. Comparison of the coumarin patterns in the
roots of P. sidoides and P. reniforme clearly showed that they express conspicuously distinct variations (Table 24.1 and 24.2). Of the twelve identified coumarins, the two
species share the ubiquitous scopoletin (22) and the unique 6,7,8-trihydroxycoumarin
(23) only, the latter may therefore serve as useful chemotaxonomic marker. Also, discrimination between P. sidoides and P. reniforme may readily be verified by characteristic
fingerprint chromatograms. It should also be noted that there is much divergence in
concentrations, with significantly higher yields of coumarins in P. sidoides. With the
exception of the characteristic 6,7,8-trihydroxy-coumarin (23), the remaining
coumarins are present only in small amounts in P. reniforme.
Aerial parts
Again, polymeric proanthocyanidins were associated with members of hydrolysable
tannins, as evidenced by the identification of brevifolin carboxyclic acid (49) and corilagin (54). Owing to difficulties regarding the characterisation of the exact molecular
structure of extended flavan-3-ol entities, emphasis is currently given to the structural
assessment of additional ellagitannins that have been detected in the herbal parts.
Additional notes concern the very limited occurrence of coumarins, in contrast to the
abundance in the roots, and the presence of flavonoids, gallic acid derivatives and related
phenolic compounds in the aerial parts. Here, the concurrent demonstration of the presence of isoorientin (47), when taken in conjunction with unpublished results, should be
indicative not only of the existence of additional C-linked glycosylflavones in this plant
source, but also of a much wider distribution of this class of secondary products in the
genus Pelargonium than hitherto anticipated. Based on similar sampling evidence, it is
ventured to say that there is a close similarity in the phenolic and flavonoid profile
between the two species, already discernible from the present data in Tables 24.1 and 24.2.

2002 Edited by Taylor & Francis

276

Herbert Kolodziej
OH
Flavonoids

OH
OH

HO

OH
O

HO
OH

OH

(64)

OGluc
OH

(65)

Coumarins
R4
R3

R2
R1

(70) R1 = H; R2 = R4 = OH; R3 = OCH3


(71) R1 = R2 = OCH3; R3 = OH; R4 = H
(72) R1 = R2 = OCH3; R3 = OAc; R4 = H
(73) R1 = R2 = R3 = OCH3; R4 = H
(74) R1 = R3 = OCH3; R2 = R4 = OH;
(75) R1 = R2 = R3 = R4 = OCH3

Essential Oil
The EO, obtained in 0.52 per cent on a dry-weight basis, was similarly analysed by
gas chromatographymass spectrophotomety (GCMS), leading to the unambiguous
identification of 102 components (Kayser et al., 1998). Again, sesquiterpenes proved
to be the dominating constituents (61 per cent, inclusive of the unknowns), with
caryophyllene (2.3 per cent) and caryophyllene epoxide (13 per cent) as the most
abundant compounds. In the monoterpene fraction, oxygenated members constitute
the most abundant group. As can be seen in Table 24.3, the composition of the EO
of P. sidoides differed significantly from that of P. reniforme by the presence of
considerable amounts of phenylpropanoids (8.5 per cent), which were apparently
absent or only present as trace components in the latter. Methyleugenol (4.3 per cent)
and elemicin (3.6 per cent) were the most abundant phenylpropanoids, accounting for
almost 94 per cent of this fraction. This divergence in the EO profiles should be of
relevance for a clear differentiation of the morphologically closely related Pelargonium
species. This finding could also be of significance for other Pelargonium species, but
requires further studies.
It is also worth noting here that the likewise detection of, e.g. anacardic acids,
furfural, geranyl acetate, linalyl acetate and phenylpropanoids, reputed for their insect
deterrent potential, in the EO of P. sidoides provides additional evidence that
Pelargonium species are effectively repellent to insects. For this purpose, Pelargonium oils
are widely employed in southern Africa by the native population.
TRADITIONAL USE

The traditional drug umckaloabo originates from the root material of P. sidoides and
P. reniforme. Etymologically, the name umckaloabo comes from the Zulu words
umKhulkane for complaints associated with lung disorders and uHlabo which means
chest pain (Bladt, 1974), reflecting a major traditional indication. Initially, only the

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277

latter species has been suggested to form the plant source of this traditional herbal
medicine (Bladt, 1974), but, according to present evidence, the origin of umckaloabo
is strongly associated with the morphologically closely related species P. sidoides (vide
supra) (Kolodziej and Kayser, 1998). Therefore, it is most likely that some medicinal
records apply to mixtures prepared from both species. In our hands, the root material
of both species comprised of pieces differing in thickness but apparently devoid of
conspicuously morphological features. Noteworthy, however, are pieces with tuberous
segments that are apparently characteristic of roots of P. sidoides, but this morphological
feature has only been found for older materials (Kolodziej et al., 1995b).
Umckaloabo enjoys a wide reputation by traditional healers and is highly valued by
the southern African native population for its curative and palliative effects in the
treatment of gastrointestinal disorders, hepatic disorders, wounds and respiratory tract
disorders (Watt and Breyer-Brandwyk, 1962; Hutchings, 1996). For example,
decoctions are used for the treatment of cough and chest pain including tuberculosis.
Infusions of the roots of P. sidoides and P. reniforme are applied to treat gastrointestinal
disorders such as diarrhoea. In addition, umckaloabo is claimed to cure hepatic
disorders and menstrual complaints such as dysmenorrhea. The aerial parts of these
Pelargonium species are employed in wound healing.
The therapeutic use of umckaloabo in traditional medicine has been noticed by
European settlers in the eighteenth century. At the turn of the century Major Stevens
introduced a secret medicine, Stevens Consumption Cure, in England for the treatment
of tuberculosis (Helmstdter, 1996). Stevens believed that he recovered from
tuberculosis by the administration of a decoction of umckaloabo prepared by a traditional healer. In 1920, the Swiss physician Sechehaye heard of Stevens cure, treated 800
patients in the following 9 years and reported successful cases to the Medical Society of
Geneva, though in most cases tuberculosis had not been definitely proven. Following
the well documented therapeutic use since then in the treatment of lung
disorders, umckaloabo has survived and found its place in modern phytomedicine.
Nowadays, ethanolic preparations using the Pelargonium species medicinally
(Umckaloabo, ISO-Arzneimittel, Ettlingen, Germany) are successfully employed to
treat ENT and respiratory tract infections.
Regarding the treatment of gastrointestinal disorders such as diarrhoea in folk medicine, the fairly high concentrations of proanthocyanidins (ca. 9 per cent) occurring in
this indigenous medicine may explain the traditional use. Owing to the high degree of
polymerisation, absorption of these tannins from the digestive tract with an intact
mucosa is highly unlikely, thereby acting as an effective astringent useful in these conditions. For example, the hitherto assumed precipitation of proteins in the epithelial
surface of the gut should form a protective layer along the intestinal lumen. Also, some
of the beneficial antisecretory effects which tannins exert in these conditions may well
follow from their interaction with toxins produced by pathogenic bacteria in the intestine (Hnsel, 1991; Hr et al., 1995).
A similar rationale explanation based on the presence of tannins may be provided for
the application of the aerial parts as wound healing agent, while curative effects, if any,
related to hepatic disorders may tentatively be explicable on the basis of the radical
scavenging activities of the broad range of phenolic compounds. In the following
sections, the therapeutic claims of umckaloabo (P. reniforme/P. sidoides) in traditional
medicine and in modern phytomedicine in Europe are evaluated and discussed in
greater detail.

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PHARMACOLOGY

Following the therapeutic use of umckaloabo (P. reniforme/P. sidoides) in traditional


medicine for the treatment of respiratory tract infections and its present utilisation in
modern phytomedicine in Europe, this herbal medicine is still the subject of considerable
research aimed at establishing the chemical and pharmacological basis of the activity
which has been clearly shown in a number of clinical studies (vide infra). In principle, the
claimed clinical efficacy in ENT and respiratory tract infections could be explained by
antibacterial activities and/or stimulation of the non-specific immune system.
To obtain clues as to whether these botanically defined Pelargonium species have antimycobacterial potencies as claimed in earlier records, extracts and some typical phenol
and coumarin isolates were tested for this particular biological activity in collaboration
with the Tuberculosis Antimicrobial Acquisition and Coordinating Facility, Alabama,
USA. At 12.5 g/ml, the crude extract of P. reniforme showed some interesting inhibitory
activity (96 per cent) against Mycobacterium tuberculosis in a primary screen, while
that of P. sidoides was inactive. This finding does not necessarily imply lack of
antimycobacterial properties of the latter species, possibly detectable at higher sample
concentrations, but clearly indicates the need for establishing with certainty the precise
botanical species traditionally used. Such a criterion is, among others, liable to lead to
inconsistencies in reported bioactivity and clinical efficacy. For example, confusions
regarding the origin of umckaloabo have led to lack of credibility in therapy
(Helmstdter, 1996). With the minimum inhibitory concentration (MIC) of 100 g/mL,
determined in a broth microdilution Alamar Blue assay, the extract of P. reniforme
was only moderately active against M. tuberculosis, when compared with the MIC
of 0.06 g/mL of the clinically used drug, rifampicin, as a reference compound.
Also, none of the isolated constituents exhibited antimycobacterial activities under the
experimental conditions.
Antibacterial activity
Due to ambiguities regarding the botanical identity of the previously studied species (vide
supra), the reported biological activities are limited to our own studies. The qualitative
evaluation of the antibacterial activity of extracts and isolated constituents was accomplished using the agar dilution method. Samples were tested for in vitro activity against
a panel of microorganisms (Kayser and Kolodziej, 1997) including three Gram-positive
(Staphylococcus aureus, Steptococcus pneumoniae, and beta-hemolytic Streptococcus 1451) and five
Gram-negative bacteria (Escherichia coli, Klebsiella pneumoniae, Proteus mirabilis, Pseudomona
aeruginosa and Haemophilus influenzae), pathogens that are primarily responsible for numerous respiratory tract infections. Whereas the crude Pelargonium root extracts were found
to be moderately active against the tested bacteria with MICs of 57.5 mg/ml, the ethyl
acetate, n-butanol and water phases exhibited fairly high antibacterial effects as evident
from MICs of 0.61.2 g/ml (Table 24.5). No significant differences were found between
P. sidoides and P. reniforme extracts regarding this particular biological activity.
Regarding the antibacterial potential of isolates, the highly oxygenated coumarins,
7-hydroxy-5,6-di-methoxycoumarin (71) and 6,8-dihydroxy-5,7-di-methoxycoumarin
(74) represented the most potent candidates with MICs of 200500 g/ml (Table
24.5). Another major contributing factor towards antibacterial activity of umckaloabo
extracts proved to be gallic acid methyl ester (2) with MICs of 250500 g/ml against

