IOBC
OILB
WPRS
In te rn atio na l O rg an isa tio n fo r B iolog ical an d In teg ra te d C on tro l o f No xiou s
A nim als a n d P lan ts: W e st Pa la ea rctic Re gio na l S e ctio n
SROP
O rg an isa tio n In te rn a tio n ale d e L utte B io lo giqu e e t In te g ré e con tre les A n im a ux et le s
P la ntes N u isibles: S e ction Ré gio na le O u est P a lé a rctiq ue
Classical and augmentative biological
control against diseases and pests:
critical status analysis and review of factors
influencing their success
Edited by Philippe C. Nicot
2011
The content of the contributions is the responsibility of the authors
Published by the International Organization for Biological and Integrated Control of Noxious
Animals and Plants, West Palaearctic Regional Section (IOBC/WPRS)
Publié par l'Organisation Internationale de Lutte Biologique et Intégrée contre les Animaux
et les Plantes Nuisibles, Section Ouest Palaéarctique (OILB/SROP)
Copyright IOBC/WPRS 2011
ISBN
978-92-9067-243-2
2
Cover page photo credits:
1and 3: M Ruocco, CNR
2: Anderson Mancini
4. P.C. Nicot, INRA
1
4
3
Preface
One of the Research Activities (RA 4.3) of the European Network for Durable Exploitation of crop
protection strategies (ENDURE*) has brought together representatives of industry and scientists
from several European countries with experience ranging from fundamental biology to applied field
work on biological control against pests and diseases. The unique diversity of expertise and
concerns allowed the group to set up very complementary approaches to tackle the issue of the
factors of success of biocontrol.
The initial part of the work accomplished by this group consisted in a thorough review of
scientific literature published on all types of biological control. Although it had to be focused on
selected key European crops and their major pests and pathogens, this review is unique in the scope
of the topics it covered and in the comprehensive inventories it allowed to gather on the potential of
biocontrol and factors of success at field level.
In parallel with identifying knowledge gaps and key factors from published research,
information was gathered on aspects linked to the production and commercialization of biocontrol
agents.
These results, complemented by the views of experts in the field of biocontrol consulted at the
occasion of meetings of IOBC-wprs, allowed the identification of majors gaps in knowledge and
bottlenecks for the successful deployment of biocontrol and lead to the proposition of key issues for
future work by the research community, the field of development and prospects for technological
improvement by industry.
Avignon, June 2011
Philippe C. Nicot
Acknowledgements: Many thanks are expressed to Ute KOCH for her assistance with the lay out of
the book
EU FR6 project 031499, funded in part by the European Commission
*
i
Contributors
ALABOUVETTE Claude,
INRA, UMR1229, Microbiologie du Sol et de l'Environnement, 17 rue Sully,
F-21000 Dijon, France
Claude.Alabouvette@dijon.inra.fr
current address: AGRENE, 47 rue Constant Pierrot 21000 DIJON, c.ala@agrene.fr
BARDIN Marc,
INRA, UR 407, Unité de Pathologie végétale, Domaine St Maurice, BP 94,
F-84140 Montfavet, France
Marc.Bardin@avignon.inra.fr
BLUM Bernard,
International Biocontrol Manufacturers Association, Blauenstrasse 57,
CH-4054 Basel, Switzerland
bjblum.ibma@bluewin.ch
DELVAL Philippe,
ACTA, Direction Scientifique, Technique et Internationale,
ICB / VetAgroSup, 1 avenue Claude Bourgelat , F-69680 Marcy l'Etoile, France
Philippe.Delval@acta.asso.fr
GIORGINI Massimo,
CNR, Istituto per la Protezione delle Piante, via Università 133,
80055 Portici (NA), Italy
giorgini@ipp.cnr.it
HEILIG Ulf,
IBMA, 6 rue de Seine, F-78230 Le Pecq, France
ulf.heilig@cegetel.net
KÖHL Jürgen,
Wageningen UR, Plant Research International, Droevendaalsesteeg 1,
P.O. Box 69, 6700 AB Wageningen, The Netherlands
jurgen.kohl@wur.nl
LANZUISE Stefania,
UNINA, Dip. Arboricoltura, Botanica e Patologia Vegetale,
Università di Napoli Federico II, via Università 100, 80055 Portici (NA), Italy
ii
LORITO Matteo
UNINA, Dip. Arboricoltura, Botanica e Patologia Vegetale,
Università di Napoli Federico II, via Università 100, 80055 Portici (NA), Italy
lorito@unina.it
MALAUSA Jean Claude,
INRA, UE 1254, Unité expérimentale de Lutte Biologique,
Centre de recherche PACA, 400 route des Chappes, BP 167,
F-06903 Sophia Antipolis, France
Jean-Claude.Malausa@sophia.inra.fr
NICOT Philippe C.,
INRA, UR 407, Unité de Pathologie végétale, Domaine St Maurice, BP 94,
F-84140 Montfavet, France
Philippe.Nicot@avignon.inra.fr
RIS Nicolas,
INRA, UE 1254, Unité expérimentale de Lutte Biologique,
Centre de recherche PACA, 400 route des Chappes, BP 167,
F-06903 Sophia Antipolis, France
Nicolas.Ris@sophia.inra.fr
RUOCCO Michelina,
CNR, Istituto per la Protezione delle Piante, via Università 133,
80055 Portici (NA), Italy
ruocco@ipp.cnr.it
VINALE Francesco,
CNR, Istituto per la Protezione delle Piante, via Università 133,
80055 Portici (NA), Italy
frvinale@unina.it
WOO Sheridan
UNINA, Dip. Arboricoltura, Botanica e Patologia Vegetale,
Università di Napoli Federico II, via Università 100, 80055 Portici (NA), Italy
woo@unina.it
iii
List of Tables
Table 1:
Scientific papers published between 1973 and 2008 on biological control
against major plant diseases (from CAB Abstracts® database). ..........................................2
Table 2:
Numbers of references on biocontrol examined per group of disease/plant
pathogen. .....................................................................................................................3
Table 3:
Numbers of different biocontrol compounds and microbial species reported as
having successful effect against key airborne pathogens/diseases of selected
crops. ..........................................................................................................................4
Table 4:
Microbial species of fungi/oomycetes, yeasts and bacteria reported to have a
significant effect against five main types of airborne diseases or pathogens in
laboratory conditions or in the field.................................................................................5
Table 5:
References extracted from the CAB Abstracts database and examined for
reviewing augmentation biological control in grapevine. .................................................13
Table 6:
Biocontrol agents evaluated in researches on augmentative biological control
of pests in grapevine. ..................................................................................................15
Table 7:
Number of references on augmentative biocontrol agents per group and
species of target pest in grapevine.................................................................................16
Table 8:
Number of references reporting data on the efficacy of augmentative
biocontrol of pests in grapevine. ...................................................................................18
Table 9:
Recent introductions of parasitoids as Classical Biocontrol agents ....................................31
Table 10:
Consulted sources of information on authorized biocontrol plant protection
products in five European countries: .............................................................................34
Table 11:
Active substances suitable for biological control listed on Annex I of
91/414/EEC (EU Pesticide Database) - Status on 21st April 2009 .....................................36
Table 12:
Evidence for, and effectiveness of, induced resistance in plants by
Trichoderma species (Harman et al., 2004a). .................................................................47
Table 13:
Trichoderma-based preparations commercialized for biological control of
plant diseases. ............................................................................................................49
Table 14:
Compared structure of the production costs for a microbial biocontrol agent
(MBCA) and a chemical insecticide (source IBMA). ......................................................59
Table 15:
Compared potential costs of registration for a microbial biocontrol agent
(MBCA) and a chemical pesticide (source IBMA) ..........................................................60
Table 16:
Compared estimated market potential for a microbial biocontrol agent
(MBCA) and for a chemical pesticide (source: IBMA) ....................................................60
iv
List of Tables (continued)
Table 17:
Compared margin structure estimates for the production and sales of a
microbial biocontrol agent (MBCA) and a chemical pesticide (source IBMA) ....................61
Table 18:
Production systems selected for a survey of factors influencing biocontrol use
in Europe (source IBMA) ............................................................................................63
Table 19:
Geographical distribution of sampling sites for a survey of factors influencing
biocontrol use in Europe (source IBMA) .......................................................................63
Table 20:
Structure of the questionnaire used in a survey of European farmers and
retailers of biological control products ...........................................................................64
Table 21:
Impact of twelve factors on the future use of biocontrol agents by European
farmers according to a survey of 320 farmers .................................................................66
v
List of Figures
Figure 1:
Evolution of the yearly number of publications dedicated to biological control
of plant diseases based on a survey of the CAB Abstracts® database. .................................1
Figure 2:
Range of efficacy of 157 microbial biocontrol agents against five main types
of airborne diseases. Detailed data are presented in Table 4.............................................10
Figure 3:
Number of papers per year published during 1998-2008 concerning
augmentative biological control of pests in grapevine......................................................13
Figure 4:
Groups of biocontrol agents investigated in augmentative biological control
researches in grapevine. Number of references for each group is reported..........................19
Figure 5:
Groups of target pests investigated in augmentative biological control
researches in grapevine. Number of references for each group is reported..........................19
Figure 6:
Large-scale temporal survey of the publications associated with classical
biological control ........................................................................................................26
Figure 7:
Relative importance of the different types of biocontrol during the temporal
frame [1999-2008] ......................................................................................................27
Figure 8:
Number of pest species and related citation rate by orders during the period
[1999 ; 2008] .............................................................................................................28
Figure 9:
Relationships between the number of publications associated to the main
pests and the relative percentage of ClBC related studies. ................................................29
Figure 10:
Frequencies of papers and associated median IF related to the different
categories of work ......................................................................................................30
Figure 11:
Estimated sales of biocontrol products in Europe in 2008 (in Million €). The
estimates were obtained by extrapolating use patterns in a representative
sample of EU farmers..................................................................................................64
Figure 12:
Estimated distribution of biocontrol use among types of crops in 2008 in
Europe ......................................................................................................................65
vi
Contents
Chapter 1
Potential of biological control based on published research.
1. Protection against plant pathogens of selected crops...................................................1
P. C. Nicot, M. Bardin, C. Alabouvette, J. Köhl and M. Ruocco
Chapter 2
Potential of biological control based on published research.
2. Beneficials for augmentative biocontrol against insect pests. The
grapevine case study .......................................................................................................12
M. Giorgini
Chapter 3
Potential of biological control based on published research.
3. Research and development in classical biological control with
emphasis on the recent introduction of insect parasitoids .......................................20
N. Ris and J.C. Malausa
Chapter 4
Registered Biocontrol Products and their use in Europe ...................................................34
U. Heilig, P. Delval and B. Blum
Chapter 5
Identified difficulties and conditions for field success of biocontrol.
1. Regulatory aspects ................................................................................................. 42
U. Heilig, C. Alabouvette and B.Blum
Chapter 6
Identified difficulties and conditions for field success of biocontrol.
2. Technical aspects: factors of efficacy ...........................................................................45
M. Ruocco, S. Woo, F. Vinale, S. Lanzuise and M. Lorito
Chapter 7
Identified difficulties and conditions for field success of biocontrol.
3. Economic aspects: cost analysis ....................................................................................58
B. Blum, P.C. Nicot, J. Köhl and M. Ruocco
Chapter 8
Identified difficulties and conditions for field success of biocontrol.
4. Socio-economic aspects: market analysis and outlook ..............................................62
B. Blum, P.C. Nicot, J. Köhl and M. Ruocco
Conclusions and perspectives
Perspectives for future research-and-development projects on biological
control of plant pests and diseases.................................................................................. 68
P.C. Nicot, B. Blum, J. Köhl and M. Ruocco
vii
Appendices....................................................................................................................... 71
For Chapter 1
Appendix 1.
Inventory of biocontrol agents described in primary literature
(1998-2008) for successful effect against Botrytis sp. in laboratory
experiments and field trials with selected crops ...........................................72
Appendix 2.
Inventory of biocontrol agents described in primary literature
(1998-2008) for successful effect against powdery mildew in
laboratory experiments and field trials with selected crops. .......................102
Appendix 3.
Inventory of biocontrol agents described in primary literature
(1973-2008) for successful effect against the rust pathogens in
laboratory experiments and field trials with selected crops.........................111
Appendix 4.
Inventory of biocontrol agents described in primary literature
(1973-2008) for successful effect against the downy mildew / late
blight pathogens in laboratory experiments and field trials with
selected crops ............................................................................................115
Appendix 5.
Inventory of biocontrol agents described in primary literature
(1973-2008) for successful effect against Monilinia in laboratory
experiments and field trials with selected crops .........................................122
Appendix 6.
Primary literature (2007-2009) on biological control against
Fusarium oxysporum .................................................................................128
For Chapter 2
Appendix 7.
Number of references retrieved by using the CAB Abstracts
database in order to review scientific literatures on augmentative
biological control in selected crops for Chapter 2. .....................................139
Appendix 8.
Collection of data on augmentative biological control of pests in
grapevine. Each table refers to a group of biocontrol agents.......................141
For Chapter 3
Appendix 9.
References on classical biological control against insect pests
(cited in Chapter 3)....................................................................................152
For Chapter 4
Appendix 10. Substances included in the "EU Pesticides Database" as of April 21
2009 ..........................................................................................................163
Appendix 11. Invertebrate beneficials available as biological control agents
against invertebrate pests in five European countries. ................................171
viii
Chapter 1
Potential of biological control based on published research.
1. Protection against plant pathogens of selected crops
Philippe C. Nicot1, Marc Bardin1, Claude Alabouvette2, Jürgen Köhl3 and Michelina Ruocco4
1
INRA, UR407, Unité de Pathologie Végétale, Domaine St Maurice, 84140 Montfavet, France
INRA, UMR1229, Microbiologie du Sol et de l'Environnement, 17 rue Sully, 21000 Dijon, France
3
Wageningen UR, Plant Research International, Droevendaalsesteeg 1, P.O. Box 69, 6700 AB
Wageningen, The Netherlands
4
CNR-IPP, Istituto pel la Protezione delle Piante, Via Univrsità 133, Portici (NA) Italy
2
Evolution of the scientific literature
The scientific literature published between 1973 and 2008 comprises a wealth of studies on
biological control against diseases and pests of agricultural crops. A survey of the CAB Abstracts®
database shows a steady increase in the yearly number of these publications from 20 in 1973 to over
700 per year since 2004 (Figure 1).
Number of publications per year
900
800
700
600
500
400
300
200
100
0
1970
1975
1980
1985
1990
1995
2000
2005
2010
Publication year
Figure 1: Evolution of the yearly number of publications dedicated to biological control of plant
diseases based on a survey of the CAB Abstracts® database.
This survey was further refined by entering keywords describing some of the major plant
pathogens/diseases of cultivated crops in Europe, alone or cross-referenced with keywords
indicating biocontrol. Among studies published in the period between 1973 and 2008 on these
plant pathogens and pests, the percentage dedicated to biological control was substantial, but
unequally distributed (Table 1). It was notably higher for studies on soil-borne (9.5% ± 1.6% as
average ± standard error) than for those on air-borne diseases (2.8% ± 0.7%).
1
Nicot et al.
Table 1: Scientific papers published between 1973 and 2008 on biological control against major
plant diseases (from CAB Abstracts® database).
Disease or plant pathogen
Total number
of references
References on biological control
%
Soil-borne:
Fusarium
Rhizoctonia
Verticillium
Pythium
Sclerotinia
Air-borne:
rusts
powdery mildews
Alternaria
anthracnose
Botrytis
downy mildews
Phytophthora infestans
Monilia rot
Venturia
34 818
10 744
7 585
5 772
5 545
1 925
1 278
592
821
456
5.5
11.9
7.8
14.2
8.2
29 505
18 026
12 766
12 390
9 295
8 456
5 303
1 861
3 870
360
251
415
351
705
80
61
81
104
1.2
1.4
3.3
2.8
7.5
1.0
1.1
4.3
2.7
Inventory of potential biocontrol agents (microbials, botanicals, other natural
compounds)
The scientific literature described above was further examined to identify biocontrol compounds
and microbial species reported to have a successful effect. Due to the great abundance of
references, it was not possible to examine the complete body of literature. The study was thus
focused on several key diseases selected for their general importance on cultivated crops, and in
particular on those crops studied in the case studies of the European Network for Durable
Exploitation of crop protection strategies (ENDURE*).
Methodology
Three steps were followed. The first step consisted in collecting the appropriate literature references
for the selected key diseases/plant pathogens to be targeted by the study. The references were
extracted from the CAB Abstracts® database and downloaded to separate files using version X1 of
EndNote (one file for each target group). The files were then distributed among the contributors of
this task for detailed analysis.
In the second step, every reference was examined and we recorded for each:
- the types of biocontrol agents (Microbial, Botanical or Other compounds) under study and their
Latin name (for living organisms and plant extracts) or chemical name
- the Latin name of the specifically targeted pathogens,
- the crop species (unless tests were carried out exclusively in vitro),
- the outcome of efficacy tests.
Two types of efficacy tests were distinguished: Controlled environment tests (including tests on
plants and in vitro tests), and field trials. The outcome of a test was rated (+) if significant effect
was reported, (0) if no significant efficacy was shown and (-) if the biocontrol agent stimulated
disease development.
*
EU FR6 project 031499, funded in part by the European Commission
2
Chapter 1
To allow for the analysis of a large number of references, the abstracts were examined for the
presence of the relevant data. The complete publications were acquired and examined only when
the abstracts were not sufficiently precise.
The data were collected in separate tables for each type of key target pest. For each table, they
were sorted (in decreasing order of priority) according to the type and name of the biocontrol
agents, the specifically targeted pest, and the outcome of efficacy tests.
In the third step, synthetic summary tables were constructed to quantify the number of different
biocontrol compounds and microbial species and strains reported to have successful effect against
each type of key pathogen/disease or pest target.
Results
A total number of 1791 references were examined for key airborne diseases including powdery
mildews, rusts, downy mildews (+ late blight of Potato/Tomato) and Botrytis and Monilia rots,
together with soilborne diseases caused by Fusarium oxysporum (Table 2). Based on the
examination of these references, successful effect in controlled conditions was achieved for all
targets under study with a variety of species and compounds (Appendices 1 to 6, Table 3).
Table 2:
Numbers of references on biocontrol examined per group of disease/plant pathogen.
Target disease / plant
pathogen
Relevance to
ENDURE Case
Studies
Number of
references
examined
Period of
publication
examined
Botrytis
OR, FV, GR*
(postharvest)
880
1998-2008
Powdery mildews
all
166
1998-2008
Rusts
AC, FV, OR
154
1973-2008
Downy mildews +
FV, GR, PO, TO
349
1973-2008
Phytophthora infestans
Monilinia rot
OR
194
1973-2008
Fusarium oxysporum
FV, TO
48
2007-2009
*AC: Arable Crops; FV: Field Vegetables; GR: Grapes; OR: orchard; PO: Potato; TO: Tomato
Concerning airborne diseases and pathogens, the largest number of reported successes was
achieved with microbials, but there is a growing body of literature on plant and microbial extracts,
as well as other types of substances (Table 3). On average, reports of success were far more
numerous for experiments in controlled conditions (in vitro or in planta) than for field trials.
Very contrasted situations were also observed depending on the type of target
disease/pathogen, with rare reports on the biocontrol of rusts and mildews compared to Botrytis,
despite the fact that the literature was examined over a 35 year period for the former diseases and
only over the last 10 years for the latter.
In total in this review, 157 species of micro-organisms have been reported for significant
biocontrol activity. They belong to 36 genera of fungi or oomycetes, 13 of yeasts and 25 of
bacteria. Among them, 29 species of fungi/oomycetes and 18 bacteria were reported as successful in
the field against at least one of the five key airborne diseases included in this review (Table 4).
3
Nicot et al.
Table 3:
Numbers of different biocontrol compounds and microbial species reported as having
successful effect against key airborne pathogens/diseases of selected crops. Detailed
information and associated bibliographic references are presented in Appendices 1 to 5
Target plant pathogen /
disease
Botanicals
laboratory
field trials
testsx
Microbialsy
laboratory
field trials
testsx
Othersz
laboratory
field trials
testsx
Botrytis
in vitro
26
31 b, 21 f
legumes
4
10 b, 12 f
2
protected vegetables
0
22 b, 24 f
1
strawberry
0
14 b, 21 f
0
field vegetables
0
5 b, 15 f
0
grapes
1
5 b, 27 f
3
pome/stone fruits
1
12 b, 35 f
0
others
3
15 b, 25 f
0
Powdery mildews
Grape
1
4b; 10f
1
Arable crops
1
2b;9f
0
Strawberry
0
4b; 6f
0
Cucurbitaceae
4
14b; 22f
0
Pome/stone fruits
0
3f
0
Pepper
1
4f
0
Tomato
5
4b; 5f
0
Various
2
2b; 10f
0
Rusts
arable crops
0
5 b, 6 f
0
others
0
8 b, 13 f
0
Downy mildews + late
blight
grapes
2
2f
4
field vegetables
0
4
0
potato
9
8 b, 10 f
1
tomato
2
5 b, 5 f
1
Monilia rot
in vitro
0
8
pome fruit
0
7
0
stone fruit
0
23b, 19
1
others
0
1b
0
x
tests conducted in vitro and/or in planta in controlled conditions
y
b: bacteria; f: fungi / oomycetes / yeasts
z
including culture filtrates and extracts from microorganisms
4
3b, 9 f
8 b, 9 f
2 b, 13 f
2f
5 b, 13 f
2 b, 6 f
6 b, 6 f
7
0
5
7
0
0
4
0
0
1
1
0
1
0
0
2b; 12f
1b
0
4b; 9f
1f
0
1f; 1b
1b; 1f
3
5
0
9
0
1
0
5
2
0
0
1
0
0
0
0
2b
0
2
1
0
0
3 b, 2 f
0
5 b, 4 f
4b
2
4
3
12
3
6
1
1
0
7b, 7f
2b, 1f
1
0
2
0
0
2
0
Chapter 1
Table 4:
Microbial species of fungi/oomycetes, yeasts and bacteria reported to have a significant
effect against five main types of airborne diseases or pathogens in laboratory conditions
or in the field (yellow highlight). Bibliographic references are presented in Appendices 1
to 5.
A. Fungi and oomycetes
Microbial species
Botrytis
Acremonium spp.
Acremonium alternatum
A. cephalosporium
A. obclavatum
Alternaria spp.
A. alternata
others
grapes
Coniothyrium spp.
C. minitans
Cylindrocladium
Drechslera hawaiinensis
Epicoccum sp
E. nigrum
E. purpurascens
Filobasidium floriforme
Fusarium spp.
F. acuminatum
F. chlamydosporum
F. oxysporum
F. proliferatum
Galactomyces geotrichum
cereals
others
grapes
others
tomato
others
fruits, grapes,
strawberry,
protected
vegetables,
others,
protected vegetables
legumes
grapes
legumes
flowers
others
others
flowers, legumes
flowers
others
others
strawberry
C. tenuissimum
Clonostachys rosea
Monillia rot
grapes
Ampelomyces quisqualis
Aspergillus spp.
A. flavus
Beauveria sp
Botrytis cinerea nonaggressive strains
Chaetomium cochlioides
C. globosum
Cladosporium spp.
C. chlorocephalum
C. cladosporioides
C. oxysporum
Target disease / pathogen
Powdery
Downy mildew,
Rust
mildew
late blight
others
cereals,
protected
vegetables
others
field vegetables,
others
flowers, legumes,
others, strawberries,
field vegetables,
protected vegetables,
grapes
field vegetables
others
others
flowers, grapes, field
vegetables
legumes, strawberries
plum, peach
apple, cherry
fruits
flowers
others
cereals
others
cereals
fruits
5
tomato
grapes
Nicot et al.
Table 4 (continued)
Gliocladium spp.
G. catenulatum
G. roseum
G. virens
G. viride
grapes, protected
vegetables, others
protected vegetables,
legumes
flowers, grapes,
legumes, others
strawberries, field
vegetables
protected vegetables
L. longisporum
Meira geulakonigii
Microsphaeropsis ochracea
Muscodor albus
Paecilomyces farinosus
P. griseofulvum
potato, others
protected vegetables,
protected vegetables
field vegetables
fruits, grapes
peach
cereals
protected
vegetables
P. fumorosoroseus
Penicillium spp.
P. aurantiogriseum
P. brevicompactum
P. frequentans
blueberry
protected
vegetables
protected
vegetables
protected
vegetables
Lecanicillium spp.
Microdochium dimerum
others
fruits, field vegetables
legumes
legumes
others
plum, peach
legumes, field
vegetables
peach
P. purpurogenum
P. viridicatum
Phytophthora cryptogea
potato
potato
grapes,
protected
vegetables,
Pseudozyma floculosa
Pythium oligandrum
P. paroecandrum
P. periplocum
Rhizoctonia
Scytalidium
S. uredinicola
Sordaria fimicola
Tilletiopsis spp.
T. minor
Trichoderma spp.
T. asperellum
T. atroviride
T. hamatum
T. harzianum
T. inhamatum
T. koningii
potato, tomato
potato
protected vegetables
grapes
grapes
flowers
grapes
potato
others
apple
grapes
others
flowers, grapes,
legumes, strawberries,
protected vegetables,
others
strawberries
legumes, strawberries
flowers, legumes
flowers, grapes,
legumes, strawberries,
field vegetables,
protected vegetables,
others
flowers
strawberries, field
vegetables
potato
peach
others,
strawberry,
protected
vegetables,
others
grapes, potato,
tomato, field
vegetables,
others
cherry, peach
peach
others
T. lignorum
6
Chapter 1
Table 4 (continued)
T. longibrachiatum
T. polysporum
T. taxi
T. virens
T. viride
Trichothecium
T. roseum
Ulocladium sp.
U. atrum
U. oudemansii
Ustilago maydis
Verticillium
V. chlamydosporium
V. lecanii
strawberries
strawberries
protected vegetables
grapes
fruits, grapes, legumes,
strawberries, field
vegetables, others
grapes
grapes, legumes
grapes, field vegetables
flowers, grapes,
strawberries, field
vegetables, protected
vegetables
grapes
protected vegetables
grapes
strawberries
apple
others
others
potato, others
peach
legumes
cereals
cereals,
protected
vegetables,
others
legumes, others
B. Yeasts
Microbial species
Aureobasidium pullulans
Candida spp.
C. butyri
C. famata
C. fructus
C. glabrata
C. guilliermondii
C. melibiosica
C. oleophila
C. parapsilosis
C. pelliculosa
C. pulcherrima
C. reukaufii
C. saitoana
C. sake
C. tenuis
Cryptococcus albidus
C. humicola
C. infirmo-miniatus
C. laurentii
Debaryomyces hansenii
Hanseniaspora uvarum
Kloeckera spp
K. apiculata
Metschnikowia fructicola
M. pulcherrima
Pichia anomala
Botrytis
Target disease / pathogen
Powdery
Downy mildew,
Rust
mildew
late blight
fruits, grapes,
strawberries, protected
vegetables
Monillia rot
apple, cherry
tomato
fruits
fruits
strawberries
strawberries
grapes, protected
vegetables
fruits
fruits, grapes,
strawberries, protected
vegetables
fruits
protected vegetables
fruits, strawberries
strawberries
fruits
fruits
fruits
fruits, strawberries,
protected vegetables
fruits
fruits
fruits, strawberries,
protected vegetables
fruits, grapes
grapes
grapes
fruits
fruits, grapes,
strawberries
fruits
grapes, fruits
peach
cherry
cherry
cherry, peach
cherry, peach
cherry, peach
apple, apricot
7
Nicot et al.
Table 4 (continued)
fruits, strawberries,
protected vegetables
P. membranaefaciens
grapes
P. onychis
field vegetables
P. stipitis
fruits
Rhodosporidium diobovatum protected vegetables
R. toruloides
fruits
Rhodotorula
flowers, fruits,
R. glutinis
strawberries, protected
vegetables
R. graminis
flowers
R. mucilaginosa
flowers
R. rubra
protected vegetables
P. guilermondii
peach
field vegetables,
protected
vegetables
Saccharomyces cerevisiae
fruits
Sporobolomyces roseus
Trichosporon sp.
fruits
fruits
fruits, grapes, protected
vegetables
T. pullulans
peach
C. Bacteria
Target disease / pathogen
Microbial species
Acinetobacter lwoffii
Azotobacter
Bacillus spp.
B. amyloliquefaciens
B. cereus
B. circulans
B. lentimorbus
B. licheniformis
B. macerans
B. marismortui
B. megaterium
B. pumilus
B. subtilis
B. thuringiensis
Bakflor (consortium of
valuable bacterial
physiological groups)
Brevibacillus brevis
Burkholderia spp.
B. cepacia
B. gladii
B. gladioli
Cedecea dravisae
Cellulomonas flavigena
Botrytis
Powdery
mildew
Rust
Downy
mildew, late
blight
Monillia rot
grapes
other
grapes, strawberry,
protected vegetables,
others
arable crops, flowers,
fruits, field vegetables,
protected vegetables
flowers, legumes
protected vegetables
protected
vegetables
others
potato, field
vegetables
apricot
peach
others
tomato
others
fruits, strawberry,
protected vegetables
legumes
strawberry
legumes, others
fruits, strawberry
flowers, fruits, grapes,
legumes, strawberry,
field vegetables,
protected vegetables
tomato, others
cereals,
grapes,
strawberry,
protected
vegetables,
others
legumes
grapes, potato,
others
apricot,
blueberry,
cherry, peach
strawberry
protected vegetables
field vegetables,
protected vegetables
grapes,
protected
vegetables
grapes
tomato
protected vegetables
cherry
apricot
flowers
others
tomato
8
Chapter 1
Table 4 (continued)
Cupriavidus campinensis
grapes, protected
vegetables, others
protected
vegetables
Enterobacter cloacae
Enterobacteriaceae
Erwinia
Halomonas sp.
H. subglaciescola
Marinococcus halophilus
Salinococcus roseus
Halovibrio variabilis
Halobacillus halophilus
H. litoralis
H. trueperi
Micromonospora coerulea
Paenibacillus polymyxa
Pantoea spp.
P. agglomerans
Pseudomonas spp.
P. aeruginosa
P. aureofasciens
P. cepacia
P. chlororaphis
P. corrugata
P. fluorescens
P. putida
P. syringae
P. reactans
P. viridiflava
Rhanella spp.
R aquatilis
Serratia spp.
S. marcescens
S. plymuthica
Stenotrophomonas
maltophilia
Streptomyces spp.
S. albaduncus
S. ahygroscopicus
S. exfoliatus
S. griseoplanus
S. griseoviridis
S. lydicus
S. violaceus
Virgibacillus marismortui
Xenorhabdus bovienii
X. nematophilus
potato
strawberry
fruits, others
strawberry, protected
vegetables
protected vegetables
protected vegetables
protected vegetables
protected vegetables
protected vegetables
protected vegetables
protected vegetables
protected vegetables
strawberry, protected
vegetables
grapes, protected
vegetables
fruits, grapes,
legumes, strawberry
apple, apricot,
blueberry,
cherry, peach,
plum
legumes
flowers, fruits, grapes,
field vegetables
protected vegetables
others
potato, tomato,
field vegetables
cherry
peach
cherry
peach
cereals
strawberry
strawberry
fruits, grapes,
legumes, strawberry,
protected vegetables,
others
flowers, legumes,
protected vegetables,
others
fruits, strawberry, field
vegetables
cereals, ,
protected
vegetables
others
apricot
legumes
grapes, potato,
tomato, others
blueberry,
cherry
cereals
grapes
apple, peach
strawberry
fruits
potato
fruits
potato
flowers
protected vegetables
legumes
tomato
legumes
protected vegetables
legumes
legumes
protected vegetables,
others
protected vegetables
legumes
strawberry
potato
protected
vegetables
9
Nicot et al.
Number of species
One striking aspect of this inventory is that although the five target diseases / pathogens
included in our review are airborne and affect mostly the plant canopy, the vast majority of cited
biocontrol microorganisms are soil microorganisms. The scarcity of biocontrol agents originating
from the phyllosphere could be due to actual lack of effectiveness, or it could be the result of a bias
by research groups in favour of soil microbes when they gather candidate microorganisms to be
screened for biocontrol activity. This question would merit further analysis as it may help to devise
improved screening strategies. As "negative" results (the lack of effectiveness of tested
microorganisms, for example) are seldom published, the completion of such an analysis would in
turn necessitate direct information from research groups who have been implicated in screening for
biocontrol agents, or the development of a specific screening experiment comparing equal numbers
of phyllosphere and of soil microbial candidates.
Another striking aspect is that most of the beneficial micro-organisms inventoried in this study
(49 fungi/oomycetes, 28 yeasts and 41 bacteria) are cited only for biocontrol of one of the five types
of airborne diseases included in the survey (Figure 2). However, several species clearly stand out
with a wide range of effectiveness, as they were successfully used against all five types of target
diseases on a variety of crops. This includes the fungi Trichoderma harzianum and Trichoderma
viride (2 of 12 species of Trichoderma reported as biocontrol-effective in the reviewed literature)
and the bacteria Bacillus subtilis and Pseudomonas fluorescens.
50
45
40
35
30
25
20
15
10
5
0
fungi / oomycetes
yeasts
bacteria
1
2
3
4
5
Number of controlled target diseases / pathogens
Figure 2: Range of efficacy of 157 microbial biocontrol agents against five main types of airborne
diseases. Detailed data are presented in Table 4.
Concerning Fusarium oxysporum. A data base interrogation with the key words “Fusarium
oxysporum AND biological control” provided 2266 for the period 1973-2009. Using these key
words we did not select only papers regarding biological control of diseases induced by F.
oxysporum but also all the paper dealing with the use of strains of F. oxysporum to control diseases
and weeds. There are quite many papers dealing with the use of different strains of F. oxysporum to
control Broom rape (orobanche) and also the use of F. oxysporum f. sp. erythroxyli to eradicate
coca crops.
We decided to limit our review to the two last years and to concentrate on references for which
full text was available on line. Finally we reviewed 48 papers. All these papers were dealing with
the selection and development of micro-biological control agents; only two were considering others
methods. One was addressing the use of chemical elicitors to induce resistance in the plant; the
10
Chapter 1
other was aiming at identifying the beneficial influence of non-host plant species either used in
rotation or in co-culture. Based on this very limited number of papers the formae speciales of F.
oxysporum the most frequently studied was F.o. f. sp. lycopersici (17 studies). Other included f. spp.
melonis, ciceris, cubense, niveum and cucumerinum. The antagonists studied included Bacillus spp
and Paenibacillus (16 papers), Trichoderma spp. (14 papers), fluorescent Pseudomonads (7 papers),
Actinomycetes (5 papers), non pathogenic strains of F. oxysporum (5 papers), mycorrhizal fungi
and Penicillium.
Most of the publications (28) reported on in vitro studies. Among them a few concerned the
mechanisms of action of the antagonists, the others just related screening studies using plate
confrontation between the antagonists and the target pathogens. In most of these papers (22) the in
vitro screening was followed by pot or greenhouse experiments aimed at demonstrating the capacity
of the antagonist to reduce disease severity or disease incidence after artificial inoculation of the
pathogen. Finally only 9 publications report results of field experiments. Most of these papers
concluded on the promising potential of the selected strains of antagonists able to decrease disease
incidence or severity by 60 to 90%. Generally speaking, this limited literature review showed that
most of the lab studies are not followed by field studies. There is a need for implementation of
biological control in the fields.
Identified knowledge gaps
Several types of knowledge gaps were identified in this review. They include:
- the near absence of information on biocontrol against diseases of certain important European
crops such as winter arable crops.
- the scarcity of reports on biocontrol against several diseases of major economic importance on
numerous crops, such as those caused by obligate plant pathogens (rusts, powdery mildews,
downy mildews)
- the still limited (but increasing) body of detailed knowledge on specific mechanisms of action
and their genetic determinism. The little knowledge available at the molecular level is
concentrated on few model biocontrol agents such as Trichoderma and Pseudomonas.
- the still very limited information on secondary metabolites produced by microbial biocontrol
agents
- the lack of understanding for generally low field efficacy of resistance-inducing compounds
- the lack of knowledge on variability in the susceptibility of plants pathogens to the action of
BCAs and on possible consequences for field efficacy and its durability.
References
Due to their high number, the references used in this chapter are presented, together with
summary tables, in Appendices 1 to 6.
11
Chapter 2
Potential of biological control based on published research.
2. Beneficials for augmentative biocontrol against insect pests.
The grapevine case study
Massimo Giorgini
CNR, Istituto per la Protezione delle Piante, via Università 133, 80055 Portici (NA), Italy
Bibliographic survey on augmentative biological control against arthropod pests in
selected crops
We carried out a preliminary bibliographic survey to quantify the literature on augmentative
biological control of pests published from 1973 to 2008. The survey was restricted to crops relevant
to case studies of ENDURE. They included grapevine; orchards: apple and pear; arable crops: corn
and wheat; field vegetables: carrot and onion. Augmentative biological control (Van Driesche &
Bellows, 1996) comprises of inoculative augmentation (control being provided by the offspring of
released organisms) and inundative augmentation (control expected to be performed by the
organisms released, with little or no contribution by their offspring).
Our bibliographic survey was conducted by using the CAB Abstracts database by entering the
name of each crop and one key word selected from the following list in order to retrieve the
maximum number of references. For each selected crop, the key words used for the bibliographic
survey were: a) augmentative biological control; b) augmentation biological control; c) inoculative
biological control; d) inundative biological control. The survey with these key words produced a
very low number of results all of which were examined. For this reason we added two key words
that were more general: e) insects biological control; f) mites biological control. For the searching
criteria a to d, total records will be examined. In this case, given the extremely high number of
records, only references within the period 1998-2008 were examined to select only the publications
concerning the augmentative biological control. The results of this survey are reported in Appendix
7.
The analytical review of the scientific literature on augmentative biological control, presented
in the rest of this chapter, was then focused on grapevine.
Status of researches on augmentation of natural enemies to control arthropod pests in
grapevine
The references extracted from the CAB Abstracts database, following the criteria described in the
previous paragraph, were examined to identify those concerning the use of natural enemies in
augmentation biological control in grapevine. The abstracts of 607 references were examined and
only 70 papers reported data on application and efficiency of augmentative biocontrol (Table 5).
12
Chapter 2
Table 5:
References extracted from the CAB Abstracts database and examined for reviewing
augmentation biological control in grapevine.
Key words
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total records
(1973-2008)
7
10
4
7
1998-2008
28
579
Total references examined
Total references showing data on
augmentative biocontrol
6
6
1
3
373
190
70
The survey includes records for grapevine, grape and vineyard.
Results
Very few papers (62) on augmentative biocontrol in grapevine have been published during the period 1998-2008, with
an average of 5.6 publications per year. Most references (93.5%) showed data on biological control of insects and only
4 papers on the biological control of mites were published (Figure 3).
Figure 3: Number of papers per year published during 1998-2008 concerning augmentative
biological control of pests in grapevine.
12
10
8
6
4
2
0
1998
1999
2000
2001
2002
2003
biocontrol of insect pests
2004
2005
2006
2007
2008
biocontrol of mite pests
The data extracted from the abstracts of the selected references were collected analytically in
separate tables for each group of biocontrol agents (Appendix 8) and references were sorted
chronologically (starting from the eldest). For each species of biocontrol agent, target species of
pest, Country, type of augmentation (inundative, inoculative), type of test (laboratory, field),
efficacy of biocontrol, additional information and results were reported.