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279

Table 24.5 Antibacterial activity of P. sidoides and P. reniforme (MIC values in g/ml)
Extract
Crude extracts
P. sidoides
P. reniforme
Fractions
P. sidoides
H2O
EtOAc
n-BuOH
P. reniforme
H2O
EtOAc
n-BuOH
Compounds
Simple Phenols
(1)
(2)
(67)
Coumarins
(22)
(71)
(73)
(74)
Penicillin G

E. coli

Klebs.
pneum.

Staph.
aureus

Pseud.
aerug.

Prot.
mirab.

-hem.
Strept.

Strep.
pneum.

Haem.
influen.

5000
7500

7500
5000

7500
2500

5000
5000

5000
5000

7500
7500

7500
7500

5000
5000

600
1200
1200

600
1200
1200

600
2500
1200

600
2500
1200

1200
2500
1200

600
1200
1200

600
2500
2500

1200
2500
2500

600
1200
1200

600
2500
1200

1200
2500
1200

1200
2500
2500

1200
2500
2500

600
2500
2500

1200
1200
2500

1200
2500
2500

2000
500
8000

1000
250
8000

500
250
8000

500
250
8000

500
250
8000

2000
500
8000

2000
1000
8000

2000
500
8000

500
200
1000
220
25

500
200
1000
250
5

500
200
1000
220
5

400
200
1000
220
5

400
200
1000
220
6

1000
500
1000
500
166

1000
500
500
500
16

1000
500
500
500
16

all of the tested bacteria but S. pneumoniae (1000 g/ml). The demonstrated antibacterial activity of umckaloabo may explain, at least in part, the documented clinical
efficacy of Pelargonium-containing herbal medicines.
Immunmodulatory properties
Clearly, the antibacterial activity of umckaloabo extracts and their constituents is considerably inferior to commercial antibiotics like penicillin G (MICs of 525 g/ml),
and, hence, these results cannot satisfactorily explain the documented clinical efficacy
in the claimed conditions. Respiratory tract infections are frequently primarily due to
viruses including coxsackie-, parainfluenza-, influenza-, echo-, adeno- and rhino-viruses,
thus leading to the assumption of an immunomodulatory activity associated with
Pelargonium-containing herbal medicines.
To assess the immunostimulating potential of this traditional medicine, functional
bioassays including an in vitro model for intracellular infection with Leishmania parasites (Kiderlen and Kaye, 1990), an extracellular Leishmania growth assay (Kayser et al.,
1997), a fibroblast-antivirus protection assay (IFN activity) (Marcucci et al., 1992), and
a fibroblast-lysis assay (TNF) (Wagner and Jurcic, 1991), as well as a biochemical assay
for nitric oxides (iNO) were employed (Ding et al., 1988). These test models serve as
a useful tool for the evaluation of activation of host defense mechanisms against intracellular microorganisms and viral infections associated with the traditional use and
present therapeutic use of umckaloabo.

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Leishmanicidal activity
In view of the use and known therapeutic effects of Pelargonium-containing herbal medicines, an in vitro model for visceral leishmaniasis was selected in which murine
macrophages are infected with the obligate intracellular protozon Leishmania donovani.
Pronounced leishmanicidal effects against intracellular amastigote forms of L. donovani
were observed for the parent methanol extracts, but also for the petrol ether, ethyl
acetate and n-butanol phases obtained thereof, as reflected by EC50 values ranging from
0.1 to 3.3 g/ml. The EC50 value of Pentostam as a reference agent was 7.9 g/ml
under the same conditions. Subsequent bioassay-guided fractionation of the active fractions led to the characterisation of gallic acid (EC50 4.4 g/ml) and its methyl ester
(EC50 12.5 g/ml) as potentially leishmanicidal active constituents, both being present
in significant amounts in umckaloabo. In contrast, coumarins isolated from the same
plant source proved to be inactive in concentrations up to 25 g/ml in this in vitro
infection model. On the other hand, neither extracts nor characteristic compounds of
umckaloabo proved to be directly toxic to extracellular, promastigote forms of L. donovani
(EC50 25 g/ml). Similarly, sample toxicity for non-parasitised macrophages were
significantly less prominent in this concentration range.
These findings suggest that the observed activity against intracellular L. donovani
might well be due to activation of sample-treated macrophages for enhanced Leishmania
kill, though stage-specific sensitivity of Leishmania amastigotes for these products can
not completely be excluded.

Release of nitric oxide


Reactive nitrogen intermediates such as nitric oxide (NO) play a firmly established role
as antimicrobial effector molecules produced by activated macrophages (Nathan and
Hibbs, 1991; Nussler and Biliar, 1993). Using the Griess assay, all samples were able
to induce NO production, but in a different amount (Figure 24.4). Compared to the

6,8-Dihydroxy-5,7dimethoxycoumarin

NO(%) 100
90

Umckalin

80

5,6,7-Trimethoxycoumarin

70
60

Scopoletin

50
40

Gallic acid

30

(+)-Catechin

20

Umckaloabo

10

rIFN

0
50 g/ml

Figure 24.4 Release of nitric oxide (NO) in macrophages infected with Leishmania donovani as compared to the stimulus interferon (rIFN).

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281

stimulus LPS, the NO-inducing effect of the samples accounted only for 1045
per cent. The most potent NO-inducers of the series of samples tested were gallic acid
(1) and the highly oxygenated coumarins 7-hydroxy-5,6-di-methoxycoumarin (71) and
6,8-dihydroxy-5,7-dimethoxy-coumarin (74). NO production increased in a dosedependent manner and reached a plateau in the range of 12.5 up to 50 g/ml. Higher
concentrations had an opposite effect by slightly decreasing the intracellular NO
release.
However, intracellular Leishmania toxicity did not correlate with NO-release. In
order to further assess the role of induced NO as a cytotoxic mechanism involved in
sample-induced intracellular destruction of Leishmania, the activity of the NO-synthase
was blocked by addition of the well-known inhibitor L-NMMA to parallel incubations.
Interestingly, the leishmanicidal effects of samples in experiments with and without
inhibitor were found to be very similar, possibly indicating the involvement of
additional leishmanicidal mechanisms in macrophages activated by umckaloabo
constituents.
Induction of the release of tumour necrosis factor
Besides oxygen-dependent cytotoxic defence mechanisms (Nathan and Hibbs, 1991;
Nussler and Biliar, 1993), induction of cytokines such as tumour necrosis factor (TNF)
represents a further parameter of macrophage activation. Beyond its role as proinflammatory cytokine, TNF plays an important regulatory role in the cytokine network
including the activation of immune cells and is required for host defence against certain
pathogens.
This factor was assayed by a protocol of determining spectrophotometrically the lysis
of actinomycin D pretreated TNF-sensitive L 929 fibroblasts in a classic cytotoxic TNF
assay (Wagner and Jurcic, 1991). At the subtoxic concentration of 25 g/ml, the ethyl
acetate (20.2 U/ml) and n-butanol phase (18.9 U/ml) were found to possess a moderate
TNF-inducing potential. Both phases contained significant amounts of gallic acid (1)
and its methyl ester (2), which proved to exhibit the strongest TNF-inducing potential
among the isolated Pelargonium constituents tested. Compared to the LPS stimulus, the
inducing potential of gallic acid and its methyl ester accounted for 24 and 19 per cent,
respectively. All coumarins exhibited only negligible effects in the concentration range
up to 50 g/ml. The considerable amounts of the simple phenols (1) and (2) in both
Pelargonium species, but also the occurrence of coumarins, albeit very weak TNF-inducers,
thus play a beneficial immune modulatory role of the underlying active principle of
umckaloabo.
Interferon-like activities
In the light of the proven clinical efficacy of Pelargonium-containing herbal medicines
in respiratory tract infections, it is noteworthy that umckaloabo extracts revealed
significant interferon (IFN)-like activities in a virus protection assay (Figure 24.5).
For this, sample-treated murine encephalo-myocarditis virus (EMCV)-sensitive L929
fibroblasts were incubated with EMCV suspensions. Inhibition of the cytopathic effect
(CPE) was determined spectrophotometrically using crystal violet as staining reagent
for protected cells and an IFN standard (100 U/ml) as positive control. Prominent

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Herbert Kolodziej
Viability (% of control)
100
Umckaloabo
80
Gallussure
60
Umckalin
40
(+)-Catechin
20
Scopoletin
0
0.8

1.6

3.12

6.25

12.5

25

50

100

g/ml

Figure 24.5 Cytoprotective effect (% of control) by Umckaloabo and its representative


constituents as assessed in the fibroblast/EMCV protection assay.

cytoprotective effects were observed for umckaloabo, as evidenced not only by complete
inhibition of CPE, but also significant proliferation of fibroblasts. In a modified experimental design which permitted differentiation between direct and indirect cytoprotective
effects, the strong CPE-inhibitory potential of sample-treated cells was clearly located
in supernatants, giving credence to IFN-like activities. Subsequent bioassay-guided
fractionation led to the detection of gallic acid (1) as potentially active constituent that
significantly reduced indirectly the cytopathic effect of EMCV on L929 cells in a
dose-dependent manner. At 100 g/ml, not only complete inhibition of cytopathic
effects, but also proliferation of fibroblasts was noticed. In contrast, ()-catechin (67) did
not show any significant IFN-like activities. Of the coumarins, umckalin (71) and 5,6,7trimethoxycoumarin (73) showed the relatively strongest inhibitory effects in the range
of 25 up to 100 g/ml with 12 and 30 per cent respectively, while the remaining compounds of this group of metabolites exhibited only negligible effects at all concentrations.
From these findings, it can be concluded that the phenolic constituents, gallic acid (1) and
its methyl ester (2), enhanced non-specific immune response in terms of macrophage
activation for intracellular parasite kill and release of NO and TNF. The results also
provide strong evidence for IFN-like activities of umckaloabo, but here it is reasoned that
co-substances synergistically contribute to its powerful overall action. Clearly, further
relevant experiments are needed to elucidate the mode of action of these phenols.
CLINICAL STUDIES

To obtain information about the efficacy and safety of the phytomedicine Umckaloabo,
elaborated from the traditional herbal medicine, a series of clinical studies were performed
(Heil and Reitermann, 1994; Dome and Schuster, 1996; Haidvogl et al., 1996). First, a
multi-centre postmarketing surveillance study was carried out in 1991/92 in 641 patients
with ENT and respiratory tract infections, e.g. tonsillitis, rhinopharyngitis, sinusitis, and
bronchitis. Outcome criteria were the change in the subjective and objective symptoms
during treatment and an assessment of treatment outcome by both physicians and patients

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Pelargonium reniforme and Pelargonium sidoides


% Patients

complete recovery

improvement

sputum
(n = 565)

wheezing chest pain


(n = 857)
(n = 278)

283

100
80
60
40
20
0
cough
(n = 1032)

shortness
of breath
(n = 263)

Figure 24.6 Umckaloabo multi-centre study in bronchitis: Bronchitis-specific symptoms.

on a 4-point rating scale. After 14 days of treatment, a total of 85 per cent of the patients
were back to normal or showed a major improvement. No adverse drug reactions were
observed.
Umckaloabo also represents a valuable therapeutic alternative in childhood infections,
particularly respiratory tract infections. Its efficacy and safety were investigated in a
prospective, open multi-centre study in 1042 children up to 12 years old suffering from
acute bronchitis. For all individual symptoms such as cough, expectoration, difficulty in
breathing, wheezing, and chest pain, the response rate (remission/improvement) was
over 80 per cent (Figure 24.6). In a prospective, randomised controlled trial, the efficacy and safety of Umckaloabo was compared with Acetylcysteine in 60 children
with acute bronchitis. The primary outcome criterion was the change in the total score
of bronchitis-specific symptoms at day 7. After 7 days of treatment, the total score
decreased similarly in both groups. The number of patients with complete recovery was
76.7 per cent in the group treated with Umckaloabo compared to 56.8 per cent in the
group treated with Acetylcysteine ( p 0.170; Fishers exact test, two-sided). Patients
treated with Umckaloabo reported to improve faster and be more satisfied with their
treatment ( p 0.006; Fishers exact test, two-sided). The results suggest that
Umckaloabo is at least as effective as Acetylcystein in the treatment of acute bronchitis.
This modern herbal medicine has also been found to be extremely effective for the
treatment of acute tonsillitis, one of the most common conditions of children and young
adults. In a prospective, randomised controlled trial involving 60 children aged between
6 and 10 years with acute tonsillitis (angina catarrhalis), the response rate after 4 days of
treatment with Umckaloabo was 76 per cent compared to that of 30 per cent with symptomatic treatment ( p 0.001, Fishers exact test, two-sided) (Figure 24.7). In another
randomised, double-bind, placebo-controlled trial, 78 children with acute tonsillitis
were treated with Umckaloabo or placebo for 6 days. The primary outcome criterion was
the response rate defined as total score of the angina-specific symptoms  4 points at

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Herbert Kolodziej

Umckaloabo (n = 30)

% Patients

Symptomatic Treatment (n = 30)

100
80
60
40
20
0
Physician assessment

Patient assessment

Figure 24.7 Assessment of efficacy in Angina catarrhalis (day 4; intention to treat-analysis;


response rate).

day 4. After four days of treatment, the response rates were 90.0 per cent in the
Umckaloabo group and 44.7 per cent in the placebo group ( p  0.0001; Fishers exact
test, two-sided). The higher response rates in the Umckaloabo group corresponded to a
more pronounced decrease of the total score of angina-specific symptoms from 8.7 1.5
points at admission to 2.0 2.3 points after 4 days (last observation carried forward) and
to 1.4 2.6 points at the final assessment as compared to a decrease from 8.8 1.6
points to 5.2 3.1 points and to 4.9 3.3 points in the placebo group. Based on the comparison of the individual last observation under treatment within the first 4 days with
the baseline value, the mean decrease of the total score was 6.8 2.8 points in the
Umckaloabo group and 3.7 3.3 points in the placebo group ( p  0.0001; Wilcoxon
rank-sum test, two-sided). No assessment was available for one patient in the
Umckaloabo group who terminated the study prior to the first control visit. The mean
total scores during the course of treatment are depicted in Figure 24.8. Tolerability was
rated as good or very good by patients and investigators in 97.5 per cent of patients
treated with Umckaloabo. Treatment of acute tonsillitis with Umckaloabo is well tolerated and demonstrated to be significantly superior compared with placebo.
A viral infection spread by droplets is often present initially. The complication most
feared is a bacterial superinfection by -hemolytic streptococci. Although viral
pathogens are not susceptible to antibiotics and are best treated symptomatically, in
practice antibiotics are often employed as prophylactic treatment. The benefits of
prophylactic antibiotic treatment is therefore questionable, but the risk of such treatment lies in the possibility of allergies to penicillin. The incidence of severe events (anaphylactic shock, localised allergic symptoms) is estimated as 25 per 100,000
administrations. Intolerance reactions caused by penicillin, e.g. disturbances of the
physiological intestinal flora and similar less serious side effects, are much more
common. Repeated administration of antibiotics also changes the flora in the
nasopharyngeal cavity in favour of pathogenic organisms. It must, therefore, be
assumed that the incidence with which tonsillitis recurs would be increased by antibiotic treatment. In view of the incidence of intolerance reactions, and of the danger of
resistance development, uncritical use of antibiotics, e.g. prophylactic treatment
against bacterial superinfection, is certainly questionable, particularly if one remembers

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285

Total score of angina-specific symptoms

12
Umckaloabo-group

10

Placebo-group
8

0
Enrollment
40/38 patients

Day 2
39/38 patients

Day 4
36/27 patients

Day 6
32/9 patients

Figure 24.8 Total score of angina-specific symptoms during treatment with Umckaloabo
compared to Placebo (arithmetic mean standard deviation).

that viral infections are not susceptible to causal treatment. Prescription of antibiotics
should be weighed up very carefully, particularly in children, in whom immunological
confrontation with the microbial environment is still going at full pace. It is
particularly at this stage that Umckaloabo offers a valuable alternative: it strengthens
the non-specific immunological response and, ideally, has bacteriostatic properties. The
antibacterial effect of Pelargonium extracts is distinctly weaker than that of antibiotics,
which is not itself surprising, but which does emphasise the therapeutic value of
antibiotics in proven bacterial infections. Further positive factors in favour
of Umckaloabo are the lack of toxicity and the low incidence of side effects indicating
a positive risk-benefit-ratio, particularly in the treatment of childrens disorders.
TOXICITY

From the long therapeutic use of umckaloabo in folk medicine and the lack of
respective reports, absence of any fatal toxic effects may be anticipated. Taken into
account clinical studies demonstrating just incidences of mild to moderate side effects
in patients treated with Umckaloabo, an extract of the titled Pelargonium species may
well represent a safe herbal medicinal product.
In a more direct approach to place non-toxicity beyond doubt, first evidences followed
from studies on the toxicity of umckaloabo constituents in some preliminary tests. For
example, this type of simple coumarins showed some antimutagenic activity against
IQ-induced mutagenesis in Salmonella typhimurium (Edenharder et al., 1995), while