13
Giorgini
Data reported in Appendix 8 were summarized in Table 6, Table 7, Table 8, Figure 4 and
Figure 5. A list of the biocontrol agents used in augmentative biological control in grapevine is
reported in Table 6 and Figure 4. A list of groups and species of the targeted pests and the
antagonists used for their control is reported in Table 7 and Figure 5; the efficacy of biocontrol
agents is reported in Table 8.
The group of pests on which the highest number of researches on augmentative biocontrol has
been carried out is Lepidoptera (60% of total references) with the family Tortricidae representing
the main target (55%) (Figure 5) including the grape berry moths key pests Lobesia botrana and
Eupecilia ambiguella (Table 7). Bacillus thuringiensis has resulted the most frequently used
biocontrol agent against Lepidoptera by achieving an effective control of different targets in
different geographic areas (Table 7, Table 8, Appendix 8.7). We sorted 28 references (39% of the
total citations) dealing with the use of B. thuringiensis of which 23 references were referred to the
control of L. botrana. The augmentation of egg parasitoids of the genus Trichogramma
(Hymenoptera: Trichogrammatidae) resulted the alternative strategy to B. thuringiensis to control
Lepidoptera Tortricidae (13 references, 16% of total citations) (Table 7, Table 8). Field evaluations
indicated T. evanescens as a promising biocontrol agent of L. botrana (El-Wakeil et al., 2008 in
Appendix 8.1).
Fewer researches were carried out on augmentative biocontrol of other group of pests. First in
the list were mealybugs (Hemiptera: Pseudococcidae) (9 references, 13% of the total citations). In
field evaluations (4 papers) parasitoid wasps of the family Encyrtidae have resulted extremely
active and promising to be used in augmentative biocontrol of mealybugs (Appendix 8.2).
Antagonists used in augmentative biocontrol in grapevine were mainly represented by insect
pathogens (59% of the total citations), including the bacterium B. thuringiensis, fungi and
nematodes (Figure 4, Table 6). Beside the efficacy of B. thuringiensis, promising results were
obtained from researches in the control of the grape phylloxera Daktulosphaira vitifolie, a gallforming aphid, by soil treatments with the fungus Metarhizium anisopliae (Table 8, Appendix 8.5).
Once controlled by grafting European grape cultivars onto resistant rootstocks, the grape phylloxera
has gone to resurgence in commercial vineyards worldwide and new biological control strategy
could be necessary to complement the use of resistant rootstocks and to avoid the distribution of
chemical insecticides in the soil.
Entomophagous arthropods, including parasitoid wasps and predators represented 41% of the
total citations (Figure 4, Table 6). Best results were obtained from researches on parasitoids (18
references), namely the use of Trichogrammatidae and Encyrtidae in augmentative biocontrol of
grape moths (Tortricidae) and mealybugs (Pseudococcidae) respectively (Table 7, Table 8,
Appendix 8.1 and 8.2). Among predators, augmentation of Phytoseiidae mites has produced some
positive results in controlling spider mites and eriophyid mites on grape (Table 7, Table 8,
Appendix 8.3).
Brief considerations
Key pests of grapevine like L. botrana and E. ambiguella can be controlled effectively with
augmentative strategies that rely on the use of B. thuringiensis. To date, formulations of B.
thuringiensis are currently used in IPM strategies. The specificity of B. thuringiensis could be a
problem in those vineyards where other pests can reach the status of economically importance, if
not controlled by indigenous and/or introduced natural enemies. Researches on augmentative
biocontrol should be implemented in order to develop new strategies to solve problems related to
emerging pests and alternatives to B. thuringiensis if resistant strains should appear in target
species.
References
Due to their high number, the references for this chapter are presented in Appendix 8.
14
Chapter 2
Table 6:
Biocontrol agents evaluated in researches on augmentative biological control of pests in
grapevine.
Target pests and biocontrol agents
References
before 1998
References
1998-2008
0
28
Number of
citations
BIOLOGICAL CONTROL OF INSECTS
Bacteria
[1 species: 2 subspecies]
- Bacillus thuringiensis
(subsp. kurstaki, subsp. aizawai)
Fungi
[5 species]
- Metarhizium anisopliae
- Beauveria bassiana
- Beauveria brongniartii
- Verticillium lecanii
- Clerodendron inerme
Nematodes
[5 species]
- Steinernema spp.
2 spp.
- Heterorabditis spp.
3 spp.
Parasitoid Hymenoptera
[15 species]
- Trichogramma spp. (Trichogrammatidae) 10 spp
- Coccidoxenoides spp. (Encyrtidae)
2 spp.
- Anagyrus spp. (Encyrtidae)
2 spp.
- Muscidifurax raptor (Pteromalidae)
1 spp.
Predators
[5 species]
- Chrysoperla (Neuroptera: Chrysopidae)
3 spp.
- Cryptolaemus montrouzieri
(Coleoptera: Coccinellidae)
- Nephus includens (Coleoptera: Coccinellidae)
28
0
10
7
2
1
1
1
1
3
2
3
2
16
13
2
3
1
2
4
3
2
1
BIOLOGICAL CONTROL OF MITES
Predators (Acari: Phytoseiidae)
- Typhlodromus pyri
- Kampimodromus aberrans
- Amblyseius andersoni
- Phytoseiulus persimilis
2
[4 species]
4
5
2
1
1
15
Giorgini
Table 7:
Number of references on augmentative biocontrol agents per group and species of target pest in grapevine.
Pest
Lepidoptera:
Tortricidae
Lobesia botrana
(grape berry moth)
Eupoecilia ambiguella
(grape berry moth)
Epiphyas postvittana
(light brown apple moth)
Argyrotaenia sphaleropa
(South American tortricid moth)
Bonagota cranaodes
(Brasilian apple leafroller)
Endopiza viteana
(grape berry moth)
Sparganothis pilleriana
(grape leafroller)
Epichoristodes acerbella
(South African carnation tortrix)
Lepidoptera:
Pyralidae
Cryptoblabes gnidiella
(honey moth)
Lepidoptera:
Arctiidae
Hyphantria cunea
(fall webworm)
Lepidoptera:
Sesiidae
Vitacea polistiformis
References
Bacillus
thuringiensis
(2 subspecies)
Trichogramma
(10 species)
28
23
5
6
3
3
other
parasitoids
(5 species)
Predators of
mites
Acari:
Phytoseidae
(4 species)
Predators of
insects
Coleoptera:
Coccinellidae
(2 species)
Predators of
insects
Neuroptera:
Chrysopidae
(3 species)
Fungi
(5 species)
Nematodes
(5 species)
39
3
3
3
1
2
2
2
2
2
1
1
1
1
1
1
1
1
1
2
2
2
16
Chapter 2
Table 7 (continued)
Hemiptera:
Pseudococcidae
Planococcus ficus
9
Pseudococcus maritimus
Pseudococcus longispinus
Maconellicoccus hirsutus
1
Hemiptera:
Cicadellidae
Erythroneura variabilis
Erythroneura elegantula
Hemiptera:
Phylloxeridae
Daktulosphaira vitifoliae
(grape phylloxera)
Diptera:
Tephritidae
Ceratitis capitata
3
Coleoptera:
Scarabeidae
Melolontha melolontha
Thysanoptera:
Thripidae
Frankliniella occidentalis
grape thrips
Acari:
Tetranichidae
Panonychus ulmi
Tetranychus urticae
Tetranychus kanzawai
Eotetranychus carpini
Acari:
Eriophyidae
Calepitrimerus vitis
Calomerus vitis
2
6
4
Encyrtidae
2
1
1
1
Encyrtidae
1
3
3
5
3
3
4
1
2
3
1
1
2
1
6
2
1
1
1
1
Pteromalidae
5
1
1
2
2
5
1
1
2
1
1
1
1
17
Giorgini
Table 8:
Number of references reporting data on the efficacy of augmentative biocontrol of
pests in grapevine.
Groups of Pests
Biocontrol agents
Total
number of
references
Number of references reporting data
on efficacy in pest and related
damage control*
Laboratory assays
Field evaluation
2+
16 +
19+
1-
Bacillus thuringiensis
26
Trichogramma spp.
parasitoids
13
Lepidoptera:
Pyralidae
Bacillus thuringiensis
1
1+
Lepidoptera:
Arctiidae
Bacillus thuringiensis
1
1+
Lepidoptera:
Sesiidae
Nematodes
2
Hemiptera:
Pseudococcidae
Encyrtidae parasitoids
5
4+
Coccinellidae
Fungi
3
1
1 + (greenhouse)
1+
Hemiptera:
Cicadellidae
Chrysopidae
3
2-
Hemiptera:
Phylloxeridae
Nematodes
1
1+
Fungi
5
1+
2+
1-
Diptera:
Tephritidae
Pteromalidae parasitoids
1
1+
1+
Acari:
Tetranichidae
Phytoseidae
6
4+
Acari:
Eriophyidae
Phytoseidae
2
1+
Coleoptera:
Scarabeidae
Nematodes
1
1+
Fungi
Fungi
1
3
Lepidoptera:
Tortricidae
Thysanoptera:
Thripidae
1-
2+
1+
* + means effective, - means not effective biocontrol agent
18
1+
1 + (greenhouse)
1+
2+
Chapter 2
Bacillus thuringiensis: 28 (39%)
Fungi: 10 (14%)
Nematodes: 4 (6%)
Parasitoid Hymenoptera: 18 (25%)
Predators of insects (Chrysopidae,
Coccinellidae): 6 (8%)
Predators of mites (Phytoseidae): 6 (8%)
Figure 4: Groups of biocontrol agents investigated in augmentative biological control
researches in grapevine. Number of references for each group is reported.
Lepidoptera Tortricidae: 39 (55%)
Lepidoptera Sesiidae: 2 (3%)
Lepidoptera Arctiidae: 1 (1%)
Lepidoptera Pyralidae: 1 (1%)
Hemiptera Pseudococcidae: 9 (13%)
Hemiptera Phylloxeridae: 5 (7%)
Hemiptera Cicadellidae: 3 (4%)
Acari Tetranichidae and Eriophyidae: 6 (8%)
Thysanoptera Thripidae: 3 (4%)
Coleoptera Scarabeidae: 2 (3%)
Diptera Tephritidae: 1 (1%)
Figure 5: Groups of target pests investigated in augmentative biological control researches
in grapevine. Number of references for each group is reported.
19
Chapter 3
Potential of biocontrol based on published research.
3. Research and Development in classical biological control with
emphasis on the recent introduction of insect parasitoids
Nicolas Ris and Jean Claude Malausa
INRA, UE 1254, Unité expérimentale de Lutte Biologique, Centre de recherche PACA,
400 route des Chappes, BP 167, F-06903 Sophia Antipolis, France
Scope of the review
Defined as “the intentional introduction of an exotic, usually co-evolved, biological control
agent [hereafter BCA] for permanent establishment and long-term pest control’, classical
biological control [hereafter ClBC] is a pest control strategy that has crystallized numerous
studies since more than one century and provided numerous efficient solutions for pest
control. The main advantages and risks of this strategy can be summarized as follows. In a
context of the globalisation of international trade and human mobility, an ever growing
number of exotic pests emerge locally. Such species can rapidly pullulate and jeopardize
cultural practices. This general trend can also be favoured by global climatic changes that
may allow the development of agronomic pests beyond their initial distribution area and
increase their demography. Within this context, ClBC appears often to be the first way to try
to regulate such pest populations. Moreover, when successful, ClBC appears to be very
economic insofar as financial costs are only associated with the identification, evaluation and
initial releases of exotic BCA. Contrary to other pest control strategy, the implication of
practitioners and other costs are not necessary after the establishment of the BCA. The
overall financial costs of such operations are consequently rather limited with regard to the
durability of the pest control, in particular when the local introduction of a new BCA benefits
from the previous experiences in other countries. Nevertheless, at least two kinds of risks are
usually associated with ClBC. First of all, the average success rate of ClBC varies between
10 and 30% according to the authors for a total of more than 5000 introductions worldwide
during the last century. As consequence, such operations may also appear too risky to be
funded. Another risk is those associated with the non-target effects. Although few cases have
been reported, their echoes may have contributed to a more harmonized approach and in
some countries to more or less stringent regulations.
As consequences, classical biological programmes are at the crossroad of several
concerns:
- agronomic; insofar as each introduction of exotic BCA is obviously an hope for the
producers ;
- scientific; ClBC namely questions both ecologist and evolutionist in order to optimize the
probability of establishment while minimizing the non-target effects. Their implication on
such issues nevertheless depends on their own interest (in term of scientific question
and/or possibility or publishing);
- political; since the introduction of BCA may depend on regulation or homologation
decided at national or international levels;
20
Chapter 3
- financial; since the development of ClBC is relying on various sources of funding
(agronomic partners, scientific partners, politic institutions) with various interests and
rationale (more or less short-term results, scientific excellence versus applied objectives).
Within this context, global evaluations of ClBC programmes are necessary to better
understand the evolution of this practice and try to improve its use and efficiency. This has
been repeatedly achieved during the last years either through reviews or meta-analysis. Based
on a large (but probably not exhaustive) bibliographic survey, the present work aims to give a
complementary point of view with the willingness to portray a realistic “state of the art” of
Research and Development programmes of ClBC against arthropods. This chapter also firstly
gives a broad temporal survey of the publication and a more precise survey of the literature
for the decade [1999; 2008]. Biocontrol programmes against arthropods were then more
precisely detailed with the objectives to give qualitative cues about the main pests and the
types of related studies. Finally, a particular emphasis has been put on recent introductions of
exotic insect parasitoids.
Based on these data, we also address some more or less important subjective
recommendations based on our own opinion.
Method
A large bibliographic survey has been conducted with the CAB abstracts. Several
combinations of key-words were used with various successes. Too broad (e.g; cases for
which discussion about ClBC are marginal) or unprecise (e.g. cases for which a pest is not
precised) publications were excluded. A total of 764 publications were found using the keywords “classical biological control” or “classical biocontrol”. 452 papers were published
during the period [1999-2008] but about 30% were not relevant with regard to the purpose of
this survey and have been discarded. Using the more complex combinations [“biological
control” AND “exotic” AND “introduction”], 329 ClBC-related publications were obtained
but only 253 dressed precisely questions related to classical biological control. 117 were
published during the selected temporal frame but only 81 were relevant with regard to our
objectives. Additionally, 47 ClBC-related publications were obtained using the more keywords association [“biological control” AND “exotic” AND “importation”] with 17 papers
for the last ten years. Most of this literature was dedicated to the risk or regulatory aspects
associated with the importation of exotic BCA so that only 7 relevant publications with
regard to our objectives. Finally, 130 publications were found using “acclimatization” AND
“biological control” for only one relevant publication for the targeted period. A total of 358
publications were also obtained which is probably for far from being exhaustive. For
instance, 37 new references about BCA introductions were found in addition to the first 35
references found with the previous key-words combinations (see Table 9). Additional
bibliographic research were also realised for some taxa (see below)
[Remark: Although the terms “classical biological control” or “classical biocontrol”
may be not as explicit as others (“introduction”, “importation”), the generalization of their
use in titles, key-words or abstracts should be nevertheless used in order to improve the
efficiency of bibliographic survey]
21
Ris & Malausa
General trends
The temporal survey shows a quite regular increase of ClBC related publications with a mean
of about 45 hits / year for the last ten years (Figure 6). Within this period, we observe a
relative stability between the different combinations of pests and BCA (Figure 7). The main
part of the publications (56%) of the cases deals with the biocontrol of phytophagous
arthropods on which we will focus here. 42% of the papers deal with the biocontrol of weed.
In this case, BCA are for 57% of the cases phytophagous insects and for 41% fungi (data not
shown).
More than 70 arthropod pests were listed which cover 7 orders and approximately 40
families. As shown in Figure 8, Hemiptera and Lepidoptera were the two main orders with a
total of 66% of the pest species and 70% of the publications. If the citation rate / order is
highly correlated with the number of pests / order, this trend hides a great variability at the
infra-order level. Indeed, the citation rate highly differs with regard to the pest species with a
median of 2 papers / pest species and a range from 1 to 13 citations. The 13 most cited pests
are listed in Figure 9. Two main observations can be drawn from this short list.
Firstly, this list is quite equally composed of either very specialist pests like
Phyllocnistis citrella (on Citrus species), Mononychellus tanajoa (on cassava) or Toxoptera
citricida (on Citrus species) or more generalist taxa like Homalodisca vitripennis, Lymantria
dispar or Pseudococcus viburni. All of them are phytophagous pests whose damage are
linked either to their herbivory, consumption of sap or virus transmission except the
particular case of the fire ant Solenopsis invicta which is responsible for direct nuisance on
farmers or indirect ecological modifications in the agrosystems.
The second observation is that the percentage of ClBC related publications / pest is
negatively correlated with the corresponding total number of references (including also
studies on other pest control strategies and/or various biological topics). For instance, 22% of
the 32 references focusing on H. vitripennis explicitly deal with classical biological control
while this percentage falls down to only 1% to 3% for well documented species like L.
dispar, S. invicta or D. virgifera virgifera. This may be explained by the fact that ClBC is
mainly considered as a “pionneer” pest control strategy that are developed either soon after
the emergence of a new invasive pest or on “non biological model” for which the
investigations on other biological aspects are limited.
[Remark: Although Classical Biological Control can be perceived as a “pioneer”
pest control strategies on non “biological models”, substantial investments are required on
several biological aspects (e.g. community ecology, population genetics)]
Biocontrol agents used
The biocontrol agents related to ClBC (hereafter ClBCA) against arthropod species were not
detailed in only 12% of the papers. These are in most of the cases either prospective works
(55%) such as faunistic inventories of natural enemies on “new” pests like Diabrotica
virgifera virgifera or retrospective studies (35%) on advanced programmes that take into
account several BCA (see Appendix 9.1). Among the documented cases, 76% of ClBC
programmes were based on the use of insect parasitoids. Pathogens and nematodes on one
side and predatory arthropods on the other side are equally represented with about 12% of the
publications for each case.
22
Chapter 3
Pathogens and Nematodes as candidate for ClBCA
The particular cases of pathogens and nematodes have been recently reviewed by Hajek and
co-workers (62, 633). Our own survey indicates that half of the papers actually deal with
entomopathogenic fungi. Six pest species were identified including two mites (Aceria
guerreronis and Mononychellus tanajoa) and two insects (Aphis gossypii and Coptotermes
formosanus). However, except for the evaluation of Neozygites species against M. tanajoa
(14, 39, 42, 43), other attempts seem to be rather limited. With regard to the catalogue of
Hajek et al.(62), two other cases of entomopathogen fungi were missed in our own survey.
These are the introductions of Entomophaga maigmaiga and Metarhizium anisopliae, against
respectively the Lymantria dispar and the Curculionidae Otiorynchus nodosus for which the
sources of Hajek and coworkers were mainly personal communications. The rather limited
use of entomopathogenic fungi in ClBC was also confirmed by the review of Shah and
Pell(156). The use of viruses as biocontrol agent for ClBC against arthropod pests were only
documented fort three cases that are the Lepidoptera species Anticarsia gemmatalis (48, 127)
and Lymantria dispar (16) and the Coleoptera Oryctes rhinoceros (81). Microspodia as
candidate for ClBC were reported in only two studies (25, 165). The sole case of the use of
nematodes is the study of Hurley et al. (79) who studied the extension of the use of parasitic
nematode Deladenus siricidicola against the woodwasp Sirex noctilio.
Predatory arthropods as candidate for ClBCA
The literature about predatory arthropods is dominated by four case-studies. The first one is
the classical biocontrol of the cassava green mites M. tanajoa by Typhlodromalus aripo and,
to a lesser extent, T. manihoti. All these studies are the extension of a very large classical
biocontrol programme at a continental scale; two main issues were addressed during the
recent decade that are the introduction and field evaluation of T. aripo in Mozambique and
Malawi (125, 194) and the ecological interactions with other species (14, 124, 193) or
plants(55). The second case-study is those of the predatory ladybird Harmonia axyridis (19,
90, 91, 137). The main concern of these publications is nevertheless not the Research and
Development in ClBC but rather the risks of non-intended effects and geographic spray of
this insect that is now considered as a world-wide invasive species. Another case of the use of
ladybird is those of Cryptolaemus montrouzieri and Scymnus coccivora which have been
successfully used to control the hibiscus mealybug Maconellicoccus hirsutus (51, 86, 103)
which is the extension of a worldwide use of these species. The fourth main case-study is the
classical biocontrol programme of Prostephanus truncatus, a serious pest of stored maize
beetle using Teretrius (formerly Teretriosa) nigrescens (73, 169, 170). The lasts reported uses
of predatory arthropods as candidate for ClBC were those of the Coleoptera Laricobius
nigrinus against the adelgid Adelges tsugae (197) and the phytoseid Neoseiulus baraki
against the coconut mite A. guerreronis (119). Contrary to other cases which were the
continuity of older programmes, these two studies are associated with new BCA inventories
undertaken during the last ten years - see respectively (196) and(99).
Insect parasitoids as BCA
Related journals papers and categorization of the studies
In total, 125 publications were used for this analysis. Only 14% were associated to
proceedings of meetings or other supports than journals. 43 different journals were identified
but 50% of the publications were published only by five: Biological Control (21%),
BioControl (8%), Biocontrol Science and Technology (7%), Florida Entomologist (7%) and
3
within this Chapter, numbers in parentheses refer to references listed in Appendix 9
23
Ris & Malausa
Bulletin of Entomological Research (7%). Impact Factors are respectively 1.805, 1.957,
0.874, 0.886 and 1.415.
The types of the works were categorized according to the simplified sequential steps in
R&D of biological programmes: BCA Inventories BCA characterization (systematic,
molecular tools) Pest or BCA rearing BCA biology (life history traits, thermal biology,
behavioural ecology) Pre-release survey BCA introduction Post-release survey.
Studies related to “non-target effects” (i.e. the direct or indirect impacts of the ClBCA on
non-target species) as well as those related to the “biocontrol disruption” (i.e. the negative
impacts of organisms on the ClBCA) (details in Appendix 9.3) were also categorized. As
shown in Figure 10, most of the ClBC related publications logically deals either with BCA
biology, BCA introductions or post-release surveys which are central steps of the ClBC
programmes. A strong discrepancy nevertheless exists between the different types of work in
term of scientific publication; highest Impact Factors are relied to studies linked to Nonintended effects, Biocontrol disruption or BCA Biology.
[Remark: The different steps of R&D in Classical Biological Control are currently
unequally promoted with regard to “scientific criteria”, with a clear emphasis on community
ecology including non target effects. Such trend may be detrimental to the short-term
development of less gratifying tasks and consequently on the whole dynamism of ClBC.]
BCA Introductions
As shown in Table 9, 65 introductions were recorded during the period of 1991-2006. This
list is probably not exhaustive insofar as “cryptic introductions” may have been missed. This
list does not also cover all the R&D in classical biocontrol programmes since some
programmes may have been interrupted before releases. A faunistic inventory of the natural
enemies of the North American leafhopper Scaphoideus titanus has for instance been led by
our lab in 2000-2002 but the rearing of BCA candidates (mainly dryinids and eggparasitoids) were not successful.
All these releases involve 55 different biocontrol agents (all hymenopteran except
the Pseudacteon species used against the fire ant Solenopsis invicta) and 35 pests. 57% of
these pests were Hemiptera, other being quite equally distributed between Lepidoptera,
Diptera, Hymenoptera and Coleoptera.
Most of these introductions were realized against pest found on orchards and in
particular Citrus. Other targeted crops were mainly tropical productions, ornamental or forest.
Most of the BCA introductions (42%) were realized in Europe or neighbouring
countries (including Mediterranean Basin) and in North America (26%). The percentages of
introductions in other geographical areas were: Australia-New Zealand and neighbouring
islands (12%), South America (8%), sub-Saharan Africa (8%), Pacific Islands (3%), Asia
(1%).
The total number of released parasitoids and number of sites were highly variable
ranging respectively from 456 to 660000 individuals and from 2 to 132 sites. The percentage
of establishment was 83% and, when established, high parasitism was found in 42% of the
cases. It is noteworthy that these values are relatively high compared to other estimates and
we are currently unable to say if this is linked to an improvement of practices or
methodological differences or biases.
[Remark: With regard to natural or other human-mediated introductions of exotic
species, species flow associated with the ClBC seems to be rather limited. Although possible
non-intended effects cannot be excluded (their studies having to be increased), we fear that
too drastic regulations could severely disturbed R&D programmes]
24
Chapter 3
[Remark: Estimating the success of ClBC is difficult because of methodological
several biases (“cryptic introductions”, barriers linked to languages and/or publishing).
Shared international database should be necessary for more accurate estimation as well as
an increasing traceability.]
[Remark: In parallel with the geographical expansion of their related pests, some
biocontrol agents have been repeatedly released and established worldwide. Population
genetics studies in such pest-BCA interactions should be particularly interesting to
understand local adaptations, co-evolutionary processes and ultimately, the durability of
Classical Biological Control.]
25
Ris & Malausa
70
60
50
40
30
20
1973
1974
1975
1976
1977
1978
1979
1980
1981
1982
1983
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
10
0
26
Figure 6: Large-scale temporal survey of the publications associated with classical
biological control
Publications in CabAbstracts
Chapter 3
100%
80%
P = Phytophagous arthropod ; BCA = not documented
60%
P = Phytophagous arthropod ; BCA = Pathogen
P = Phytophagous arthropod ; BCA = Predator
P = Phytophagous arthropod ; BCA = Parasitoid
40%
P = Other animals
P = Weed
20%
0%
1999
2000
2001
2002
2003
2004
2005
2006
2007
2008
Figure 7: Relative importance of the different types of biocontrol during the temporal frame [1999-2008]
27
Ris & Malausa
0,5
Hemiptera
Percentage of citations
0,4
0,3
Lepidoptera
0,2
0,1
Coleoptera
Acari
Diptera
Hymenoptera
Thysanoptera
0,0
0,0
0,1
0,2
0,3
0,4
0,5
Percentage of pests
Figure 8: Number of pest species and related citation rate by orders during the period
[1999 ; 2008]
28
Chapter 3
0,25
4
% dedicated to ClBC
0,20
0,15
8
2
3
0,10
6
0,05
13
1
12
9
10
11
7
5
0,00
0
100
200
300
400
500
600
700
800
900
number of publications [1999 ; 2008]
Figure 9: Relationships between the number of publications associated to the main pests and
the relative percentage of ClBC related studies.
Pest species are ranked in the decreasing order in number of publications : 1 : Phyllocnistis citrella ; 2 :
Mononychellus tanajoa ; 3 : Toxoptera citricida ; 4 : Homalodisca vitripennis ; 5 : Lymantria dispar ; 6 :
Pseudococcus viburni ; 7 : Solenopsis invicta ; 8 : Aleurocanthus spiniferus ; 9 : Bactrocera oleae ; 10 : Chilo
partellus ; 11 : Diabrotica virgifera virgifera ; 12 : Diatraea saccharalis ; 13 : Maconellicoccus hirsutus.
Specialist and generalist pests are respectively indicated by white and dark diamonds.
29
Ris & Malausa
2,0
Biocontrol
disruption
1,8
Non-target effects
BCA Biology
1,6
median IF
1,4
BCA
characterization
1,2
Post-release survey
1,0 Pre-release survey
Rearing
0,8
BCA inventories
0,6
0,4
0,2
0,0
0,00
0,05
BCA
introduction
0,15
0,10
0,20
0,25
Frequencies of Type of work
Figure 10: Frequencies of papers and associated median IF related to the different categories
of work
30
Chapter 3
Table 9:
Recent introductions of parasitoids as Classical Biocontrol agents
Targeted pest
Crop
BCA Name
Introduction
Area
Aleurocanthus woglumi
Citrus
Amitus hesperidum
Trinidad
Aleurodicus dispersus
Banana
Encarsia guadeloupae
Lecanoideus floccissimus
Encarsia haitiensis
Spain (Tenerife)
Aleurolobus niloticus
Aonidiella aurantii
Aphis gossypii
Bactrocera dorsalis
Bemisia tabaci
Ceratitis capitata
Orchard
Citrus
Vegetable
Orchard
Arable crops
Vegetable
Orchards
(incl. Citrus)
Introduction
Date
Australia
_
_
1992-1996
Individuals
(sites)
1600
(3)
_
_
_
Eretmocerus siphonini
Egypt
1998-1999
237000
Aphytis lingnanensis
Lysiphlebus testaceipes
Spain
Bulgaria
2000
_
_
_
Fopius arisanus
French Polynesia
2003
Eretmocerus hayati
Egypt
2000-2002
200700
Establishment
(Abd-Rabou, 2004)*
Diachasmimorpha krausii
Fopius arisanus
Fopius ceratitivorus
Psyttalia concolor (complex)
Israel
2002-2004
2002-2004
2002-2004
2002-2004
75881
258750
58860
75881
2200
(2)
5000
(5)
Establishment
?
Establishment
?
(Argov and Gazit, 2008)*
2000
Ceroplastes rubens
Orchard
(incl. Citrus)
Anicetus beneficus
Papua New Guinea
2002
Chilo sacchariphagus
Sugarcane
Xanthopimpla stemmator
Mozambique
2001
Pauesia juniperorum
Mauritius
2003-2004
1500
Diversinervus sp. near stramineus
Australia
_
_
(4)
Psyllaephagus pilosus
Chile
2001
_
Diaphorencyrtus aligarhensis
USA
_
_
Tamarixia radiata
USA
_
_
Cinara cupressivora
Coccus viridis
Ctenarytaina eucalypti
Diaphorina citri
Forest
Ornamenta
Citrus
Coffee
Forest
Ornamental
Citrus
Diatraea saccharalis
Sugarcane
Cotesia flavipes
USA
2001-2002
Dryocosmus kuriphilus
Forest
Ornamental
Torymus sinensis
Italy
2005-2006
Legend : _ : data not available ; ? : long-term establishment not sure ; * : additional references
_
(4)
1100
(14)
Outcome
Establishment
High parasitism
_
_
Establishment
Establishment
High parasitism
Establishment
Establishment
Establishment
High parasitism
Establishment
?
?_
Establishment
High parasitism
Establishment
High parasitsm
_
_
References
(White et al., 2005)
(Nijhof et al., 2000)
(Lambkin, 2004)*
(Abd-Rabou, 2002)
(Pina and Verdu, 2007)*
(Dimitrov et al., 2008)*
(Vargas et al., 2007)*
(Krull and Basedow,
2005)
(Conlong and Goebel,
2002)
(Alleck et al., 2006)
(Smith et al., 2004)*
(Rodriguez and Saiz,
2006)*
(Hoy, 2005)
Failure
(White et al., 2004)*
Establishment
(Aebi et al., 2007)
31
Ris & Malausa
Table 9: Recent introductions of parasitoids as Classical Biocontrol agents (continued)
Hemiberlesia pitysophila
Forest
Coccobius azumai
China
2002
_
Homalodisca vitripennis
Wide range
Gonatocerus ashmeadi
Tahiti
2005
14000
(27)
Hypothenemus hampei
Coffee
Cephalonomia stephanoderis
Cuba
_
Phymastichus coffea
Colombia
_
Diaparsis jucunda
USA
_
_
_
_
_
1700
(21)
90000
90000
66000
(121)
_
Lilioceris lilii
Ornamental
Lemophagus errabundus
2001
Tetrastichus setifer
Liriomyza trifolii
Vegetables
Dacnusa sibirica
Diglyphus isaea
Egypt
Listronotus bonariensis
Pasture
Microctonus hyperodae
New Zealand
Maconellicoccus hirsutus
Wide range
Anagyrus kamali
North America
Metcalfa pruinosa
Wide range
Neodryinus typhlocybae
Greece
Ophelimus maskelli
Forest
Ornamental
Closterocerus chamaeleon
Israel
2005-206
Closterocerus sp.
Italy
_
Acerophagus papayae
Palau
2003-2004
_
Anagyrus loecki
2003-2004
_
Pseudleptomastix mexicana
2003-2004
_
Paracoccus marginatus
Wide range
Legend : _ : data not available ; ? : long-term establishment not sure ; * : additional references
_
_
_
(2)
_
(41)
1991-1998
2006
_
_
12000
(6)
_
(5)
Establishment
Establishment
High parasitism
?
Establishment
_
?
?
(Wang et al., 2004)*
(Grandgirard et al.,
2007a)
(Grandgirard et al.,
2008)
(Petit et al., 2008)
(Murguido Morales et
al., 2008)*
(Aristizabal et al.,
2004)*
(Casagrande and
Tewksbury, 2005)*
(Tewksbury et al.,
2005)*
(Abd-Rabou, 2006)*
_
(McNeill et al., 2002)
(Phillips et al., 2008)
Establishment
High parasitism
(Kairo et al., 2000)
Establishment
(Anagnou-Veroniki et
al., 2008)
Establishment
High parasitism
Establishment
High parasitism
Establishment
High parasitism
Establishment
High parasitism
Failure
(Protasov et al., 2007)*
(Rizzo et al., 2006)*
(Muniappan et al., 2006)
32
Chapter 3
Table 9: Recent introductions of parasitoids as Classical Biocontrol agents (continued)
Phyllocnistis citrella
Citrus
Ageniaspis citricola
Cirrospilus ingenuus
Cirrospilus quadristriatus [C.
ingenuus]
Citrostichus phyllocnistoides
Morocco
1995-1996
_
USA
_
_
Italy
1995
_
Italy
1996-1997
_
USA
1999
25000
(132)
Argentina
Brazil
Morocco
2001-2004
1999
_
25000
_
USA
_
_
Italy
1995
_
Morocco
2000
_
Spain
1996-1999
_
1995
1996-1997
1996-1997
2001
2001-2003
_
_
_
_
_
300000
Pseudococcus viburni
Saissetia coffeae
Orchard
Olive
Semielacher petiolatus
Pseudaphycus maculipennis
Coccophagus cowperi
Morocco
Italy
Italy
Morocco
New Zealand
Egypt
Siphoninus phillyreae
Orchard
Eretmocerus siphonini
Egypt
1998-1999
237000
Sirex noctilio
Forest
Ibalia leucospoides
South Africa
1998-2001
Solenopsis invicta
_
Pseudacteon curvatus
USA
2003
456
10100
(2)
Pseudacteon obtusus
Pseudacteon tricuspis
USA
USA
2006
1999-2001
Quadrastichus sp
Failure
Establishment
High parasitism
Failure
Establishment
High parasitism
(Hoy, 2005)
(Siscaro et al., 2003)
(Siscaro et al., 1999)
(Paiva et al., 2000)
?
_
_
Establishement
Establishment
(Zaia et al., 2006)
(Paiva et al., 2000)*
(Rizqi et al., 2003)
(Hoy, 2005)
(Siscaro et al., 2003)
Establishment
Establishment
High parasitism
_
Failure
Failure
Establishment
_
Establishment
Establishment
High parasitism
Establishment
(Rizqi et al., 2003)
(Garcia-Mari et al.,
2004)*
(Rizqi et al., 2003)
(Siscaro et al., 2003)
(Siscaro et al., 1999)
(Rizqi et al., 2003)
(Charles, 2001)
(Abd-Rabou, 2005)*
Establishment
(Vazquez et al., 2006)
?
Establishment
(Gilbert et al., 2008)
(Alvarenga et al., 2005)
Tephritidae sp.
Orchard
(incl. Citrus)
Diachasmimorpha longicaudata
Brazil
2002
34000
(2)
Failure
Toxoptera citricida
Citrus
Lipolexis oregmae
USA
2000-2002
33500
Establishment
Yponomeuta malinellus *
Orchard
Ageniaspis fuscicollis
Canada
1987-1997
_
Legend : _ : data not available ; ? : long-term establishment not sure ; * : additional references
(Rizqi et al., 2003)
Establishment
(Abd-Rabou, 2002)
(Tribe and Cillie, 2004)*
(Hoy, 2005)
(Persad et al., 2007)
(Cossentine and
Kuhlmann, 2007)*
33
Chapter 4
Registered Biocontrol Products and their use in Europe
Ulf Heilig1, Philippe Delval2 and Bernard Blum1
1
International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel,
Switzerland
2
ACTA, 1 avenue Claude Bourgelat, F-69680 Marcy l'Etoile, France
Collection of information
A small team formed by ACTA and IBMA conducted a survey on biological active substances
approved in the European Union and on Biological Control Products (BC products) authorised in
five European countries. The investigation focused on crops covered by ENDURE RA1case studies.
The frame of the present survey was defined in a meeting on 9th January 2009 in Basle, and the
work was performed during the period from April to September 2009.
To compile a list of registered biocontrol products, the online EU Pesticides Database was
consulted on 21st April 2009. Data were retrieved and the list was reorganised and the information
about use categories complemented with the help of the inclusion directives where necessary.
Substances deemed suitable for biocontrol were identified and it was decided to distinguish four
major groups: micro-organisms, semiochemicals (attractants), botanicals and "other plant protection
substances of natural origin".
This study was complemented by an analysis of specific uses of products commercialized in
four countries of the EU (France, Germany, Spain and the United Kingdom). A fifth country,
Switzerland was included in the study for comparison, because it has not been restricted by the
implementation of Directive 91/414/EEC (superceded in June 2011 by EC regulation No
1107/2011) until recently. For each country, official national online databases on authorised plant
protection products (Table 10) were screened for authorised biocontrol active substances:
Table 10: Consulted sources of information on authorized biocontrol plant protection products in
five European countries:
Country
France
Germany
Spain
Switzerland
United
Kingdom
Official source / website
e-phy database of the Ministry of Agriculture & Fisheries
http://e-phy.agriculture.gouv.fr
Online-Datenbank Pflanzenschutzmittel of the Federal Office of Consumer
Protection and Food Safety (BVL)
http://www.bvl.bund.de/DE/04_Pflanzenschutzmittel/01_Aufgaben/02_Zulassung
PSM/01_ZugelPSM/01_OnlineDatenbank/psm_onlineDB_node.html
Registro de productos Fitosanitarios of the Ministerio de Ambiente y Medio Rural
y Marino
http://www.mapa.es/es/agricultura/pags/fitos/registro/menu.asp
Plant protection index ("Pflanzenschutzmittelverzeichnis") of the Federal Office
for Agriculture (BWL, Fachbereich Pflanzenschutzmittel)
http://www.psa.blw.admin.ch/index_de_5_2_A.htm
Pesticides Register of UK approved products under the responsibility of the
Chemicals Regulation Directorate Pesticides
https://secure.pesticides.gov.uk/pestreg/ProdSearch.asp
34
Reference date
31/8/2009
12 /8/2009
31/7/2009
4/2009
Chapter 4
The survey was limited to uses concerning seven crops or cropping groups which are subject to
ENDURE case studies: pomefruit (apples and pears), grapevine, cereals, rape, maize, potatoes and
tomatoes (greenhouse and field), the latter being extended to other vegetables where deemed of
interest. Country lists of representative products (generally up to two) were created and sorted
according to uses in crops, target pests and pathogens were identified by English and scientific
names wherever possible.
Biocontrol substances registered on Annex 1 of the EU (Pesticides Database)
The complete list compiled from data retrieved in April 2009 in the EU Pesticides Database is
presented in Appendix 10. Excerpts concerning the four categories of substances compatible with
biological control are presented in Table 11.