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Herbert Kolodziej

distinct coumarins were found to be potent inhibitors of tumorigenesis (Nair et al.,


1991; Noguchi et al., 1993). Also, catechin and proanthocyanidins are reported to have
some antimutagenic potentials (Dauer et al., 1998). Using a human small cell lung
carcinoma (GLC4) and a colorectal cancer cell line (COLO 320) for evaluating the cytotoxicity, most coumarins exhibited only low cytotoxicity with IC50 values 100 M
(Kolodziej et al., 1997). The most potent cytotoxic coumarin, 6,8-dihydroxy-5,7dimethoxycoumarin (74) with an IC50 of 22 M (GLC4) and 9.5 M (COLO 320)
respectively, was only moderately cytotoxic, when compared with the respective IC50
values (1 and 2.7 M, respectively) of the reference compound cisplatin. In a similar
study, proanthocyanidins were also found to possess only low cytotoxicity. (Kolodziej
et al., 1995a). Finally, the brine shrimp lethality bioassay (McLaughlin, 1991) was
used to get an idea of the toxicity of Pelargonium extracts and their phenolic constituents
including benzoic and cinnamic acid derivatives, hydrolysable tannins and C-glycosylflavones. With LC50 values 1000 and 200 g/ml for extracts and test compounds
respectively (Latt, 1999), the cytotoxic potential of the samples may be negligible
(Anderson et al., 1992).

ACKNOWLEDGEMENTS

Sincere appreciation is expressed to Dr O. Kayser, Dr K.P. Latt (FU Berlin),


Dr A.F. Kiderlen and U. Folkens (Robert Koch-Institut, Berlin) for the enthusiastic
support, valuable discussions and skilled technical assistance. Special thanks are
extended to Dr M. Heger, Research Center HomInt, Karlsruhe, Germany, for her great
interest to this work, invaluable advice on the clinical studies section, and the assistance
with graphics. Thanks are also due to TAACF for antimycobacterial tests. The plant
material was kindly provided by the pharmaceutical company Dr Willmar Schwabe,
Karlsruhe, Germany.

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25 Interactions between arthropod


pests and pelargoniums
Monique S.J. Simmonds

INTRODUCTION

Species of Pelargonium vary in their susceptibility to predation by insects and mites. This
variation depends in part in their chemistry and their morphology. Pelargoniums
(colloquially known also as geranium), like most species have evolved an array of defence
mechanisms that will deter a high proportion of phytophagous insects and mites. However,
some insects will usually overcome these defence systems and then cause damage and
become pests. The success of these pests often depends on whether the defence mechanisms
that the pest has overcome will also protect it from predation. Thus the pest is able to
exploit a new plant host until a predator or parasitoid is able to exploit the pest host on the
plant. The defence systems can be seen as two types: direct and indirect. The former will
consist of morphological features such as the presence of trichomes and the latter with the
presence of plant secondary metabolites that deter or are toxic to insects.
Understanding the mechanisms by which geranium plants modulate insects will
assist in the design of pest control strategies. In natural conditions wild geraniums are
not often reported to suffer greatly from herbivory, the main problems occur when
plants are cultivated in high densities under glass. Under these conditions geraniums
vary in their susceptibility, especially to pests such as whitefly and mites. Mites and
whitefly appear to have a preference for Regals, Angels and some scented varieties. This
chapter outlines our knowledge about some of the pests of geraniums and it also
provides an overview of pest resistant mechanisms in geraniums and how geraniums
could be used in the control of insect pests.
RESISTANCE TO ARTHROPOD PESTS

Anacortes acids are important in determining the susceptibility of zonal geranium


plants to attack by insects and mites. These compounds are secreted from the glandular trichomes on leaves and inflorescences. They can prevent insects and mites from
moving about on the plant by acting as sticky traps (Walters et al., 1989). They can kill
pests via their toxic properties (Gerhold et al., 1984) and they can decrease the build up
of pest populations by reducing the fecundity of pests (Grazzini et al., 1991). These
compounds also occur in representatives of other families, for example cashews
(Anacardiaceae) and ginkgo (Ginkgoaceae) (Walters et al., 1990).

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Up to 1990 there were thought to be about six of these 6-alkyl salicyclic acid derivatives called anacardic acids, in which the composition and the length of the side chain
varied (Walters et al., 1988). The glandular trichomes on resistant plants
(Pelargonium  hortorum red-flowered plant line 71-17-7) contain higher levels of the C22
and C24 unsaturated anacardic acids with olefinic groups at the -5 position in the side chain,
whereas trichomes in susceptible plants contain higher concentration of C22 and C24
saturated anacardic acids (Figure 25.1). These plants also contain C23 and C25 anteiso
anacardic acids, but in low concentrations (Hesk et al., 1992). The anacardic acids were
thought to be synthesised by the addition of acetate units to fatty acid precursors that
occur in high concentrations in these cultivars. The synthesis of these compounds was
thought to be similar to that used to produce fatty acids, but in the production of anacardic acids the keto groups formed during chain elongation are not all reduced and
dehydrated (Geissman, 1963, Gerhold et al., 1984). The evidence for this scheme was
provided by Walters et al. (1990). They were able to show, using 14C amino acids, that
anacardic acids were biosynthesised from saturated, unsaturated C16 and C18 fatty acids
by the addition of three acetate groups and the production of the aromatic ring via
reduction, dehydration and intra-molecular aldol condensation, a process very similar
to that proposed for the biosynthesis of salicylic acids (Walters et al., 1990).
Initially researchers investigating arthropodgeranium interactions concentrated
their research on the profile of anacardic acids in resistant plants but Hesk et al. (1992)
used high performance liquid chromatography (HPLC) to compare the profiles of anacardic acids in pest-resistance and susceptible plants. Hesk et al. (1992) characterised
19 anacardic acids in the geranium plants. In this study, they also used a wide range of
14C-labelled fatty acids to study the biosynthesis of anacardic acids in geranium plants
resistant to mites and aphids (plant line 71-17-7) and mite and aphid susceptible plants
(plant line 85-26-8). Hesk et al. (1992) showed that both lines of plants produced
anacardic acids from fatty acids and amino acid precursors in a similar way. However,
the resistant plants can oxidise and re-incorporate the acetate groups from whatever
fatty acid or amino acid precursor more readily than the susceptible geraniums. Hesk
et al. (1992) suggest that the resistant plants use this indirect method to produce -5
unsaturated anacardic acids, which are not found in susceptible plants. In an earlier
study, Winner (1975) showed the insect susceptible and resistant plants differed by one
or two genes. It could be that the susceptible plants lack the gene associated with the
production of the enzyme involved in the oxidation of the saturated anacardic acids.
Researchers at Penn State University, USA have concentrated on investigating
the mechanisms associated with the inheritance of the resistant factors. A selection of
16 South African species of Pelargonium were screened for the presence of anacardic
acids and glandular trichomes. The -5 anacardic acids and presence of glandular
trichomes were restricted in their distribution to P. frutetorum and P. inquinans
(Grazzini et al., 1995a). In another study, 13 diploid and 25 tetraploid cultivars of

Figure 25.1 Structure of anacardic acid.

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Pelargonium  hortorum were screened for anacardic acids (Grazzini et al., 1995b). All 38
cultivars contained anacardic acids but no diploid cultivars produced both -5 and -9
anacardic acids, although three of the tetraploid cultivars did produce both forms of
anacardic acids. Overall, there was no relationship between the production of anacardic
acids and ploidy levels. However, there were significant differences in the production of
specific anacardic acids in different cultivars. This suggested that traditional breeding
methods could be used to increase the resistance of Pelargonium cultivars to insect pests.
Further horticultural experiments have been undertaken with crosses between diploid
zonal geraniums that differ in their susceptibility to two-spotted mites (Grazzini et al.,
1997). In these experiments the level of anacardic acids and density of the long
glandular trichomes that secrete anacardic acids in F-1, F-2 and backcross generations
were measured. A selection of the F-2 plants were also tested for resistance to mites.
They found that the mite-resistant plants had low densities of trichomes, high levels
of -5 unsaturated anacardic acids and this condition was controlled by a single
dominant allele.
Recently, Grazzini et al. (1999) studied the distribution of -5 fatty acids in tissue
from mite-resistant plants, as these fatty acids could be precursors of the -5 anacardic
acids. In resistant plants the -5 fatty acids were found in the glandular trichomes and
pedicel trichomes but not in trichome-free tissue or seeds. Grazzini et al. (1999) demonstrate that these fatty acids are available for the biosynthesis of anacardic acids. Thus the
current data shows that anacardic acids play a key role in the resistance of geraniums to
mites, aphids and whitefly. The levels of these compounds vary among cultivars and also
within a resistant cultivar depending on the part of the plant being attacked by the
pest and the environmental conditions. For example, a resistant plant could become
susceptible if rain washed off the acids from the leaf surface or the temperature increases
to over 25.5 C resulting in a reduction in the viscosity of the exudates secreted by the
glandular trichomes and thus reducing the ability of the exudates to trap insects
(Walters et al., 1991). Overall, anacardic acids play an important role in the ecology of
geraniumarthropod interactions (Scultz et al., 2000). Any resistance mechanisms can
alter with time. Harmen et al. (1996) developed a short-term bioassay to evaluate the
factors in geraniums that influenced their susceptibility to mites. These authors were
able to show that leaves can loose their resistance to mites but it can be regained after
14 days. This resistance can be induced. The fact that the fatty acids precursors of
anacardic acids occur in the trichomes on the leaves of resistant geraniums ensures their
replacement and thus the leaves potential resistance to pests.
Anacardic acids are not the only compounds in geraniums that modulate insects.
Geraniums also contain a range of phenolics that could contribute to their susceptibility
to attack by herbivores. For example, some of the phenolics associated with the
medicinal properties of geraniums could modulate insectgeranium interactions, such as
the hydrolysable tannins (ellagitannins), geraniin (Okuda et al., 1982), corilagin (Tanaka
et al., 1985) and elaeocarpusin (Nonaka et al., 1986). Although, as yet we have no direct
experimental data to indicate they influence the susceptibility of geraniums to insects.
Geraniums also contain indole alkaloids, a group of compounds with known insecticidal activity. However, as yet there is very little information about the role of these
compounds in geraniuminsect interactions. Observations in the glasshouses at Kew
showed that when the glasshouse whitefly lay their eggs on the leaves of zonal varieties
they often lay their eggs on the margin of the distinct dark horse shoe-shaped region
on the leaves. The factors that influence this behaviour have not been fully studied.

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Lis-Balchin et al. (1996) identified two indole alkaloids elaeocarpidine 1 and


epielaeocarpidine 2 in zonal cultivars of Pelargonium but not in non-zonal varieties. In
a preliminary study (Simmonds et al., unpublished), these compounds were applied to
the centre of leaves from non-zonal varieties of Pelargonium and the number of whitefly
eggs laid on the treated plants decreased. A laboratory experiment also showed that
elaeocarpidine 1 but not epielaeocarpidine 2 was toxic to whitefly adults at 1000 ppm
(Figure 25.2). Whether the levels of these compounds influence the susceptability of
geraniums to herbivory by insects still needs to be evaluated.

IMPORTANT PESTS OF GERANIUMS

Whitefly
The glasshouse whitefly Trialeurodes vaporariorum (Westwood) can be an important
pest of geraniums. Adult and nymphs feed on the plant sap and when present in high
numbers they can cause a decrease in plant vigour as well as spread viruses. The
insects also produce a sticky secretion called honeydew that acts as a substrate for
fungal growth.
Adult whitefly are usually found on the underside of leaves were they lay their eggs
in a horse-shoe configuration. These eggs turn from a light yellow to black in about
24 days. Pale green nymphs hatch from the eggs, they are mobile and move over the
surface of the plant to find a suitable feeding place. They then settle and form what are
often called scales. The immature nymphal stages feed on plant sap via stylets that
they insert into the plant tissue. The duration of the lifecycle depends on the
temperature and the suitability of the plant. For example, at 21 C the life cycle of the
whitefly from egg to adult takes about 27 days.
Whitefly can be controlled by insecticides or via beneficial organisms such as the
parasitoid Encarsia formosa or fungal pathogens. The chalcid wasp, E. formosa, is a very
effective parasitoid and is used commercially to control whitefly in many glasshouses.
The female wasp lays eggs into the second or third nymphal stage of the whitefly.
The parasitoid then develops within the scale and emerges from the whitefly pupae
after the whitefly has pupated. The presence of the parasitoid in the whitefly pupae

Figure 25.2 Structure of indole alkaloids: (i) elaeocarpidine and (ii) epielaeocarpidine.

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causes the pupae to turn black. This colour change in the whitefly pupae can be used
to monitor the effectiveness of E. formosa in controlling whitefly on different plants.
E. formosa can parasitise whitefly on geraniums. However, we do not know what
influence the exudates produced by glandular trichomes on geranium leaves have on the
ovipositing behaviour of these parasitoids. Recent laboratory based studies have shown
that E. formosa and fungi can be used in an Integrated Pest Management (IPM) strategy
to control whitefly on geraniums (Avery, unpublished data). Further research is needed
into how whitefly-resistant lines of geraniums might influence the interactions among
whitefly, their parasitoids and fungal pathogens.
Mites
Two-spotted mite, Tetranychus urticae (Kock), formerly known as the red-spider mite is
an important pest of geraniums, especially those grown in glasshouses. The
susceptibility of geranium plants to mites appears to be similar to their susceptibility
to whitefly. Many of the zonal geraniums (Pelargonium  hortorum) that have resistance
to mites, are associated with the density of tall glandular trichomes, which secrete
anacardic acids (Gerhold et al., 1984; Harman et al., 1996).
Thrips
The pest status of thrips has increased in the last decade, especially the damage caused
by the western flower thrips, Frankliniella occidentalis. These insects can directly damage
plants by feeding on the flowers and indirectly by spreading viruses, such as Pelargonium
flower break carmovirus (Krczal et al., 1995). As yet there are no validated IPM
programmes available for the control of thrips on geraniums, as the effect of mite- and
whitefly-resistant cultivars on predators of thrips has to be still evaluated.
The level of thrips infestations can be monitored by the use of blue sticky traps,
which should be placed just above the height of the plants. Currently there is a range
of biological control agents that are available for the control of thrips. These include
predatory mites, bugs such as species of Orius as well as nematodes and fungi.
Traditionally predatory mites such as Iphiseius degenerans (Berlese) have been used for
thrips control. These mites can be effective against the immature nymphal stages but
do not attack eggs or adults. Predatory mites are usually supplied in culture packs
which can be placed on plants or the contents sprinkled over plants when flowers
first appear.
Orius are more effective foragers than mites and are able to attack thrips nymphs and
adults. However, it is difficult to establish a populations of Orius in a glasshouse as they
breed slowly and lay eggs in parts of plants that are frequently removed during routine
pruning (Jacobson, 1993).
Vine weevil
Larvae of the vine weevil Otiorhynchus sulcatus (Fabricius) can cause damage to roots of
geraniums. The adult weevils are nocturnal and feed on leaves. They lay their eggs in
the soil. After an incubation period of 824 days the larvae emerge from the egg and
search for suitable roots to feed on. The larvae are white, legless with a brown head.
When fully grown the larvae construct earthen cells in the soil and pupate in these cells.

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The flightless female adults emerge from these pupae. As yet, no male beetles have been
discovered. It is the larvae that do the most damage to the plants, although adults can
cause damage to leaves by biting notches along the edge of the leaves. Larvae are usually
targets for control programmes: they can be killed by beneficial nematodes such as
Heterorhabditis. However, if the damage is extensive due to high densities of larvae then
insecticides will have to be used and these will need to be applied to the soil to kill the
larvae.
Other pests
The glasshouse and potato aphid Aulacorthum solani (Kaltenbach) is a common pest of
geraniums in glasshouses. The adult and nymphal stages are greenish-yellow with
brown markings. Acyrthosiphon malvae (Mosley), the Pelargonium aphid, is another
common pest of geraniums, however, unless infestations are high or the aphids are
transmitting viral infections, these insects do not normally cause economic loss.
The cyclamen mite, Phytonemus pallidus (Banks), can be a another pest of geraniums
in glasshouses. The mites prefer young leaves and flower buds and their life cycle can
be between 2 and 3 weeks at 2025 C. Infestations can result in the margin of the
leaves curling inwards, leaves become brittle and the plants become stunted with
deformed leaves and buds.
There are a few Lepidopteran pests that can damage geraniums. For example, the
larvae of the geranium bronze butterfly can damage geraniums by boring into their
stems. The adults lay their eggs on the flower buds and the larvae when they emerge
move from the flowers into the stems. Here they feed on the stem causing wilting and
if the infestation is high, the death of the plant. This pest was reported in Europe in
the late 1980s. It is a native of South Africa, where the natural predators and parasitoids
help to keep caterpillar numbers down. However, in Europe there are no natural
predators and the pest is through to be on the increase. Other lepidoptera pests include
the silver moth, Autographa gamma (Linnaeus), which can attack plants in glasshouses
in Europe. It can cause damage to plants growing outside in the southern parts of
Europe but it will not survive winters in northern Europe.
The flax totrix moth, Cnephasia asseclana (Denis and Schiffermuller), is a less
important pest and can, like other totrix moths, be identified by the fact that larvae
produce silk to spin a web between leaves or flowers. The web provides protection for
the feeding larvae and the pupae.
The glasshouse leafhopper Hauptidia maroccana (Melichar) can cause speckling,
silvering or mottling to the foliage. However, unless the infestations are very high this
pest does not usually result in the death of the plant. The common green capsid,
Lygocoris pabulinus (Linnaeus), can cause damage to new foliage and flowers. The new
shoots become red to brown and the flowers are often distorted and the buds can be
aborted.