Botanicals
Botanicals are plant-substances resulting from simple processing e.g. pressing or from extraction.
By extension the definition applies to a small numbers of compounds or even single ones extracted
from plants and purified e.g. laminarine.
Fourteen botanicals have been identified (Table 11) including two borderline cases for which
single molecules identical to naturally occurring substances have been synthesised.
- Four botanicals are authorised as repellents only: Extract from the tea tree, garlic extract, clove
oil (plant oils) and pepper.
- Six botanicals enter into the category of plant growth regulators.
- The phytohormones gibberellic acid and gibberelline are botanicals produced in fermenters
acting on plant growth. Spearmint oil and sea-alga extract are listed for their effect on plant
growth as well.
- The phytohormone ethylene is naturally present in plants and in soil and can be included here
although it is typically produced in the petrochemical industry by steam cracking.
- Carvone is a terpene produced by aromatic plants in particular by the mint. It can also be
classified among the botanicals. To obtain a pure grade it is generally synthesised. In plant
protection it is used as a growth regulator.
- Laminarin is extracted from sea weed and is classified as elicitor. Rape seed oil enters into the
category of insecticides/acaroids. Citronella oil is the only BCA approved as herbicide.
- Pyrethrins are extracted from Pyrethrum flowers, from cultivars of Chrysanthemum
cinerariaefolium. By their origin they are botanicals but their structures are analogous and their
properties are similar to those of synthetic pyrethroids. Due to their mode of action which is
analogous to conventional insecticides and their toxicity for aquatic and other non target
organisms, they are not typical biological substances although they are accepted in organic
farming.
35
Heilig et al.
Table 11: Active substances suitable for biological control listed on Annex I of 91/414/EEC (EU
Pesticide Database) - Status on 21 April 2009
Category1, 2
Substance
Botanicals
Extract from tea tree
Garlic extract
Gibberellic acid
Gibberellin
Laminarin
Pepper
Plant oils / Citronella oil
Plant oils / Clove oil
Plant oils / Rape seed oil
Plant oils / Spearmint oil
Sea-algae extract (formerly sea-algae extract and
seaweeds)
Botanicals copied by synthesis (s) or excluded (e)
Carvone (s)
RE
RE
PG
PG
EL
RE
HB
RE
IN, AC
PG
PG
List3 Inclusion Date
Expiry Date
Legislati
on
A4
A4
A4
A4
C
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/04/2005
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/03/2015
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
05/3/EC
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
PG
C
01/08/2008
31/07/2018
Ethylene (s)
Pyrethrins (e)
Microbials
Ampelomyces quisqualis strain AQ10
Bacillus subtilis str. QST 713
Bacillus thuringiensis subsp. aizawai (ABTS-1857 and
GC-91)
Bacillus thuringiensis subsp. israelensis (AM65-52)
Bacillus thuringiensis subsp. kurstaki (ABTS 351, PB
54, SA 11, SA12 and EG 2348)
Bacillus thuringiensis subsp. tenebrionis (NB 176)
Beauveria bassiana (ATCC 74040 and GHA)
Coniothyrium minitans
Cydia pomonella granulosis virus (CpGV)
Gliocladium catenulatum strain J1446
Lecanicillimum muscarium (Ve6) (former Verticillium
lecanii)
Metarhizium anisopliae (BIPESCO 5F/52)
Paecilomyces fumosoroseus Apopka strain 97
Paecilomyces lilacinus
PG
IN
A4
A4
01/09/2009
01/09/2009
31/08/2019
31/08/2019
2008/44/
EC
2008/127
2008/127
FU
BA, FU
[IN]
C
C
A4
01/04/2005
01/02/2007
01/01/2009
31/03/2015
31/01/2017
31/12/2018
05/2/EC
07/6/EC
2008/113
[IN]
[IN]
A4
A4
01/01/2009
01/01/2009
31/12/2018
31/12/2018
2008/113
2008/113
[IN]
IN
FU
[IN]
FU
IN
A4
A4
C
A4
C
A4
01/01/2009
01/01/2009
01/01/2004
01/01/2009
01/04/2005
01/01/2009
31/12/2018
31/12/2018
31/12/2013
31/12/2018
31/03/2015
31/12/2018
2008/113
2008/113
03/79/EC
2008/113
05/2/EC
2008/113
IN
[IN]
[IN]
A4
C
C
01/01/2009
01/07/2001
01/08/2008
31/12/2018
30/06/2011
31/07/2018
Phlebiopsis gigantea (several strains)
Pseudomonas chlororaphis strain MA342
Pythium oligandrum (M1)
Spodoptera exigua nuclear polyhedrosis virus
Streptomyces K61 (K61) (formerly Streptomyces
griseoviridis)
Trichoderma aspellerum (ICC012) (T11) (TV1)
(formerly T. harzianum)
Trichoderma atroviride (IMI 206040) (T 11) (formerly
Trichoderma harzianum)
Trichoderma gamsii (formerly T. viride) (ICC080)
Trichoderma harzianum Rifai (T-22) (ITEM 908)
Trichoderma polysporum (IMI 206039)
Verticillium albo-atrum (WCS850) (formerly
Verticillium dahliae)
FU
FU
FU
FU
FU
A4
C
A4
C
A4
01/01/2009
01/10/2004
01/01/2009
01/12/2007
01/01/2009
31/12/2018
30/09/2014
31/12/2018
30/11/2017
31/12/2018
2008/113
01/47/EC
2008/44/
EC
2008/113
04/71/EC
2008/113
07/50/EC
2008/113
FU
A4
01/01/2009
31/12/2018
2008/113
FU
A4
01/01/2009
31/12/2018
2008/113
FU
FU
FU
FU
A4
A4
A4
A4
01/01/2009
01/01/2009
01/01/2009
01/01/2009
31/12/2018
31/12/2018
31/12/2018
31/12/2018
2008/113
2008/113
2008/113
2008/113
36
Chapter 4
Table 11 (continued)
Other Natural
Abamectin (aka avermectin)
Acetic acid
Aluminium silicate (aka kaolin)
Blood meal
Carbon dioxide
Fat distilation residues
Ferric phosphate
Kieselguhr (diatomaceous earth)
Milbemectin
Quartz sand
Spinosad
Other Natural, produced by synthesis
Benzoic acid
Potassium hydrogen carbonate
Urea
Other Natural, fatty acid
Capric acid (CAS 334-48-5)
Caprylic acid (CAS 124-07-2)
Fatty acids C7 to C20
Fatty acids C7-C18 and C18 unsaturated potassium
salts (CAS 67701-09-1)
Fatty acids C8-C10 methyl esters (CAS 85566-26-3)
Lauric acid (CAS 143-07-7)
Methyl decanoate (CAS 110-42-9)
Methyl octaonate (CAS 111-11-5)
Oleic acid (CAS 112-80-1)
Pelargonic acid (CAS 112-05-0)
Other Natural, repellent
Calcium carbonate
Limestone
Methyl nonyl ketone
Sodium aluminium silicate
Repellents by smell/Fish oil
Repellents by smell/Sheep fat
Semiochemical
(Z)-13-Hexadecen-11yn-1-yl acetate
(Z,Z,Z,Z)-7,13,16,19-Docosatetraen-1-yl isobutyrate
Ammonium acetate
Hydrolysed proteins
Putrescine (1,4-Diaminobutane)
Trimethylamine hydrochloride
Straight Chain Lepidoptera Pheromones
AC, IN
HB
RE
RE
IN, RO
RE
MO
IN
IN, AC
RE
IN
A3
A4
A4
A4
A4
A4
C
A4
C
A4
C
01/01/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/11/2001
01/09/2009
01/12/2005
01/09/2009
01/02/2007
31/12/2018
31/08/2018
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/10/2011
31/08/2019
30/11/2015
31/08/2019
31/01/2017
2008/107
2008/127
2008/127
2008/127
2008/127
2008/127
01/87/EC
2008/127
05/58/EC
2008/127
07/6/EC
BA, FU, OT
FU
IN
C
A4
A4
01/06/2004
01/09/2009
01/09/2009
31/05/2014
31/08/2019
31/08/2019
04/30/EC
2008/127
2008/127
IN, AC, HB, PG
IN, AC, HB, PG
IN, AC, HB, PG
IN, AC, HB, PG
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
IN, AC, HB, PG
IN, AC, HB, PG
IN, AC, HB, PG
IN, AC, HB, PG
IN, AC, HB, PG
IN, AC, HB, PG
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
RE
RE
RE
RE
RE
RE
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
AT
AT
AT
IN
AT
AT
AT
A4
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/01/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/12/2018
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
37
Heilig et al.
Table 11 (continued)
Semiochemical / SCLP
(2E, 13Z)-Octadecadien-1-yl acetate
(7E, 9E)-Dodecadien 1-yl acetate
(7E, 9Z)-Dodecadien 1-yl acetate
(7Z, 11E)-Hexadecadien-1-yl acetate
(7Z, 11Z)-Hexadecdien-1-yl acetate
(9Z, 12E)-Tetradecadien-1-yl acetate
(E)-11-Tetradecen-1-yl acetate
(E)-5-Decen-1-ol
(E)-5-Decen-1-yl-acetate
(E)-8-Dodecen-1-yl acetate
(E,E)-8,10-Dodecadien-1-ol
(E/Z)-8-Dodecen-1-yl acetate
(Z)-11-Hexadecen-1-ol
(Z)-11-Hexadecen-1-yl acetate
(Z)-11-Hexadecenal
(Z)-11-Tetradecen-1-yl acetate
(Z)-13-Octadecenal
(Z)-7-Tetradecenal
(Z)-8-Dodecen-1-ol
(Z)-8-Dodecen-1-yl acetate
(Z)-9-Dodecen-1-yl acetate
(Z)-9-Hexadecenal
(Z)-9-Tetradecen-1-yl acetate
Dodecyl acetate
Tetradecan-1-ol
1
2
3
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
AC=acaricide, AT= attractant, BA=bactericide, EL=elicitor, FU=fungicide, HB=herbicide, IN=insecticida, MO=molluscicide,
NE=nematicide, PA=Plant Activator, PG=Plant Growth, RE=repellent, RO=rodenticide.
Category in [ ] added by author
A: Existing active substances divided into four lists for phased evaluations; C: New active substances
Micro-organisms
The term micro-organism is defined in regulation (EC) No 1107/2009: ‘micro-organisms’ means
any microbiological entity, including lower fungi and viruses, cellular or non-cellular, capable of
replication or of transferring genetic material.. This definition applies to, but is not limited to,
bacteria, fungi, protozoa, viruses and viroids. It does not include multicellular organisms, such as
nematodes or insects.
Twenty five microbial species are included in annex I, some of which are represented by
several strains. Six bacterial (sub)species (Bacillus subtilis, Pseudomonas chlororaphis and four
subspecies of Bacillus thuringiensis) and two virus species (Cydia pomonella Granulose Virus and
Spodoptera exigua NPV) are included. All B.t. subspecies and viral agents are approved for insect
control. Pseudomonas is approved for fungicidal seed treatments and Bacillus subtilis can be used
against plant pathogenic fungi and bacteria. Seventeen fungal agents belonging to twelve genera are
listed, Trichoderma being represented by five species. Beauveria bassiana, Lecanicillimum
muscarium and Metarhizium anisopliae are approved for use as insecticides, the other fungal agents
for use against fungal diseases.
Semiochemicals (attractants)
Semiochemicals are chemical substances such as pheromones, kairomones and allomones that act to
modify the behaviour of pests or their natural enemies.
In the table based on the EU Pesticides Database, Straight Chain Lepidopteran Pheromones (SCLP)
are highlighted in green, non-SCLP-pheromones in light cyan and other attractants (including
hydrolysed proteins) are highlighted in yellow. There is one repellent which is marked in light red.
38
Chapter 4
SCLPs are included in annex I as a group but 25 compounds of this group are also listed
individually. In the inclusion directive 2008/127/EC, some molecules are mentioned three times, as
an individual substance, in a blend of the same type, e.g. acetates and in mixed blends, e.g. alcohols
and acetates. Often single SCLP compounds show attraction to one or more moth species and
typically a combination of two or more of these compounds in a precise ratio enhances the
attraction and the specificity. Thus SCLPs should be considered as a whole group and it must not be
concluded that each compounds stands for one species.
The SCLPs listed individually are typical examples found in the pheromone blends of moth
pest species currently of economic importance. A large variety of compounds and isomers, an
estimated number of about 300 identified molecules, used by Lepidopterans are not listed here.
They differ in carbon chain length, in the number of double bonds and/or their positions and in their
chemical functional group (alcohol, acetate or aldehyde). SCLPs can be used for mass trapping,
mating disruption or in attract and kill devices (A&K) or formulations. When associated with an
insecticide, i.e in A&K products, attractants do not need to be included in annex I.
Two non SCLP pheromones, (Z)-13-Hexadecen-11yn-1-yl acetate and (Z,Z,Z,Z)-7,13,16,19Docosatetraen-1-yl isobutyrate, as well as four semiochemicals other than pheromones attractive to
different fly (Diptera) species are listed in the EU Pesticides Database: Ammonium acetate,
hydrolysed proteins, putrescine (1,4-diaminobutane) and Trimethylamine hydrochloride.
Other Plant Protection substances of natural origin
This group has been created for the purpose of the survey. It includes mineral substances as well as
substances produced by or derived from animals or from micro-organisms. Thus very diversified
substances and products like limestone powder, kaolin as well as diatomaceous earth (Kieselguhr),
fatty acids and their derivates (e.g. soaps) can be found in this group. Not all substances of this
group do meet the expectation of low non-target toxicity and low environmental impact.
Some active substances included in annex I are produced by micro-organisms. Spinosad which
is produced by the bacterium Saccharopolyspora spinosa finds its place here; it is accepted for
organic farming. Milbemectin is a mixture of natural compounds (milbemycins) isolated from
fermentation broth of the fungus Streptomyces hygroscopicus subsp. aureolacrimosus. The
substance is active against insects of different families and a large range of mites. Abamectin
contains avermectins which are biosynthesised by Streptomyces avermitilis. The substance shows
very high toxicity in Mammals and in aquatic organisms. Milbemectin and abamectin are not
authorised in organic crop protection.
Potassium hydrogen carbonate is a slightly basic substance used for its fungicidal properties.
The US FDA considers this substance as GRAS (Generally Recognised as Safe). Six natural
substances are specifically marked in the EU List, they are used as animal repellents: three are
minerals (Calcium carbonate, limestone, sodium aluminium silicate), two are of animal origin (fish
oil and sheep fat) while methyl nonyle ketone is either produced by synthesis or extracted from
plant oils (rue). The latter repellent acts by its strong odour. It is naturally present in some edible
crops and spices.
Limit cases and exclusions
With regards to their (eco)toxicological profile and environmental impact neither sulphur and its
derivates (iron sulphate) nor cupric compounds i.e. Bordeaux mixture, copper hydroxide, copper
oxichloride and cuprous oxide are considered here as typical biological substances although they
might be accepted in organic agriculture.
Tall oils (crude or pitch) are a by-product in the Kraft process used in the paper industry. Thus
they are substances resulting from a chemical process and are classified as chemicals here. Calcium
carbide is produced from lime and coke in electric arc furnaces. It is fitted among chemicals but is
used as a repellent like some other minerals. 1-Methyl-cyclopropene is an inhibitor of the effects of
39
Heilig et al.
the phytohormone ethylene and is mainly used to conserve cut flowers. It is placed among the
chemicals.
Uses of biocontrol products in five European countries
Registered plant protection substances
In each country all BCAs authorised for uses in seven crops or cropping groups were identified.
Lists of representative products (generally up to two) were created and sorted according to uses in
crops: pomefruit (apples and pears), vine, cereals, rape, maize, potatoes and tomatoes (greenhouse
and field), the latter was extended to other vegetables where deemed of interest.
In France twelve different microbial BCA species (or sub-species in the case of Bacillus
thuringiensis) are authorised among which two species, Beauveria tenella and Candida oleophila
are not yet included in 91/414 Annex I. Only four botanical active substances are authorised,
including rotenon (EU non-inclusion decision in April 2008 but temporary authorisation in FR) and
pyrethrum which were excluded from our survey. Fenugreek extracts benefited from a specific
French approach to plant extracts under former national rules, while EU approval was given in
2010, after the survey. Laminarin is included in Annex I. Five Straight Chain Lepidopteran
Pheromones (SCLP) blends or associations (one just specifying minor components used for the
single target codling moth) are registered for mating disruption in orchards or vineyard.
In Germany nine microbial BCAs are authorised in Plant Protection Products (all included).
Only four botanical substances are listed for plant protection, two of which are included in Annex I
(pyrethrins and rape seed oil), two are not (azadirachtin and lecithin). Three different SCLP
associations are authorised for mating disruption against Codling Moth or Vine Moths.
For Germany only fully registered BC products according to the rules of the PPP directive
were included in the survey. As a consequence, plant strengtheners authorised according to the
Federal Plant Protection Act §§ 31ff were excluded. Plant Strengtheners can avoid the EU
procedures and requiremments for plant protection products but they must not claim specific
protective properties either.
In Spain ten microbial BCAs are authorised, all of which are included in EU Annex 1. Only
three botanical substances could be identified: Pyrethrins and rotenon which are excluded from the
survey and Azadirachtin (Neem extract) which was re-included in EU Annex I in 2011. The plant
growth regulators gibberellinic acid/gibberellin are not explored in the survey. Only four SCLP
associations are authorised for mating disruption in vine and orchards including two for oriental
fruit moth and peach twig borer typical for peach orchards.
In Switzerland twelve different microbial BCA species (or sub-species in the case of Bacillus
thuringiensis) are authorised, among which is one species not included in 91/414 Annex I:
Beauveria brognartii. Eleven botanicals are approved, among which the insecticides Pyrethrum
(included in EU Annex I) and rotenon (rejected from Annex I) have been excluded from the survey
because of their toxicological profile. The plant growth regulators gibberellic acid and gibberellin
were also excluded from the survey. Five substances not included in EU Annex I are authorised:
Azadirachtin (Neem extract), fennel oil, lecithin, mustard powder and Quassia extract. An
impressive number of semiochemicals, eleven different SCLP associations are authorized for
mating disruption allowing the control a large variety of moths in orchards (including one
association of 8 compounds against five different species) and vineyards. This can be related to the
facilitated approval of pheromone products in Switzerland.
In the UK eight microbial BCAs are approved but only a single botanical (Laminarin, EU
approved) and a single pheromone blend (for codling moth). No biological plant protection products
are available for use in grapevine, rape, maize or potatoes. With regard to the global availability of
biological control products in the different crops, pomefruit, vegetables and vine are generally in a
better position than arable crops in the countries included in the survey. In the UK e.g. only
40
Chapter 4
laminarin is available on wheat and cereals, and no biological plant protection products are
registered for rape, maize or potatoes.
None of the EU Member States covered in the present survey shows such a variety of BCAs as
Switzerland where we find the largest numbers of microbials, botanicals and pheromone blends
authorised in the crops subject of the inquiry. Only France reaches the number of twelve microbial
BCAs in registered products. The privileged situation in the Helvetic Confederation can be
explained by the flexible regulatory approach of the competent authorities in the past, until the
progressive implementation of EU directive 91/414/EEC and the related framework, as well as the
sustained support by experts in confederal agronomic institutes.
Invertebrate biocontrol agents
Invertebrate biocontrol agents (BCAs) used in the five European countries of this survey are listed
in Appendix 11.
In France invertebrate BCAs cannot be registered and they do not yet need to be formally
declared, but a law passed on 12th July 2010 created the basis to establish rules governing the
introduction into the environment of non-indigeneous macro-organisms useful to plants. Procedures
and requirements for authorisations which will also cover non-indigeneous beneficial are expected
to be set up for the in the coming months. The list provided in the present survey is based on the
voluntary declarations to ACTA by the producers wishing to have their beneficials published in the
non-official Index Phytosanitaire.
Invertabrate BCAs must be registered in Germany. An official list which is regularly updated
is published by the Julius Kühn Institute.
In Spain companies which are responsible of commercialisation of IBCAs must give
information to the Ministry of Agriculture to allow the inscription into a register before
commercialisation (Orden APA/1470/2007). This information given is about name of commercial
product, identification of the organism, the manufacturer, the company responsible for
commercialisation. Another law (43/2002; 20th of November 2002) covers the introduction of exotic
organisms (article 44).
In Switzerland invertebrate BCAs must be formally approved by the BLW (Bundesamt für
Landwirtschaft) and they are listed together with the plant protection products.
In the United Kingdom no authorisation is required to release indigenous beneficials but the
import (and release) of non indigenous species must be approved by the Advisory Committee for
the Release of Exotics (ACRE acting under DEFRA).
41
Chapter 5
Identified difficulties and conditions for field success of biocontrol.
1. Regulatory aspects
Ulf Heilig1, Claude Alabouvette2* and Bernard Blum1
1
International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel,
Switzerland
2
INRA, UMR1229, Microbiologie du Sol et de l'Environnement, 17 rue Sully, F -21000 Dijon,
France
Objectives
The objective of the work was to identify typical hurdles for the placing of biological plant
protection products on the market experienced by biocontrol industry or evaluators in the recent
past under the European directive 91/414/EEC. In parallel, we examined the new regulation (No
1107/2009/EC of the European Parliament and of the Council of 21 October 2009) concerning the
placing of plant protection products on the market and repealing Council Directives 79/117/EEC
and 91/414/EEC and the new directive (N° 2009/128/EC of the European Parliament and of the
Council of 21 October 2009) establishing a framework for Community action to achieve the
sustainable use of pesticides. These two texts were examined for provisions creating new
opportunities for the approval biocontrol agents, their placing on the market and use. In fine, it was
the intent to establish a dialogue with EU regulators and evaluators in European institutions, i.e. in
the European Commission and in the European Food Safety Agency (EFSA) and to seek solutions
in common for the problems encountered.
Working method
An ad hoc group of representatives from the biocontrol industry and INRA called "Regulatory
Review Team" was set up. Two full-day working sessions were organised in which regulatory
experts identified difficulties and questions but also described positive experience and perspectives.
The work of the Regulatory Review Team active under Reasearch Activity RA4.3 of the
ENDURE network was then summarised and reported in a meeting of a delegation of ENDURE
partners (IBMA, INRA and ACTA) with representatives of the European Commission (DG
SANCO, DG Agriculture, DG Research) and the EFSA in Brussels (24 September 2009).
Results
A PowerPoint presentation entitled "Gaps - Problems - Opportunities for BCAs in E.U.
Regulation - From Past to Future" was prepared for the ENDURE – Commission meeting, with
inputs on general regulatory issues, micro-organisms, straight chain lepidopteran pheromones and
botanicals. In this document, two key issues related to directive 2001/36/EC annex II B which fixed
requirements for microbial active substances were highlighted. Readers may note that since 14th
June 2011 Regulation (EU) No 544/2011 implements these data requirements unchanged to reg.
*
Current address: AGRENE, 47 rue Constant Pierrot 21000 DIJON, c.ala@agrene.fr
42
Chapter 5
(EC) No 1109/2009. Tests suggested by evaluation experts and intended to establish the genetic
stability of a strain do not reflect practical conditions, while in the case of potential microbial
contaminants no European reference list is available. The incidence of many pathogens can be
excluded by production methods or the geographic location of production sites. Tolerance limits for
contamination levels could take into consideration thresholds used in food industry, application
levels for the microbial product and naturally occurring background levels. The two issues
presented here but also other examples put forward to the Regulatory Review Team lead to the
statement that "not all the studies or tests that can be performed for microbials will necessarily
yield relevant data".
The most important experience with semiochemicals was made during the on-going reassessment of Straight Chain Lepidopteran Pheromones (SCLPs), which were supported by an
IBMA Task Force. Regulators and evaluators were flexible in accepting a single common dossier
for all compounds notified but although an OECD guidance document recommends data waiving
for numerous SCLP requirements, the Rapporteur Member State insisted that all existing data and
study reports on all compounds be submitted on the grounds that the requirements of the directive
are superior to the guidance document recommendations. So far, the re-assessment procedure
resulted in the inclusion with postponed peer review of SCLPs as a group, but 25 substances are
also listed individually. New substances can be included in a simplified procedure provided that the
applicant has access to the existing dossier. Remaining questions include what industry input will
be required during the peer review by EFSA, the E.U. status of a revised OECD guidance document
for semiochemicals other than SCLPs, the decision if MRLs are required for sprayable SCLP
formulations, and equivalence criteria for SCLP substances. It was also noted that under the
Biocidal Product Directive, rules and fees applied to SCLPs created an economic hurdle which
resulted in the submission of a dossier for only one compound.
Extracts from plants - as long as not purified - consist of mixtures of molecules while data
requirements of directive 91/414/EEC maintained under new regulation (EC) No 1107/2009 are
basically designed for defined single substances. Thus those requirements often do not fit for
mixtures of several substances. It must be decided if the most “active” substance, the one with the
highest content in the extract or the whole extract shall be used in studies required for different
sections of a dossier i.e. for data on physical-chemical properties, metabolism, toxicology, residues,
environmental fate and behaviour, and which data shall be used in risk assessment. While the whole
extract can be recommended for use in toxicity studies, it is not convenient for residue, metabolism
or environmental studies because in practice it is generally not possible to determine the fate of all
compounds contained in an extract. Questions asked by evaluators from several Member States
after the issuing of a draft assessment report for Neem extract and its lead substance Azadirachtin A
illustrate the difficulties experienced by an applicant in the evaluation process for a botanical.
Regulation (EC) No 1107/2009 concerning the placing of plant protection products on the
market provides for a specific status for "low risk active substances" (article 22). Many biocontrol
substances can be expected to qualify for this new category but one exclusion criterion, the half-life
in soil, may cause problems for microbial active substances unless it is clearly limited to chemicals.
A full set of data is required to gain the status of low risk active substance but products containing
them exclusively and without co-formulants of concern will benefit from reduced dossier
requirements and time lines for approval. Micro-organisms, plant extracts or other natural
substances may also meet the criteria for "Basic substances" provided for in article 23 but the
discussion in the ENDURE-Commission meeting made it clear that this category is without interest
for manufacturers who intend to market their substances for plant protection. It was noted that the
new regulation does not provide for generic waivers i.e. for justifications of non submission of data
or exemptions from requirements for groups of substances or products.
43
Heilig et al.
In the sustainable use directive 2009/128/EC a number of provisions in favour of biological
pest control measures or non-chemical methods have been identified. The new regulation also
mentions in recital 35 that priority should be given to "non-chemical and natural alternatives
wherever possible" but since the definition of non-chemical methods refers to "physical, mechanical
or biological pest control" and does not specifically mention microbials, semiochemicals, botanicals
or other natural substances with non-toxic mode of action it must be clarified how those groups are
covered by the definition.
Conclusion
In the meeting between the ENDURE delegation and representatives of the European
Commission, the need for discussions between regulators, evaluators and industry about
requirements especially those relevant for microbial and botanical substances was recognised.
Article 77 of the new plant protection product regulation authorises the Commission to "adopt or
amend technical and other guidance documents e.g. explanatory notes or guidance documents on
the content of the application concerning micro-organisms, pheromones and biological products."
Thus at least part of the problems experienced by applicants can be addressed in guidance
documents. Industry representatives and companies directly concerned by evaluations or reviews of
biocontrol agents should enter into discussions with evaluators (EFSA or Competent Authorities in
Member States) without forgetting the leading role of the Commission. Industry should fix
priorities, prepare rationales and make substantiated proposals dealing with data requirements
considered inappropriate, unnecessary or unrealistic.
44
Chapter 6
Identified difficulties and conditions for field success of biocontrol.
2. Technical aspects: factors of efficacy
Michelina Ruocco1, Sheridan Woo1,2, Francesco Vinale1, Stefania Lanzuise2, Matteo Lorito1,2
1
CNR-IPP, Consiglio Nazionale delle Ricerche, Istituto per la Protezione delle Piante, via
Università 133, 80055 Portici, Italy
2
Dip. Arboricoltura, Botanica e Patologia Vegetale, Università di Napoli Federico II, via
Università 100, 80055 Portici, Italy
Quality of the BCAs formulations
Numerous investigations on the development of biopesticides have been initiated as legislation and
government policy have demanded less reliance on chemical pesticides and greater adoption of
IPM. In Europe, some countries have set goals of reducing pesticide use by 50%. Successes have
been achieved through better timing of applications, so that lower dosages are effective and
substituting less hazardous and more active materials, to reduce the number of applications.
Biopesticides are distinguished from conventional chemical pesticides as many are very
selective and are non-toxic towards non-target organisms. While biopesticides are likely to be less
harmful to the environment than the conventional ones, care needs to be taken that wastage is
minimised, by selecting the most appropriate droplet spectrum. A disadvantage of biological agents
relative to chemicals, is that many are not sufficiently persistent and are relatively slow acting;
therefore, research has been directed at extending the period of activity. However, some such agents
may persist in the field or the forest for many months, and a risk–benefit analysis should be
performed to establish their environmental acceptability.
Transition from the optimised conditions of a laboratory experiment to the harsh conditions
experienced in the field has so far proved more difficult for application of biopesticides in contrast
to chemicals. This has undoubtedly been due to lack of investment in the development of effective
formulations and delivery systems, in order to commercialise more potential biopesticides. The
relatively small effort invested in target-specific sprayers, compared with the investment in
laboratory studies, has led to unbalanced development, and exemplifies the need for closer
integration between formulation and engineering research. The challenge is to get effective
formulations so that biological control agents can be easily applied by farmers.
A good example, the case of Trichoderma: direct and indirect mode of action against
plant pathogens
Trichoderma species have long been recognized as biological control agents (BCAs) for the control
of plant disease and for their ability to increase plant growth and development. They are widely
used in agriculture, and some of the most useful strains demonstrate a property known as
‘rhizosphere competence’, the ability to colonize and grow in association with plant roots (Harman
2000). Much of the known biology and many of the uses of these fungi have been documented
recently (Harman et al. 2004a; Kubicek et al. 1998; Perello et al. 2009). The taxonomy of this
fungal genus is continually being revised, and many new species are being described (KomonZelazowska et al. 2007; Kubicek et al. 2008; Overton et al. 2006; Samuels 2006; Samuels and
45
Ruocco et al.
Ismaiel 2009). The mechanisms that Trichoderma uses to antagonize phytopathogenic fungi include
competition, colonization, antibiosis and direct mycoparasitism (Harman 2006, 2011; Howell
2003). This antagonistic potential serves as the basis for effective biological control applications of
different Trichoderma strains as an alternative method to chemicals for the control of a wide
spectrum of plant pathogens (Harman et al. 1991; Lorito et al. 2010).
The colonization of the root system by rhizosphere competent strains of Trichoderma results in
increased development of root and/or aerial systems and crop yields (Bae et al. 2011; Chacon et al.
2007; Kubicek et al. 1998; Yedidia et al. 2003). Trichoderma has also been described as being
involved in other biological activities such as the induction of plant systemic resistance (Shoresh et
al. 2010; Tucci et al. 2011) and antagonistic effects on plant pathogenic nematodes (Jegathambigai
et al. 2008; Sharon et al. 2001).Some strains of Trichoderma have also been noted to be aggressive
biodegraders in their saprophytic phases, in addition to acting as competitors to fungal pathogens,
particularly when nutrients are a limiting factor in the environment (Worasatit et al. 1994). These
facts strongly suggest that in the plant root environment Trichoderma actively interacts with the
components in the soil community, the plant, bacteria, fungi, other organisms, such as nematodes or
insects, that share the same ecological niche (Lorito et al. 2010).
Trichoderma spp. are important participants in the nutrient cycle. They aid in the
decomposition of organic matter and make available to the plant many elements normally
inaccessible. Yedidia et al. (2001) noted that the presence of the fungus increased the uptake and
concentration of a variety of nutrients (copper, phosphorus, iron, manganese and sodium) in the
roots of plants grown in hydroponic culture, even under axenic conditions. These increased
concentrations indicated an improvement in plant active-uptake mechanisms. Corn that developed
from seeds treated with T. harzianum strain T-22 produced higher yields, even when a fertilizer
containing 40% less nitrogen was applied, than the plants developed from seed that was not treated
with T-22 (Harman 2000). This ability to enhance production with less nitrate fertilizer, provides
the opportunity to potentially reduce nitrate pollution of ground and surface water, a serious adverse
consequence of large-scale maize culture. In addition to effects on the increase of nutrient uptake
and the efficiency of nitrogen use, the beneficial fungi can also solubilize various nutrients in the
soil, that would be otherwise unavailable for uptake by the plant (Altomare et al. 1999b).
The cross-talk that occurs between the fungal BCA and the plant is important both for
identification of each component to one another and for obtaining beneficial effects. Somehow, the
plant is able to sense, possibly by detection of the released fungal compounds, that Trichoderma is
not a hostile presence, therefore the plant defence system is not activated as it is when there is pest
attack and the BCA is recognized as a plant symbiont rather than a plant pathogen (Woo and Lorito,
2006). Molecules produced by Trichoderma and/or its metabolic activity also have potential for
promoting plant growth (Chacón et al., 2007; Vinale et al. 2008a; 2008b; Yedidia et al. 1999).
Applications of T. harzianum to seed or the plant resulted in improved germination, increased plant
size, augmented leaf area and weight, greater yields (Altomare et al. 1999a; Harman et al. 2004c, b;
Inbar and Chet 1995; Tucci et al. 2011; Vinale et al. 2008a).
Numerous studies indicated that metabolic changes occur in the root during colonization by
Trichoderma spp., such as the activation of pathogenesis-related proteins (PR-proteins), which
induce in the plant an increased resistance to subsequent attack by numerous microbial pathogens
(Table 12)
46
Chapter 6
Table 12:
Evidence for, and effectiveness of, induced resistance in plants by Trichoderma
species (Harman et al., 2004a).
The induction of systemic resistance (ISR) observed in planta determines an improved control
of different classes of pathogens (mainly fungi and bacteria), which are spatially and temporally
distant from the Trichoderma inoculation site. This phenomenon has been observed in many plant
species, both dicotyledons (tomato, pepper, tobacco, cotton, bean, cucumber) and monocotyledions
(corn, rice). For example, Trichoderma induces resistance towards Botrytis cinerea in tomato,
tobacco, lettuce, pepper and bean plants, with a symptom reduction ranging from 25 to 100% (Tucci
et al. 2011). Moreover, Trichoderma determined an overall increased production of defence-related
plant enzymes, including various peroxidases, chitinases, β-1,3-glucanases, and the lipoxygenasepathway hydroperoxide lyase (Harman et al. 2004c; Howell et al. 2000; Yedidia et al. 1999) of T.
harzianum strain T-39, the active ingredient of the commercial product TricodexTM.
Thus far, Trichoderma is able not only to produce toxic compounds with a direct antimicrobial
activity against pathogens, but also to generate fungal substances that are able to stimulate the plant
to produce its own defence metabolites. In fact, the ability of T. virens to induce phytoalexin
accumulation and localized resistance in cotton has already been discussed (Hanson and Howell
2004). In cucumber, root colonization by strain T-203 of T. asperellum caused an increase in
phenolic glucoside levels in the leaves; the aglycones, which are phenolic glucosides with the
carbohydrate moieties removed, are strongly inhibitory to a range of bacteria and fungi (Yedidia et
al. 2003).
47
Ruocco et al.
A fundamental part of the Trichoderma antifungal capability consists in the production and
secretion of a great variety of extracellular cell wall degrading enzymes (CWDEs), including
endochitinases, β-N-acetylhexosaminidase (N-acetyl-β-D-glucosaminidase), chitin-1,4-β-chitobiosidases, proteases, endo- and exo-β-1,3-glucanases, endo β-1,6-glucanases, lipases, xylanases,
mananases, pectinases, pectin lyases, amylases, phospholipases, RNAses, DNAses, etc. (Benitez et
al. 2004; Lorito et al. 1998). The chitinolytic and glucanolytic enzymes are especially valuable for
their CWDE activity on fungal plant pathogens, hydrolyzing polymers not present in plant tissues
(Woo et al. 1999). Each of these classes of enzymes contains diverse sets of proteins with distinct
enzymatic activities. Some have been purified, characterized and their encoding genes cloned (AitLahsen et al. 2001; de la Cruz et al. 1992; 1995a; 1995b; Garcia et al. 1994; Limon et al. 1995;
Lora et al. 1995; Lorito et al. 1993,. 1994b; Montero et al. 2007; Peterbauer et al. 1996; Suarez et
al. 2004; Viterbo et al. 2001, 2002). Once purified, many Trichoderma enzymes have shown to
have strong antifungal activity against a wide variety of phytopathogens, and they are capable of
hydrolyzing not only the tender young hyphal tips of the target fungal host, but they are also able to
degrade the hard, resistant conservation structures such as sclerozi.
Trichoderma spp. have been widely studied, and are presently marketed as biopesticides,
biofertilizers and soil amendments, due to their ability to protect plants, enhance vegetative growth
and contain pathogen populations under numerous agricultural conditions (Harman 2000, 2004;
Vinale et al. 2008b). The commercial success of products containing these fungal antagonists can
be attributed to the large volume of viable propagules that can be produced rapidly and readily on
numerous substrates at a low cost in diverse fermentation systems. The living microorganisms,
conserved as spores, can be incorporated into various formulations, liquid, granules or powder etc.,
and stored for months without losing their efficacy (Jin et al. 1996). To date more than 50 different
Trichoderma-based preparations are commercialized and used to protect or increase the
productivity of numerous horticultural and ornamental crops (Table 13; Lorito et al. 2006).
The case Trichoderma: mode of application, persistence on the target and new
formulations.
Effectiveness under controlled conditions (even under field conditions) does not necessarily
guarantee that the organism will perform successfully; proper formulation is a prime condition for
meeting market requirements. For instance an efficient biocontrol agent of soilborne and airborne
pathogens must first and foremost protect the young seedling against detrimental attack by infective
inoculum. Therefore some factors may be considered:
(a) soil ecosystem factors such as moisture, pH, structure, and temperature;
(b) root colonization capacity;
(c) reasonable shelf life;
(d) efficiency of application of the biocontrol agent in terms of its specific habitat and target
(Spiegel and Chet 1998)
48
Chapter 6
Table 13: Trichoderma-based preparations commercialized for biological control of plant diseases.
Commercial
Biocontrol
Product
Formulation,
Uses - Location,
Uses, Pathogens
Product
Organism(s)
Type
Application
Crops
controlled
Ago Biocontrol
T. harzianum
Biological
fungicide
n/a
Flowers, vegetables,
fruits, other crops
Fusarium, Rhizoctonia,
Alternaria, Rosellinia,
Botrytis, Sclerotium,
Phytophthora spp
Ago Biocontrol, Colombia
(http://www.sipweb.org/directorymcp/fungi.html)
Antagon
Trichoderma
spp.
Biological
fungicide
powder
damping-off diseases
De Ceuster Meststoffen N.V. (DCM), Belgium
(http://www.agroBiologicals.com/products/P1609.htm)
Binab T
T. harzianum,
T. polysporum
Biological
fungicide
Pellets, wettable
powder or
granules; spray,
drench, mixed in
soil
T. viride
Biological
fungicide
Seed treatment,
root/tuber dip,
drench; Used
alone or in
combination with
chemicals.