USE OF GERANIUM EXTRACTS IN PEST CONTROL

The control of insect pests continues to challenge scientists. As the concern about the
overuse of broad spectrum synthetic insecticides increases, there is a need to find
alternative strategies. These alternatives could include plant-derived compounds which

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Insecticidal effect of Pelargonium extracts

297

are usually more host specific in their activities and are biodegradable. For example,
plants have already provided a range of insecticides such as nicotine, rotenone, pyrethrum
and azadirachtin. However, there is an increased interest in aromatic plants and many
essential oils (EOs) have been screened for insecticidal activity (Regnault-Roger, 1997).
The EOs obtained by steam distillation of the aerial parts of Pelargonium species,
especially. P. graveolens (L.), P. capitatum Ait., P. odoratissimum and P. radula (Cav.) (syn.
P. radens and P. roseum Willd.) used in perfumes can be used to deter insects. The oil can
contain over 120 different mono- and ses-quiterpenoids (Vernin et al., 1983). The composition of the oils differ depending in part on the source of the plants. The main compounds
in EOs are citronellol, geraniol, linalol, nerol, myrene, camphene, limonene, carvone and
farnesene. Many of these compounds have known insecticidal or deterrent activity against
insects. For example, citronellol has known insecticidal activity and citronellol extracted
from cloves has been used as a mothprooofing agents (Riedel et al., 1989).
Extracts from wild geraniums are repellant to the cockroach Blatella germanica and
extracts from the rose geranium are repellant to flies such as Musca domestica and Culex
fatigans (Jacobson, 1990). However, to date very little research has been undertaken on
the use of geranium extracts in pest control. Although from our knowledge about the
anti-insect activity of the compounds in the plants the extracts from geraniums should
have some potential as insect deterrents. A problem encountered in comparing some of
the ethnobotanical reports about the use of Geranium oil relates to inadequate information about the species or variety of geranium used. As yet there has been very little
research into the effect of geranium-derived compounds on non-geranium feeding
insects. However, the information we have suggests they could be sources of active
molecules. For example, geraniin the bound form of ellagic acid found in geraniums
inhibits the development of Heliothis virescens (Klocke et al., 1986).
ACKNOWLEDGEMENTS

I thank Dr Nigel Veitch for drawing the chemical structures and to Dr Maria
Lis-Balchin for introducing me to the complexity of Pelargoniuminsect interactions.
REFERENCES
Geissman, T.A. (1963) The biosynthesis of phenolic plant products. In P. Bernfield (ed.),
Biogenesis of Natural Compounds. Macmillan, New York, pp. 563616.
Gerhold, D.L., Craig, R. and Mumma, R.O. (1984) Analysis of trichome exudates from
mite-resistant geraniums. J. Chem. Ecol., 10, 713722.
Grazzini, R., Hesk, D., Heininger, E., Hildenbrandt, G., Reddy, C.C., CoxFoster, D., Medford,
J., Craig, R. and Mumma, R.O. (1991) Inhibition of lipoxygenase and prostaglandin
endoperoxide synthase by anacardic acids. Biochem. Biophys. Res. Commun., 176, 775780.
Grazzini, R., Hesk, D., Yerger, E., CoxFoster, D., Medford, J., Craig, R. and Mumma, R.O.
(1995a) Species distribution of biochemical and morphological characters associated with
small pest resistance in Pelargonium  hortorum. J. Am. Soc. Hort. Sci., 120, 336342.
Grazzini, R., Hesk, D., Yerger, E., CoxFoster, D., Medford, J., Craig, R. and Mumma, R.O.
(1995b) Distribution of anacardic acids associated with small pest resistance among cultivars
of Pelargonium  hortorum. J. Am. Soc. Hort. Sci., 120, 343346.
Grazzini, R., Walters, D., Harmon, J., Hesk, D.J., CoxFoster, D., Medford, J., Craig, R. and
Mumma, R.O. (1997) Inheritance of biochemical and morphological characters associated

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with two-spotted spider mite resistance in Pelargonium  hortorum. J. Am. Soc. Hort. Sci., 122,
373379.
Grazzini, R.A., Paul, P.R., Hage, T., CoxFoster, D.L., Medford, J.I., Craig, R. and Mumma,
R.O. (1999) Tissue-specific fatty acid composition of glandular trichomes of mite-resistant
and susceptible Pelargonium  hortorum. J. Chem. Ecol., 25, 955968.
Harman, J., Paul, P., Craig, R., CoxFoster, D., Medford, J. and Mumma, R.O. (1996)
Development of a mite bioassay to evaluate plant resistance and its use in determining regeneration of spider mite resistance. Entomol. Exper. Applic., 81, 301305.
Hesk, D., Craig, R. and Mumma, R.O. (1992) Comparison of anacardin acid biosynthetic capability between insect-resistant and -susceptible geraniums. J. Chem. Ecol., 18, 13491364.
Jacobson, M. (1990) Glossary of Plant-derived insect deterrents. CRC Press, Florida.
Jacobson, R.J. (1993) Egg laying sites of Orius majusculus, a thrips predator, on cucmber. In:
B.L., Parker, M. Skinner and T. Lewis (eds), Thrips Biology and Management. Plenum Press,
New York, pp. 241244.
Klocke, J.A., Van Wagenen, B. and Balandrin, M.P. (1986) The ellagitannin geraniin and
its hydrolysis products isolated as inset inhibitors from semi-arid land plants. Phytochem.,
25, 85.
Krczal, N.K.K., Albouy, J., Damy, I., Kusiak, C., Deogratias, J.M., Moreau, J.P., Berkelmann,
B. and Wohanka, W. (1995) Transmission of pelargonium flower break virus (PFBV) in
irrigation systems and by thrips. Plant Dis., 79, 163166.
Lis-Balchin, M., Houghton, P. and Woldermarian, T. (1996) Elaeocarpidine alkaloids from
Pelargonium species (Geraniaceae). Natl. Prod. Lett., 8, 105112.
Nonaka, G., Morimoto, S. and Nishioka, I. (1986) Elaeocarpusin, a proto-type of geraniin from
Geranium thunbergii. Chem. Pharmaceut. Bull., 34, 941943.
Okuda, T., Yoshida, T. and Hatano, T. (1982) Constituents of Geranium thunbergii Seb. Et Zucc.
Part 12. Hydrated sterostructure and equilibration of geraniin. J. Chem. Soc. Perkins Trans., 1,
914.
Regnault-Roger, C. (1997) The potential of botanical essential oils for insect pest control. Integr.
Pest Manag. Rev., 2, 2534.
Riedel, G., Heller, G. and Voigt, M. (1989) Detia Freyberg GmbH, Germany (Federal
Republic). Citronellol and eugenol as mothproofing agents. Patent DE 98-3901341 890118.
Scultz, D.J., Medford, J.I., Cox-Foster, D., Grazzini, R.A., Craig, R. and Mumma, R.O. (2000)
Anacardic acids in trichomes of Pelargonium: Biosynthesis, molecular biology and ecological
effects. Adv. Bot. Res. (incorp.) Adv. Plant Path., 31, 175192.
Tanaka, T., Nonaka, G. and Nishioka, I. (1985) Punicafolin, an ellagitannin from the leaves of
Punica granatum. Phytochem., 24, 20752078.
Vernin, G., Metzger, J., Fraisse, D. and Scharf, C. (1983) Etude des huiles essentielles par
GC-SM-banque specma: essences de geranium. Parfum. Cosmet. Arom., 52, 5161.
Walters, D.S., Minard, R., Craig, R. and Mumma, R.O. (1988) Geranium defensive agents III.
Structural determination and biosynthetic considerations of anacardic acids in geranium.
J. Chem. Ecol., 14, 743751.
Walters, D.S., Grossman, H., Craig, R. and Mumma, R.O. (1989) Geranium defensive agents
IV. Chemical and morphological bases of resistance. J. Chem. Ecol., 15, 357372.
Walters, D.S., Craig, R. and Mumma, R.O. (1990) Fatty acid incorporation in the biosynthesis
of anacardic acids in Geraniums. Phytochem., 29, 18151822.
Walters, D.S., Harman, J., Craig, R. and Mumma, R.O. (1991) Effect of temperature on glandular trichome exudates composition and pest resistance in Geraniums. Entomol. Exper. Applic.,
60, 6169.
Winner, B.L. (1975) Inheritance of resistance to the two-spotted spider mite, Tetranychus uriticae
(Kock) in the geranium Pelargonium  hortorum (Bailey). MS Thesis. Pennsylvania State
University, University Park, Pennsylvania.

2002 Edited by Taylor & Francis

26 Correlation of the chemical


profiles of the essential oil of
Pelargonium (Geranium oil) and
others separately and in mixes,
with their relaxant or stimulant
properties in man and smooth
muscle preparations in vitro
Maria Lis-Balchin and Stephen Hart

INTRODUCTION

Geranium oil, like other plant essential oils (EOs) has been used for many years in the
manufacture of perfumes and these have been designed to either stimulate or relax
the wearer or possibly even to attract the opposite sex. Perfumes are made up of a large
number of EOs and nowadays also numerous synthetic chemical components, but the
basis of a good perfume is to have a specific blend of top notes, middle notes and
base notes. Perfumes were originally designed for either men or for women individually, but nowadays there is a tendency for unisex perfumes, which suggests that the
emphasis lies more on the stimulant or relaxant nature of the perfume rather than
sexual attraction.
Essential oils have also been individually categorised by aromatherapists as being
either relaxant (sedative) or stimulant. It is not clear whether this refers to the action
on the brain or to some or all of the muscles, as many EOs are also classified as antispasmodic. Most EOs are used by aromatherapists in mixes of 3 or more, diluted by
95 per cent with almond or other carrier oil and then massaged into the skin. The
mixture almost inevitably has the three notes as its theme, in order to give the correct
balance.
The overall effect of this perfume together with the massage is supposed to relieve
stress and in so doing may also cure or at least alleviate many of the stress-related
conditions like eczema, stomach ache, back ache, headache. Whether or not the aroma
of the perfume mix has any effect is unclear as clinical studies have not provided
any statistically significant results (see Chapter 21).
There are many studies on the effects of aroma on psychology as well as physiology
of the recipient, however, there is so far no published evidence for the role of the
chemistry of the EO, component and mixture of these in a perfume or aromatherapy
mix. These parameters were therefore studied using smooth muscle.

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Stress: biochemical and physiological implications


Changes in the body which occur outside of the brain, as a result of stress, are not under
conscious control but are mediated by the sympathetic branch of the autonomic
nervous system. The activity of most organs of the body is controlled by the autonomic
nervous system and as a general rule the sympathetic system may be considered to be
activated in times of flight or fight which will include stress. Stress-related changes in
the body will also be mediated by hormones, such as those released from the adrenal
gland. Stimulation of the sympathetic system, and adrenaline released from the adrenal
gland, will increase heart rate and stroke volume and by dilating and contracting different blood vessels will cause blood to be distributed to those organs such as skeletal
muscle, heart and lungs which are involved in exercise.
Smooth muscle will also be either contracted or relaxed such that the body is prepared for exercise, thus bronchial muscle relaxes and sphincters of the gastro-intestinal
system contract. If one considers the fight response in animals, smooth muscle contracts
to give dilated pupils and make hair stand on end. In both man and other animals,
stimulation of the sympathetic system will cause metabolic changes which favour activity, such as an increase in blood glucose. The nerves of the sympathetic system which
innervate smooth, cardiac and vascular smooth muscle all release noradrenaline as their
neurotransmitter and the differential response, either contraction or relaxation, is
brought about by the presence of different adrenoceptors on the innervated tissue.
In general, alpha adrenoceptors mediate contraction and beta-adrenoceptors relaxation, but of course there are exceptions to this rule. Further differentiation and control
of the system is obtained by the presence of sub-types of alpha and beta adrenoceptors.
Occupation of a receptor by an appropriate agonist results in a change in cell activity
(such as contraction or relaxation) which is mediated via a secondary messenger within
the cell. Alpha-2 adrenoceptors mediate their actions via a fall in cyclic AMP (cAMP),
whilst beta-adrenoceptor activation is associated with a rise in cAMP. Alpha-adrenoceptors
are linked to the phosphoinositide pathway. In general, contraction is associated with an
increase in the concentration of calcium ions within the muscle fibre whilst relaxation
involves either a removal of calcium, the blocking of calcium channels or the opening
of potassium channels.
Many tissue of the body receive a dual innervation from the two branches of the autonomic nervous system (sympathetic associated with activity and parasympathetic with
feeding and the restoration of energy). In the gastro-intestinal tract, we have this dual
innervation plus an additional plexus of nerves in the wall of the intestine, often called
the enteric nervous system, which involves several other neutotransmitters.
It is on account of this rich innervation of the intestine that we have studied the
action of EOs on the smooth muscle of the guinea-pig ileum in vitro.
Smooth muscle preparation
The preparation of the smooth muscle of the guinea-pig ileum will remain viable for
several hours after removal from the animal and will respond to electrical field
stimulation with reproducible contractions which are due to the stimulation of the
parasympathetic nerve with the release of acetylcholine.
Essential oils which stimulate smooth muscle contraction can be recognised immediately whilst the site of action of those which reduce the size of the electrically-induced

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301

contraction can be determined. Possible sites of action include inhibition of the release
of acetylcholine, or relaxation of the tissue via stimulation of adrenoceptors, action on
secondary messengers or on calcium or potassium channels. This preparation thus
allows us to recognise spasmogenic and spasmolytic activity, to determine whether or
not the activity is dose-related, to measure duration of action and also attempt to determine the mechanism of action.
The question arises whether the knowledge of the activity of EOs on smooth muscle
gives us any clues about the likely actions of these compounds if and when they enter
the central nervous system (CNS).
A famous English pharmacologist suggested that the intestine could be considered
a paradigm of the CNS, but it still remained almost impossible to infer action in the
CNS from activity on isolated smooth muscle.
The reason for this is simply the complexity of the CNS, with the interaction
between excitatory and inhibitory fibres being such that reduced activity in one neurone can lead either to sedation or excitation. Thus alcohol appears to stimulate some
behaviour although it is a CNS depressant, the explanation being that the inhibition of
inhibitory pathways removes a normal break and behaviour therefore changes.
Another aspect of the complexity of the CNS is that any one particular behaviour
is controlled by several neurotransmitters, each of which is likely to be able to bind to
different sub-groups of receptors.
If one for example considers pain, this involves neurotransmitters in the afferent
pathway such as Substance P, glutamate and nitric oxide (NO) and this afferent
pathway can be modulated by neuronal pathways releasing a range of neurotransmitters including opioid peptides, acetyl choline, histamine, 5-hydroxytryptamine and
cholecystokinin.
With so many neurotransmitters involved in the pain pathway it is not surprising
that the experience of pain can be influenced by many different compounds. For
example, monoterpenes like menthone and -terpineol (administered by the
subcutaneous route) showed activity similar to that of accepted analgesics
e.g. indomethacin and naproxen in reducing the behavioural activity of the mouse to a
noxious stimulus (Hart et al., 1994).
In experiments studying the motor activity of mice after exposure to the aroma of
various EOs (Buchbauer, 1991, 1992; Jager et al., 1992) rosemary, jasmine and Ylang
ylang increased activity whilst lavender, neroli, lime-blossom, passiflora, citronellol and
linalool (both the latter found in Geranium oil in high concentrations) decrease motor
activity. The presence of components in the blood when applied by inhalation has also
been demonstrated ( Jager et al., 1992). The effect on the motor activity has been shown
to be similar to that when the EO was injected. It has been assumed that changes in
motor activity are a central effect but the possible action on neuromuscular transmission has not been investigated.
However, recent experiments on the motor-nerve skeletal muscle preparation (rat
phrenic-nerve diaphragm) by the authors has shown that geranium, lavender and tea
tree oils cause a reduction in the size of the twitch of the skeletal muscle in response to
electrical stimulation of the motor nerve.
Linalool, which was shown to reduce motor activity in the mouse has also been shown
to have an action within the brain itself: using membranes from rat cerebral cortex,
linalool exhibited a dose-related inhibition of the binding of glutamate, a main
excitatory neurotransmitter of the CNS (Elisabetsky et al., 1995).

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The effect of EOs in man has been studied in several different ways including measuring the alertness and reaction times (Manley, 1993) and human brain activity (Torii
et al., 1988; Kubota et al., 1992) using contingent negative variation (CNV). The latter is the brain potential which occurs between a warning stimulus and an imperative
stimulus i.e. when the subject is expecting something to happen. The CNV amplitude
is increased by caffeine, jasmine and peppermint and decreased by chlorpromazine,
lavender and marjoram. There is some discrepancy between results from different
groups regarding many oils.
The present experiments were designed to see whether the effect of stress on man
could be mimicked using isolated segments of small intestine and by monitoring
their spasmogenic or spasmolytic effects, it could be possible to assess their relaxant or
stimulant nature.

MATERIALS AND METHODS

Essential oils were obtained from various commercial sources and each oil was analysed
by GC using a Shimadzu GC 8A with a 50 m  0.32 mm OV101 column; the temperature program was set at 4 C min1 from 100 to 230 C.
The percentage of all the components was calculated in each selected retention time
(RT) interval of under 10 min, 1115 min, 1620 min, 2130 min and 30  min.
The main components present in each RT interval was also determined. The EOs were
diluted in methanol (usually  1000) and 0.1 to 0.2 ml was applied to the tissue
preparations in the organ bath giving a final dilution of 200,000 to
400,000 (a concentration of 2.5  106 to 5  106).
Pharmacological studies, carried out on guinea-pig ileum were contrasted against
many practising Aromatherapists predictions of the effect of EOs on the patient (alone
or as mixtures).

RESULTS OF THE STUDIES

Monoterpenes versus contractions of smooth muscle


Previous comparisons of the pharmacological activity of many components and EOs
suggested that monoterpenes were responsible for contractions in the guinea-pig ileum
in vitro (Lis-Balchin et al., 1996a,b).
This was best illustrated by work on two New Zealand EOs Manuka and Kanuka.
The former was largely composed of sesquiterpenes and produced a relaxation in the
gut, whilst the latter was composed largely of monoterpenes and produced a contraction (Lis-Balchin et al., 1996a). Further work on over 70 EOs suggested that there was
a considerable correlation of contraction of the small intestine with a high percentage
of monoterpenes and not sesquiterpenes (Lis-Balchin et al., 1996b, 1998).
These results therefore suggested that it was simply the actual percentage
composition of the monoterpenes, but not sesquiterpenes, which determined
whether the effect on the smooth intestinal muscle would be contractile or relaxant.
This was therefore investigated further.