Wood rots causing
internal decay, or
originating from pruning
wounds; Didymella,
Chondrostereum,
Heterobasidion, Botrytis,
Verticillium, Pythium,
Fusarium, Phytophthora,
Rhizoctonia
Pythium, Rhizoctonia,
Fusarium, Sclerotium,
other root rots; for
Botrytis in combination
with chemicals
BINAB Bio-Innovation AB, Sweden
(http://www.algonet.se/~binab/index2.html); Henry
Doubleday Research Association, United Kingdom;
Svenska Predator AB, Sweden; E.R. Butts International,
Inc., USA
BioFit
Bio-Fungus
Trichoderma
spp.
Biological
fungicide
granular, wettable
powder, sticks,
crumbles; soil
incorporation;
spray or injection
Horticulture
(commercial), parks,
recreational areas,
sports fields
Wood products;
ornamental, shade,
forest trees;
greenhouse, nursery,
field; cut flowers,
potted plants,
vegetables,
mushrooms, flower
bulbs
Gram, pepper,
groundnut, wheat,
potato, ginger,
turmeric, peas,
matki, mung, urid ,
tomato, bhindi,
onion, other
vegetables, grapes.
Flowers,
strawberries, trees,
vegetables
Sclerotinia,
Phytophthora,
Rhizoctonia solani,
Pythium spp., Fusarium,
Verticillium
BioPlant, Denmark (www.bioplant.dk); De Ceuster
Meststoffen N.V. (DCM), Belgium
Trichoderma
50
(formerly
Anti-Fungus),
Supresivit
Manufacturer/Supplier, Country, Internet Reference
Ajay Bio-tech (India) Ltd., India
(http://www.ajaybio.com)
49
Ruocco et al.
Table 13 (continued): Trichoderma-based preparations commercialized for biological control of plant diseases.
Commercial
Biocontrol
Organism(s)
Product
Type
Formulation,
Application
Uses - Location,
Crops
Uses, Pathogens controlled
Manufacturer/Supplier, Country, Internet Reference
Combat
T. harzianum,
T. virens
(=T. lignorum
G. virens),
Bacillus
subtilis
Biological
fungicide
Talc; seed
treatment,
broadcast, root
dip, drench,
foliar spray
Grapes, cotton,
pulses, tea, potato,
tomato, oil seeds,
tobacco, spices,
cereals, vegetables,
horticultural crops
Downy mildew, powdery
mildew, die back,
Verticillium, Fusarium,
Panama wilt; pod, seedling,
late blight; root, collar, stem,
red, soft, clump, dry, bean,
fruit, pod rot; black leg,
damping off, abnormal leaf
fall, black thread, canker
BioAg Corporation USA
(http://www.bioag.com/products.html)
Harzian 20
T. harzianum
Biological
fungicide
n/a
orchard crops,
vineyards
Armillaria spp., Pythium
spp., Sclerotinia spp.
Natural Plant Protection (NPP), France
(http://www.agroBiologicals.com/products/P1362.htm)
PlantShield
T. harzianum
Biological
fungicide
Granules,
wettable powder;
soil drench,
foliar spray
Pythium, Fusarium,
Rhizoctonia,
Cylindrocladium,
Thielaviopsis; suppresses
Botrytis
BioWorks, Inc., USA
(http://www.bioworksbiocontrol.com)
Primastop
G. catenulatum Biological
fungicide
Greenhouse,
flowers,
ornamentals,
herbs, nursery,
vegetable crops;
hydroponic,
orchard trees
ornamental,
vegetable, tree
crops
pathogens causing seed, root,
stem rot, wilt disease
Kemira Agro Oy, Finland (http://growhow.kemiraagro.com); AgBio Development Inc.USA
Root Pro,
T. harzianum,
T. cornedia
Seedling, rooting
stage in nursery;
Horticulture flowers,
vegetables,
potatoes
Rhizoctonia solani, Pythium
spp., Fusarium spp.,
Sclerotium rolfsii
Mycontrol Ltd., Israel; Efal Agri, Israel
(http://www.efal.com/main.htm,
http://www.agroBiologicals.com/company/C1096.htm)
Product
(under
development)
RootProtato
Biological
fungicide
Powder; drench,
spray, irrigation
Powder; spores
mixed with
growing media
50
Chapter 6
Many preparations have been developed to ensure a good shelf life of the product based on
Trichoderma. Some of that formulation are stable in terms of pH, that remains constant and low
(5.5) during the entire growth period, thus preventing bacterial contamination. Moreover the shelf
life of the fungus at 25 °C is 1 year and from 1 to 2 years, the number of colonies-forming-units
(CFUs) decreases by one order of magnitude. Many of that formulation have been proven
successful in several experiments in the greenhouse and field. The rapid mass production of
promising antagonists in the form of spores, mycelia or mixtures of both, has been achieved by
liquid-fermentation technology: mass production of biomasses of T. hamatum, T. harzianum, and T.
viride was reached by utilizing commercially available, inexpensive ingredients such as molasses,
brewer's yeast, cotton seed flour, or corn-steeped liquor.. Other techniques have been employed to
improve the delivery of the biocontrol agents. A lignite-stillage (a by-product of sorghum
fermentation) carrier system was tested for applying a T. harzianum preparation to the soil.
Encapsulation of the biocontrol agent in an alginate-clay matrix, using Pyrax as the clay material,
improved yield and propagule viability over time.
Pelletized formulations of wheat bran or kaolin clay in an alginate gel containing conidia,
chlamydospores or fermentex biomass of several Trichoderma isolates revealed increased viability
of stored pellets, and the number of CFUs formed after adding these pellets to the soil was
comparable to that formed from freshly prepared pellets. These growth media and delivery systems
for formulations of biocontrol fungi show promise because they are able to introduce high levels
(106-1010 CFU/g) of fungi into soils not steamed, fumigated, or treated with other biocides.
To enhance biocontrol efficacy, appropriate introduction of the antagonist into the
microenvironment appears to be crucial: formulations have been applied to seedlings prior to
planting or to seeds in furrows. Economic considerations have forced biotechnologists to improve
the application techniques: seed-coating, a technique involving minimal amounts of inoculum was
developed.
Increased biocontrol activity may be achieved by combining two types (or more, if possible) of
biocontrol agents, for example combining Trichoderma with a bacterium, or another beneficial
fungus. The combined activity of the antifungal compounds produced by both microorganisms
could expand the spectrum of pathogens controlled. In fact, in field trials combining T. koningii
with certain fluorescent pseudomonads, greater suppression of take-all disease and increased wheat
yield were achieved relative to plants treated with T. koningii alone (Duffy et al. 1996).Delivery
systems must ensure that biocontrol agents will grow well and achieve their purpose. It is generally
recognized that delivery and application processes must be developed on a crop by crop and
application by application basis. No general solutions exist, and so biocontrol systems must be
developed for each crop. It is very important to use the organism properly and to have appropriate
expectations. Any biocontrol organism will be unable to protect seeds as well as chemical
fungicides. However, it colonizes roots, increases root mass and health, and consequently frequently
provides yield increases, which chemical fungicides applied at reasonable rates cannot do. An
effective method of use is to use the biocontrol fungus in conjunction with chemical fungicides. The
chemicals provide good short-term seed protection, and the biocontrol fungus provides long-term
root protection. As a consequence, yields frequently are increased over use of the chemical alone.
Some experiences evidence that Trichoderma spp. is also highly effective when applied to
blossoms or fruits for control of B. cinerea. Even low levels of the organism applied to strawberry
blossoms by bee delivery or by sprays of liquid formulations are effective. For maximum control of
the Botrytis bunch rot of grape, this initial application needs to be augmented by sprays as fruits
mature, and addition of iprodione as a tank mix to this late application appears to have synergistic
activity over either the biocontrol agent or the chemical fungicide alone.
Novel applications of Trichoderma spp. Trichoderma spp. produce a variety of lytic enzymes that
have a high diversity of structural and kinetic properties, thus increasing the probability of this
fungus to counteract the inhibitory mechanisms used by neighbouring microorganisms. Further,
51
Ruocco et al.
Trichoderma hydrolytic enzymes have been demonstrated to be synergistic, showing an augmented
antifungal activity when combined with themselves, other microbial enzymes, PR proteins of plants
and some xenobiotic compounds (Fogliano et al. 2002; Lorito et al. 1994a, 1994b, 1994c, 1996,
1998; Schirmbock et al. 1994; Woo et al. 2002). In fact, the inhibitory effect of chemical fungicides
for the control of the foliar pathogen B. cinerea was substantially improved by the addition of
minute quantities (10-20 ppm) of Trichoderma CWDEs to the treatment mixture (Lorito et al.,
1994b).
Extensive testing of T. harzianum strain T22 conducted for the registration of this biocontrol
agent in the USA by the Environmental Protection Agency (EPA) has found that the CWDEs do not
have a toxic effect on humans and animals (ED50 and LD50), and that they do not leave residues,
but degrade innocuously in the environment. Therefore, these Trichoderma hydrolytic enzymes
present a novel product for plant disease control based on natural mycoparasitic compounds used by
the antagonistic fungi. Single or mixed combinations of CWDEs with elevated antifungal effects,
obtained from fermentation in inducing conditions, over-expression of the encoding genes in strains
of Trichoderma, or heterologous expression of the encoding genes in other microbes are possible
alternatives for pathogen control. These natural substances originating from the BCA are an
improvement over the use of the living microorganism in the production of commercial
formulations because they are easily characterized, resist desiccation, are stable at temperatures up
to 60° C, and are active over a wide range of pH and temperatures in the agricultural environment.
The important factors to consider in a commercial bio-formulation are product stability, the capacity
to produce consistent results by preserving the characteristics producing the biological effects; the
storability of the material, the ability to be conserved in unspecialized conditions similar to those of
chemical pesticides; and a reasonable shelf-life or time that the product can be stored and used
without compromising the efficacy (Agosin and Aguilera, 1998; Agosin et al., 1997; Powell and
Jutsum, 1993). When a formulation contains the living microorganism component, the treatment
must consist of stabilizing the viability of the BCA. For liquid formulations this can be achieved by
maintaining the product in refrigeration (<10° C) or by freezing in the presence of cryoprotectant
substances. However, conservation of a commercial product in these conditions is not economic for
maintaining low temperatures or efficient because the liquid is both bulky and heavy, plus it is
difficult to sustain these conditions in storage and transportation. In comparison, it is preferable to
obtain formulations that contain a dehydrated product, stored as a powder, granule, talc, etc. Some
works (Ruocco et al. unp) demonstrated that lyophilisation did not reduce chitinolytic activity and
spore vitality when the fermented cultures were treated with compounds that protect the osmotic
integrity of the living material such as glycerol. Generally, lyophilisation is the method that best
maintains viability, but its cost is very high. At the industrial level and in order to obtain a low-cost
product, the methods preferred is spray- or fluidized bed- drying. Many products are obtained by
spray-drying, but this method produces a high loss of viability in some microorganisms (observed
also in this formulation), due to the thermal treatment.
In spite of the relatively abundant number of patents filed for microbial pesticides, the number
of commercial applications has not been as dramatic as expected (Montesinos, 2003). In Europe, the
limiting factor for registration, apart from the cost, is undoubtedly the slow process of decisiontaking. As an example, the first application for patenting a biopesticide, Paecilomyces
fumosoroseus, was submitted to the European Union in 1994 and approved only in 2001. In most
cases, excessive specificity is a problem difficult to solve because it is intrinsic to the biological
control system. In fact, success depends on three living systems: the pathogen or pest, the BCA and
the host plant. Biosafety and environmental concerns are also major limiting factors for microbial
pesticide prospects. Furthermore, the registration procedure to approve a biopesticide formulation
on the market has not been altered to consider the biological aspects of the product, criteria which
are different than those considered for the testing of chemical based products.
52
Chapter 6
Persistence, physiological stresses, timing and coverage of others biological agents
Other references have been screened for biocontrol agents considering the analysis of:
persistence on the target,
resistance to physiological stresses,
timing and coverage.
Cladosporium cladosporioides. The antagonist has been effective in reducing sporulation of
Venturia inaequalis under orchard conditions. Furthermore, the results of the pre-screening indicate
that it is cold and drought tolerant and results of experiments on spore production in solid state
fermentation show that mass production is economically feasible. These results have been obtained
in a stepwise selection approach (Köhl, 2009, Köhl et al., 2009).
Ulocladium atrum and Gliocladium roseum. Köhl et al., 1998 described the effect of treatments
with conidial suspensions of Ulocladium atrum and Gliocladium roseum on leaf rot of cyclamen
caused by Botrytis cinerea was investigated under commercial greenhouse conditions. Spraying U.
atrum (1 × 106 conidia per ml) or G. roseum (2 × 106 conidia per ml and 1 × 107 conidia per ml) at
intervals of 2 to 3 weeks during the production period and spraying U. atrum (1 × 106 conidia per
ml) at intervals of 4 to 6 weeks resulted in a significant reduction of natural infections of petioles by
B. cinerea. U. atrum or G. roseum (1 × 107 conidia per ml) was as effective as the standard
fungicide program. B. cinerea colonized senesced leaves within the plant canopy and infected
adjacent petioles and leaves later. The antagonists colonized senesced leaves and reduced B. cinerea
development on these leaves. Thus, the inoculum potential on petioles adjacent to necrotic leaf
tissues was reduced. The fate of U. atrum conidia on surfaces of green cyclamen leaves during a 70day period after application was studied. The number of conidia per square centimetre of leaf
surface remained relatively constant during the entire experiment. Sixty percent of the conidia
sampled during the experiments retained the ability to germinate. When green leaves were removed
from the plants to induce senescence and subsequently were incubated in a moist chamber, U.
atrum colonized the dead leaves. Senesced leaves also were colonized by other naturally occurring
fungi including B. cinerea. On leaves treated with U. atrum from all sampling dates, sporulation of
B. cinerea was significantly less as compared with the untreated control. Our results indicate that
early applications of U. atrum before canopy closure may be sufficient to achieve commercially
satisfactory control of Botrytis leaf rot in cyclamen.
Kessel et al., 2005 developed a spatially explicit model describing saprophytic colonization of
dead cyclamen leaf tissue by the plant-pathogenic fungus Botrytis cinerea and the saprophytic
fungal antagonist Ulocladium atrum. Both fungi explore the leaf and utilize the resources it
provides. Leaf tissue is represented by a two-dimensional grid of square grid cells. Fungal
competition within grid cells is modelled using Lotka-Volterra equations. Spatial expansion into
neighbouring grid cells is assumed proportional to the mycelial density gradient between donor and
receptor cell. Established fungal biomass is immobile. Radial growth rates of B. cinerea and U.
atrum in dead cyclamen leaf tissue were measured to determine parameters describing the spatial
dynamics of the fungi. At temperatures from 5 to 25°C, B. cinerea colonies expanded twice as
rapidly as U. atrum colonies. In practical biological control, the slower colonization of space by U.
atrum thus needs to be compensated by a sufficiently dense and even distribution of conidia on the
leaf. Simulation results confirm the importance of spatial expansion to the outcome of the
competitive interaction between B. cinerea and U. atrum at leaf scale. A sensitivity analysis further
emphasized the importance of a uniform high density cover of vital U. atrum conidia on target
leaves.
53
Ruocco et al.
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57
Chapter 7
Identified difficulties and conditions for field success of biocontrol.
3. Economic aspects: cost analysis
Bernard Blum1, Philippe C. Nicot2, Jürgen Köhl3 and Michelina Ruocco4
1
International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel, Switzerland
INRA, UR407, Unité de Pathologie Végétale, Domaine St Maurice, 84140 Montfavet, France
3
Wageningen UR, Plant Research International, Droevendaalsesteeg 1, P.O. Box 69,
6700 AB Wageningen, The Netherlands
4
CNR-IPP, Istituto pel la Protezione delle Piante, Via Univrsità 133, Portici (NA) Italy
2
The industrial and commercial development of biological control agents, although needed as an
alternative to chemical pesticides in both organic farming and IPM systems is facing different
constraints which are particularly difficult to overcome due to the size of the involved companies
and the early development stage of the market. These constrains can be classified within four
categories:
- size of the targeted market
- cost of production
- costs of registration
- business profitability
In this paper, in order to be more specific, we shall consider the situation regarding microbial
biocontrol agents (MBCAs), using the real case of a well defined product that we cannot mention
here due to proprietary rights.
Size of the targeted markets
In most of the situations MBCAs are being developed with rather small, if not niche markets. The
total value of MBCAs sold worldwide amounted in 2008 to 620 Mio Euro (122 Mio Euro in
Europe) including products with insecticidal or fungicidal effects. This value can be compared with
the sales of chemical insecticides and fungicides amounting to a total of 21 000 Mio Euros.
MBCAs, with the exception of Bt products which can be used in larger crops such as grapes,
forestry or even cereals, are presently still used in speciality crops, greenhouses and covered crops.
The size of these crops is not growing anymore or at a very reduced rate. The only optimistic
perspective is the intention to develop organic faster farming (objective 20% of the production area
in France in 2030) where MBCAs can find a good market.
Additionally the potential market is widely fragmented within a long list of crops such as
carrots, petersillium, onions, etc, usually referred to as “Minor crops”. These markets are so small
that even large chemical companies refrain from the investments that would cover the needs and the
manufacturers of MBCAs, due to the specificity of their products, are obliged to invest and cover
costs where scale economy can never be reached.
Cost of production
Contrary to the synthesis of chemicals, producing MBCAs requires a complicated and extremely
expensive process of production which can be divided into four phases: fermentation, extraction,
58
Chapter 7
purification, formulation and packaging. All these phases are difficult and require relatively heavy
costs.
Fermentation. This first step has to be undertaken either with solid or with liquid phase
technology. Although the liquid phase fermentation is usually simple and cost effective, the process
is more risky because the produced spores are more fragile. In the contrary using solid fermentation
substrates will produce stronger, but it becomes more difficult to increase the production volume.
Extraction. Here again, there is a very strong difference between the MBCAs produced in
liquid or in solid fermenters. In a liquid, the extraction will be rather easy by filtration, but the
product will need to be dried, which is a very long, energy-demanding and expensive process. From
a solid fermentation process, the extraction will be mechanical. Such a process is rather harmful for
the spores: It is again energy demanding and it is extremely difficult to extract more that 60% of the
spores from a substrate. In such a case the productivity becomes rather poor.
Purification. This step is very important to ensure the stability of the MBCAs produced. The
industrially produced MBCAs always contain impurities which, although biologically inactive, may
become critical over time, potentially creating risks of degradation, inactivation etc. In all situations
the purification step requires a high level of sophistication and expensive processes.
Formulation and packaging. Formulation and packaging of MBCAs, due to their living state
(and the requirement that they remain alive for satisfactory effectiveness of the product), constitute
an extremely difficult step and in any case more expensive than the equivalent process for
chemicals. The choice of co-formulants, adjuvants and packaging material must secure the quality
of the MBCAs and its vitality. This is again a source of problems and heavy costs.
Additionally to all the above mentioned hurtles, it has to be secured that no contamination will
occur, during the fermentation process naturally, but also during the extraction, the purification, the
formulation and the packaging. All the safety measures are very expensive to carry out, but they are
necessary in order to ensure the quality of the product brought to the market. As a consequence of
all these extra expenses and technical difficulties the MBCAs used for this analysis were more than
2.5 times more expensive to produce than an equivalent chemical pesticide (Table 14).
Table 14: Compared structure of the production costs for a microbial biocontrol agent (MBCA)
and a chemical insecticide (source IBMA).
Sales value
Type of production cost
Raw materials
Packaging
Energy and miscellaneous
Manpower
Consumables
Amortisation
TOTAL
Typical Insecticide
100
%*
MBCA
Comments
100
8
29
1
1
5
2
4
2
2
9
3
11
21
56
40% lost material for
MBCA by solid
fermentation process
* costs are expressed as percent of the sales value of the commercial product
Cost of registration
It has been already mentioned that biological control agents suffer from a highly unfavourable
situation compared to chemical pesticides. The regulations for registration have initially been set up
to reduce the risks attached to molecules and the regulator is trying to extrapolate these
requirements for the registration of living organisms.
59
Blum et al.
The estimated cost for registering a microbial biocontrol agent is currently lower than that for a
chemical pesticide (Table 15). However, the size of this investment is still very high for a company
in comparison with the market potential (Table 16).This evaluation indicates that the introduction
on the market of a MBCA is about 4 times less effective than its chemical equivalent.
Table 15: Compared potential costs of registration for a microbial biocontrol agent (MBCA) and a
chemical pesticide (source IBMA)
Area
Toxicity of the
active substance
Toxicity of the
formulation
Environmental
fate
Biology
Ecotoxicology of
active substance
Ecotoxicology of
formulation
Residues
Formulation
Efficacy
TOTAL
Cost for
Chemical (€)
140 000
140 000
40 000
10 000
140 000
10 000
Study Type
Acute studies (6 tests)
Sub-acute (rat study)
Mutagenicity
Toxicity on cultured cells
Acute studies
Toxicity on cultured cells
Soil, water, air
200 000
Mode of action etc
Birds, fish, bees, algae, daphnia, earthworm
Beneficials
Birds, fish, bees, algae,daphnia, earthworm
Beneficials
8 trials / crop
Development of analytical methods
Physical properties, shelf life, etc.
8 field trials
150 000
60 000
20 000
60 000
20 000
80 000
100 000
200 000
40 000
1 410 000
Cost for
MBCA (€)
140 000
120 000
may be waived
not required
140 000
not required
70 000
*50 000
40 000
may be waived
40 000
may be waived
**variable
220 000
40 000
860 000
* cost of strain identification
** e.g. development of strain-specific markers
Table 16: Compared estimated market potential for a microbial biocontrol agent (MBCA) and for a
chemical pesticide (source: IBMA)
Year
1
2
3
4
5
Total early sales
Plateau sales
Registration costs
Ratio registration/ early
sales
Ratio registration/
Plateau sales
Estimated sales value ( Mio€)
Chemical pesticide
MBCA
0.1
0.05
1.2
0.15
6.0
0.90
15.0
1.50
35.0
3.50
57.3
6.10
120.0
15.00
1.410
0.860
2.4 %
14.0 %
1.1 %
5.7 %
60
Chapter 7
Business profitability
Comparing estimated production and other costs, relative to the sales value at plateau level, points
out large differences between chemical pesticides and microbial biocontrol agents (Table 17). The
gap between the two in terms of estimated profit is nearly 10-fold in favour of the chemical
industry.
Table 17: Compared margin structure estimates for the production and sales of a microbial
biocontrol agent (MBCA) and a chemical pesticide (source IBMA)
%*
Sales value at plateau level
Costs of production
Gross margin
Cost of sales
Cost of research
Cost of administration
Earnings before investments taxes
and amortisation (EBITA)
Profit after taxes, provisions and
amortisation
Chemical pesticide
100
21
79
21
8
4
46
18
MBCA
100
56
44
15
12
3
14
2
* costs and margins are expressed as percent of the sales value of the commercial product
Conclusion and outlook for industry
These data show clearly that the profitability of a biocontrol business is much less attractive than
that of chemical pesticides and may explain why the large chemical companies decided in the 90’s
to retreat from this business. Although these companies show presently some new signs of interest,
they seem to remain basically reluctant to re-enter despite the new attractiveness of a fast growing
biocontrol market. Contrary to European and US-based companies, several Japanese firms, such as
Sumitomo chemicals or Mitsui appear to have invested for a potential long term return. Taking
advantage of the divestment by the chemical majors, they have been able to acquire a good business
basis at very attractive conditions. This should enable them to consider optimistically the future
development of the biocontrol industry and its positive trend.
The smaller companies which have invested in this business and try to overcome their financial
problems have only two alternatives:
- Either develop, often at a loss, into larger markets (grapevine, field crops etc), if they can. In
order to sustain these efforts, they will need a strong support from venture capital
companies;
- or enter into venture agreements with other manufacturers/suppliers, in order to build up a
product portfolio which will make them successful in the future.
61
Chapter 8
Identified difficulties and conditions for field success of biocontrol.
4. Socio-economic aspects: market analysis and outlook
Bernard Blum1, Philippe C. Nicot2, Jürgen Köhl3 and Michelina Ruocco4
1
International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel, Switzerland
INRA, UR407, Unité de Pathologie Végétale, Domaine St Maurice, 84140 Montfavet, France
3
Wageningen UR, Plant Research International, Droevendaalsesteeg 1, P.O. Box 69,
6700 AB Wageningen, The Netherlands
4
CNR-IPP, Istituto pel la Protezione delle Piante, Via Univrsità 133, Portici (NA) Italy
2
With estimated sales amounting to only 200 Mio€ in Europe in 2008, the market for biological
control agents appears to be extremely small compared with the 7 000 Mio€ turnover achieved with
chemical pesticides. However, very important efforts have been undertaken for the development of
biocontrol agents. The OECD estimated that 5 000 Mio$ have been spent worldwide in public
research for biocontrol during the last 40 years. This amounts to a yearly average of 500Mio$, not
far from the 600 Mio$ spent yearly in research by the agrochemical industry, but with a
comparatively poor result!
In the Conference on biological control organised in 2003 by IBMA in Béziers, France, the
major stakeholders (farmers, retailers, distributors, regulators etc.) have provided a list of gaps
considered to play a role in preventing wide adoption of biocontrol products. This list was meant to
cover all potential explanations, but provided neither figures nor priority ranking, making it difficult
to prioritize actions for improvement. It was however a general opinion that the complicated and
costly system of registration was the major reason of the problem. As a result, important efforts
have been undertaken to convince the regulators to adopt more facilitating procedures for the
registration of biologicals. These efforts were not without effect and the newly adopted “Pesticides
package” makes it easier, under certain conditions, to register biologicals. In the meantime, several
EU member states have adopted easier registrations tracks, such as the Biopesticides Scheme in the
UK, for example.
In reality, the unique assumption that the current regulations in Europe significantly hamper
the development and the use of biologicals does not seem to be proven by the facts. During a very
long period, the biologicals were not subject to registration and very few products were brought
successfully to the market. At the same time countries such as the USA, New Zealand or Japan have
adopted very liberal registration procedures, but the sales of biologicals remain marginal.
In the frame of ENDURE, it has been therefore decided to get a detailed and quantified idea on
the gaps which, in Europe, restrain the adoption of biologicals, especially at the users and
commercial levels. In order to achieve this objective, a Pan-Europa survey was undertaken from
2007 until 2008, with the assistance of the public opinion organisation Agridata.
Methodological approach: survey of European farmers
Since no validated data were available about the real market and the use of biological control agents
in Europe, it has been necessary to build up a form of electronic map of the European agriculture
and of the distribution of the potential users.
62
Chapter 8
A survey was carried out to evaluate the size of the biocontrol market in Europe and to identify key
factors that could influence its future evolution. This study included four main steps:
-
-
-
Localisation of the main crops and cropping systems.
Using the data from EUROSTAT and national statistics a model of European agriculture was
constructed.
Randomised sampling of farmers and retailers.
The model was used for the selection of 12 production systems (Table 18) located on 25 sites in
9 countries (Table 19) where 2000 farmers and 21 retailers were identified.
The selected sample was contacted by phone directly and a questionnaire (Table 20) was sent to
those who agreed to participate in the survey. A total of 675 full responses were obtained and
analysed.
Complementary survey.
In order to validate the process, more specific data was collected in a survey concerning the
biological control of wood diseases of grapevine in France
Table 18: Production systems selected for a survey of factors influencing biocontrol use in Europe
(source IBMA)
Type of cropping system
Large arable crops
Multicropping
arable crops dominant
animal production dominant
Fruit production
orchards
grapes
Tomato production
protected
field
Geographical sub-categories
North, South
Mountains, North, South
Mountains, North South
Table 19: Geographical distribution of sampling sites for a survey of factors influencing biocontrol
use in Europe (source IBMA)
number of
sampling site
2
1
4
2
4
4
3
3
2
Country
Austria
Denmark
Germany
Greece
France
Italy
Poland
Spain
United Kingdom
63
Blum et al.
Table 20: Structure of the questionnaire used in a survey of European farmers and retailers of
biological control products
Categories of questions
Geographical identification
System of production concerned
Ownership and social related aspects
Crop protection issues / pest occurrence, etc
Economy of the farm, actual costs, revenues etc
Expectations for future, cropping systems, investments, etc
Relations with input suppliers
Relations with advisors
Relations with authorities
Relation with the food chain (coops, supermarkets etc.)
Relations with the consumers
Relations with the public
Expectations about innovations, role of science
Open comments
Nbr of Questions
5
12
5
18
12
9
18
18
18
18
18
18
12
2
Survey Results: The estimated market of biocontrol in Europe
The questionnaire made it possible to estimate the total biological market in ha and in value (Figure
11) and its partition among different crops (Figure 12).
These data confirm that in 2008, the main use of biologicals was in protected crops, followed
by grapevine and fruit production. Nearly 40% of the estimated biocontrol market consisted in sales
of beneficial insects, compared to 25% for microorganisms and 21% for semiochemicals (Figure
11).
Total estimated EU sales of biocontrol products = 204 Mio € in 2008
18 Mio€
Beneficial insects
43 Mio€
79 Mio€
Beneficial nematods
Microbial biocontrol agents
Semiochemicals
Natural substances
52 Moi€
12 Mio€
Figure 11: Estimated sales of biocontrol products in Europe in 2008 (in Million €). The estimates
were obtained by extrapolating use patterns in a representative sample of EU farmers.
64
Chapter 8
80
% of supply
70
% of acreage
60
% of total
50
40
30
20
10
0
ot
Pr
te
ec
d
s
op
cr
d
el
Fi
v
s
le
ab
t
e
eg
ra
G
s
pe
ts
ui
Fr
d
el
Fi
cr
s
op
ns
de
r
a
G
am
rn
o
,
ta
en
ls
Figure 12: Estimated distribution of biocontrol use among types of crops in 2008 in Europe
Survey results: Factors of development of biocontrol
The exploitation of the questionnaires was somewhat difficult due to the large variety of farmers
and situations. Additionally, several open ended questions were introduced to collect opinions on
possible additional gaps and opportunities which were not mentioned in the form.
Qualitative analysis. In a first step, the analysis of the responses led to the identification of 12
factors deemed to have a significant influence on the future development of biological control
Nine factors with a positive influence:
o Ability of manufacturers to invest in R&D
o Financial strength of manufacturers
o Direct involvement of leading distributors
o Pull from the fresh food wholesalers and from the food industry
o Demand from consumers and NGOs
o Incentives given to growers
o Education of advisors and growers
o Availability of Decision Support Systems (DSS)
o Regulatory obstacles to chemical pesticides
Three factors with a negative influence:
o Regulations not adapted to Biological control
o Discovery of novel effective and safe chemicals
o Development of new resistant crops
Quantitative analysis. In a second step, a quantitative analysis was conducted to estimate the
influence of the identified factors. For this, 320 contacts (50% of the sample) were requested to
65
Blum et al.
indicate which of the 12 factors they considered as important in terms of their potential impact on
the evolution of future use of biological control agents. For those factors selected as important, the
respondents were asked to weigh the expected impact positively or negatively on a scale from 0 to
20.
The data were used to compute for each of the 12 factors:
a) an Influence Index, calculated as the percentage of respondents who selected the factor as
important
b) a Weight Index, calculated as the average of the weights attributed to the factor by those
respondents who selected it as important
c) a Growth Index, combining the two other indices according to the following formula:
GI = (Influence Index)*(Weight Index)/10
This index represents the overall estimate of the influence of a factor on the future use of
biological control agents by European farmers.
The scores computed for each of the 12 factors are presented in Table 21. Among the factors
deemed to carry the most impact on future use of biological control by European farmers the action
by far the most cited was the establishment of incentives for farmers (factor D).
Table 21: Impact of twelve factors on the future use of biocontrol agents by European farmers
according to a survey of 320 farmers
Factors
A
Registration for biological control
products remains as present
Influence
Index (%)*
12
B
C
D
E
F
Involvement of distribution
65
Size / strength of the manufacturers
55
Incentives to growers
87
Education of advisors and growers
27
Decision Support Systems available
12
Pull from wholesalers and food
G
43
industry
H
Stringent registration of chemicals
16
I
New safe chemical pesticides
42
J
Progress in R&D of Biocontrol
8
K
New resistant varieties
16
L
Pull from Consumers
67
* see main text above for the specific definition of the indices
Weight Index*
(scale from
-20 to +20)
Growth
Index*
Rank of
positive
influence
- 15
- 18.0
8
12
18
8
7
52.0
66.0
156.6
21.6
7.2
4
3
1
5
9
16
66.8
2
14
- 12
14
-4
2
22.4
- 3.0
11.2
- 6.4
13,4
6
8
7
The second most important factors based on the Growth Index (G, C and B in Table 21) were
linked to the influence of key economic actors (the wholesalers, the food industry, the distributors
and manufacturers of biocontrol products). The factors with the lowest scores were those related to
scientific innovation (factors K, I, J). Interestingly, both factors linked to regulatory aspects (factors
H and A) also had a relatively low Growth Index. The registration requirements are obviously more
a concern for the industry than for the users of the plant protection products. Surprisingly, the
66
Chapter 8
efficacy and the price of the biologicals, usually considered as two critical factors, were not
mentioned as real constraints. This may be due to two reasons:
(1) It is anticipated that only “effective” solutions will be registered in the EU, showing the high
confidence of the farmers and the retailers in the registration systems
(2) The selling price of the new solutions (biological control products) will necessarily cope with
the current price levels. Too highly priced, the new solutions will simply be ignored.
Conclusions
The gaps and the opportunities for the development of biological crop protection products are
extremely relative to people concerned. While the industry, due to the heavy factor time/cost to the
market, considers the regulation requirements as a major obstacle, the users and the retailers are
much more influenced by the pull and push actions exercised at the market level. Somewhat
disappointing is the relative low concern about the technical progress offered by the biological
solutions.
67
Conclusions and perspectives
Perspectives for future research-and-development projects on biological
control of plant pests and diseases
Philippe C. Nicot1, Bernard Blum2, Jürgen Köhl3 and Michelina Ruocco4
1
INRA, UR407, Unité de Pathologie Végétale, Domaine St Maurice, 84140 Montfavet, France
International Biocontrol Manufacturers Association, Blauenstrasse 57, CH-4054 Basel, Switzerland
3
Wageningen UR, Plant Research International, Droevendaalsesteeg 1, P.O. Box 69,
6700 AB Wageningen, The Netherlands
4
CNR-IPP, Istituto pel la Protezione delle Piante, Via Univrsità 133, Portici (NA) Italy
2
The review of published scientific literature on the biological control of selected pests and diseases
has lead to the identification of clear knowledge gaps highlighted in previous chapters. Further
bottlenecks were revealed by seeking the possible reasons for the striking discrepancy between the
rich inventory of potential biocontrol agents described by scientists and a very small number of
commercial products on the market.
To complement these analyses, the participants of Research Activity 4.3 of the European
Network ENDURE organized consultations of experts (scientists, extension specialists and
representatives of the Biocontrol industry) at the occasion of scientific meetings of three Working
Groups of IOBC-wprs.
-
Working Group "Integrated Control of Plant Pathogens": meeting on "Molecular Tools for
Understanding and Improving Biocontrol" in Interlaken (Switzerland) September 9-12, 2008.
(attended by P.C. Nicot and B. Blum – discussion session about the outlook on biocontrol
against plant diseases)
-
Working Group “Multitrophic Interactions in Soil” meeting in Uppsala (Sweden), 10-13 June
2009. (attended by C. Alabouvette – roundtable about the outlook on biocontrol of soilborne
pests and diseases)
Working Group "Insect Pathogens and Insect Parasitic Nematodes": meeting on "Future
Research and Development in the Use of Microbial Agents and Nematodes for Biological Insect
Control" in Pamplona (Spain), 22-25 June, 2009 (attended by C. Alabouvette – his plenary
presentations about the outlook on biocontrol of diseases and pests has been published*).
These consultations were further complemented by discussions at the occasion of various
meetings of participants of Research Activity 4.3 to identify the most prominent issues that could be
tackled by future research and development activities. The key elements are organised below in
three categories, based on their relevance to the concern of the research community, development or
industry.
-
Research issues
Five key issues have been identified in term of research needs:
Devise better strategies for the screening of biocontrol agents. The demand for new
biocontrol agents is already high. It is expected to increase sharply in the EU, with the ongoing
*
Alabouvette, C, Cordier, C. 2009 Biological control of plant diseases: Future research goals to make it successful.
IOBC/WPRS Bulletin 45:3-5.
68
Conclusions and perspectives
reduction of available chemical pesticides and the need for new non-chemical plant protection tools
to comply with Directive 2009/128/EC. Current methods need to be improved both in terms of
logistics (high throughput to allow rapid mass screening of large numbers of candidates) and in
terms of the pertinence of criteria for efficacy, production and commercialization. This topic has
been tackled within Research Activity 4.3 of the European Network ENDURE for microbial
biocontrol agents against diseases (Deliverable DR4.9) and the results have been published (Köhl et
al., 2011*).
Improve knowledge on efficacy-related issues. The criteria traditionally used to asses the
efficacy of biological control methods may be misleading because contrarily to conventional
pesticides, biocontrol does not intend to eradicate pests and diseases but, rather, to install a
biological balance which will enable the plants to grow more healthily. However the consistency of
field efficacy remains one of the constraints for the large scale use of biological control of plant
diseases. Despite much recent progress, research efforts are still necessary for (1) a better
understanding of key parameters of field efficacy in relation to the type of biocontrol agent and their
modes of action and (2) implementing the most promising methods for efficacy improvement.
Promising avenues of research are to be sought both in terms of exploiting the biological properties
of the biocontrol agents and enhancing their effectiveness through formulation of the products.
Results obtained on these topics should provide key information both for the design of optimised
production and application strategies, but also for improving the screening process of future
biocontrol agents as mentioned in the point above.
Promote multidisciplinary approaches to integrate better biocontrol with IPM and other
production issues. Based on passed published experience, it is clear that levels of protection
provided by a single biocontrol agent alone will seldom be sufficient, especially when faced with
field conditions unfavourable to their effectiveness or with very high inoculum pressures of a pest
or plant pathogen. More emphasis will need to be placed on the compatibility of biocontrol agents
with the implementation of IPM, preferably in a systemic approach of integrated production.
Among the many possible interactions to be considered, compatibility and combined used of
biocontrol and plants genetically modified for improved resistance to pest or plant diseases should
not be overlooked.
Develop adapted delivery technologies. Much progress has been made in packaging
technology and delivery for macrobial biocontrol agents (e.g. beneficial arthropods). In contrast,
treatments with microbial biocontrol agents (against pests or diseases) still rely on sprayers
developed for the application of pesticides. Research is needed to provide growers with low
pressure spraying equipment to preserve the viability of the microbials. Technological
improvements are also needed for optimal coverage of the target plant surfaces to be protected by
the biocontrol agents.
Safeguard the durability of biocontrol. Certain pests and pathogens are known for their
capacity to develop resistance to chemical pesticides or to overcome varietal resistance. The
durability of biological control has often been assumed to be higher than that of chemical control,
but several examples of resistance of pests have already been reported. Much less is known about
plant pathogens, probably in part because biological control against diseases is still very rare.
Significant research efforts are needed to anticipate the potential hurtles in this domain and integrate
durability concerns both in the screening of new biocontrol agents and in the careful management of
their use once they become commercially available.