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303

Table 26.1 The predicted effect on guinea-pig ileum based on the percentage of components at different
retention time (RT) intervals
RT

10

1115

1620

2130

30

Effect

a
b
c
d
e
f
g
h
i
j
k
l
m
n
o
p
q
r
s
t
u
v
w
x
y
z

19
13

82
97
57
69
2
82
6
46
8

99
1
14
16
67
1

58
4

66
64
3
1
3

25

41
22
30

29
92
52

30

32

12

2
85

45
30
5

58
2
37

51
1
76
2
34

5
7
47
5

32
2
2
4
5

39
59
78

5
69

9
56
89

76

45

10
48
34

R
R
R
S
S
S/R
S/R
R
S
R
S/R
R
R
R
R
R
R
S
R
S/R
S/R
S
R
R
S/R
R

Retention times versus percentage of components


This hypothesis was put to the test, using EOs alone or in mixes, by calculating the
total per cent of components in different RT intervals (Table 26.1) and predicting what
the effect on the smooth muscle would be.
It was noted that monoterpenes were in the RT 10 interval, with the exception of
1,8-cineole which was also found here, whilst alcohols, ketones and aldehydes occurred
in the 1115 min interval, esters and phenols in the 1520 min interval and sesquiterpenes thereafter.
Chemical predictions versus actual effect on ileum
Whenever there was a considerable percentage of components in the 10 min interval,
this would be associated with a small to large contraction of the ileal muscle
(depending on the actual percentage). Predictions of pharmacological activity could
therefore be easily made based on the chemical composition, with the exception of EOs
containing 1,8-cineole e.g. Eucalyptus globulus (Table 26.2). Geranium oil showed a very
high proportion of the non-stimulating components and therefore was stated to be
relaxant according to the chemical prediction.

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Maria Lis-Balchin and Stephen Hart

Table 26.2 Comparison of the actual effect of essential oils on Guinea-pig ileum and the predicted effects
using chemical composition and Aromatherapists predictions

a. Tea tree
b. Neroli
c. Camomile German
d. Frankincense
e. Camphor
f. Black Pepper
g. Rosemary
h. Lemongrass
i. Juniper
j. Lavender
k Bergamot
l. Ylang Ylang
m. Sandalwood
n. Vetivert
o. Petitgrain
p. Rosewood
q. Geranium Bourbon
r. Eucalyptus globulus
s. Clary Sage
t. Ginger
u. Dillweed
v. Nutmeg
w. Manuka
x. Spikenard
y. Camomile Roman
z. Valerian

Actual effect on tissue

Chem prediction

Aromather. prediction

R & S/R
R
R
S
S
S/R
S/R
R
R
R & S/R
S/R
R
R
R
S/R
R
R
R
S & S/R
R
S/R
S
R
R
S/R & S/R
R

S/R
S/R
R
S
S
S/R
S/R
R
S
R
S/R
R
R
R
R
R
R
S
R
S/R
S/R
S
R
R
S/R
R

S/R
S/R
R
R
S
S/R
S
S/R
S
R
S/R
R
R
R
S/R
R
R
S
R
S/R
R
R
R
R
R
R

Chemical predictions versus Aromatherapists predictions of effect on patient


The chemical predictions were largely similar to both the actual observed effect
on the smooth muscle and also similar to the Aromatherapists prediction on
the patient. The latter effect was either a relaxant effect or a stimulant effect on the
patient; the stimulant effect could be directly related to a contraction on the isolated
muscle. The chemical prediction for Geranium oil was confirmed by the actual effect
and that of the Aromatherapists predictions.
Effect of mixtures of EOs
Mixtures of two or more EOs also showed the same trend, some of which are shown in
Tables 26.3 and 26.4. This proves that contractions of smooth muscle are largely as
a result of a high monoterpene concentration, regardless of the actual monoterpene
component. Geranium oil added to other components caused a swing towards chemical readjustment towards a greater concentration of relaxant components and therefore
it was predicted to be a more relaxant mixture than the components like frankincense
(mix 6), frankincense and bergamot (mix 7) would have been alone, due to their high
concentration of monoterpenes.

2002 Edited by Taylor & Francis

Chemical profiles versus relaxation or stimulation

305

Table 26.3 The predicted effect on guinea-pig ileum based on the percentage of components at different
retention time (RT) intervals
RT

10

1115

1620

2130

30

Effect

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17

41
85
78
86
44
37
4
9

98
99

22
10
10
78

85
5
1
22
2
45
47
90
56

69
26
39
9

2
49

1
2

12

4
36
3

6
14
1
5
4
2
15
58

71

41
9
5

37

19

R
S/R
S
S/R
S
S/R
S/R
R
S/R
R
S
S
R
S/R
S/R
S/R
S

Table 26.4 Comparison of the predicted effect of essential oil blends on clients/patients by
Aromatherapists and by the chemical composition with their actual effect on guinea-pig ileum
Blend

1.
2.
3.
4.
5.
6.
7.
9.
10.
11.
12.
13.
14.
15.
16.
17.

Effects predicted

Orange 2: Nutmeg 1: Dill 1


Lemongrass 1: Juniper 1: Rosemary 2
Frankincense 1: Rose Abs. 1: Clary Sage 2
Eucalyptus glob. 1: Black pepper 1: Ginger 1
Ginger 1: Tea Tree 1: Rosemary 2
Frankincense 2: Ylang Ylang 1: Geranium 1
Frankincense 1: Geranium 1: Bergamot 2
Camomile Roman 1: Lavender 1: Geranium 1
Frankincense 1: Mandarin 2: Scotch Pine 1
Camomile Roman 1: Valerian 1: Rose Abs.1
Ylang Ylang 1: Marjoram 1: Thyme Red 1
Petitgrain 1: Melissa 1: Sage Dalmatian 1
Kanuka 1: Lavender 1: Frankincense 1
Manuka 1: Lavender 1: Frankincense 1
Fennel 1: Orange 1: Bergamot 1
Basil 1: Bergamot 1: Clary Sage 1: Jasmine 1

Actual effect

Aromatherapist

Chemical
prediction

S
S
R/S
S
S
R/S
S/R
R/S
S/R
R/S
R
S/R
R
S
S/R
S

S
S
R/S
S
S/R
S/R
S/R
S/R
S
S/R
S/R
R
S/R
S/R
S/R
S/R

S/R
R
S/R
S/R
S/R
R
S/R
S/R
S/R
R
R
R
R
R
S/R
S/R

As before, the correlation broke down if 1,8-cineole was involved e.g. in mixtures
with rosemary or Eucalyptus globulus. There is no easy explanation for this discrepancy.
It is also of interest that if Eucalyptus globulus, containing 95 per cent of 1,8-cineole is
presented to the smooth muscle preparation it will cause a relaxation, whereas if
1,8-cineole alone is presented it causes a contraction.

2002 Edited by Taylor & Francis

306

Maria Lis-Balchin and Stephen Hart

Studies on well known commercial perfumes were only effected on their chemical
composition. There seemed to be a very positive correlation between the chemical
distribution and the products intention, as determined by the publicity information.
Thus, the lavender-containing Eau de colognes, were refreshing and stimulating only
because there was a predominance of monoterpenes (largely limonene) from the citrus
EOs used in greater concentration than lavender in the formulation. Paris by Kenzo,
showed a similar over-preponderance of monoterpenes again due to the limonene of its
citrus components. These are obviously stimulating oils and their predicted effect
would be contractile on smooth muscle. Geranium oil containing perfumes, with
a more rose-like odour (with either the synthetic components or real Geranium oil
added) would have a preponderance of relaxant components and therefore be
predictably relaxant on smooth muscle. The effect on the wearer or those smelling
the wearer would also be predictably of a relaxant nature i.e. its holistic effect would
also be of a relaxant nature, unless the wearer or person sniffing that perfume had
a great dislike for that particular odour. . . but that is an unpredictable idiosyncratic,
psychological effect, which could completely contradict the chemical findings.
CONCLUSION

The present results indicate that there is a very close correlation between the pharmacological activity of EOs on the isolated smooth ileal muscle of the guinea pig and
the predicted effect on the human psyche by aromatherapists, as with the use of
Geranium oil.
This holistic effect would probably have originated from the direct effect of EOs on
the CNS with the concomitant effect of the massage (and of course counselling and
possible placebo effect). The actual effect on the isolated smooth muscle is less complex
and probably involves various adrenoceptors, but there could also be a simple direct
action of components on the membrane with all monoterpenes initiating a rise in
calcium levels which cause contraction of the muscle.
It is suggested that perfumes containing large proportions of relaxant components,
i.e. other than monoterpenes, would be of a relaxant nature to the wearer and those
around the wearer.
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Buchbauer, G., Jirovetz, L. and Jager, W. (1992) Passiflora and Limeblossom: Motility effects
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Elisabetsky, E., Marschner, J. and Souza, D.O. (1995) Effects of linalool on glutamatergic system
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Jager, W., Buchbauer, G., Jirovetz, L. and Fritzer, M. (1992) Percutaneous absorption of lavender oil from a massage oil. J. Soc. Cosmet. Chem., 43, 4954.

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2002 Edited by Taylor & Francis

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