*
Köhl, J., Postma, J., Nicot, P., Ruocco, M., Blum, B. 2011. Stepwise screening of microorganisms for commercial use
in biological control of plant pathogenic fungi and bacteria. Biological Control 57, 1-12.
69
Nicot et al.
Issues for development
Three key issues have been identified in terms of development. They are directly related to
improving the efficacy of crop protection but also to acceptability of biocontrol by farmers.
Training of advisers and farmers. Compared to chemical control, the implementation of
biological control presents an additional level of technical complexity when the "active substance"
is a living organism or microorganism, whose liveliness and development on the target crop
underpins the effectiveness of the protection. In many situations, achievement of successful
biocontrol of pests has been linked to an active role of advisers in accompanying the farmers, at
least during their initial phase of adoption and implementation. The success of large scale use of
biological control in the future will require stepping up the technical training of farmers and of
advisors. Such action will also positively influence the adoption issues mentioned below.
Development and dissemination of Decision Support Systems (DSS). Growers routinely
make decisions that take into account multiple constraints (both technical and economic) of their
activity. However, the complexity of biocontrol and its necessary integration in a systems approach
of crop protection and crop production make DSS more and more indispensible, including in their
function as easily consultable repositories of knowledge on available choices.
Establishment of demonstration schemes and development of farmers' networks. This
action is needed to stimulate the dissemination of information to and among farmers, but also to
facilitate exchange between the end users of biocontrol and the other actors of research,
development and commercialization of the products. Breaking up regional and national barriers and
including a European dimension to such networks is desirable for optimal efficacy of multisite
experimental trials.
Industrial issues
Quality control. Ongoing efforts by the manufacturers of biological control agents to
guarantee the quality of their products need to be stepped up. The definition of tests and their
routine implementation is crucial to ensure reliable effectiveness and maintain confidence of
farmers for biocontrol. Whenever possible, such tests should include not only an evaluation of
viability of the biocontrol agent but also an evaluation of physiological parameters related to its
efficacy, based on knowledge of its modes of action.
Improve distribution systems. Distibution systems need to be improved to safeguard the
quality of the products and provide technical advice for the users. In many cases, the distribution of
biocontrol products is common with that of chemical pesticides. One possible avenue of progress
would be to improve awareness on the specificities of handling biocontrol products, especially those
containing living organisms or micro-organisms. Another would be the development of sizeable
distributions networks focused on biocontrol, which could be brought together by groups of
(currently often small) producers of biocontrol products.
70
Appendices
For Chapter 1
Appendix 1. Inventory of biocontrol agents described in primary literature (1998-2008) for
successful effect against Botrytis sp. in laboratory experiments and field trials
with selected crops
Appendix 2. Inventory of biocontrol agents described in primary literature (1998-2008) for
successful effect against powdery mildew in laboratory experiments and field
trials on selected crops.
Appendix 3. Inventory of biocontrol agents described in primary literature (1973-2008) for
successful effect against the rust pathogens in laboratory experiments and field
trials on selected crops
Appendix 4. Inventory of biocontrol agents described in primary literature (1973-2008) for
successful effect against the downy mildew / late blight pathogens in laboratory
experiments and field trials on selected crops
Appendix 5. Inventory of biocontrol agents described in primary literature (1973-2008) for
successful effect against Monilinia in laboratory experiments and field trials on
selected crops
Appendix 6. Primary literature (2007-2009) on biological control against Fusarium oxysporum
For Chapter 2
Appendix 7. Number of references retrieved by using the CAB Abstracts database in order to
review scientific literatures on augmentative biological control in selected crops
for Chapter 2.
Appendix 8. Collection of data on augmentative biological control of pests in grapevine. Each
table refers to a group of biocontrol agents.
For Chapter 3
Appendix 9. References on classical biological control against insect pests (cited in Chapter 3)
For Chapter 4
Appendix 10. Substances included in the "EU Pesticides Database" as of April 21 2009
Appendix 11. Invertebrate beneficials available as biological control agents against invertebrate
pests in five European countries.
71
Appendix 1. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1998-2008) for
successful effect against Botrytis sp. in laboratory experiments and field trials with selected crops
Tomato + Cucumber + Pepper (target pathogen = B. cinerea)
Success in field trials
Bacteria
Bacillus amyloliquefaciens BL3, pepper (Park et al., 1999)
Bacillus licheniformis > FG (Lee et al., 2006)
Bacillus subtilis strain QST 713 (Serenade ASO) (Ingram and Meister, 2006),
Quadra 136, preventive (Utkhede and Mathur, 2006)
Brevibacillus brevis (Seddon et al., 2000) (McHugh et al., 2002) (Schmitt et al.,
2001)
Brevibacillus brevis WT + Milsana / cucumber (Konstantinidou-Doltsinis et al.,
2002)
Paenibacillus polymyxa BL4, pepper (Park et al., 1999)
Pseudomonas putida Cha94, pepper (Park et al., 1999)
Streptomyces (Mycostop(R), (Lahdenpera and Korteniemi, 2008)actinomyces
(Yao et al., 2007), strains III-61 and A-21 (Pan et al., 2005)
Bakflor (consortium of valuable bacterial physiological groups) (Kornilov et al.,
2007)
M
Fungi + yeasts:
Clonostachys rosea (ADJ 710 OMRI), (Shipp et al., 2008)
Gliocladium sp. (Georgieva, 2004)
Gliocladium catenulatum Prestop(R), preventive (Utkhede and Mathur, 2006)
(Utkhede and Mathur, 2002) (Lahdenpera and Korteniemi, 2008)
Gliocladium viride (Lisboa et al., 2007)
Microdochium dimerum (Nicot et al., 2003) (Trottin-Caudal et al., 2001)
Rhodosporidium diobovatum S33 preventive (Utkhede and Mathur, 2006)
curative (Utkhede and Mathur, 2002), /cucumber (Utkhede and Bogdanoff,
2003)
Trichoderma sp. (Georgieva, 2004)
Trichoderma harzianum (Lisboa et al., 2007), T39 (Trichodex) tomato (Apablaza
and Jalil R, 1998) (Moreno Velandia et al., 2007), tomato + cucumber
(Elad, 2000b) (Dik and Wubben, 2001) / cucumber (Elad, 2000a), TM /
pepper (Park et al., 1999), RootShield curative (Utkhede and Mathur, 2002),
T22 PlantShield(R) curative (Utkhede and Mathur, 2006)
Variable little or no effect once in the field (good in lab):
Brevibacillus brevis WT / cucumber (Konstantinidou-Doltsinis et al., 2002)
Gliocladium catenulatum (Prestop). (Ingram and Meister, 2006)
Trichoderma (tomato + pepper) (Salas Brenes and Sanchez Garita, 2006)
Trichoderma harzianum T39 Trichodex with BOTMAN (Moyano et al., 2003)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus antagonists (Tsomlexoglou et al., 2000) (Enya et al., 2007) (Tsomlexoglou et al., 2001) (Tsomlexoglou et
al., 2002)
Bacillus circulans (Wang et al., 2008b)
Bacillus subtilis (Wang et al., 2008b) (Sadfi-Zouaoui et al., 2007a) (Gu et al., 2008) (Sadfi-Zouaoui et al., 2007b)
Bacillus licheniformis (Lee et al., 2006) (Sadfi-Zouaoui et al., 2007a)
Brevibacillus brevis (White et al., 2001) (Seddon and Schmitt, 1999) (Seddon et al., 2000) (Allan et al., 2003)
Cupriavidus campinensis / cuc, tom (Schoonbeek et al., 2007)
Halomonas subglaciescola, Halobacillus litoralis, Marinococcus halophilus, Salinococcus roseus, Halovibrio
variabilis, Halobacillus halophilus, Halobacillus trueperi (Sadfi-Zouaoui et al., 2008)
Halomonas sp. K2-5 (Sadfi-Zouaoui et al., 2007b)
Micromonospora coerulea (Kim et al., 1999)
Pantoea (Enya et al., 2007)
Pseudomonas aeruginosa (Hernandez-Rodriguez et al., 2004) 7NSK2 (Audenaert et al., 2002)
Pseudomonas fluorescens (Yildiz et al., 2007) (Hernandez-Rodriguez et al., 2004)
Burkholderia cepacia (Hernandez-Rodriguez et al., 2004)
Serratia plymuthica HRO-C48 (Ma et al., 2007), IC1270 (Meziane et al., 2006), IC14 / cucumber (Kamensky et
al., 2002, Kamensky et al., 2003)
Streptomyces ahygroscopicus var. wuyiensis (Sun et al., 2004)
Streptomyces lydicus/ cucumber (Farrag, 2003)
Fungi + yeasts:
Aureobasidium pullulans (Dik et al., 1999) (Dik and Elad, 1999)
Beauveria sp. (Diaz et al., 2007)
Candida guilliermondii strains 101 and US 7 (Saligkarias et al., 2002)
Candida oleophila strain I-182 (Saligkarias et al., 2002)
Candida pelliculosa (Bello et al., 2008)
Clonostachys rosea (Nobre et al., 2005) (Sutton et al., 2002) (Yohalem, 2001)
Cryptococcus laurentii (Xi and Tian, 2005)
Cryptococcus albidus (Dik et al., 1999) (Dik and Elad, 1999)
Gliocladium (Hmouni et al., 2005) (Hmouni et al., 2006, Hmouni et al., 1999)
Gliocadium viride (Bocchese et al., 2007) (Lisboa et al., 2007)
Microdochium dimerum (Bardin et al., 2008) (Bardin et al., 2004b) (Bardin et al., 2004a) (Decognet and Nicot,
1999) (Decognet et al., 1999) (Trottin-Caudal et al., 2001) (Nicot et al., 2002)
Pichia guilliermondii (Zhao et al., 2008)
Rhodosporidium diobovatum (S33), (Utkhede et al., 2001)
Rhodotorula glutinis Y-44 (Kalogiannis et al., 2006)
Rhodotorula rubra (Bello et al., 2008)
Trichoderma (Hmouni et al., 2005) (Hmouni et al., 1999)
Trichoderma harzianum (Hmouni et al., 2006) (Fiume et al., 2008) (Barakat and Al-Masri, 2005) (Lisboa et al.,
72
Appendix 1
2007) T115 (Meyer et al., 2001) Trichodex T39 (Elad et al., 1998) (Yohalem et al., 1998) (Meyer et al., 1998)
(Jalil R et al., 1997) (Dik et al., 1999) (Dik and Elad, 1999), RootShield (Utkhede et al., 2001), Th-B /pepper
(Li et al., 2004), Rifai (Gromovikh et al., 1998)
Trichoderma taxi ZJUF0986 (Wang et al., 2008a)
Trichosporon pullulans (Cook, 2002)
Ulocladium atrum (Nicot et al., 2002) (Fruit and Nicot, 1999) (Yohalem, 2001) / cucumber (Yohalem, 1997)
Ustilago maydis (Teichmann et al., 2007)
Oomycetes
Pythium oligandrum (Floch et al., 2001) (Wang et al., 2007a)
Little or no effect once in the field (good in lab):
Trichoderma spp. commercial preparations/ cucumber (Yohalem, 1997)
B
O
Milsana + Brevibacillus brevis WT / cucumber (Konstantinidou-Doltsinis et al.,
2002)
Variable little or no effect once in the field:
Reynoutria sachalinensis extract (Milsana); (Ingram and Meister, 2006)
calcium foliar fertilizers (CaH2O2, CaSO4, Ca(NO3)2, CaCl2 and CaO),
(Mizrakci and Yildiz, 2002)
volatile substances produced by grape cv. Isabella (Vitis labrusca) (postharvest) (Kulakiotu et al., 2004) (Kulakiotu
and Sfakiotakis, 2003)
Compost water extracts prepared from animal sources (horse, sheep, and cattle) and a plant source (olive),
(Hmouni et al., 2006)
Adipic acid monoethyl ester (Vicedo et al., 2005)
Calcium foliar fertilizers (CaH2O2, CaSO4, Ca(NO3)2, CaCl2 and CaO), (Mizrakci and Yildiz, 2002)
Chitosan Elexa (Acar et al., 2008)
Benzothiadiazole (BTH) (Hernandez-Rodriguez et al., 2004)
Variable little or no effect :
Vital pasta, Vital gel and Elot-Vis (Gielen et al., 2004)
73
Nicot et al. (Appendix for Chapter 1)
Grapes (target pathogen = B. cinerea)
Success in field trials
Bacteria
Acinetobacter lwoffii PTA-113, (Magnin-Robert et al., 2007)
Pseudomonas fluorescens PTA-CT2, (Magnin-Robert et al., 2007)
Pantoea agglomerans PTA-AF1 (Magnin-Robert et al., 2007)
Bacillus (isolate UYBC38) (Rabosto et al., 2006)
Bacillus subtilis strain QST 713 (serenade) (Benuzzi et al., 2006) Serenade,
moderate to good control (Schilder et al., 2002)
M
B
O
Fungi + yeasts:
Acremonium cephalosporium, strain B11 (Zahavi et al., 2000)
Candida guilliermondii, strain A42 (Zahavi et al., 2000)
Chaetomium cochlioides (Lennartz et al., 1998)
Gliocladium (Cherif and Boubaker, 1998)
Gliocladium roseum (Holz and Volkmann, 2002)
Hanseniaspora uvarum (isolate UYNS13) (Rabosto et al., 2006)
Trichoderma (Cherif and Boubaker, 1998)
Trichoderma harzianum (Holz and Volkmann, 2002), Rootshield(R) (Marco and
Osti, 2007) Rifai, 1295-22, (Harman et al., 1996), Trichodex 25 WP
(Turcanu, 1997)
Trichoderma virens 31 (Harman et al., 1996)
Trichosporon pullulans (Holz and Volkmann, 2002)
Ulocladium atrum, low disease pressure (Metz et al., 2002) (Roudet and Dubos,
2001) (Schoene et al., 1999) (Holz and Volkmann, 2002) (Lennartz et al.,
1998) (Schoene and Köhl, 1999), isolate 385 (Schoene et al., 2000)
Ulocladium oudemansii + 5-chlorosalicylic acid in combination (Reglinski et al.,
2005)
Variable little or no effect once in the field:
Trichoderma harzianum partial effect (Monchiero et al., 2005)
Ulocladium oudemansii partial effect (Monchiero et al., 2005)
Ulocladium atrum, high disease pressure (Metz et al., 2002) (Roudet and Dubos,
2001)
Croplife (citrus and coconut extract) + Plantfood (foliar fertilizer), moderate to
good control (Schilder et al., 2002)
Milsana (giant knotweed [Fallopia sp.] extract), moderate control (Schilder et al.,
2002)
Chitosan (Amborabe et al., 2004)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus sp., (Paul et al., 1998) (Krol, 1998) (Trotel-Aziz et al., 2003), isolate UYBC38 (Rabosto et al., 2006)
Cupriavidus campinensis (Schoonbeek et al., 2007)
Pseudomonas sp. (Trotel-Aziz et al., 2003), strain PsJN (Barka et al., 2002)
Pseudomonas fluorescens (Krol, 1998)
Pantoea (Trotel-Aziz et al., 2003)
Fungi + yeasts:
Alternaria spp., (Walter et al., 2006)
Aureobasidium pullulans, L47 postharvest (Lima et al., 1997), LS-30 postharvest (Castoria et al., 2001)
Candida oleophila (Lima et al., 1997), postharvest (El-Neshawy and El-Morsy, 2003)
Coniothyrium (Sesan et al., 2002)
Debaryomyces hansenii (Santos et al., 2004)
Epicoccum spp (Sesan et al., 2002) (Walter et al., 2006) (Fowler et al., 1999)
Gliocladium, (Sesan et al., 2002)
Hanseniaspora uvarum (isolate UYNS13) (Rabosto et al., 2006)
Kloeckera spp. (Cirvilleri et al., 1999)
Metschnikowia fructicola, postharvest (Karabulut et al., 2003), postharvest (Kurtzman and Droby, 2001)
Muscodor albus, postharvest (Gabler et al., 2006)
Pichia anomala (strain FY-102) (Masih et al., 2000) (Santos et al., 2004)
Pichia membranaefaciens (Masih and Paul, 2002) (Masih et al., 2001) (Santos and Marquina, 2004) (Santos et al.,
2004)
Scytalidium, (Fowler et al., 1999)
Trichoderma spp. (Walter et al., 2006) (Fowler et al., 1999)
Trichoderma harzianum CECT 2413 – mutant (Rey et al., 2001), Rifai postharvest (Batta, 2007)
Trichoderma viride, (Sesan et al., 2002)
Trichothecium, (Sesan et al., 2002)
Tricothecium roseum (Fowler et al., 1999)
Ulodadium spp (Walter et al., 2006) (Fowler et al., 1999)
Ulocladium atrum isolate 385 (Schoene et al., 2000)
Verticillium, (Sesan et al., 2002)
Oomycetes
Pythium paroecandrum (Abdelghani et al., 2004)
Pythium periplocum (Paul, 1999b)
volatile substances produced by grape cv. Isabella (Vitis labrusca) (postharvest) (Kulakiotu et al., 2004) (Kulakiotu
and Sfakiotakis, 2003)
74
Appendix 1
Strawberry (target pathogen = B. cinerea)
Success in field trials
Bacteria
Paenibacillus polymyxa 18191 (Helbig, 2001b)
Pseudomonas fluorescens (Abada et al., 2002)
M
Fungi + yeasts:
Aureobasidium pullulans (Stromeng et al., 2006)
Candida fructus, (El-Neshawy and Shetaia, 2003)
C. glabrata, (El-Neshawy and Shetaia, 2003)
C. oleophila (El-Neshawy and Shetaia, 2003)
Cryptococcus albidus (Helbig, 2002)
Epicoccum nigrum, (Stromeng et al., 2006)
Metschnikowia fructicola (=FG) (Karabulut et al., 2004)
Pichia guilermondii + Bacillus mycoides mixture (Guetsky et al., 2001)
(Guetsky et al., 2002)
Rhodotorula glutinis (Helbig, 2001a)
Trichoderma harzianum (Abada et al., 2002) (Antoniacci et al., 2000)
(Maccagnani et al., 1999), 1295-22 (Kovach et al., 2000), (atroviride) P1
(Hjeljord et al., 2001), T39 (Shafir et al., 2006), Trichodex (Freeman et al.,
2001) (Freeman et al., 2002) (Freeman et al., 2004)
Trichoderma products (BINAB) (Ricard and Jorgensen, 2000)
Ulocladium atrum (Boff, 2001) (Boff et al., 2002a) (Boff et al., 2002b) (Köhl et
al., 2001) (Köhl et al., 2004) (Köhl and Fokkema, 1998)
Variable little or no effect once in the field:
Bacillus subtilis (Gengotti et al., 2002)
Gliocladium roseum (Chaves and Wang, 2004)
Gliocladium catenulatum, (Prokkola et al., 2003), but low disease incidence
(Prokkola and Kivijarvi, 2007)
Trichoderma sp (Stensvand, 1997), (Stensvand, 1998) (Hjeljord et al., 2000)
(Prokkola et al., 2003), but low disease incidence (Prokkola and Kivijarvi,
2007)
Trichoderma harzianum (atroviride) (Hjeljord, 2002) (Hjeljord et al., 2001),
(Gengotti et al., 2002), Trichodex 40 WP (Meszka and Bielenin, 2004)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus sp. (isolate 17141) (Helbig et al., 1998)
Bacillus pumilus (Essghaier et al., 2007), NCIMB 13374 (Swadling and Jeffries, 1998)
Bacillus subtilis, (Essghaier et al., 2007) (Sardi et al., 2008) (Helbig and Bochow, 2001) (Marquenie et al., 1999)
(Zhao et al., 2007) (Abada et al., 2002) (Gengotti et al., 2000)
Bacillus marismortui, (Essghaier et al., 2007)
Bacillus licheniformis, (Essghaier et al., 2007)
Bacillus thuringiensis (Bacikol) (Kandybin, 2003)
Virgibacillus marismortui, (Essghaier et al., 2007)
Enterobacteriaceae (10B1, 5B4) (Guinebretiere et al., 2000)
Halomonas sp. (Essghaier et al., 2007)
Pantoea agglomerans strain EPS125, postharvest (Bonaterra et al., 2004)
Pseudomonas fluorescens (Abada et al., 2002), NCIMB 13373 (Swadling and Jeffries, 1998)
Pseudomonas cepacia (Marquenie et al., 1999)
Pseudomonas chlororaphis isolate I-112 (Gulati et al., 1999)
Pseudomonas syringae but phytotox (Pellegrini et al., 2007)
Fungi + yeasts:
Aureo basidium pullulans (Adikaram et al., 2002)
Candida reukaufii, (Guinebretiere et al., 2000)
Candida pulcherrima, (Guinebretiere et al., 2000)
Clonostachys rosea (Cota et al., 2008), IK726 (Mamarabadi et al., 2008)
Cryptococcus albidus (Helbig, 2002)
Cryptococcus laurentii (Zheng et al., 2003)
Gliocladium virens (Tehrani and Alizadeh, 2000)
Metschnikowia fructicola (Shemer(R) postharvest (Ferrari et al., 2007)
Pichia guilermondii + Bacillus mycoides mixture (Guetsky et al., 2002b) (Guetsky et al., 2001b) (Guetsky et al.,
2001a) (Guetsky et al., 2002a)
Rhodotorula glutinis, postharvest (Zhang et al., 2007a), (Helbig, 2001a)
Trichoderma sp (Santorum et al., 2002)
Trichoderma harzianum (Abada et al., 2002) (Tehrani and Alizadeh, 2000) (Sanz et al., 2002), T39 (Bilu et al.,
2004) (Levy et al., 2004a) (Levy et al., 2006) (Levy et al., 2004b), atroviride P1 (Hjeljord, Stensvand et al.
2001)
Trichoderma asperellum (Sanz et al., 2005) (Sanz et al., 2002)
Trichoderma longibrachiatum (Sanz et al., 2002)
Trichoderma atroviride (Sanz et al., 2002)
Trichoderma koningii, (Tehrani and Alizadeh, 2000)
Trichoderma viride (Tehrani and Alizadeh, 2000)
Ulocladium atrum (Boff, 2001) (Berto et al., 2001) (Boff et al., 2001)
Verticillium lecanii (Koike et al., 2004)
Variable little or no effect once in the field:
Pichia guilermondii (Wszelaki and Mitcham, 2003)
75
Nicot et al. (Appendix for Chapter 1)
B
O
Messenger (harpin), (Meszka and Bielenin, 2004)
Variable little or no effect once in the field:
Biosept 33 SL (grapefruit extract) (Meszka and Bielenin, 2004)
seaweed, garlic, and compost extracts (Prokkola et al., 2003), but low disease
incidence (Prokkola and Kivijarvi, 2007)
sodium bicarbonate (Funaro, 1997)
Variable little or no effect once in the field:
Biochicol 020 PC (chitosan) (Meszka and Bielenin, 2004)
silicon (Prokkola et al., 2003), but low disease incidence (Prokkola and Kivijarvi,
2007)
Field vegetables (lettuce, onion, cabbage, melon) (target pathogen = B. cinerea)
Success in field trials
M
Microsphaeropsis ochracea / onion (Carisse et al., 2006)
Ulocladium atrum 385, onion (Köhl and Fokkema, 1998) (Köhl et al., 1999)
B
O
Natural volatile compounds : benzaldehyde, methyl benzoate, methyl salicylate, 2-nonanone, 2-hexenal
diethyl acetal, hexanol, and E-2-hexen-1-ol (Archbold et al., 1997)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus subtilis / lettuce (Fiddaman et al., 2000), L-form / Chinese cabbage (Walker et al., 2002), / melon (Wang
et al., 2008c)
Brevibacillus brevis / lettuce (McHugh and Seddon, 2001)
Bacillus amyloliquefaciens/ melon (Wang et al., 2008c)
Pseudomonas spp. (LC8, PF13, PF14, PF15), /lettuce (Card et al., 2002)
Pseudomonas syringae pv. phaseolicola / Chinese cabbage (Daulagala and Allan, 2003)
Fungus + yeast:
Clonostachys rosea / onion (Nielsen et al., 2000) (Yohalem et al., 2004)
Coniothyrium minitans / lettuce (Fiume and Fiume, 2005)
Epicoccum sp. (E21) /lettuce (Card et al., 2002)
Gliocladium virens [Trichoderma virens], / lettuce (Lolas et al., 2005)
Penicillium griseofulvum, / onion (Tylkowska and Szopinska, 1998)
Penicillium sp. 90/22, / onion (Tylkowska and Szopinska, 1998)
Pichia onychis /onion postharvest (German Garcia et al., 2001) (Cotes, 2001)
Ulocladium sp. (U13), /lettuce (Card et al., 2002)
Ulocladium atrum / onion (Köhl et al., 2003), 385 and 302 / onion (Nielsen et al., 2000) (Yohalem et al., 2004)
Trichoderma harzianum, / onion (Tylkowska and Szopinska, 1998), T39 / lettuce (Meyer et al., 1998) (Lolas et al.,
2005), 'Supresivit' / cress (Borregaard, 2000)
Trichoderma koningii / onion (Tylkowska and Szopinska, 1998)
T. viride / onion (Tylkowska and Szopinska, 1998)
Variable little or no effect :
Trichoderma-Promot / onion (El-Neshawy et al., 1999)
76
Appendix 1
Fruits - postharvest (apple, pears, peach, sweet cherry, kiwi) (target pathogen = B. cinerea)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Success in field trials
Bacteria
Bacillus licheniformis (EN74-1) (Jamalizadeh et al., 2008)
Bacillus subtilis (Ongena et al., 2005) , GA1 (Toure et al., 2004), Rizo-N (El-Sheikh Aly et al., 2000)
Bacillus amyloliquefaciens 2TOE, /pears (Mari et al., 1996)
Bacillus pumilus 3PPE, /pears (Mari et al., 1996)
Erwinia sp (Floros et al., 1998)
Pantoea agglomerans (Sobiczewski and Bryk, 1999) (Nunes et al., 2001a)
Pseudomonas sp (Sobiczewski and Bryk, 1999)
Pseudomonas syringae Strain ESC-11 BioSave (Janisiewicz and Jeffers, 1997), / pear (Sugar and Benbow, 2002)
(Benhow and Sugar, 1997), MA-4 (Zhou et al., 2002), CPA5 (Nunes et al., 2007)
Pseudomonas fluorescens (Mikani et al., 2007) (Mikani et al., 2008)
Pseudomonas viridiflava (Bryk et al., 1999)
Rahnella aquatilis (Calvo et al., 2007)
M
Bacteria
Pantoea agglomerans (CPA-2) (Nunes et al., 2002b) (Nunes et al., 2001b)
Pseudomonas syringae, MA-4, MB-4, MD-3b and NSA-6 (=FG) (Zhou et al., 2001)
Fungi + yeasts:
Aureobasidium pullulans, Rhodotorula glutinis and Bacillus subtilis in combination
(=FG) (Leibinger et al., 1997)
Candida saitoana (El-Ghaouth et al., 2001a) , with chitosan (Bio-Coat) or lyric enzyme
(Biocure) (El-Ghaouth et al., 2001b)
Candida sake strain CPA-1 combined with diphenylamine (Zanella et al., 2003), CPA1 + ammonium molybdate /pear (Nunes et al., 2002a)
Metschnikowia pulcherrima (Migheli et al., 1997)
Pichia anomala strain K beta -1,3-glucans and calcium chloride (Jijakli et al., 2002)
Fungi + yeasts:
Aureobasidium pullulans (Achbani et al., 2005) (Lima et al., 2005) (Schena et al., 1999), LS-30 (Lima et al., 1999)
(Lima et al., 2003), + calcium chloride or sodium bicarbonate (Ippolito et al., 2005b) (Ippolito et al., 2005a)
Candida butyri JCM 1501, (Wagner et al., 2006)
Candida melibiosica 2515 (Wagner et al., 2006)
Candida parapsilosis DSM 70125 (Wagner et al., 2006)
Candida oleophila Aspire (Droby et al., 2003), Aspire/pear (Sugar and Benbow, 2002) (Benhow and Sugar, 1997),
Aspire + 2% sodium bicarbonate (Wisniewski et al., 2001), strain O (Jijakli, 2000) (Bajji and Jijakli, 2007)
(Jijakli et al., 2004) (Lahlali et al., 2007), /peach (Karabulut and Baykal, 2004),
Candida saitoana (El-Ghaouth et al., 2001c) (El-Ghaouth et al., 2000a) (El-Ghaouth et al., 2000b) (El-Ghaouth et
al., 2001b)
Candida sake (Vinas et al., 1998) (Nunes et al., 2002d) (Giraud and Crouzet, 2004) (Cook, 2002b), CPA-1 +
Pantoea agglomerans (Nunes et al., 2002c)
Candida famata (21-D), (Lima et al., 1999)
Candida tenuis, (Faten, 2005)
Candida pulcherrima (Cook, 2002b)
Cryptococcus laurentii (Benhow and Sugar, 1997) (Zhang et al., 2005) (Zhang et al., 2007b) (Sugar and Benbow,
2002) (Tian et al., 2004a) (Jing et al., 2008) (Colgan, 1997) (Lima et al., 2005) (Filonow, 1998) + Gibberellic
acid (Yu and Zheng, 2007), +IAA (Yu et al., 2008), + salicilic acid (Yu et al., 2007), LS28 (Lima et al.,
2006) (Lima et al., 1998) (Lima et al., 1999) (Lima et al., 2003)
Cryptococcus albidus, (Fan et al., 2001a) (Fan and Tian, 2001) (Tian et al., 2002)
Cryptococcus humicola (Anderson et al., 1997) (Filonow et al., 1996)
Cryptococcus infirmo-miniatus (Benhow and Sugar, 1997) (Sugar and Benbow, 2002)
Debaryomyces hansenii (strain 43E) / citrus (Arras and Arru, 1999)
Filobasidium floriforme NRRLY7454, (Filonow et al., 1996)
Galactomyces geotrichum (Cook, 2002b)
77
Nicot et al. (Appendix for Chapter 1)
Kloeckera apiculata / peach (Karabulut and Baykal, 2003) (Karabulut et al., 2005)
Metschnikowia pulcherrima (Spadaro et al., 2002) (Piano et al., 1998) (Spadaro et al., 2004), MACH1 (Duraisamy
et al., 2008)
Metschnikowia fructicola (Karabulut et al., 2005)
Muscodor albus (Mercier and Jimenez, 2004) (Ramin et al., 2008) (Schotsmans et al., 2008)
Penicillium spp. (El-Sheikh Aly et al., 2000)
Pichia stipitis CBS 5773 (Wagner et al., 2006)
Pichia anomala strain K (Grevesse et al., 2003) (Jijakli, 2000) (Friel and Jijakli, 2007) (Friel et al., 2007) (Jijakli
and Lepoivre, 1998) (Lahlali et al., 2007)
Pichia guilliermondii (29-A), (Lima et al., 1999)
Rhodotorula glutinis (Sugar and Benbow, 2002) (Benhow and Sugar, 1997) (Lima et al., 2005) (Lima et al., 1998)
(Sansone et al., 2005), LS-11 (Lima et al., 1999) (Lima et al., 2003),
Rhodosporidium toruloides NRRL Y1091, (Filonow et al., 1996)
Sporobolomyces roseus FS-43-238 (Filonow et al., 1996) (Filonow, 1998)
Saccharomyces cerevisiae, (Faten, 2005)
Trichoderma harzianum Plant-guard (El-Sheikh Aly et al., 2000), Rifai (Batta, 2004)
Trichoderma Viride (El-Sheikh Aly et al., 2000),
Trichosporon sp., (Fan et al., 2001b) (Tian et al., 2002)
Trichosporon pullulans (Cook, 2002b)
R. glutinis SL 1 + C. laurentii SL 62 mixture (Calvo et al., 2003)
Variable little or no effect :
Candida oleophila (Aspire), (Colgan, 1997)
volatile substances produced by grape cv. Isabella (Vitis labrusca) (Kulakiotu and Sfakiotakis, 2003b) (Kulakiotu
et al., 2004a)
Chitosan, (Faten, 2005)
Calcium (Chardonnet et al., 2000) (Holmes et al., 1998)
Phosphonate (Holmes et al., 1998)
sodium bicarbonate (Karabulut et al., 2005)
B
O
78
Appendix 1
Legumes (Fabaceae) (target pathogen = B. cinerea)
Success in field trials
Bacteria
Bacillus subtilis K-3 / lupin (Kuptsov et al., 2004)
Pantoea agglomerans / lentil (Huang and Erickson, 2002), LRC 954, / lentil (Huang
and Erickson, 2005)
Pseudomonas fluorescens, / lentil (Huang and Erickson, 2002) LRC 1788 / lentil
(Huang and Erickson, 2005)
M
Fungi + yeasts:
Clonostachys rosea / alfalfa (Li et al., 2004a)
Gliocladium catenulatum, / alfalfa (Li et al., 2004a)
Penicillium aurantiogriseum LRC 2450 / lentil (Huang and Erickson, 2005)
Penicillium griseofulvum / lentil (Huang and Erickson, 2002)
Trichoderma hamatum / lentil (Huang and Erickson, 2002)
Trichoderma harzianum LRC 2428 / lentil (Huang and Erickson, 2005)
Trichoderma viride / chickpea (Abha et al., 1999)
Trichoderma atroviride, / alfalfa (Li et al., 2004a)
Trichothecium roseum / alfalfa (Li et al., 2004a)
Mixture: Streptomyces exfoliatus + Trichoderma harzianum / faba bean (Mahmoud et
al., 2004)
B
Eucalyptus citriodora + Ipomoea carnea extracts / faba bean (Mahmoud et al., 2004)
O
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus subtilis (Saad et al., 2005)
Bacillus megaterium (Saad et al., 2005)
Bacillus cereus (Kishore and Pande, 2007)
Bacillus macerans BS 153 (Sharga, 1997)
Pantoea agglomerans (Huang and Erickson, 2002), LRC 954, (Huang and Erickson, 2005)
Pseudomonas fluorescens, (Huang and Erickson, 2002) LRC 1788 (Huang and Erickson, 2005)
Pseudomonas putida BTP1 (Ongena et al., 2002)
Streptomyces albaduncus (Razak et al., 2000)
Streptomyces griseoplanus (Razak et al., 2000)
Streptomyces violaceus T118 (Ahmad et al., 2002)
Fungi + yeasts:
Botrytis cinerea non-aggressive strains /bean leaves (Weeds et al., 2000)
Chaetomium globosum (Pradeep et al., 2000)
Cladosporium cladosporioides (Jackson et al., 1997)
Epicoccum nigrum, (Szandala and Backhouse, 2001)
Gliocladium roseum (Li et al., 2002) (Szandala and Backhouse, 2001) (Burgess and Keane, 1997)
Penicillium brevicompactum (Jackson et al., 1997)
Penicillium aurantiogriseum LRC 2450 (Huang and Erickson, 2005)
Penicillium griseofulvum (Huang and Erickson, 2002)
Trichoderma (Burgess and Keane, 1997)
Trichoderma harzianum (Szandala and Backhouse, 2001), T39 (Bigirimana et al., 1997) (Kapat et al., 1998) (Elad
et al., 2004), LRC 2428 (Huang and Erickson, 2005)
Trichoderma viride /pigeon pea (Pradeep et al., 2000), / chickpea (Abha and Tripathi, 1999) (Mukherjee et al.,
1997)
Trichoderma hamatum (Huang and Erickson, 2002)
extracts from green parts of tomato, potato, rape (Smolinska and Kowalska, 2006)
pterocarpan phytoalexin maackiain from chickpea (Stevenson and Haware, 1999)
79
Nicot et al. (Appendix for Chapter 1)
Flowers (target pathogen = B. cinerea)
Success in field trials
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus amyloliquefaciens / lily (Chiou and Wu, 2001)
Bacillus subtilis / rose buds (Tatagiba et al., 1998)
Burkholderia gladioli, / lily (Chiou and Wu, 2001)
Pseudomonas sp. 677 /geraldton waxflower (Beasley et al., 2001)
Serratia marcescens strain B2 / cyclamen (Someya et al., 2001)
Bacteria
Bacillus amyloliquefaciens B190 / lily (Chiou and Wu, 2003)
Bacillus cereus / lily (Liu et al., 2008)
Bacillus amyloliquefaciens / lily (Chiou and Wu, 2001)
Burkholderia gladioli, / lily (Chiou and Wu, 2001)
Pseudomonas putida / lily (Liu et al., 2008)
M
Fungi + yeasts:
Clonostachys rosea /rose (Morandi et al., 2003)
Ulocladium atrum / cyclamen (Köhl et al., 2000) (Köhl et al., 1998)
Variable little or no effect :
Trichoderma harzianum / cyclamen (Minuto et al., 2002) (Minuto et al., 2004)
Fungi + yeasts
Cladosporium spp. / rose (Morandi et al., 1999)
Cladosporium oxysporum, / rose debris + buds (Tatagiba et al., 1998)
Cladosporium cladosporioides / rose buds (Tatagiba et al., 1998)
Clonostachys rosea /rose (Morandi et al., 1999) (Morandi et al., 2006) (Morandi et al., 2001) (Morandi et al.,
2007) (Morandi et al., 2008) (Morandi et al., 2000b) (Morandi et al., 2000a) (Yohalem, 2004) (Yohalem,
2000)
Epicoccum sp. / Geraldton waxflower (Beasley et al., 2001)
Fusarium sp., / Geraldton waxflower (Beasley et al., 2001)
Gliocladium roseum FR136 / rose debris (Tatagiba et al., 1998)
Rhizoctonia (BNR), / geranium (Olson and Benson, 2007)
Rhodotorula glutinis PM4 / geranium (Buck and Jeffers, 2004) (Buck, 2004)
Rhodotorula graminis, / geranium (Buck, 2004)
Rhodotorula Mucilaginosa / geranium (Buck, 2004)
Trichoderma spp / Geraldton waxflower (Beasley et al., 2001)
Trichoderma harzianum (Trichodex) / Geraldton waxflower (Beasley et al., 2005)
Trichoderma hamatum / statice (Diaz et al., 1999), 382 / geranium (Olson and Benson, 2007)
Trichoderma inhamatum, / rose debris (Tatagiba et al., 1998)
Ulocladium atrum / cyclamen (Kessel, 1999) (Kessel et al., 2001) (Kessel et al., 2005) (Köhl and Molhoek, 2001)
(Kessel et al., 2002) (Kessel et al., 1999), /lily (Kessel et al., 1999) (Elmer and Köhl, 1998) (Kessel et al.,
2001), / geranium (Gerlagh et al., 2001), / rose (Yohalem and Kristensen, 2004) (Yohalem, 2004) (Köhl and
Gerlagh, 1999) (Yohalem et al., 2007) (Yohalem, 2000), / pelargonium (Yohalem et al., 2007)
Variable little or no effect :
Trichoderma hamatum 382 in compost / begonia (Horst et al., 2005)
Trichoderma harzianum preparations (Yohalem, 2000) (Trichodex and Supresivit) (Yohalem, 2004)
grapefruit [Citrus paradisi] extract / lily, peony and tulip (Orlikowski et al., 2002), / tulips, Gerbera jamesonii and
carnations (Orlikowski and Skrzyoczak, 2003), Biosept 33 SL / tulip (Orlikowski and Skrzypczak, 2001)
chitosan / tulips, Gerbera jamesonii and carnations (Orlikowski and Skrzyoczak, 2003)
B
O
80
Appendix 1
Miscellaneous crops (target pathogen = B. cinerea)
Success in field trials
Bacteria
Streptomyces griseoviridis (Mycostop) / Pinus sylvestris (Capieau et al., 2001)
(Capieau et al., 2004)
M
Fungi + yeasts
Gliocladium sp (GlioMix) / Pinus sylvestris (Capieau et al., 2001) (Capieau et al.,
2004)
Gliocladium roseum / Eucalyptus nurseries (Stowasser and Ferreira, 1997)
Trichoderma harzianum and T. polysporum (Binab TF.WP), / Pinus sylvestris (Capieau
et al., 2001) (Capieau et al., 2004)
Trichoderma viride (Trichosemin 25 PTS (25% Tv), / sunflower (Eva, 2003)
Variable little or no effect :
Penicillium sp. / Eucalyptus nurseries (Stowasser and Ferreira, 1997)
Trichoderma harzianum , Trichoderma viride / Eucalyptus nurseries (Stowasser and
Ferreira, 1997)
B
O
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus spp./ Ginseng (Kim et al., 1997) (Chung et al., 1998)
Bacillus subtilis Cot1 and CL27 / Astilbe hybrida, Aster hybrida, Daphne blayana, Photinia fraseri (Li et al., 1998)
Bacillus amyloliquefaciens / oilseed rape (Danielsson et al., 2007)
Bacillus licheniformis / Perilla (Son et al., 2002)
B. megaterium / Perilla (Son et al., 2002)
Cupriavidus campinensis / Arabidopsis thaliana (Schoonbeek et al., 2007)
Erwinia / Ginseng (Kim et al., 1997)
Pseudomonas fluorescens / castor crop (Raoof et al., 2003), WCS374r / Eucalyptus (Ran et al., 2005)
Pseudomonas putida WCS358r / Eucalyptus (Ran et al., 2005)
Streptomyces griseoviridis (Mycostop) / Pinus sylvestris (Capieau et al., 2001) (Capieau et al., 2004)
Fungi + yeasts
Clonostachys (A-10) / Pinus radiate, Eucalyptus globulus (Molina Mercader et al., 2006)
Cylindrocladium spp. / Eucalyptus (Fortes et al., 2007)
Gliocladium sp (GlioMix) / Pinus sylvestris (Capieau et al., 2001) (Capieau et al., 2004)
Gliocladium roseum / Picea mariana (Zhang et al., 1996)
Trichoderma spp. / Eucalyptus (Fortes et al., 2007)
Trichoderma harzianum / Arabidopsis thaliana (Korolev and Elad, 2004) / castor crop (Tirupathi et al., 2006)
(Raoof et al., 2003) (Bhattiprolu and Bhattiprolu, 2006), / hazelnut (Machowicz-Stefaniak et al., 2004)
Trichoderma viride / castor crop (Tirupathi et al., 2006) (Raoof et al., 2003) (Bhattiprolu and Bhattiprolu, 2006), T
13-82 (Trichodermin-BL) / flax (Pristchepa et al., 2006), / hazelnut (Machowicz-Stefaniak et al., 2004)
Trichoderma harzianum and T. polysporum (Binab TF.WP), / Pinus sylvestris (Capieau et al., 2001) (Capieau et
al., 2004)
Mature leaf extract of Lantana camera / castor crop (Bhattiprolu and Bhattiprolu, 2006)
Cryptogein, elicitor secreted by Phytophthora cryptogea / tobacco (Blancard et al., 1998)
81
Nicot et al. (Appendix for Chapter 1)
Successful inhibition in vitro (target pathogen = B. cinerea)
M
Bacteria
Alcaligenes faecalis (Honda et al., 1999)
Azotobacter (Khan et al., 2006)
Bacillus sp mutant strain (Bernal et al., 2002)
Bacillus amyloliquefaciens CCMI 1051 (Caldeira et al., 2007), BL-3 (Lee et al., 2001)
Bacillus brevis [Brevibacillus brevis](Gu et al., 2001) (Edwards and Seddon, 2001)
Bacillus cereus (Guven et al., 2008) (Huang and Chen, 2004)
Bacillus circulans (Paul et al., 1997)
Bacillus licheniformis W10 (Ji et al., 2007) (Gu et al., 2001)
Bacillus subtilis (Gu et al., 2001) (Chen et al., 2008) (Chen et al., 2004b) (Zhao et al., 2003) (Chen et al., 2004a) (Zakharchenko et al., 2007) (Gu et al., 2004) (Novikova et al., 2003) (Hsieh et al.,
2003) (Feng et al., 2003) (Liu et al., 2007b)
Bacillus thuringiensis CMB26 (Kim et al., 2004)
Paenibacillus polymyxa BL-4 (Lee et al., 2001)
Photorhabdus luminescens ATCC 29999 (Hsieh et al., 2004)
Plutella xylostella (Indiragandhi et al., 2008)
Pseudomonas (Lian et al., 2007) (Cornea et al., 2007) (Kim et al., 2000) (Woo et al., 2002) (Bryk et al., 2004)
Pseudomonas aeruginosa PUPa3 (Kumar et al., 2005)
Pseudomonas antimicrobica (Walker et al., 2001)
Pseudomonas corrugata strain P94 (Guo et al., 2007)
Pseudomonas fluorescens (Nian et al., 2007) (Khan and Almas, 2002)
Pseudomonas putida (Cornea et al., 2007), Cha 94 (Lee et al., 2001)
Pseudomonas syringae pv. syringae strain B359 (Fogliano et al., 2002)
Lysobacter capsici sp. Nov (Park et al., 2008)
Serratia plymuthica C48 (Frankowski et al., 2001a) (Frankowski et al., 2001b)
Streptomyces + actinomycetes (Tian et al., 2004b) (Nadkarni et al., 1998) (Liang et al., 2007, Yan et al., 2004) (Han et al., 2004) (Liang et al., 2007) (Long et al., 2005) (Stoppacher et al., 2007) (Kim
et al., 2007b)
Streptomyces ahygroscopicus (Sun et al., 2003) (Yang et al., 2007) (Zhao et al., 1998)
Streptomyces luteogriseus ECO 00001 (Li et al., 2008)
Streptomyces rimosus subsp. daheishanensis strain MY02 (Liu et al., 2004)
Streptomyces roseoflavus strain LS-A24 (Park et al., 2006)
Tripterygiun wilfordii (Shentu et al., 2006)
Xenorhabdus sp. strain CB43 (Xiao et al., 2005)
Xenorhabdus nematophilus YL001 (Liu et al., 2006)
marine bacteria (Nie et al., 2007)
Fungi + yeasts
Acremonium strictum (Kim et al., 2002)
Aspergillus fumigatus and A. terreus (El-Zayat, 2008)
Aspergillus clavatonanicus (Zhang et al., 2008)
Cryptococcus laurentii (isolate LS-28) (Castoria et al., 1997)
Fusarium lateritium extracts (Anitha, 2006)
Fusarium semitectum (Altomare et al., 2000)
82
Appendix 1
Lecanicillium muscarium (Fenice and Gooday, 2006)
Muscodor albus (Mercier and Jimenez, 2007)
Rhodotorula (Calvente et al., 2001)
Rhodotorula glutinis (Castoria et al., 1997)
Trichoderma (Pezet et al., 1999) (Chen et al., 2005) (Liu et al., 2007a)
Trichoderma viride (Machowicz-Stefaniak, 1998) T15 and T17 (Silva-Ribeiro et al., 2001)
Trichoderma atroviride (Navazio et al., 2007) (Klemsdal et al., 2006) GMO (Brunner et al., 2005)
Trichoderma harzianum (Dana et al., 2001) (Ding et al., 2002) (Limon et al., 2004) (Mach et al., 1999) T5A, T1 and T1A (Silva-Ribeiro et al., 2001) (Lee et al., 2001), T-33 (Witkowska and Maj,
2002)
Trichoderma hamatum C-1 (Witkowska and Maj, 2002)
Trichoderma reesei [T. longibractiatum] M7-1 (Witkowska and Maj, 2002)
Oomycetes
Pythium bifurcatum (Paul, 2003)
Pythium citrinum (Paul, 2004)
Pythium contiguanum (Paul, 2000)
Pythium radiosum (Paul, 1999a)
B
O
Antifungal metabolites of endophytic fungus, A10 (Qian et al., 2006)
antimicrobial peptide Ar-AMP from Amaranthus retroflexus L. (Lipkin, Anisimova et al. 2005)
basic haem-peroxidase (WP1) from wheat (Triticum aestivum) kernels (Caruso, Chilosi et al. 2001)
Extracts from Bazzania trilobata, Diplophyllum albicans, Sphagnum quinquefarium, Dicranodontium denudatum and Hylocomium splendens (Tadesse, Steiner et al. 2003)
Extracts of Sophora flavescens (Zheng et al., 2000) (Zheng et al., 1999)
Irpex lacteus (Fr.) Fr., Trametes versicolor (L.:Fr.) Pilat, and Chondrostereum purpureum (Pers.:Fr.) Pouzar (White and Traquair, 2006)
Pyrrolnitrin, produced by several bacteria (Okada et al., 2005)
Ten sesquiterpenes and six diterpenes from Pilgerodendron uviferum wood and bark (Solis et al., 2004)
chlorine dioxide (Zoffoli et al., 2005)
earthworm (Eisenia fetida) polysaccharides (Wang et al., 2007b)
chitosan derivatives (Rabea et al., 2003)
83
Nicot et al. (Appendix for Chapter 1)
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Appendix 2. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1998-2008) for
successful effect against powdery mildew in laboratory experiments and field trials on selected crops.
Powdery mildew on cereals
Success in field trials
General paper:
Crop protection: management strategies (Prasad, 2005)
Fungi + yeasts:
Bacteria
Rhizobacteria (Yigit, 2004)
Bacteria, (Azarang, 2004)
Fungi + yeasts:
Acremonium alternatum (Kasselaki, 2006a, b)
Alternaria alternata, Aspergillus niger, Bipolaris spicifera, Cladosporium cladosporioides, Curvularia lunata,
Fusarium acuminatum F. semitectum, Penicillium rubrum, (Simian, 2008)
BCAs mix (David, 2007)
Fungi (Azarang, 2004)
Fusarium oxysporum f. sp. radicis-lycopersici (Nelson, 2005)
Paecilomyces farinosus (Szentivanyi, 2006)
Verticillium lecanii (Koike, 2004)
M
Bryophyte extracts (Tadesse, 2003)
Aromatic substances (Koitabashi, 2002)
Mycelial extracts (Haugaard, 2002)
PAF from Penicillium chrysogenum (Barna, 2008)
Secondary metabolic products of strain A19 of actinomycetes (Shen et al., 2008)
Verlamelin (Kim, 2002)
B
O
Powdery mildew on pome/stone fruits
Success in field trials
Bacteria
Fungi + yeasts:
yeast (Y16) (Alaphilippe, 2007)
M
B
O
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Pseudomonas aureofaciens ; Bacillus subtilis ; P. fluorescens
(Sanin et al., 2008)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
General paper:
Bacteria
Fungi + yeasts:
Ampelomyces quisqualis (Harvey, 2006)
Ampelomyces quisqualis (Sonali, 2005)
yeast (Y16) (Alaphilippe, 2008)
102
Appendix 2
Powdery mildew on grapes
Success in field trials
M
B
O
Bacteria
Bacillus subtilis (Crisp, 2006)
Photosynthetic bacteria (Robotic, 2002)
Fungi + yeasts:
Ampelomyces hyperparasites (Fuzi, 2003)
Ampelomyces quisqualis (Angeli, 2006a, b, c, 2007a, b)
Ampelomyces quisqualis (Hoffmann, 2007)
Ampelomyces quisqualis 94013 (Lee, 2004)
BCAs (Amaro, 2003)
BCAs (Ari, 2004)
BCAs (Kaine, 2003)
BCAs (Linder et al., 2006)
BCAs (Zulini, 2004)
Pseudozyma flocculosa (Schmitt, 2001)
Yeast (Robotic, 2002)
Milsana (VP99) (Schmitt, 2001, 2002)
fresh or dried milk (10%),pinolene 1%, calcium chloride (2%),
tripotassium phosphate (1%) and a mixture of mineral oil
(1%),sodium bicarbonate/sodium silicate (0.5%) (Casulli, 2002)
mycophagous mite (Melidossian, 2005)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
General paper:
Bacteria
Brevibacillus brevis (Schmitt, 2001, 2002)
PGPR (Konstantinidou-Doltsinis, 2007)
Pseudomonas syringes pv. Syringe (Kassemeyer, 1998)
Serenade (Bacillus subtilis)(Schilder, 2002)
Fungi + yeasts:
Ampelomyces quisqualis (Angeli, 2006a, b, c, 2007a, b)
Ampelomyces quisqualis 94013 (Lee, 2004)
Ampelomyces quisqualis AQ10, (Schweigkofler, 2006)
BCA mix (David, 2007)
BCAs (Kaine, 2003)
BCAs {Amaro, 2003 #177
Pseudozyma flocculosa (Schmitt, 2001)
Pseudozyma flocculosa (SporodexReg. L) (Konstantinidou-Doltsinis, 2007)
Tilletiopsis spp (Haggag, 2007)
Milsana (VP99) (Konstantinidou-Doltsinis, 2001)
Milk, whey, whey protein, Bacillus subtilis, yeast extract medium (Crisp, 2006)
Mycophagous mite (Melidossian, 2005)
Orthotydeus lambi mites (English-Loeb, 1999, 2006, 2007)
Powdery mildew on strawberry pathogen: Podosphaera aphanis f.sp. fragariae; Sphaerotheca macularis f.sp. fragariae
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Success in field trials
Bacteria
Fungi + yeasts:
M
Bacteria
B. subtilis QST (Fiamingo, 2007a)
Bacillus subtilis (Amsalem, 2004)
Bacillus subtilis (Pertot, 2004) (Pertot, 2008)
Pseudomonas reactans (Fiamingo, 2007b)
Fungi + yeasts:
Ampelomyces quisqualis, Trichoderma harzianum T39, Bacillus sp. F77, Cladosporium tenuissimum (Amsalem,
2004)
BCAs mix (David, 2007)
T. harzianum T39 (Fiamingo, 2007a)
Trichoderma harzianum Rifai strain T-22 (Picton, 2003)
Trichoderma harzianum T39 (Pertot, 2004) (Pertot, 2008)
103
Nicot et al. (Appendix for Chapter 1)
B
O
Powdery mildew on tomato, pathogen: Leveillula taurica, Oidium neolycopersici, Oidium lycopersicum, Oidium spp.
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Success in field trials
Bacteria
Pseudomonas fluorescens (Shashi, 2007)
Fungi + yeasts:
Trichoderma harzianum (Shashi, 2007)
M
B
General paper:
Bacteria
Bacillus brevis (Seddon, 1999)
Bcillus subtilis (Jacob, 2007)
Rhizobacteria B101R, B212R, and A068R, (Silva, 2004)
Serenade ; Pseudomonas strains (Laethauwer, 2006)
Fungi + yeasts:
Acremonium alternatum (Kasselaki, 2006a, b)
Lecanicillium lecanii (Mycotal) (Bardin, 2004)
Lecanicillium muscarium (Bardin, 2008)
Sporothrix flocculosa (Jarvis, 2007)
Trichoderma spp. (Moreno-Velandia, 2007) (Velandia, 2007)
Milsana (Seddon, 1999)
MilsanaReg. (VP 1999)(Malathrakis, 2002)
Milsana (Trottin-Caudal, 2003)
Malsana (Bardin, 2004) (Bardin, 2008)
Milsana ; (Laethauwer, 2006)
O
Powdery mildew on pepper, pathogen: Podosphaera leucotricha
Success in field trials
Bacteria
Fungi + yeasts:
M
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
General paper:
Bacteria
Fungi + yeasts:
AQ10 (Ampelomyces quisqualis) (Tsror, 2004)
Trichoderma harzianum (Gupta, 2005)
Trichoderma harzianum T39; Ampelomyces quisqualis (Brand, 2002)
Verticillium lecanii, Tilletiopsis minor (Haggag, 2008)
B
O
Milsana (Haggag, 2008)
Water extract of cattle manure compost, grape marc compost, , Kaligrin and Rifol (Tsror, 2004)
104
Appendix 2
Powdery mildew on cucurbits, pathogen: Podosphaera fusca
Success in field trials
Bacteria
Bacillus brevis (Schmitt, 1999)
Bacillus isolates (Koumaki, 2001)
Brevibacillus brevis (Abd-El-Moneim, 2004)
M
Fungi + yeasts:
Acremonium alternatum (Kasselaki, 2006a)
Ampelomyces quisqualis (Kristkova, 2003)
Ampelomyces quisqualis isolate M-10 (Benuzzi, 2006)
Ampelomyces quisqualis, Verticillium lecanii, Sporothrix
flocculosa (Dik, 1998)
Cryptococcus laurentii and Aureobasidium pullulans (Lima,
2002)
PlantShield Trichoderma harzianum (Utkhede, 2006)
Rhodotorula glutinis (Lima, 2002)
T. harzianum T39 (Levy, 2004)
Tilletiopsis washingtonensis (yeast) (El-Hafiz-Mohamed,
1999)
Verticillium lecanii; (Verhaar, 1999)
B
O
fresh or dried milk (10%), pinolene 1%, calcium chloride (2%),
tripotassium phosphate (1%) and a mixture of mineral oil
(1%),sodium bicarbonate/sodium silicate (0.5%) (Casulli, 2002)
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Bacteria
Bacillus spp (Romero, 2004a)
Bacillus spp (Romero, 2004b)
Bacillus subtilis (Abd-El-Moneim, 2004) (Gilardi, 2008) (Keinath, 2004) (Romero, 2007b) (Romero, 2007d)
BCAs mix (David, 2007)
Brevibacillus brevis (Allan, 2007) (Konstantinidou-Doltsinis, 2002) (Schmitt, 2001) (White, 2001)
Enterobacter cloacae (Georgieva, 2003)
Xenorhabdus nematophilus (Shi, 2004)
Fungi + yeasts:
Acremonium alternatum, Ampelomyces quisqualis , Lecanicillium lecanii (Romero, 2003)
Acremonium alternatum, Verticillium lecanii (Romero, 2007b)
Ampelomyces quisqualis (Gilardi, 2008) (Rankovic, 1998)
AQ10Reg. (Ampelomyces quisqualis) and MycotalReg. (Lecanicillium lecanii) (Romero, 2007b)
BCAs mix (David, 2007)
Acremonium alternatum and Verticillium lecanii, (Romero, 2001)
Lecanicillium longisporum (Kim, 2008)
Lecanicillium spp. (Goettel, 2008)
Meira geulakonigii (Sztejnberg, 2004)
Paecilomyces fumosoroseus (Kavkova, 2005)
Paecilomyces fumosoroseus; Verticillium lecanii (Kavkova, 2001)
Pseudozyma flocculosa (Konstantinidou-Doltsinis, 2002) (Schmitt, 2001)
Pseudozyma flocculosa, Ampelomyces quisqualis, Verticillium lecanii, Trichoderma harzianum (Dik, 2002)
Saccharomyces cerevisiae (El-Gamal, 2003)
Trichoderma harzianum (Abd-El-Moneim, 2004) (Elad, 2000)
Trichoderma harzianum T39; Ampelomyces quisqualis AQ10 (Elad, 1998)
Verticillium lecanii (Askary, 1998) (Verhaar, 1998)
Ampelomyces quisqualis isolate M-10 (Benuzzi, 2006)
Milsana (VP99) (Dik, 2002) (Schmitt, 2001) (White, 2001)
Milsana (VP99) from Fallopia sachalinensis (Konstantinidou-Doltsinis, 2001)
Fresh or dried milk (Casulli, 2002)
gramicidin S; (Schmitt, 1999)
lactoperoxidase system (Ravensberg, 2007)
lipopeptide antibiotic neopeptins from Streptomyces sp. (Kim, 2007)
lipopeptides (iturin and fengycin families of Bacillus subtilis) (Romero, 2007c)
Lipopeptides of antagonistic strains of Bacillus subtilis (Romero, 2007a)
oil formulations (Verhaar, 1999)
Psyllobora bisoctonotata (Soylu, 2002)
undiluted homogenised milk (Utkhede, 2006)
105
Nicot et al. (Appendix for Chapter 1)
Powdery mildew on various crops, pathogen: Oidium spp. Sphaerotheca spp., Erysiphe spp
Success in laboratory conditions (in vitro and/or in planta in controlled conditions)
Success in field trials
Bacteria
Bacillus subtilis (Nofal, 2006)
Fungi + yeasts:
Verticillium lecanIi, Tilletiopsis minor (Nofal, 2006)
M
Bacteria
Pseudomonas fluorescens (Vimala, 2006)
P. fluorescens (Hooda, 2006)
Fungi + yeasts:
Acremonium spp., Ampelomyces spp., Penicillium spp., Cladosporium spp., Trichoderma spp., Bacillus spp.,
Pseudomonas spp., Bradyrhizobium spp., Brachybacterium spp., Curtobacterium spp., Cryptocoocus spp.,
Rhodosporidium spp (Mmbaga, 2008)
Ampelomyces mycoparasites (Kiss, 2004)
BCAs (Dhananjoy, 2008)
BCAs (Eken, 2005)
BCAs(Casey, 2007)
Cladosporium cladosporioides, Cladosporium oxysporum, Drechslera hawaiensis,T richoderma viride (Sankar,
2007b)
Cladosporium oxysporum (Sankar, 2007a)
Gliocladium roseum (Lahoz, 2004)
Kyu-W63 (Koitabashi, 2005)
Trichoderma viride, T. harzianum, Pseudomonas fluorescens, mixture of T. harzianum P. fluorescens (Hooda, 2006)
B
O
Exudates from sclerotia of two Sclerotium rolfsii isolates (Pandey, 2007)
Mycophagous Ladybird (Sutherland, 2005)
Phyllactinia corylea (Krishnakumar, 2004)
Psyllobora bisoctonotata (Muls.) (Soylu, 2002)
Psyllobora vigintimaculata, (Sutherland, 2008; Sutherland, 2006)
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108
Appendix 2
Malathrakis, N. E. (2002). Efficacy of MilsanaReg. (VP 1999), a formulated plant extract from Reynoutria sachalinensis, against powdery mildew of tomato (Leveillula taurica). BulletinOILB/SROP 25, 175-178.
Melidossian, H. S. (2005). Suppression of grapevine powdery mildew by a mycophagous mite. Plant-Disease 89, 1331-1338.
Mmbaga, M. T. (2008). Identification of microorganisms for biological control of powdery mildew in Cornus florida. Biological-Control 44, 67-72.
Moreno-Velandia, C. A. (2007). Biological control of foliar diseases in tomato greenhouse crop in Colombia: selection of antagonists and efficacy tests. Bulletin-OILB/SROP 30, 59-62.
Nelson, H. E. (2005). Fusarium oxysporum f. sp. radicis-lycopersici can induce systemic resistance in barley against powdery mildew. Journal-of-Phytopathology 153, 366-370.
Nofal, M. A. (2006). Integrated management of powdery mildew of mango in Egypt. Crop-Protection 25, 480-486.
Pandey, M. K. (2007). Biochemical investigations of sclerotial exudates of Sclerotium rolfsii and their antifungal activity. Journal-of-Phytopathology 155, 84-89.
Pertot, I. (2004). Use of biocontrol agents against powdery mildew in integrated strategies for reducing pesticide residues on strawberry: evaluation of efficacy and side effects. BulletinOILB/SROP 27, 109-113.
Pertot, I. (2008). Integrating biocontrol agents in strawberry powdery mildew control strategies in high tunnel growing systems. Crop-Protection 27, 622-631.
Picton, D. D. (2003). Control of powdery mildew on leaves and stems of gooseberry. HortTechnology- 13, 365-367.
Prasad, D. (2005). Crop protection: management strategies. Crop-protection:-management-strategies.
Rankovic, B. (1998). Conidia production of Ampelomyces quisqualis in culture using suspension method and artificial infection of powdery mildew pathogens (Erysiphe artemisiae and E.
cichoracearum) by the mycoparasite. Zastita-Bilja 49, 77-84.
Ravensberg, W. (2007). The lactoperoxidase system as a novel, natural fungicide for control of powdery mildew. Bulletin-OILB/SROP 30, 19-22.
Robotic, V. (2002). Biological control of grapevine powdery mildew with Effective Microorganisms (EM). Bulletin-OILB/SROP 25, 191.
Romero, D. (2001). Biological control of cucurbit powdery mildew by mycoparasitic fungi. Bulletin-OILB/SROP 24, 143-146.
Romero, D. (2003). Effect of mycoparasitic fungi on the development of Sphaerotheca fusca in melon leaves. Mycological-Research 107, 64-71.
Romero, D. (2004a). Effect of relative humidity on the efficacy of mycoparasitic fungi and antagonistic bacteria towards cucurbit powdery mildew. Bulletin-OILB/SROP 27, 301-304.
Romero, D. (2004b). Isolation and evaluation of antagonistic bacteria towards the cucurbit powdery mildew fungus Podosphaera fusca. Applied-Microbiology-and-Biotechnology 64, 263-269.
Romero, D. (2007a). Effect of lipopeptides of antagonistic strains of Bacillus subtilis on the morphology and ultrastructure of the cucurbit fungal pathogen Podosphaera fusca. Journal-ofApplied-Microbiology 103, 969-976.
Romero, D. (2007b). Evaluation of biological control agents for managing cucurbit powdery mildew on greenhouse-grown melon. Plant-Pathology 56, 976-986.
Romero, D. (2007c). The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Molecular-Plant-Microbe-Interactions 20,
430-440.
Romero, D. (2007d). Management of cucurbit powdery mildew on greenhouse-grown melons by different biological control strategies. Bulletin-OILB/SROP 30, 427-431.
Sanin, S. S., Neklesa, N. P., and Strizhekozin, Y. A. (2008). Wheat protection from powdery mildew (supplement). Zashchita i Karantin Rastenii.
Sankar, N. R. (2007a). Cladosporium oxysporum as a mycoparasite on Uncinula tectonae - a new record. Journal-of-Plant-Disease-Sciences 2, 182-183.
Sankar, N. R. (2007b). Evaluation of teak phylloplane mycoflora for biocontrol of powdery mildew of teak caused by Uncinula tectonae. Journal-of-Plant-Disease-Sciences 2, 203-205.
Schilder, A. M. C. (2002). Evaluation of environmentally friendly products for control of fungal diseases of grapes. 10th-International-Conference-on-Cultivation-Technique-andPhytopathological-Problems-in-Organic-Fruit-Growing-and-Viticulture-Proceedings-of-a-conference,-Weinsberg,-Germany,-4-7-February-2002.
Schmitt, A. (1999). Antifungal activity of gramicidin S and use of Bacillus brevis for control of Sphaerotheca fuliginea. Modern-fungicides-and-antifungal-compounds-II-12th-InternationalReinhardsbrunn-Symposium,-Friedrichroda,-Thuringia,-Germany,-24th-29th-May-1998.
Schmitt, A. (2001). Improved plant health by the combination of biological disease control methods. Bulletin-OILB/SROP 24, 29-32.
Schmitt, A. (2002). Use of Reynoutria sachalinensis plant extracts, clay preparations and Brevibacillus brevis against fungal diseases of grape berries. 10th-International-Conference-onCultivation-Technique-and-Phytopathological-Problems-in-Organic-Fruit-Growing-and-Viticulture-Proceedings-of-a-conference,-Weinsberg,-Germany,-4-7-February-2002.
Schweigkofler, W. (2006). Effects of fungicides on the germination of Ampelomyces quisqualis AQ10, a biological antagonist of the powdery mildew of the grapevine. Bulletin-OILB/SROP 29,
79-82.
Seddon, B. (1999). Integrated biological control of fungal plant pathogens using natural products. Modern-fungicides-and-antifungal-compounds-II-12th-International-ReinhardsbrunnSymposium,-Friedrichroda,-Thuringia,-Germany,-24th-29th-May-1998.
Shashi, K. (2007). Field efficacy of bioagents and fungicides against tomato (Lycopersicon esculentum Mill.) diseases. Environment-and-Ecology 25S, 921-924.
109
Nicot et al. (Appendix for Chapter 1)
Shen, D., Wei, S., Ji, Z., and Wu, W. (2008). Primary studies on the secondary metabolic products of strain A19 of actinomycetes. Journal of Northwest A & F University - Natural Science
Edition 36, 173-178.
Shi, Y. (2004). Studies on 0.25% aqueous solution of Xenorhabdus nematophilus for the control of cucumber powdery mildew. Plant-Protection 30, 79-81.
Silva, H. S. A. (2004). Rhizobacterial induction of systemic resistance in tomato plants: non-specific protection and increase in enzyme activities. Biological-Control 29, 288-295.
Simian, B. (2008). Inhibitory effect of phylloplane fungi on Erysiphe polygoni DC inciting powdery mildew disease of Trigonella foenum-graecum. Annals-of-Plant-Protection-Sciences 16,
150-152.
Sonali, V. (2005). Ampelomyces quisqualis Ces. - a mycoparasite of apple powdery mildew in western Himalayas. Indian-Phytopathology 58, 250-251.
Soylu, S. (2002). Feeding of mycophagous ladybird, Psyllobora bisoctonotata (Muls.), on powdery mildew infested plants. Bulletin-OILB/SROP 25, 183-186.
Sutherland, A. (2008). A preliminary predictive model for the consumption of powdery mildew by the obligate mycophage Psyllobora vigintimaculata (Coleoptera: Coccinellidae). BulletinOILB/SROP 32, 209-212.
Sutherland, A. M. (2005). Effects of selected fungicides on a Mycophagous Ladybird (Coleoptera: Coccinellidae): ramifications for biological control of powdery mildew. Bulletin-OILB/SROP
28, 253-256.
Sutherland, A. M. (2006). Quantification of powdery mildew removal by the mycophagous beetle Psyllobora vigintimaculata (Coleoptera: Coccinellidae). Bulletin-OILB/SROP 29, 281-286.
Szentivanyi, O. (2006). Paecilomyces farinosus destroys powdery mildew colonies in detached leaf cultures but not on whole plants. European-Journal-of-Plant-Pathology 115, 351-356.
Sztejnberg, A. (2004). A new fungus with dual biocontrol capabilities: reducing the numbers of phytophagous mites and powdery mildew disease damage. Crop-Protection 23, 1125-1129.
Tadesse, M. (2003). Bryophyte extracts with activity against plant pathogenic fungi. Sinet,-Ethiopian-Journal-of-Science 26, 55-62.
Trottin-Caudal, Y. (2003). Efficiency of plant extract from Reynoutria sachalinensis (Milsana) to control powdery mildew on tomato (Oidium neolycopersici). Colloque-international-tomatesous-abri,-protection-integree-agriculture-biologique,-Avignon,-France,-17-18-et-19-septembre-2003.
Tsror, L. (2004). Control of powdery mildew on organic pepper. Bulletin-OILB/SROP 27, 333-336.
Utkhede, R. S. (2006). Reduction of powdery mildew caused by Podosphaera xanthii on greenhouse cucumber plants by foliar sprays of various biological and chemical agents. Journal-ofHorticultural-Science-and-Biotechnology 81, 23-26.
Velandia, C. A. M. (2007). Survival in the phylloplane of Trichoderma koningii and biocontrol activity against tomato foliar pathogens. Bulletin-OILB/SROP 30, 557-561.
Verhaar, M. A. (1998). Selection of Verticillium lecanii isolates with high potential for biocontrol of cucumber powdery mildew by means of components analysis at different humidity regimes.
Biocontrol-Science-and-Technology 8, 465-477.
Verhaar, M. A. (1999). Improvement of the efficacy of Verticillium lecanii used in biocontrol of Sphaerotheca fuliginea by addition of oil formulations. BioControl- 44, 73-87.
Vimala, R. (2006). Enhancing resistance in bhendi to powdery mildew disease by foliar spray with fluorescent pseudomonads. International-Journal-of-Agricultural-Sciences 2, 549-556.
White, D. (2001). Interaction of the biocontrol agent Brevibacillus brevis with other disease control methods. Bulletin-OILB/SROP 24, 229-232.
Yigit, F. (2004). Integrated biological and chemical control of powdery mildew of barley caused by Blumeria graminis f.sp. hordei using rhizobacteria and triadimenol. Pakistan-Journal-ofBiological-Sciences 7, 1671-1675.
Zulini, L. (2004). Biocontrol agents and their integration in organic viticulture in Trentino, Italy: characteristics and constrains. Bulletin-OILB/SROP 27, 49-52.
110
Appendix 3. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1973-2008)
for successful effect against the rust pathogens in laboratory experiments and field trials on selected crops
Rust on wheat, oat, soybean, groundnut, bean
Success in field trials
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Bean – target pathogen = Uromyces appendiculatus
Pantoea agglomerans B1 (Yuen et al., 2001)
Stenotrophomonas maltophilia C3 (Yuen et al., 2001)
Cladosporium tenuissimum (Assante et al., 2004)
Groundnut – target pathogen = Puccinia arachidis
Bean – target pathogen = Uromyces appendiculatus
Bacillus subtilis (Baker et al., 1985)
M
Groundnut – target pathogen = Puccinia arachidis
Pseudomonas fluorescens strain Pf1 (Meena et al., 2002)
Bacillus subtilis AF 1 (Manjula et al., 2004)
Pseudomonas fluorescens strain Pf1 (Meena et al., 2000) (Meena et al., 2002)
Acremonium obclavatum (Gowdu and Balasubramanian, 1993)
Fusarium chlamydosporum (Mathivanan and Murugesan, 2000) (Mathivanan et
al., 1998)
Soybean – target pathogen = Phakopsora pachyrhizi
Verticillium psalliotae, Verticillium lecanii (Saksirirat and Hoppe, 1990)
(Saksirirat and Hoppe, 1991)
Wheat, Oat – target pathogens = Puccinia recondite, P. coronata
Pseudomonas putida strain BK8661 (Flaishman et al., 1996)
Chaetomium globosum strain F0142 (Park et al., 2005b)
Verticillium chlamydosporium (Leinhos and Buchenauer, 1992)
endophytic fungi (Dingle and McGee, 2003)
Fusaric acid from Fusarium oxysporum EF119 (Son et al., 2008)
B
O
Bean – target pathogen = Uromyces appendiculatus
2,6-dichloro-isonicotinic acid (CGA 41396) (Dann and Deverall, 1995)
111
Nicot et al. (Appendix for Chapter 1)
Rust on other crops
Success in field trials
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Chrysanthemum
Verticillium lecanii (Whipps, 1993)
Coffee – target pathogen = Hemileia vastatrix
Bacillus lentimorbus (Shiomi et al., 2006)
Bacillus cereus (Shiomi et al., 2006)
Bacillus (Haddad et al., 2004)
Cedecea davisae (Silva et al., 2008)
Pseudomonas (Haddad et al., 2004)
Acremonium (Haddad et al., 2004)
Aspergillus (Haddad et al., 2004)
Cladosporium (Haddad et al., 2004)
Fusarium (Haddad et al., 2004)
Penicillium (Haddad et al., 2004)
Coffee – target pathogens = Hemileia vastatrix
M
Bacillus sp. (Haddad et al., 2006)
Pseudomonas sp. (Maffia et al., 2005), variable effect (Haddad et al., 2006)
Geranium – target pathogen = Puccinia pelargonii-zonalis
Bacillus subtilis (Rytter et al., 1989)
Safflower – target pathogen = Puccinia carthami
Trichoderma viride and T. harzianum, Bacillus subtilis, B. cereus, B. thuringiensis,
Pseudomonas fluorescens added alone and in combination (Tosi and Zazzerini,
1994)
Poplar – target pathogen = Melampsora ciliata
Alternaria alternata and Cladosporium oxysporum (Sharma et al., 2002)
Pine – target pathogens = Cronartium and Peridermium
Cladosporium tenuissimum (Moricca et al., 2001)
Scytalidium uredinicola (Moltzan et al., 2001)
Plant-growth-promoting rhizobacteria (Enebak and Carey, 2004)
B
O
Coffee – target pathogens = Hemileia vastatrix
acibenzolar-S-methyl (ASM) (Patricio et al., 2008)
112
Appendix 3
References on biocontrol against the rust pathogens
Assante, G., Maffi, D., Saracchi, M., Farina, G., Moricca, S., and Ragazzi, A. (2004). Histological studies on the mycoparasitism of Cladosporium tenuissimum on urediniospores of Uromyces appendiculatus.
Mycological Research 108, 170-182.
Baker, C. J., Stavely, J. R., and Mock, N. (1985). Biocontrol of bean rust by Bacillus-subtilis under field conditions. Plant Disease 69, 770-772.
Dann, E. K., and Deverall, B. J. (1995). Effectiveness of systemic resistance in bean against foliar and soilborne pathogens as induced by biological and chemical means. Plant Pathology 44, 458-466.
Dingle, J., and McGee, P. A. (2003). Some endophytic fungi reduce the density of pustules of Puccinia recondita f. sp tritici in wheat. Mycological Research 107, 310-316.
Enebak, S. A., and Carey, W. A. (2004). Plant growth-promoting rhizobacteria may reduce fusiform rust infection in nursery-grown loblolly pine seedlings. Southern Journal of Applied Forestry 28, 185-188.
Flaishman, M. A., Eyal, Z., Zilberstein, A., Voisard, C., and Haas, D. (1996). Suppression of Septoria tritici blotch and leaf rust of wheat by recombinant cyanide-producing strains of Pseudomonas putida.
Molecular Plant-Microbe Interactions 9, 642-645.
Gowdu, B. J., and Balasubramanian, R. (1993). Biocontrol potential of rust of groudnut by Acremonium-obclavatum. Canadian Journal of Botany-Revue Canadienne De Botanique 71, 639-643.
Haddad, F., Maffia, L. A., Mizubuti, E. S., and Teixeira, H. (2006). Biological control of leaf rust in organically-grown coffee. Phytopathology 96, S44-S44.
Haddad, F., Maffia, L. A., Mizubuti, E. S. G., and Romeiro, R. S. (2004). Biocontrol of coffee leaf rust with antagonists isolated from organic crops. Phytopathology 94, S37-S37.
Leinhos, G. M. E., and Buchenauer, H. (1992). Inhibition of rust diseases of cereals by metabolic products of verticillium-chlamydosporium. Journal of Phytopathology-Phytopathologische Zeitschrift 136,
177-193.
Maffia, L., Haddad, F., Mizubuti, E., Teixeira, H., and Saraiva, R. (2005). Biocontrol of leaf rust in an organically-grown coffee planting. Phytopathology 95, S63-S64.
Manjula, K., Kishore, G. K., and Podile, A. R. (2004). Whole cells of Bacillus subtilis AF 1 proved more effective than cell-free and chitinase-based formulations in biological control of citrus fruit rot and
groundnut rust. Canadian Journal of Microbiology 50, 737-744.
Mathivanan, N., Kabilan, V., and Murugesan, K. (1998). Purification, characterization, and antifungal activity of chitinase from Fusarium chlamydosporum, a mycoparasite to groundnut rust, Puccinia
arachidis. Canadian Journal of Microbiology 44, 646-651.
Mathivanan, N., and Murugesan, K. (2000). Fusarium chlamydosporum, a potent biocontrol agent to groundnut rust, Puccinia arachidis. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of
Plant Diseases and Protection 107, 225-234.
Meena, B., Radhajeyalakshmi, R., Marimuthu, T., Vidhyasekaran, P., Doraiswamy, S., and Velazhahan, R. (2000). Induction of pathogenesis-related proteins, phenolics and phenylalanine ammonia-lyase in
groundnut by Pseudomonas fluorescens. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 107, 514-527.
Meena, B., Radhajeyalakshmi, R., Marimuthu, T., Vidhyasekaran, P., and Velazhahan, R. (2002). Biological control of groundnut late leaf spot and rust by seed and foliar applications of a powder formulation
of Pseudomonas fluorescens. Biocontrol Science and Technology 12, 195-204.
Moltzan, B. D., Blenis, P. V., and Hiratsuka, Y. (2001). Temporal occurrence and impact of Scytalidium uredinicola, a mycoparasite of western gall rust. Canadian Journal of Plant Pathology-Revue
Canadienne De Phytopathologie 23, 384-390.
Moricca, S., Ragazzi, A., Mitchelson, K. R., and Assante, G. (2001). Antagonism of the two-needle pine stem rust fungi Cronartium flaccidum and Peridermium pini by Cladosporium tenuissimum in vitro
and in planta. Phytopathology 91, 457-468.
Park, J. H., Choi, G. J., Jang, K. S., Lim, H. K., Kim, H. T., Cho, K. Y., and Kim, J. C. (2005). Antifungal activity against plant pathogenic fungi of chaetoviridins isolated from Chaetomium globosum. Fems
Microbiology Letters 252, 309-313.
Patricio, F. R. A., Almeida, I. M. G., Barros, B. C., Santos, A. S., and Frare, P. M. (2008). Effectiveness of acibenzolar-S-methyl, fungicides and antibiotics for the control of brown eye spot, bacterial blight,
brown leaf spot and coffee rust in coffee. Annals of Applied Biology 152, 29-39.
Rytter, J. L., Lukezic, F. L., Craig, R., and Moorman, G. W. (1989). Biological-control of geranium rust by Bacillus-subtilis. Phytopathology 79, 367-370.
Saksirirat, W., and Hoppe, H. H. (1990). Verticillium-psalliotae, an effective mycoparasite of the soybean rust fungus Phakopsora-pachyrhizi syd. Zeitschrift Fur Pflanzenkrankheiten Und PflanzenschutzJournal of Plant Diseases and Protection 97, 622-633.
Saksirirat, W., and Hoppe, H. H. (1991). Secretion of extracellular enzymes by Verticillium-psalliotae treschow and Verticillium-lecanii (zimm) viegas during growth on uredospores of the soybean rust
fungus (Phakopsora-pachyrhizi syd) in liquid cultures. Journal of Phytopathology-Phytopathologische Zeitschrift 131, 161-173.
Sharma, S., Sharma, R. C., and Malhotra, R. (2002). Effect of the saprophytic fungi Alternaria alternata and Cladosporium oxysporum on germination, parasitism and viability of Melampsora ciliata
urediniospores. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-Journal of Plant Diseases and Protection 109, 291-300.
Shiomi, H. F., Silva, H. S. A., de Melo, I. S., Nunes, F. V., and Bettiol, W. (2006). Bioprospecting endophytic bacteria for biological control of coffee leaf rust. Scientia Agricola 63, 32-39.
Silva, H. S. A., Terrasan, C. R. F., Tozzi, J. P. L., Melo, I. S., and Bettiol, W. (2008). Endophytic bacteria inducing enzymes correlated to the control of coffee leaf rust (Hemileia vastatrix). Tropical Plant
Pathology 33, 49-54.
113
Nicot et al. (Appendix for Chapter 1)
Son, S. W., Kim, H. Y., Choi, G. J., Lim, H. K., Jang, K. S., Lee, S. O., Lee, S., Sung, N. D., and Kim, J. C. (2008). Bikaverin and fusaric acid from Fusarium oxysporum show antioomycete activity against
Phytophthora infestans. Journal of Applied Microbiology 104, 692-698.
Tosi, L., and Zazzerini, A. (1994). Evaluation of some fungi and bacteria for potential control of safflower rust. Journal of Phytopathology-Phytopathologische Zeitschrift 142, 131-140.
Whipps, J. M. (1993). A review of white rust (Puccinia horiana Henn) disease on chrysanthemum and the potential for its biological control with Vertillium lecanii (Zimm) Viegas. Annals of Applied Biology
122, 173-187.
Yuen, G. Y., Steadman, J. R., Lindgren, D. T., Schaff, D., and Jochum, C. (2001). Bean rust biological control using bacterial agents. Crop Protection 20, 395-402.
114
Appendix 4. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1973-2008) for
successful effect against the downy mildew / late blight pathogens in laboratory experiments and field trials on selected crops
Potato (target pathogen = Phytophthora infestans)
Success in field trials
M
Bacillus subtilis (Basu et al., 2001)
Bacillus sp. isolate PB2 (Atia, 2005) effect < fungicides
Pseudomonas fluorescens (Basu et al., 2001)
Pseudomonas fluorescens isolate PPfl (Atia, 2005) effect < fungicides
Pseudomonas (El-Sheikh et al., 2002)
Gliocladium virens (Basu et al., 2001)
Phytophthora cryptogea (Quintanilla, 2002)
Trichoderma spp (Saikia and Azad, 1999)
Trichoderma viride (Basu et al., 2001) (Basu and Srikanta, 2003) but no effect in other studies
(Singh et al., 2001) (Arora, 2000) (Arora et al., 2006)
little or no effect once in the field (good in lab):
Acremonium strictum, Penicillium viridicatum and Penicillium aurantiogriseum (Arora, 2000)
(Arora et al., 2006)
Myrothecium verrucaria and Chaetomium brasiliense (Arora et al., 2006)
B
carvone (Quintanilla, 2002)
O
culture filtrates from Streptomyces padanus (Huang et al., 2007)
negative effect:
salicylic acid (Quintanilla, 2002)
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Serenade (Bacillus subtilis strain QST 713) (Stephan et al., 2005) (Olanya and
Larkin, 2006)
Bacillus subtilis B5 (Ajay and Sunaina, 2005)
Bacillus, Pseudomonas, Rahnella, and Serratia (Daayf et al., 2003)
Enterobacter cloacae (Slininger et al., 2007)
Pseudomonas fluorescens (Slininger et al., 2007)
Xenorhabdus bovienii (Eibel et al., 2004)
Penicillium aurantiogriseum (Jindal et al., 1988)
Penicillium viridicatum (Hemant et al., 2004)
Trichodex (Stephan et al., 2005)
Trichoderma viride (Hemant et al., 2004)
Penicillium, Rhizoctonia and Trichoderma spp (Phukan and Baruah, 1991)
various microorganisms (Stephan and Koch, 2002)
carvone , thymol, pinochamphone, plumbagin (Quintanilla, 2002)
extracts of Rheum rhabarbarum and Solidago canadensis (Stephan et al., 2005)
oregano extract (Olanya and Larkin, 2006)
Elot-Vis (Stephan et al., 2005)
patatin J from potato tuber (Sharma et al., 2004)
chitosan ElexaTM (Acar et al., 2008)
cyclic lipopeptides from Pseudomonas: massetolide A (Tran Thi Thu, 2007)
extracts from Pseudomonas fluorescens (Martinez and Osorio, 2007)
115
Nicot et al. (Appendix for Chapter 1)
Tomato (target pathogen = Phytophthora infestans)
Success in field trials
M
Bacillus cereus (Silva et al., 2004)
Burkholderia (Lozoya-Saldana et al., 2006),
Pseudomonas (Lozoya-Saldana et al., 2006),
Streptomyces (Lozoya-Saldana et al., 2006)
B
Nochi leaf extract (Vanitha and Ramachandram, 1999)
O
compost extracts (Zaller, 2006)
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Bacillus pumilus (Yan et al., 2002)
Cellulomonas flavigena (Lourenco Junior et al., 2006)
Pseudomonas fluorescens (Yan et al., 2002) (Ha et al., 2007) (Tran Thi Thu,
2007)
Streptomyces sp. AMG-P1 (Lee et al., 2005)
Aspergillus sp., (Lourenco Junior et al., 2006)
Candida sp. (Lourenco Junior et al., 2006)
Cryptococcus sp. (Lourenco Junior et al., 2006)
Fusarium oxysporum (Kim et al., 2007a)
Penicillium sp. (Perez Mancia and Sanchez Garita, 2000)
Trichoderma harzianum T39 (Ferrari et al., 2007)
capsidiol (El-Wazeri and El-Sayed, 1977)
Elot-vis (Ferrari et al., 2007)
acibenzolar-S-methyl (Becktell et al., 2005)
beta -amino butyric acid (Yan et al., 2002)
Bion (benzothiadiazole) (Surviliene et al., 2003)
bikaverin and fusaric acid (Son et al., 2008)
cellulose (Perez Mancia and Sanchez Garita, 2000)
chaetoviridin A (Park et al., 2005a)
chitosan ElexaTM (Acar et al., 2008)
Chitoplant (Ferrari et al., 2007)
extracts from actinomycete isolates (Mutitu et al., 2008)
extracts from Bazzania trilobata and Diplophyllum albicans (Tadesse et al., 2003)
extract from Gibberella zeae (Kim et al., 1995)
phosphate (Becktell et al., 2005)
116
Appendix 4
Grapes (target pathogen = Plasmopara viticola)
Success in field trials
M
B
O
Bacillus brevis (Schmitt et al., 2002)
Bacillus subtilis (Serenade) (Schilder et al., 2002)
Pseudomonas fluorescens (Rizoplan) (Kilimnik and Samoilov, 2000) (Rajeswari et al., 2008)
Fusarium proliferatum (Falk et al., 1996)
Trichoderma harzianum T39 (Vecchione et al., 2007)
little or no effect once in the field:
Bacillus licheniformis (Cravero et al., 2000)
Biorange (Bacillus subtilis, Candida oleophila, Pseudomonas spp. and Streptomyces spp.)
(Spera et al., 2003)
Croplife (citrus and coconut extract) (Schilder et al., 2002)
Plantfood (foliar fertilizer) (Schilder et al., 2002)
Milsana (giant knotweed extract) (Schilder et al., 2002) (Schmitt et al., 2002)
neem (Rajeswari et al., 2008)
acylbenzolar-s methyl (Dagostin et al., 2006)
chitosan (Elexa) (Schilder et al., 2002)
Mycosin (Angeli et al., 2006)
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Alternaria alternata (Musetti et al., 2004)
Fusarium proliferatum (Bakshi et al., 2001)
neem (Achimu and Schlosser, 1992)
extract of giant knotweed (Schmitt, 1996)
Alternaria alternata extracts (Musetti et al., 2006)
EXP1, copper gluconate, salt of fatty acid, plant based alcohol extract (Dagostin et
al., 2006)
Pearl millet Pennisetum glaucum (target pathogen = Sclerospora graminicola)
M
B
O
Success in field trials
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Bacillus pumilus strain INR7, strain SE34 (Raj et al., 2003)
Bacillus subtilis (Raj et al., 2003) (Raj et al., 2005)
Pseudomonas fluorescens (Umesha et al., 1998) (Latake and Kolase, 2007)
Gliocladium virens (Arun et al., 2004) (Raj et al., 2005)
Trichoderma harzianum (Raj et al., 2005) (Latake and Kolase, 2007)
Trichoderma lignorum (Raj et al., 2005)
Pseudomonas fluorescens (Raj et al., 2004)
Aspergillus flavus, Trichoderma harzianum and T. viride (Surender et al., 2005)
milk (cow) (Arun et al., 2004)
117
Nicot et al. (Appendix for Chapter 1)
Other Vegetables and fruits
Success in field trials
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Cauliflower and other crucifers (target pathogen = Peronospora parasitica)
Pseudomonas sp. XBC-PS (Li et al., 2007)
Trichoderma harzianum (Pratibha et al., 2004)
M
B
O
Bion (Pratibha et al., 2004)
phosphonate (Kofoet and Fischer, 2007)
Bion (Gawande and Sharma, 2003)
Lettuce (Bremia lactucae)
M
B
O
phosphonate (Kofoet and Fischer, 2007)
Trichodermin (Borovko, 2005)
Pimonex, Timorex and also Alkalin potassium+silicon (Robak and Ostrowska, 2006)
Melon / cucumber (target pathogen = Pseudoperonospora cubensis)
actinomycete (Shu and An, 2004)
Bacillus strains, Z-X-3 and Z-X-10 (Li et al., 2003)
M
B
O
phosphonate (Kofoet and Fischer, 2007)
attenuated cucumber mosaic cucumovirus (Qin et al., 1992)
chitosan ElexaTM (Acar et al., 2008)
compost extracts (Winterscheidt et al., 1990)
Miscellaneous
M
Azotobacter slight effect against Peronospora arborescens on opium poppy (Chakrabarti and
Yadav, 1991)
Cladosporium chlorocephalum against Peronospora arborescens (Chaurasia and
Dayal, 1985) (Nalini and Rai, 1988)
phosphonate against Peronospora destructor on Allium (Kofoet and Fischer, 2007)
DL- beta -amino-n-butyric acid (BABA) against Plasmopara helianthi (Tosi and
Zazzerini, 2000)
B
O
118
Appendix 4
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121
Appendix 5. Inventory of biocontrol agents (M: microbials; B: botanicals; O: others) described in primary literature (1973-2008) for
successful effect against Monilinia in laboratory experiments and field trials on selected crops
Apple (target pathogens = Monilinia fructigena; M. laxa)
Success in field trials
Aureobasidium pullulans, Epicoccum purpurascens, Sordaria fimicola and
Trichoderma polysporum (Falconi and Mendgen, 1994)
Metschnikowia pulcherrima and (Spadaro et al., 2002), (Migheli et al., 1997)
Pseudomonas syringae (Migheli et al., 1997)
(M laxa)
Pantoea agglomerans strain EPS125 (Bonaterra et al., 2004)
M
Apricot (target pathogen = Monilinia laxa)
Success in field trials
bacteria
M
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
Burkholderia gladii OSU 7 (Altindag et al., 2006) (Esitken et al., 2005)
Bacillus OSU-142 and Pseudomonas BA-8 (Esitken et al., 2005)
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
bacteria
Pantoea agglomerans strain EPS125 (Bonaterra et al., 2003)
(M fructicola)
Bacillus subtillis strain B3 (Pusey and Wilson, 1984)
fungi, yeasts
Metschnikowia pulcherrima (Grebenisan et al., 2006) (Grebenisan et al., 2008)
Plum (target pathogen = Monilinia laxa)
Success in field trials
M
remark: no B or O for any of the crops
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
bacteria
Pantoea agglomerans strain EPS125 (Bonaterra et al., 2004)
Epicoccum nigrum (Larena et al., 2001)
Penicillium frequentans (Cal et al., 2002)
(M fructicola)
Bacillus subtillis strain B3 (Pusey and Wilson, 1984)
122
Appendix 5
Cherry (target pathogens = Monilia fructicola, M. laxa, M. fructigena)
Success in field trials
bacteria
(M laxa)
Serenade (Bacillus subtilis QRD137) (Haseli and Weibel, 2002),
M
B
O
(M fructicola)
Bacillus subtilis (15 isolates) (Utkhede and Sholberg, 1986)
Burkholderia cepacia, Bacillus subtilis (Fan et al., 2001)
(M laxa)
Risoplan (Pseudomonas fluorescens), Gaupsin (Pseudomonas aureofaciens = P.
chlororaphis) (Shevchuk, 2006)
Pantoea agglomerans strain EPS125 (Bonaterra et al., 2004)
fungi, yeasts
(M fructicola)
Cryptococcus laurentii (Tian et al., 2004a)
Epicoccum purpurascens (E. nigrum) and Gliocladium roseum (Wittig et al., 1997)
(M laxa)
Aureobasidium pullulans isolates 533 and 547 (Schena et al., 2003)
fungi, yeasts
(M fructicola)
Candida guilliermondii, Kloeckera apiculata, Debaryomyces hansenii (Fan et al.,
2001)
Cryptococcus infirmo-miniatus (Spotts et al., 2002)
Cryptococcus laurentii (Wang and Tian, 2007) (Qin and Tian, 2005) (Qin et al.,
2006)
(M laxa + M fructigena)
Trichodex (Trichoderma harzianum) (Cardei, 2001)
(M laxa)
Trilogy (azadirachtin-free Neemoil) (Haseli and Weibel, 2002)
(M laxa)
lime sulphur (calcium polysulfide) (Haseli and Weibel, 2002)
Blueberry (target pathogen = Monilinia vaccinii-corymbos)
Success in field trials
bacteria
M
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
bacteria
Serenade (Bacillus subtilis QRD137) (Ngugi et al., 2005) (Dedej et al., 2004) (Scherm and Stanaland,
2001) (Schilder et al., 2006)
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
bacteria
BlightBan (Pseudomonas fluorescens A506) (Scherm et al., 2004)
Serenade (Bacillus subtilis QRD137) (Scherm et al., 2004) (Thornton et al., 2008)
Pantoea agglomerans C9-1Sv (Thornton et al., 2008)
fungi, yeasts
Gliocladium roseum H47 (Thornton et al., 2008)
B
O
123
Nicot et al. (Appendix for Chapter 1)
Peach / Nectarine (target pathogens = Monilia fructicola, M. laxa, M. fructigena)
Success in field trials
bacteria
(M fructicola)
Pseudomonas corrugata and P. cepacia; Bacillus subtilis strain B3 (Smilanick et al., 1993)
Success in laboratory conditions (in vitro and/or in planta in controlled
conditions)
bacteria
(M fructicola)
Rizo-N (Bacillus subtilis) (El-Sheikh Aly et al., 2000)
Bacillus amyloliquefaciens C06 (Zhou et al., 2008)
Bacillus subtillis (Gueldner et al., 1988)
Bacillus subtillis strain B3 (Pusey et al., 1986) (Pusey et al., 1988) (Pusey, 1989)
(Pusey and Wilson, 1984)
Pantoea agglomerans strain IC1270 (Ritte et al., 2002)
Pseudomonas syringae NSA-6 (Zhou et al., 1999)
(M laxa)
Pantoea agglomerans strain EPS125 (Bonaterra et al., 2003) (Bonaterra et al.,
2004)
fungi, yeasts
M
B
O
Epicoccum nigrum (Mari et al., 2007)
(M laxa)
Epicoccum nigrum (Cal et al., 2004) (Foschi et al., 1995) (Larena et al., 2005) (Madrigal et al.,
1994) (Melgarejo et al., 1986)
Penicillium frequentans (Cal et al., 1990) (Melgarejo et al., 1986) (Pascual et al., 2000)
Penicillium purpurogenum (Melgarejo et al., 1986)
fungi, yeasts
(M fructicola)
Candida sp(Karabulut et al., 2002)
Cryptococcus laurentii (Yao and Tian, 2005)
Debaryomyces hansenii (Stevens et al., 1997) (Stevens et al., 1998)
Kloeckera apiculata yeast (Karabulut and Baykal, 2003) (McLaughlin et al., 1992)
Muscodor albus (Mercier and Jimenez, 2004) (Schnabel and Mercier, 2006)
Pichia membranaefaciens (Xu et al., 2008)
Trichoderma atroviride (2 isolates), T viride & Rhodotorula sp (Hong et al., 1998)
Plant-guard (T. harzianum) (El-Sheikh Aly et al., 2000)
(M laxa)
Penicillium purpurogenum (Foschi et al., 1995) (Larena and Melgarejo, 1996)
Penicillium frequentans (Foschi et al., 1995)
Trichoderma koningii (Foschi et al., 1995)
(
Sodium bicarbonate enhances effect of Aspire (Candida oleophila) (Droby et al., 2003)
Extract from Bacillus subtillis (McKeen et al., 1986)
Iturin peptides from Bacillus subtillis (Gueldner et al., 1988)
Sodium bicarbonate (Wisniewski et al., 2001); enhances effect of Aspire (Candida
oleophila) (Droby et al., 2003)
124
Appendix 5
Successful inhibition in vitro (target pathogen = B. cinerea)
Bacteria
M
Pseudomonas syringae pv. morsprunorum BA35, Erwinia herbicola C9- (Voland et al., 1999)
Serratia plymuthica, isolate EF-5 (Frommel et al., 1991)
Fungi + yeasts
Penicillium frequentans (Cal and Melgarejo, 1994) (Melgarejo et al., 1985)
Aspergillus flavus, Epicoccum nigrum, Penicillium chrysogenum and P. purpurogenum (Melgarejo et al., 1985)
B
O
Thiolutin from Streptomyces luteosporeus (Deb and Dutta, 1984)
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Appendix 5
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127
Appendix 6. Primary literature (2007-2009) on biological control against Fusarium oxysporum
Abo-Elyousr, K. A. M. and H. M. Mohamed (2009). "Biological Control of Fusarium Wilt in Tomato by Plant Growth-Promoting Yeasts and Rhizobacteria." Plant Pathology Journal 25(2): 199-204.
Three plant growth-promoting yeasts and two rhizobacteria were tested for controlling tomato wilt caused by Fusarium oxysporum L sp. lycopersici under greenhouse and field conditions. Under
greenhouse and field conditions, all treatments were significantly reduced disease severity of tomato wilt relative to the infected control. The highest disease reductions in pots (75.0, 67.4%) and field
(52.5, 42.4%) were achieved by Azospirillum brasilense and Bacillus subtilis compared to infected control. Under field condition all treatments produced the highest tomato yield compared to the control
plants inoculated with the pathogen
.
Al-Jedabi, A. A. (2009). "Biological control of Fusarium root-rot of sorghum." Research Journal of Agriculture and Biological Sciences 5(4): 465-473.
several crops including sorghum that result in low grain yield. All antagonists showed inhibition of mycelial growth of F. oxysporum and the maximum inhibition was recorded when Bacillus subtilis as
biocontrol agent (67.7%). The in vitro root colonization study demonstrated that after four days of germination, the cell counts obtained from the roots have increased and the maximum count is achieved
by B. subtilis (16.9*105 cfu/cm root). The greenhouse pot experiment demonstrated that T. viride and B. subtilis resulted in more than 80% suppression of root rot. The reduction in fresh weight of roots
amounted to 93.6% in the control treatment inoculated with F. oxysporum alone, whereas 71.1% reduction in fresh root weight was recorded for the treatments inoculated with both the pathogen and B.
subtilis; 66.8% reduction in fresh root weight was recorded for the treatments inoculated with both the pathogen and T. harzianum. Root dry weight of the control treatment inoculated with only F.
oxysporum decreased by 94.5% in relation to the non-inoculated control. Among the potential biological control agents in this study, B. cereus resulted in 42.3 reduction in root dry weight compared to
the 94.5% reduction recorded for the control inoculated with F. oxysporum alone. 100% of the roots from the control treatment (F. oxysporum only) rendered growth of F. oxysporum compared to an
incidence ranging from 20 to 55% for plants treated with B. subtilis, B. lecheniformis, B. cereus, T. harzianum and T. viride. Both chlorophyll fractions increased when treated with antagonist and the
maximum enhancement was recorded when Bacillus subtilis used as antagonist compared with that of control. The maximum values of the carbohydrate components were recorded when Bacillus
subtilis used as antagonist relative to those of control.
Amini, J. (2009). "Induced Resistance in Tomato Plants Against Fusarium Wilt Invoked by Nonpathogenic Fusarium, Chitosan and Bion." Plant Pathology Journal 25(3): 256-262.
The potential of nonpathogenic Fusarium oxysporum strain Avr5, either alone or in combination with chitosan and Bion, for inducing defense reaction in tomato plants inoculated with E oxyysporum f.
sp lycopersici, was studied in vitro and glasshouse conditions. Application Bion at concentration of 5, 50, 100 and 500 mu g/ml, and the highest concentration of chitosan reduced in vitro growth of the
pathogen. Nonpathogenic F oxysporum Avr5 reduced the disease severity of Fusarium wilt of tomato in split plants, significantly. Bion and chitosan applied on tomato seedlings at concentration 100 mu
g a.i./plant; 15, 10 and 5 days before inoculation of pathogen. All treatments significantly reduced disease severity of Fusarium wilt of tomato relative to the infected control. The biggest disease reduction
and increasing tomato growth belong to combination of nonpathogenic Fusarium and Bion. Growth rate of shoot and root markedly inhibited in tomato plants in response to tomato Fusarium wilt as
compared with healthy control. These results suggest that reduction in disease incidence and promotion in growth parameters in tomato plants inoculated with nonpathogenic Fusarium and sprayed with
elicitors could be related to the synergistic and cooperative effect between them, which lead to the induction and regulation of disease resistance. Combination of elicitors and nonpathogenic Fusarium
synergistically inhibit the growth of pathogen and provide the first experimental support to the hypothesis that such synergy can contribute to enhanced fungal resistance in tomato. This chemical could
provide a new approach for suppression of tomato Fusarium wilt, but its practical use needs further investigation.
Anand, R., S. Kulothungan, et al. (2009). "Assay of chitinase and beta-1,3 glucanase in Gossypium hirsutum seedlings by Trichoderma spp. against Fusarium oxysporum." International Journal of Plant
Sciences (Muzaffarnagar) 4(1): 255-258.
wilt in cotton. In this regard, the six species of Trichoderma, namely T. viride, T. virens [Gliocladium virens], T. hamatum, T. harzianum, T. koningii and T. reesi, were evaluated for its biocontrol
properties and induction of defence-related enzymes, namely chitinase and beta1-3-glucanase in 30 days old cotton (G. hirsutum) seedlings. Trichoderma spp. could efficiently control the growth rate of
F. oxysporum. In vitro assay of chitinase and beta-1,3-glucanase revealed the maximum production by T. harzianum (56 U/ml) and T. hamatum (80 U/ml), respectively. It also produced appreciable
quantities of defence enzymes. The maximum induction of chitinase and beta1-3-glucanase in plants was found to be 80 U/ml when challenged with T. harzianum, in addition to the enhancement of
defence mechanism in plants. Trichoderma spp. improved the germination rate of seedlings.
Anitha, A. and M. Rebeeth (2009). "Self-fusion of Streptomyces griseus enhances chitinase production and biocontrol activity against Fusarium oxysporum f. sp. lycopersici." Biosciences, Biotechnology
Research Asia 6(1): 175-180.
Protoplasts were isolated from Streptomyces griseus (MTCC - *4734) strain using lysing enzymes and self-fusion of Streptomyces griseus protoplasts was carried out using 50% polyethylene glycol
(MW 1000, Sigma Chemicals Co., USA) in protoplast buffer. The regenerated 8 self fused Streptomyces griseus were studied detailed for chitinase production and biocontrol activity. Parent strain (PSg)
128
Appendix 6
showed protein content of 2.7 mg/ml with chitinase activity of 120 IU/ml. High chitinase activity was measured in the culture filtrates of most of the self-fusants (87%) than the parent. Among the
fusants, the strain SFSg 5 produced protein content of 7.8 mg/ml, maximum chitinase activity of 283.3 IU/ml with a two-fold increase as compared to the parent strain. All the self-fusants exhibited
increased antagonistic activity against F. oxysporum f. sp. lycopersici than the parent. Maximum inhibition (82%, 80%) of mycelial growth of F. oxysporum was recorded with fusant of SFSg 5, SFSg 1
as against 61.1% with PSg. The result implies that, the self-fused Streptomyces griseus resulted in appreciable increase of chitinase production and biocontrol activity also the significance of the
protoplast fusion technique, which could successfully be used to develop hybrid strains also for commercial formulation.
Baysal, O., M. Calskan, et al. (2008). "An inhibitory effect of a new Bacillus subtilis strain (EU07) against Fusarium oxysporum f. sp. Radicis-lycopersici." PMPP Physiological and Molecular Plant
Pathology 73(1/3): 25-32.
destructive disease on tomato (Lycopersicon esculentum Mill.) transplant seedlings and the causal organism of crown and root rot of tomato plants growing in southern coast greenhouses of Turkey. An
isolate of Bacillus subtilis (EU07) identified by the 16s RNA region code gene was selected as the best antagonist and evaluated against FORL in vitro studies. Strain EU07 at 106 CFU ml-1 was able to
reduce disease incidence by 75%, when applied as an inoculant. It efficiently inhibited FORL compared to the control and QST 713 (AgraQuest, Davis, CA) whose inhibition ratio was only 52% in vivo.
Random amplified polymorphic DNA analyses showed banding (genetic) differences between EU07 and QST 713 whereas there were no differences between DNAs of strains that have high homology
to genes involved in the synthesis of antibiotics fengycin, bacillomycin and iturin when screened by oligonucleotide primers designed based on sequence information obtained from the NCBI database.
Furthermore, one specific fragment in the EU07 genome showed the highest similarity to YrvN protein by 99% and AAA ATPase domain protein (72.2%) after amplifying oligonucleotide primers that
are specific to the N-acyl-homoserine lactonase (HLS) gene as a biocontrol activity marker. These results suggested an effect of EU07 on control FORL by YrvN protein as subunit of protease enzyme.
Furthermore, this fragment associated with HLS gene may be a potential molecular marker for selecting effective biological control agent belonging to Bacillus in order to control soilborne pathogens
such as Fusarium, suggesting impairment in FORL invasion by signaling in the plant rhizosphere.
Bernal-Vicente, A., M. Ros, et al. (2009). "Increased effectiveness of the Trichoderma harzianum isolate T-78 against Fusarium wilt on melon plants under nursery conditions." Journal of the Science of Food
and Agriculture 89(5): 827-833.
BACKGROUND: The use of isolates of the genus Trichoderma to control Fusarium wilt in melon plants is one of the most recent and effective alternatives to chemical treatments. In this work we have
studied the immobilization of the isolate Trichoderma harzianum T-78 on different carriers as an efficient method to control vascular Fusarium wilt of melon in nurseries. Different formulations were
developed: liquids (spore suspension, guar gum and carboxymethylcellulose) and solids (bentonite, vermiculite and wheat bran). RESULTS: The introduction of F. oxysporum resulted in a significant
decrease in seedling fresh weight. The treatments which gave a lesser reduction in weight and showing a greater biocontrol effect were the liquid conidial suspension and the solid treatments with
bentonite and superficial vermiculite. Microbiological analyses revealed that the conidial suspension and all the solid treatments, except wheat bran, significantly decreased F. oxysporum populations. Of
all the treatments assayed, bentonite produced the greatest decline in the F. oxysporum population. CONCLUSIONS: The most effective treatments against Fusarium wilt on melon plants were the solid
treatments bentonite and superficial vermiculite. These two treatments gave the greatest plant weight, the lowest percentage of infected plants and the greatest T. harzianum population throughout the
assay. (C) 2009 Society of Chemical Industry
Boureghda, H. and Z. Bouznad (2009). "Biological control of Fusarium wilt of chickpea using isolates of Trichoderma atroviride, T. harzianum and T. longibrachiatum." Acta Phytopathologica et
Entomologica Hungarica 44(1): 25-38.
The efficiency of the antagonist species Trichoderma atroviride (strains Ta.3, Ta.7 and Ta.13), T. harzianum (Th.6, Th.12, Th.15, Th.16 and Th.18) and T. longibrachiatum (TL.1, TL.2, TL.4, TL.5, TL.8,
TL.9, TL.10, TL.11, TL.14 and TL17) against Fusarium wilt (caused by Fusarium oxysporum f.sp. ciceris) was compared using in vitro- and in vivo-based bioassay. A significant decrease of both
growth and conidia production of the pathogen was obtained compared to the control. The highest percentages of diameter colony reduction and conidial production were obtained with Ta.13, causing
65.64% reduction in colony diameter (direct confrontation), 48.71% reduction in colony diameter (indirect confrontation), and a complete inhibition of conidial production. Once more in direct
confrontation, T. atroviride overgrowth the pathogen colony and sporulate above. The seed treatment by Trichoderma spp. isolates before sowing in a soil already infested by the pathogen led to a
significant decrease of disease severity compared to the untreated control. The weakest index of disease severity was obtained with Ta.13, which caused 83.92% reduction compared to the control. The
most effective isolates in protecting chickpea seedlings against the disease were Ta.3, Ta.7 and Ta.13 as well as Th.16. The reduction of disease severity was associated with an increase of the vegetal
growth including the stem height as well as the plant fresh and dry weights.
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Casimiro Michel-Aceves, A., M. Antonio Otero-Sanchez, et al. (2009). "In vitro biocontrol of Fusarium subglutinans (Wollenweb. and Reinking) Nelson, Toussoun and Marasas and F. oxysporum Schlecht.,
causal agents of "Witches' broom" of mango (Mangifera indica L.) by Trichoderma spp." Revista Mexicana de Fitopatologia 27(1): 18-26.
The antagonistic effect of native strains of Trichoderma spp. was evaluated in vitro against Fusarium oxysporum (Fo) and Fusarium subglutinans (Fs), causal agents of mango "witches' broom". Ten
strains of the antagonistic fungus were isolated, one of which was selected and identified to the species level (T. harzianum); this species showed the highest percentage of antagonism inhibiting mycelial
growth of Fo by 62.9% and 42.0% of Fs. In dual Cultures between Fo and/or Fs with the selected strains of Trichoderma, the time for the first contact for Fo was between 3 and 4 days, and between 2 and
3 for Fs. The greatest intersection area (0.87 cm) was observed in T. lignorum against Fo, while the intersection area in Fs with the native strain Thzn-2 was 0.85 cm. Native strains Thzn-2 and Thzcf-12,
and the commercial one showed antagonism class 2, being able to stop growth of both plant pathogens. Strain Thzn-2 is promising as an alternative for biocontrol of Fo and Fs; however, it is necessary to
evaluate it under field conditions.
Chebotar, V. K., N. M. Makarova, et al. (2009). "Antifungal and phytostimulating characteristics of Bacillus subtilis Ch-13 rhizospheric strain, producer of bioprepations." Applied Biochemistry and
Microbiology 45(4): 419-423.
Bacillus subtilis Ch-13 industrial strain was shown to have a wide spectrum of antagonistic activities against different species of phytopathogenic fungi and bacteria. The B. subtilis Ch-13 strain produces
lytic enzymes; cyanide and other antifungal metabolites; stimulates plant growth, producing phytohormones-auxin derivatives. This strain by 2.5 times reduced the quantity of tomato plants infected with
phytopathogenic fungus Fusarium oxysporum during inoculation. Fungi abundance on roots with bacterial inoculation was 6.9 times less than in the absence of inoculation. The application of detected
antifungal metabolites as biochemical markers for the strain enables to control the stability of physiologic and biochemical characteristics of the producer, and ensures a rapid quality assay of
biopreparations with high performance liquid chromatography (HPLC).
Chen, L. and W. Chen (2009). "Genome shuffling enhanced antagonistic activity against Fusarium oxysporum f. sp. melonis and tolerance to chemical fungicides in Bacillus subtilis BS14." Journal of Food,
Agriculture & Environment 7(2): 856-860.
enhance antagonistic activity against Fusarium oxysporum f. sp. melonis (FOM) and tolerance to two chemical fungicides. Strain BS14 was identified as a strain of Bacillus subtilis by the analysis of 16S
rDNA sequences. A stable recombinant F35 was obtained after three rounds of shuffling. Antagonistic activity of recombinant F35 against FOM was increased by 34.52% and 65.48% compared to that
of the parent strain HN8-7 with highest activity and another parent strain utilized, BS14. The tolerance to chemical fungicides was also significantly improved (p0.05) compared to that of strain BS14.
Reduction of FOM of 94% was observed by using recombinant F35, which was increased by 45% compared to that of strain BS14 (p0.05) and no significant differences (p>0.05) compared to that of
thiophanate methyl (MRL). Reduction of FOM of 100% was dramatically observed by using an integrated treatment combining MRL (50% of usual dosage) with recombinant F35. Strain F35 with these
improved traits would be a promising biocontrol agent in the control of FOM. Here genome shuffling was proved to be a practical methodology for strain improvement of antagonistic microorganism
Bacillus subtilis BS14 for enhancing antagonistic activity against FOM and tolerance to chemical fungicides.
Clematis, F., M. L. Gullino, et al. (2009). "Antagonistic activity of microorganisms isolated from recycled soilless substrates against Fusarium crow rot." Protezione delle Colture(3): 29-33.
We report the results obtained in biological control trials against crown and root rot of tomato incited by Fusarium oxysporum f. sp. radicis lycopersici by using microorganisms isolated from soilless
cultivation systems that showed suppressiveness against this disease. Among the tested microorganisms belonging to fluorescent bacteria (32 isolates) and to fungi belonging to Trichoderma (39 isolates)
and Fusarium (38 isolated), 5 bacteria and 6 fungi showed a good activity against the pathogen. Such strains will be used in greenhouse trials, under situations closer to the field, in order to evaluate their
potential to be adopted under practical conditions.
Eden Paredes-Escalante, J., J. Armando Carrillo-Fasio, et al. (2009). "Antagonistic microorganismos for control of the fungal complex that cause wilt in chickpea (Cicer arietinum L.) in the state of Sinaloa,
Mexico." Revista Mexicana de Fitopatologia 27(1): 27-35.
The antagonistic activity in vitro of microorganisms isolated from chickpea rhizosphere, was evaluated against Fusarium oxysporum, Sclerotium rolfsii, and Rhizoctonia solani, causal agents of chickpea
wilt. The native strains with the higher percentage of pathogen mycelial growth inhibition were selected and identified as Trichoderma lignorum (CIAD 06-540903), T. harzianum (CIAD 05-550903),
Bacillus subtilis (CIAD-940111), and Pseudomonas fluorescens (CIAD-990111). These strains and a commercial strain of T. harzianum (T-22) were mixed with Glomus intraradices and their
effectiveness to reduce chickpea wilt was compared against a chemical treatment (PCNB) and all absolute control in the field. The seed was treated with the microorganisms before sowing and
evaluations of disease severity were conducted each 15 days, while root colonization by the antagonistic microorganisms was assessed 45 days after sowing. Colonization of T, harzianum CIAD 05550903 + G. infraradices was 33 x 10(3) ufc/g fresh root-75% and B. subtilis + G. intraradices was 1.3 x 10(8) Ufc/g fresh root-75%; while the combination P.fluorescens + G. intraradices was 1.4 x
10(7) Ufc/g fresh root-88%. These treatments also showed a reduction of disease severity in 64, 57, and 51%, respectively in comparison with the control.
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Appendix 6
El-Khallal, S. M. (2007). "Induction and modulation of resistance in tomato plants against Fusarium wilt disease by bioagent fungi (arbuscular mycorrhiza) and/or hormonal elicitors (jasmonic acid & salicylic
acid): 2 - changes in the antioxidant enzymes, phenolic compounds and pathogen related-proteins." Australian Journal of Basic and Applied Sciences 1(4): 717-732.
Induction of plant defense against pathogen attack is regulated by a complex network of different signals. In the present study interaction between hormonal signals [jasmonic acid (JA) or salicylic acid
(SA)] and bioagent [arbuscular mychorrhiza (AM) fungi] was used as new strategy to enhance tomato defense responses against wilt disease caused by Fusarium oxysporum (Fo). Thus changes in
various physiological defenses including antioxidant enzymes, phenolic compounds and pathogenesis related (PR) proteins were investigated in leaves of tomato plants. Results appeared that production
of reactive oxygen species (ROS), mainly H2O2 and O2 increasing the time of infection. Application with bioagent AM fungi and/or hormonal elicitors (JA & SA) markedly decreased these levels,
while LOX activity greatly increased as compared with infected control. SA - treated plants had the highest MDA level but JA+AM fungi treated plants recorded the highest LOX activity. Infection by
Fusarium oxysporm significantly increased activity of antioxidant enzymes (SOD, APX and CAT) in tomato leaves at different stages of growth. The highest activity was recorded in leaves of AM
fungi+JA-treated plants, while treatments with SA especially when applied alone markedly decreased H2O2 scavenging enzymes (APX and CAT) and greatly increased SOD activity. Thus, imbalance
between H2O2 - generation and scavenging enzymes in leaves may reflect a defense mechanism in tomato or a pathogenicity strategy of the fungus. Levels of certain phenolic acids greatly changed in
tomato leaves in response to Fusarium oxysporum, AM fungi and hormonal elicitors. Benzoic and Galleic acids contents markedly decreased, however, contents of coumaric, cinnamic, chlorogenic and
ferulic acids increased in leaves of all treatments. Also, activity of lignification enzymes POX, PPX and PAL significantly increased in leaves of infected tomato plants. JA-treated plants caused the
highest POX and PPX activities, while SA-treated plants having the highest PAL activities. High accumulation of phenolic compounds and activity POX, PPX and PAL in these plants may reflect a
component of many defense signals activated by bioagent and hormonal inducers which leading to the activation of power defense system in tomato against attack. Analysis of protein electrophoresis
revealed that interaction between hormone signal (JA & SA) and bioagent AM fungi mediating the expression of the majority of different PR-proteins leading to increasing defense mechanism against
Fusarium oxysporum infection. Thus, induction of protein bands of molecular weights 35, 33, 32, 31 (PR-2, beta-1, 3 glucanase), 30.5 and 27 (PR-3,-4, chitinase) in infected leaves indicated the
important role which played in disease resistance. Finally, the new mechanism of the combination strategy between bioagent and hormonal signals (either synergistically or antagonistically) played
important roles for increasing various defense systems and altering expression of defense genes which leading to different PR-proteins working together to increased resistance in tomato plants against
wilt disease caused by Fusarium oxysporum. In addition, results revealed that defense mechanism in plants treated with AM fungi and JA are more effective than AM fungi plus SA-treated plants.
Floch, G. l., J. Vallance, et al. (2009). "Combining the oomycete Pythium oligandrum with two other antagonistic fungi: root relationships and tomato grey mold biocontrol." Biological Control 50(3): 288298.
To reduce Pythium oligandrum biocontrol variability and improve its efficacy, experiments were performed by combining the oomycete with two other antagonistic fungi, Fusarium dishes, Fo47 or T.
harzianum hyphae destroyed P. oligandrum cells by antibiosis and mycoparasitism processes; in the rhizosphere of tomato plants (Lycopersicon esculentum), the same antagonistic features were
observed. However, in the rhizosphere, hyphae are frequently separated by a certain distance; this allows the coexistence and the persistence of the three microorganisms on the root systems. When
introduced in the rhizosphere, Fo47 and P. oligandrum were able to penetrate the root tissues with Fo47 limited to the epidermal and upper layers of cortical cells while P. oligandrum colonized deeper
tissue at a faster rate. The two antagonists were killed in few days within roots following elicited plant-defense reactions. T. harzianum was not able to penetrate root tissues. Root colonization with either
P.oligandrum alone or in combination with Fo47 and/or T. harzianum resulted in systemic plant resistance which provided plant protection against Botrytis cinerea infection of leaves. The level of control
and the expression of pathogenesis-related proteins (PR-proteins) in leaves were similar whatever the antagonistic microbial treatment applied to roots.
Gay, M. I. T., Anonymous, et al. (2009). Substrates containing a Trichoderma asperellum strain for biological control of Fusarium and Rhizoctonia, Universidad de Barcelona.
The strain of Trichoderma asperellum T34(2) CECT No. 20417 is useful for preparing substrates for biological control of vascular fusariose and death of plants caused by Rhizoctonia solani. The
substrates can be peats, composts (hardwood compost, pine bark compost, cork compost, sludge compost from sewage treatment plants, garden residues, etc.) or formulations based on CPV-type
compost (compost+peat+vermiculite). The fact that the substrates suppress both Fusarium oxysporum f. sp. lycopersici and Rhizoctonia solani provides an advantage in comparison with other substrates
known in prior art. Another advantage is that the use of methyl bromide, a highly harmful product for the environment, in the control of vascular fusariose is avoided.
Huang, X., J. Luo, et al. (2009). "Isolation and bioactivity of endophytic fungi in Derris hancei." Journal of South China Agricultural University 30(2): 44-47.
Derris hancei Hemsl. The antagonism of endophytic fungi against fungal pathogens was tested in vitro. Penicillium sp. Q1, Rhizoctonia sp. S1, Phomopsis sp. N2, and Corticium sp. F1 isolated from the
caudex of D. hancei, and Penicillium sp. Q2 isolated from the leaf, inhibited the hyphal growth of Colletotrichum gloeosporioides Penz, Fusarium oxysporum f. niveum (E. F. Smith) Snyber et Hansen,
Rhizoctonia sp. S1 against Colletotrichum orbiculare Arx, and Phomopsis sp. N2 against Colletotrichum musae (Berk1 & Curt1) Arx1 on dual culture with inhibition index II. It was reported that
endophytic fungus in D.hancei could produced antibacterial substances in this paper. The culture filtrates of Penicillium sp. Q2 treated in 48 h after treatment possessed 100.00% of adjusted mortality
against the 2nd larvae of Spodoptera litura by leaves disc feeding bioassays, and 75.10% against Lipaphis erysimi Kaltenbach (apterous adult) by insect-soaking method, respectively, which showed that
the activity of Penicillium sp. Q2 was higher than that of other endophytic fungi.
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Jadeja, K. B. and D. M. Nandoliya (2008). "Integrated management of wilt of cumin (Cuminum cyminum L.)." Journal of Spices and Aromatic Crops 17(3): 223-229.
Four components of integrated management namely, soil solarization, crop rotation, chemicals and biocontrol agents were tested under field condition at Junagadh (Gujarat) for the management of wilt of
cumin (Cuminum cyminum) caused by Fusarium oxysporum f. sp. cumini. Growing of sorghum (Sorghum bicolor) or maize (Zea mays) during kharif season did not reduce wilt incidence during the
following rabi season. Soil solarization with 25 m LLDPE plastic cover for 15 days in summer proved most effective in reducing wilt incidence to 26.27% as against 44.90% in non-solarization and
increasing yield to 396 kg ha-1 as against 286 kg ha-1 in non-solarized plots. Application of carbendazim granules @ 10 kg ha-1 one month after sowing or Trichoderma viride in organic carrier @ 62.5
kg ha-1 at sowing time were also effective. Integrating soil solarization followed by growing of sorghum in kharif and application of either carbendazim granules @ 10 kg ha-1 one month after sowing or
application of T.viride in organic carrier @ 62.5 kg ha-1 was effective for the management of cumin wilt.
Kamilova, F., S. Validov, et al. (2009). Biological control of tomato foot and root rot caused by Fusarium oxysporum f.sp. radicis-lycopersici by Pseudomonas bacteria. Proceedings of the Second
International Symposium on Tomato Diseases, Kusadasi, Turkey, 8-12 October 2007.
Rhizobacteria are a natural and most suitable source for the isolation of potential microbiological control agents that can protect plants from soilborne pathogens and consequently improve crop quality
and yield. The beneficial effect of such bacteria on plant health depends in many cases on their ability to aggressively colonize the rhizosphere and compete with the indigenous, including pathogenic,
microflora for nutrients and niches on the plant root. Bacterial strains Pseudomonas chlororaphis PCL1391 and P. fluorescens WCS365 employ antibiosis and induced systemic resistance, respectively, to
control tomato foot and root rot (TFRR) caused by phytopathogenic fungus Fusarium oxysporum f.sp. radicis-lycopersici (Forl). For the selection of biocontrol bacteria acting via the mechanism
"competition for nutrients and niches" we have developed an enrichment method for enhanced tomato root tip colonizers, starting from a crude mixture of rhizobacteria coated on the seed, using a sterile
quartz sand/plant nutrient solution gnotobiotic system. As a result of this enrichment procedure, and subsequent tests on competitive tomato root tip colonization, the strongly competitive biocontrol
strains P. fluorescens PCL1751 and P. putida PCL1760 were isolated. Both strains effectively suppress TFRR under soil and hydroponic cultivation conditions.
Kamilova, F., S. Validov, et al. (2009). "Biological control of tomato foot and root rot caused by Fusarium oxysporum f.sp. radicis-lycopersici by Pseudomonas bacteria." Acta Horticulturae(808): 317-320.
isolation of potential microbiological control agents that can protect plants from soilborne pathogens and consequently improve crop quality and yield. The beneficial effect of such bacteria on plant
health depends in many cases on their ability to aggressively colonize the rhizosphere and compete with the indigenous, including pathogenic, microflora for nutrients and niches on the plant root.
Bacterial strains Pseudomonas chlororaphis PCL1391 and P. fluorescens WCS365 employ antibiosis and induced systemic resistance, respectively, to control tomato foot and root rot (TFRR) caused by
phytopathogenic fungus Fusarium oxysporum f.sp. radicis-lycopersici (Forl). For the selection of biocontrol bacteria acting via the mechanism "competition for nutrients and niches" we have developed
an enrichment method for enhanced tomato root tip colonizers, starting from a crude mixture of rhizobacteria coated on the seed, using a sterile quartz sand/plant nutrient solution gnotobiotic system. As a
result of this enrichment procedure, and subsequent tests on competitive tomato root tip colonization, the strongly competitive biocontrol strains P. fluorescens PCL1751 and P. putida PCL1760 were
isolated. Both strains effectively suppress TFRR under soil and hydroponic cultivation conditions.
Kannan, V. and R. Sureendar (2009). "Synergistic effect of beneficial rhizosphere microflora in biocontrol and plant growth promotion." Journal of Basic Microbiology 49(2): 158-164.
Biological systems are getting more relevance than chemical control of plant pathogens as they are not only eco-friendly and economic in approach but are also involved in improving the soil consistency
and maintenance of natural soil flora. Plant growth promoting rhizosphere microorganisms were isolated from three different tree rhizospheres using selective culture media. Five microorganisms were
selected from each rhizosphere soil based on their efficiency and screened for their ability to promote plant growth as a consortium. Each of the developed consortium has a phosphate solubilizer,
nitrogen fixer, growth hormone producer, heterotrophic member and an antagonist. The plant growth promoting ability of the microbial members present in the consortium was observed by estimating
the IAA production level and also by the nitrogenase activity of the nitrogen fixers. The biocontrol potentiality of the consortium and the antagonist present in the consortium were checked by both dual
plate assay and cross-streaking technique. Consortial treatments effected very good growth promotion in Lycopersicon esculentum Mill and the treated plants also developed resistance against wilt
pathogen, Fusarium oxysporum f. sp. lycopersici though the effect was well pronounced with consortium developed from Santalum album.
Li, J., Q. Yang, et al. (2009). "Evaluation of biocontrol efficiency and security of A Bacillus subtilis strain B29 against cucumber Fusarium wilt in field." China Vegetables(2): 30-33.
cucumerinum, was isolated from cucumber rhizosphere. After twice of 4-field-plot experiments, the control efficiencies of 100, 250 and 500 dilution times to cucumber Fusarium wilt were 70.3-88.2%,
62.3-85.9%, and 54.7-80.6%, respectively. The average efficiency of field trials with B29 was 84.9% during 2 years and the yield of cucumber increased by 12.57%. The acute toxicity of Bacillus subtilis
strain B29 to big mouse through its mouth and skin was examined, and the LD50 was more than 5000 mg/kg. The application of strain B29 on cucumber, tomato, bean and seed pumpkin was safe based
on the observed seedling rate, growth and development.
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Liu, Q., J. C. Yu, et al. (2009). "Antagonism and Action Mechanism of Antifungal Metabolites from Streptomyces rimosus MY02." Journal of Phytopathology 157(5): 306-310.
The genus of Streptomyces, a saprophytic Gram-positive bacterium, has properties, which make them useful as pharmaceutical and biocontrol agents. A streptomyces strain MY02 from soil samples
showed significant antagonism against 14 plant pathogenic fungi including Fusarium oxysporum f. sp. cucumarinum. Antifungal metabolite(s) SN06 from the culture of the strain MY02 were extracted
with n-butanol and purified by silica gel column chromatography. The minimum concentration of SN06 inhibiting any visible fungal growth of F. oxysporum f. sp. cucumarinum is 12.5 mu g/ml by
twofold serial dilutions method. The mycelia of F. oxysporum f. sp. cucumarinum treated with SN06 were observed under the normal optics microscope. The results showed that some cells of hyphae
began to dilate and formed some strings of beads. The cytoplasm oozed out of the cells with the culture time and so most of the cells became empty. The hyphae broke into many segments and then
collapsed after 48 h. After inoculated in potato dextrose medium for 48 h, the filtrate of mycelia treated with 1% NaCl containing 12.5 mu g/ml SN06 was scanned using ultraviolet spectrophotometer
and absorption peak at 260 nm showed that the mycelia cell membrane of F. oxysporum f. sp. cucumarinum was broken and that nucleic acid oozed out of the cell.
Maina, M., R. Hauschild, et al. (2008). "Protection of tomato plants against fusaric acid by resistance induction." Journal of Applied Biosciences(JABs) 1: 18-31.
Objectives: The rhizobacteria Bacillus sphaericus B43, Pseudomonas fluorescens T58, and P. putida 53 are able to induce systemic resistance (ISR) against Fusarium oxysporum f.sp. lycopersici (FOL)
in tomato. This study investigated if the ISR reduced the damage by the toxin fusaric acid (FA) produced by FOL. Methodology and Results: The bacteria were applied to the rhizosphere of tomato
plants. Chlorophyll content and ion leakage were determined after placing the leaf discs in FA. Active oxygen species (AOS), superoxide and hydrogen peroxide levels were determined in leaves of
plants injected with FA. Activities of superoxide dismutase (SOD), ascorbate (AS) and guaiacol peroxidases (GPX) involved in AOS metabolism were quantified. In untreated plants, FA led to high ion
leakage and chlorophyll degradation caused by H2O2 accumulation. All the bacteria treatments decreased the chlorophyll degradation. Ion leakage was reduced by treatment with P. fluorescens T58 and
B. sphaericus B43, while P. putida 53 was less effective. Treatment of plants with bacteria resulted in increased superoxide contents, but varying over time. Increased SOD and GPX activities in untreated
plants were suppressed after bacteria treatment. Plants treated with P. fluorescens T58 showed only a transient increase in superoxide. P. putida 53-treated plants removed AOS, but high initial superoxide
levels led to membrane damages. Treatment with B. sphaericus B43 suppressed the effects of FA, but AOS metabolism showed only slight alterations. Conclusions and potential applications of findings:
ISR could also protect plant tissues from damage by pathogen toxins, which is a potential new dimension to the known mechanisms of action of biological control agents.
Martinez-Medina, A., J. A. Pascual, et al. (2009). "Interactions between arbuscular mycorrhizal fungi and Trichoderma harzianum and their effects on Fusarium wilt in melon plants grown in seedling
nurseries." Journal of the Science of Food and Agriculture 89(11): 1843-1850.
BACKGROUND: Biological control through the use of Trichoderma spp. and arbuscular mycorrhizal fungi (AMF) could contribute to a reduction of the inputs of environmentally damaging
agrochemical products. The objective of this study was to evaluate the interactions between four AMF (Glomus intraradices, Glomus mosseae, Glomus claroideum and Glomus constrictum) and
Trichoderma harzianum for their effects on melon plant growth and biocontrol of Fusarium wilt in seedling nurseries. RESULTS: AMF colonisation decreased fresh plant weight, which was unaffected
by the presence of T. harzianum. Dual inoculation resulted in a decrease in fresh weight compared with AMF-inoculated plants, except for G. intraradices. AMF colonisation level varied with the AM
endophyte and was increased by T. harzianum, except in G. mosseae-inoculated plants. Negative effects of AMF on T. harzianum colony-forming units were found, except with G. intraradices. AMF
alone were less effective than T. harzianum in suppressing disease development. Combined inoculation resulted in a general synergistic effect on disease control. CONCLUSION: Selection of the
appropriate AMF species and its combination with T. harzioanum were significant both in the formation and effectiveness of AM symbiosis and the reduction of Fusarium wilt incidence in melon plants.
The combination of G. intraradices and T. harzianum provided better results than any other tested. (C) 2009 Society of Chemical Industry
Matar, S. M., S. A. El-Kazzaz, et al. (2009). "Antagonistic and inhibitory effect of Bacillus subtilis against certain plant pathogenic fungi, I." Biotechnology 8(1): 53-61.
subtilis isolates (B1 to B14), obtained from different Egyptian sites, were tested against six fungal isolates belonging to four different genera, Rhizoctonia solani, Helminthosporium spp., Alternaria spp.
and Fusarium oxysporum. Cultural, morphological and physiological characteristics of these isolates were found to be identical to B. subtilis. Four B. subtilis isolates (B1, B4, B7, B8) had more
antagonistic effect on all fungal isolates. Supernatant of B. subtilis isolate B7 had antagonistic effect on 6 fungal isolates but it was more effective on Helminthosporium spp., Alternaria spp. and F.
oxysporum. B. subtilis as well as isolate B7 showed effectiveness in reducing disease incidence and severity levels of tomato plants when added to the F. oxysporum and R. solani-infested soil. Also, it
stimulated the growth of tomato plants compared to the other. HPLC analysis of the HCl precipitate of B.subtilis isolate B7 culture supernatant revealed that an identical pattern of five peaks to that of a
purified preparation of iturin A was obtained.
Matar, S. M., S. A. El-Kazzaz, et al. (2009). "Bioprocessing and scaling-up cultivation of Bacillus subtilis as a potential antagonist to certain plant pathogenic fungi, III." Biotechnology 8(1): 138-143.
isolate G-GANA7 (GenBank accession No. EF583053), collected from Abo-Homos in Egypt, was tested against six fungal isolates belonging to four different genera, i.e. Rhizoctonia solani,
Helminthosporium sp., Alternaria sp. and Fusarium oxysporum. B. subtilis isolate G-GANA7 was cultured in 3 litre bench-top New Brunswick Scientific BioFlow III bioreactor for producing the
maximum yield of biomass and antifungal compound. Fed-batch processes were automated through a computer aided data bioprocessing system AFS-BioCommand multi-process management program
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to regulate the cell growth rate by controlling interactively the nutrient feed rate, temperature, pH and agitation speed based on dissolved oxygen. In batch cultivation, the process suffered from low yield
of cell mass (3.2 g litre-1) and antifungal activity because of high initial glucose concentration followed by acetate formation which the causal agent for inhibition of cell growth. Constant and exponential
fed-batch strategies were adopted to circumvent this potential problem. Fed-batch cultivation of B. subtilis was conducted at the specific growth rate of 0.13 and 0.1 h-1 for constant and exponential
strategies, respectively. High cell density of 12.8 and 14.6 g litre-1 for both operations, with an overall biomass yield of 0.45 g g-1 was achieved. The inhibitory activity of antifungal in supernatant
reached its maximum value of 2 and 2.2 cm for constant and exponential fed-batch cultivations.
Mazurier, S., T. Corberand, et al. (2009). "Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt." ISME Journal 3(8): 977-991.
Natural disease-suppressive soils provide an untapped resource for the discovery of novel beneficial microorganisms and traits. For most suppressive soils, however, the consortia of microorganisms and
mechanisms involved in pathogen control are unknown. To date, soil suppressiveness to Fusarium wilt disease has been ascribed to carbon and iron competition between pathogenic Fusarium oxysporum
and resident non-pathogenic F. oxysporum and fluorescent pseudomonads. In this study, the role of bacterial antibiosis in Fusarium wilt suppressiveness was assessed by comparing the densities,
diversity and activity of fluorescent Pseudomonas species producing 2,4-diacetylphloroglucinol (DAPG) (phlD+) or phenazine (phzC+) antibiotics. The frequencies of phlD+ populations were similar in
the suppressive and conducive soils but their genotypic diversity differed significantly. However, phlD genotypes from the two soils were equally effective in suppressing Fusarium wilt, either alone or in
combination with non-pathogenic F. oxysporum strain Fo47. A mutant deficient in DAPG production provided a similar level of control as its parental strain, suggesting that this antibiotic does not play a
major role. In contrast, phzC+ pseudomonads were only detected in the suppressive soil. Representative phzC+ isolates of five distinct genotypes did not suppress Fusarium wilt on their own, but acted
synergistically in combination with strain Fo47. This increased level of disease suppression was ascribed to phenazine production as the phenazine-deficient mutant was not effective. These results
suggest, for the first time, that redox-active phenazines produced by fluorescent pseudomonads contribute to the natural soil suppressiveness to Fusarium wilt disease and may act in synergy with carbon
competition by resident non-pathogenic F. oxysporum.
Minerdi, D., S. Bossi, et al. (2009). "Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35." Environmental Microbiology
11(4): 844-854.
Fusarium oxysporum MSA 35 [wild-type (WT) strain] is an antagonistic Fusarium that lives in association with a consortium of bacteria belonging to the genera Serratia, Achromobacter, Bacillus and
Stenotrophomonas in an Italian soil suppressive to Fusarium wilt. Typing experiments and virulence tests provided evidence that the F. oxysporum isolate when cured of the bacterial symbionts [the
cured (CU) form], is pathogenic, causing wilt symptoms identical to those caused by F. oxysporum f. sp. lactucae. Here, we demonstrate that small volatile organic compounds (VOCs) emitted from the
WT strain negatively influence the mycelial growth of different formae speciales of F. oxysporum. Furthermore, these VOCs repress gene expression of two putative virulence genes in F. oxysporum
lactucae strain Fuslat10, a fungus against which the WT strain MSA 35 has antagonistic activity. The VOC profile of the WT and CU fungus shows different compositions. Sesquiterpenes, mainly
caryophyllene, were present in the headspace only of WT MSA 35. No sesquiterpenes were found in the volatiles of ectosymbiotic Serratia sp. strain DM1 and Achromobacter sp. strain MM1. Bacterial
volatiles had no effects on the growth of the different ff. spp. of F. oxysporum examined. Hyphae grown with VOC from WT F. oxysporum f. sp. lactucae strain MSA 35 were hydrophobic whereas
those grown without VOCs were not, suggesting a correlation between the presence of volatiles in the atmosphere and the phenotype of the mycelium. This is the first report of VOC production by
antagonistic F. oxysporum MSA 35 and their effects on pathogenic F. oxysporum. The results obtained in this work led us to propose a new potential direct long-distance mechanism for antagonism by F.
oxysporum MSA 35 mediated by VOCs. Antagonism could be the consequence of both reduction of pathogen mycelial growth and inhibition of pathogen virulence gene expression.
Nam, M. H., M. S. Park, et al. (2009). "Biological Control of Strawberry Fusarium Wilt Caused by Fusarium oxysporum f. sp fragariae Using Bacillus velezensis BS87 and RK1 Formulation." Journal of
Microbiology and Biotechnology 19(5): 520-524.
Two isolates, Bacillus sp. BS87 and RK1, selected from soil in strawberry fields in Korea, showed high levels of antagonism towards Fusarium oxysporum f. sp. fragariae in vitro. The isolates were
identified as B. velezensis based on the homology of their gyrA sequences to reference strains. BS87 and RK1 were evaluated for control of Fusarium wilt in strawberries in pot trials and field trials
conducted in Nonsan, Korea. In the pot trials, the optimum applied concentration of BS87 and RK1 for pre-plant root-dip application to control Fusarium wilt was 10(5) and 10(6) colony-forming units
(CFU)/ml, respectively. Meanwhile, in the 2003 and 2005 field trials, the biological control efficacies of formulations of RK1 were similar to that of a conventional fungicide (copper hydroxide) when
compared with a non-treated control. The RK1 formulation was also more effective than BS87 in suppressing Fusarium wilt under field conditions. Therefore, the results indicated that formulations of B.
velezensis BS87 and RK1 may have potential to control Fusarium wilt in strawberries.
Narayan, M., P. Tini, et al. (2009). "Biological and chemical management of tomato wilt caused by Fusarium oxysporum f.sp. lycopersici." Journal of Soils and Crops 19(1): 118-121.
Wilt of tomato is one of the most important known disease caused by Fusarium oxysporum f. sp. lycopersici. In the present study four bioagents (Trichoderma harzianum, T. viride, Bacillus subtilis and
Pseudomonas fluorescens) and two fungicides (Carbendazim and Thiram) were evaluated both in vitro and in vivo conditions. In vitro evaluation, of Carbendazim (0.1%) completely inhibited the growth
134
Appendix 6
of tomato wilt pathogen Fusarium oxysporum f.sp. lycopersici and was found significantly superior over the rest of fungicides. While, among the biological agents Trichoderma viride was found
significantly superior to the rest in checking the growth of pathogens and showed 85.69 per cent inhibition. In vivo under field condition, seedling dip treatment of Carbendazim (1 gl-1 water) was found
most significant followed by Carbendazim+ T.viride (1+100 gl-1 water) and T. viride (100 gl-1 water) significantly reduced wilt incidence by 73.91, 69.56 and 68.11 per cent respectively as against
71.88 per cent wilting in control (under epiphytotic condition i.e. wilt sick soil).
Ortega-Morales, B. O., F. N. Ortega-Morales, et al. (2009). "Antagonism of Bacillus spp. Isolated from Marine Biofilms Against Terrestrial Phytopathogenic Fungi." Marine Biotechnology 11(3): 375-383.
We aimed at determining the antagonistic behavior of bacteria derived from marine biofilms against terrestrial phytopathogenic fungi. Some bacteria closely related to Bacillus mojavensis (three isolates)
and Bacillus firmus (one isolate) displayed antagonistic activity against Colletotrichum gloeosporioides ATCC 42374, selected as first screen organism. The four isolates were further quantitatively tested
against C. gloeosporioides, Colletotrichum fragariae, and Fusarium oxysporum on two culture media, potato dextrose agar (PDA) and a marine medium-based agar [yeast extract agar (YEA)] at different
times of growth of the antagonists (early, co-inoculation with the pathogen and late). Overall antagonistic assays showed differential susceptibility among the pathogens as a function of the type of culture
media and time of colonization (P < 0.05). In general, higher suppressive activities were recorded for assays performed on YEA than on PDA; and also when the antagonists were allowed to grow 24 h
earlier than the pathogen. F. oxysporum was the most resistant fungus while the most sensitive was C. gloeosporioides ATCC 42374. Significant differences in antagonistic activity (P < 0.05) were found
between the different isolates. In general, Bacillus sp. MC3B-22 displayed a greater antagonistic effect than the commercial biocontrol strain Bacillus subtilis G03 (KodiakA (R)). Further incubation
studies and scanning electronic microscopy revealed that Bacillus sp. MC3B-22 was able to colonize, multiply, and inhibit C. gloeosporioides ATCC 42374 when tested in a mango leaf assay, showing
its potential for fungal biocontrol. Additional studies are required to definitively identify the active isolates and to determine their mode of antifungal action, safety, and biocompatibility.
Padghan, P. R. and M. M. Baviskar (2009). "Efficacy of bioagent and different root extracts for supression of chickpea wilt in vitro." Asian Journal of Bio Science 4(1): 56-58.
udid, sorghum (Sorghum bicolor), groundnut and mung bean and biological control agents (Trichoderma viride, T. harzianum, T lignorum and T. koningii) against the chickpea wilt pathogen, Fusarium
oxysporum f.sp. ciceris (FOC), was studied in the laboratory. A lower radial mycelial growth and a higher inhibitory effect were recorded in sorghum root extract medium (28.00 mm and 54.34%),
respectively, however, it was at par with groundnut root extract medium (30.00 mm and 51.08%), compared to the control (61.33 mm). In dual culture technique, the growth of FOC was restricted by T.
viride (56.16%), followed by T. harzianum (50.57%). T. lignorum recorded the minimum zone of inhibition (40.45%).
Qiu, W., H. Huang, et al. (2009). "Screening of actinomycete against Fusarium oxysporum f. sp. cubense and identification of strain DA07408." Research of Agricultural Modernization 30(1): 126-128.
samples, and 8 of these strains showed significant activities against F. oxysporum f.sp. cubense. One actinomycete (DA07408) isolated from an arboretum in Danzhou, Hainan, China, exhibited marked
antagonism towards F. oxysporum f.sp. cubense. The conditions for the fermentation of the actinomycete were optimized. Based on the morphological, physiological and biochemical characteristics of
the strain, and on the analysis of 16S rDNA and phylogenetic tree, DA07408 was identified as Streptomyces olivochromogenes.
Raddadi, N., A. Belaouis, et al. (2009). "Characterization of polyvalent and safe Bacillus thuringiensis strains with potential use for biocontrol." Journal of Basic Microbiology 49(3): 293-303.
Sixteen Bacillus thuringiensis (Bt) strains were screened for their anti-insect, antibacterial and antifungal determinants by phenotypic tests and PCR targeting major insecticidal proteins and complements,
chitinases, lactonases, beta-1,3-glucanases and zwittermicin A. Six strains had genes of at least two major insecticidal toxins and of insecticidal complements. With regard to fungal biocontrol, all the
strains inhibited Fusarium oxysporum and Aspergillus flavus growth and four strains had all or most of the antifungal determinants examined, with strain Bt HD932 showing the widest antifungal activity
spectrum. Autolysins, bacteriocin and AHL-lactonases were produced by all or most of the tested strains with different activity spectra including pathogens like Listeria monocytogenes. Safety evaluation
was carried out via PCR by screening the B. cereus psychrotolerance-related genes, toxin genes and the virulence pleiotropic regulator plcR. Diarrheal enterotoxins and other toxin genes were widespread
among the collection with strains Bt HD9 and H45 lacking psychrotolerance-related genes, while five strains were positive. Only three strains (BMG1.7, H172, H156) resulted positive with primer sets
targeting partial or complete plcR gene. By Vero Cell Assays, Bt HD868 followed by Bt HD9 were shown to be the safest strains. These polyvalent and safe Bt strains could be very promising in field
application.
Rasal, P. H., J. R. Shelar, et al. (2009). "Effect of endophytic antagonist on pigeonpea." Journal of Maharashtra Agricultural Universities 34(1): 52-53.
resistant (ICP 8863) and resistant (BDN2) cultivars of pigeon pea were screened against Fusarium oxysporum f. udum [F. udum]. The inoculation of endophytic antagonists into different cultivars of
pigeon pea improved germination, plant height, branching, nodulation, root length and biomass production, and reduced wilt intensity significantly over the un-inoculated control. Among the inoculants,
Pseudomonas-2 was the most beneficial, followed by Pseudomonas-3, Bacillus-3, Pseudomonas-1, and Bacillus-1 and -2. Antagonists isolated from resistant cultivar were the most beneficial, followed
by antagonists from the moderately resistant cultivar, and antagonists isolated from the susceptible cultivar.
135
Nicot et al. (Appendix for Chapter 1)
Recep, K., S. Fikrettin, et al. (2009). "Biological control of the potato dry rot caused by Fusarium species using PGPR strains." Biological Control 50(2): 194-198.
In this study, a total of 17 Plant Growth Promoting Rhizobacteria (PGPR) strains, consisting of eight different species (Bacillus subtilis, Bacillus pumilus, Burkholderia cepacia, Pseudomonas putida,
Bacillus amyloliquefaciens, Bacillus atrophaeus, Bacillus macerans and Flavobacter balastinium), were tested for antifungal activity in in vitro (on Petri plate) and in vivo (on potato tuber) conditions
against Fusarium sambucinum, Fusarium oxysporum and Fusarium culmorum cause of dry rot disease of potato. All PGPR strains had inhibitory effects on the development of at least one or more fungal
species on Petri plates. The strongest antagonism was observed in B. cepacia strain OSU-7 with inhibition zones ranging from 35.33 to 47.37 mm. All PGPR strains were also tested on tubers of two
potato cultivars 'Agria' and 'Granola' under storage conditions. Only B. cepacia strain OSU-7 had significant effects on controlling potato dry rot caused by three different fungi species on the two potato
cultivars. There were no significant differences in rot diameters among the treatments in comparison to the negative control (with water). This is the first study showing that B. cepacia has great potential
to be used as effective biocontrol agent of Fusanium dry rot of potatoes (F. oxysporum and F culmorum) under storage conditions. (C) 2009 Elsevier Inc. All rights reserved.
Riaz, T., S. N. Khan, et al. (2009). "Effect of co-cultivation and crop rotation on corm rot disease of Gladiolus." Scientia Horticulturae 121(2): 218-222.
Field and pot experiments were conducted to evaluate the effect of co-cultivation and crop rotation on the growth and corm rot disease of gladiolus (Gladiolus grandiflorus sect. Blandus) cv. Aarti caused
by Fusarium oxysporum f.sp. gladioli (Massey) Snyd. and Hans. In the field experiment, gladiolus was co-cultivated with 10 agricultural/horticultural crops viz. Allium cepa L., Brassica campestris L.,
Capsicum annuum L., Eruca sativa Mill., Helianthus annuus L., Tagetes erectus L., Zea mays L., Vinca rosea L. and Rosa indica L., in a soil infested with F. oxysporum. All the crops except V. rosea and
R. indica reduced disease incidence. The effect of H. annuus and T. erectus was significant and more pronounced than other co-cultivated crops. In general, root and shoot dry biomass, corm fresh weight,
number of cormlets and number of flowers per spike decreased as compared to the un-inoculated monoculture gladiolus treatment (negative control) but these parameters enhanced as compared to the F.
oxysporum inoculated monoculture gladiolus treatment (positive control). In a pot experiment, all the crops of the field experiment except V. rosea and R. indica were sown in rotation with gladiolus. Pot
grown plants of different species were harvested at maturity and the soil was inoculated with F oxysporum. Gladiolus was cultivated I week after inoculation. Disease incidence was significantly
suppressed in all the treatments ranging from 29% to 53%. The highest suppression of disease incidence was recorded in T erectus (53%) followed by B. campestris (49%). The effect of preceding crops
on various vegetative parameters was similar in the pot experiment to that of the field experiment. The present study suggests that corm rot disease of gladiolus can be managed by mixed cropping of H.
annuus and T erectus or cultivation of T. erectus and B. campestris in rotation. (c) 2009 Elsevier B.V. All rights reserved.
Saidi, N., S. Kouki, et al. (2009). "Characterization and selection of Bacillus sp strains, effective biocontrol agents against Fusarium oxysporum f. sp radicis-lycopersici, the causal agent of Fusarium crown
and root rot in tomato." Annals of Microbiology 59(2): 191-198.
The antagonistic activities of 20 Bacillus isolates were tested with dual culture and greenhouse conditions against Fusarium oxysporum f. sp. radicis-lycopersici (FORL) race 0, the causal agent of
Fusarium crown and root rot of tomato. Under dual culture, 10 isolates inhibited mycelial growth > 38% and the most effective inhibited fungal growth > 50%. The 20 Bacillus isolates were tested for
production of volatiles, cyanide, antibiotics, and phosphorus solubilisation; 15 isolates produced volatiles that inhibited growth of pathogens, 9 isolates produced cyanide, 10 produced antibiotics, and five
solubilised phosphorus. Greenhouse experiments with the same 20 isolates revealed the effectiveness of 12 strains, which increased the percentage of healthy plants in the tested cultivar from 66 to 96%.
The best disease control was achieved by isolates B11, B5, B17, and B18. However, B11 and B17 were the only isolates that produced cyanide, antibiotics, solubilised phosphate and showed 44%
inhibition of fungal growth. The selected strains could be considered in plant growth promotion and biological disease control.
Shi, Y. W., K. Lou, et al. (2009). "Isolation, quantity distribution and characterization of endophytic microorganisms within sugar beet." African Journal of Biotechnology 8(5): 835-840.
The present investigation was undertaken in order to document the spectrum of endophytes colonizing healthy leaves of sugar beet cultivars in Xinjiang Province ( China) and to determine the degree of
colonization at three growth stages. From the 360 sugar beet leaf and root segments incubated, 221 bacterial isolates, 34 fungal isolates and 5 actinomycete isolates were obtained. Of all the isolates, 7
bacterial species and 6 fungal species were identified. The actinomycete isolates were characterized as Streptomyces griseofuscus and Streptomyces globisporus. There were significant differences
between microorganisms, stages of growth, and stages of microorganism interaction. The number of microorganisms isolated increased during the growth period of the sugar beet. At the same time, the
number of microorganisms affecting different parts of the sugar beet tissue was quite different. The greatest number of microorganisms was found in the secondary root emergence zone of the sugar beet
tissue. Endophytic microorganisms in sugar beet promote growth and increase the yield of the beet.
Son, S. H., Z. Khan, et al. (2009). "Plant growth-promoting rhizobacteria, Paenibacillus polymyxa and Paenibacillus lentimorbus suppress disease complex caused by root-knot nematode and fusarium wilt
fungus." Journal of Applied Microbiology 107(2): 524-532.
Paenibacillus strains against disease complex caused by Meloidogyne incognita and Fusarium oxysporum f. sp. lycopersici interactions. Methods and Results: Paenibacillus strains were collected from
rotten ginseng roots. The strains were tested under in vitro and pots for their inhibitory activities, and biocontrol potential against disease complex caused by M. incognita and F. oxysporum f. sp.
lycopersici on tomato. In in vitro experiments, among 40 tested strains of Paenibacillus spp., 11 strains showed antifungal and nematicidal activities against F. oxysporum f. sp. lycopersici and M.
136
Appendix 6
incognita, respectively. Paenibacilluspolymyxa GBR-462; GBR-508 and P. lentimorbus GBR-158 showed the strongest antifungal and nematicidal activities. These three strains used in pot experiment
reduced the symptom development of the disease complex (wilting and plant death), and increased plant growth. The control effects were estimated to be 90-98%, and also reduced root gall formation by
64-88% compared to the untreated control. Conclusion: The protective properties of selected Paenibacillus strains make them as potential tool to reduce deleterious impact of disease complex plants.
Significance and Impact of the Study: The study highlights biocontrol potential of Paenibacillus strains in management of disease complex caused by nematode-fungus interaction.
Srinivasan, K., G. Gilardi, et al. (2009). "BACTERIAL ANTAGONISTS FROM USED ROCKWOOL SOILLESS SUBSTRATES SUPPRESS FUSARIUM WILT OF TOMATO." Journal of Plant
Pathology 91(1): 147-154.
Five bacterial E,trains (FC-6B, FC-7B, FC-8B, FC-9B and FC-24B) isolated from used rockwool soilless substrates were identified using 16S ribosomal DNA (16S rDNA) sequence analysis as
belonging to the Pseudomonas genus. Seven glasshouse trials were conducted in order to evaluate the efficacy of these bacteria strains (Pseudomonas putida FC-6B, Pseudomonas sp. FC-7B,
Pseudomonas putida FC-8B, Pseudomonas sp. FC-9B and Pseudomonas sp. FC-24B) together with Achromobacter sp. AM1 and Serratia sp. DM1 obtained from suppressive sod, against Fusarium wilt
of tomato. Two commercial bioproducts, Trichoderma harzianum T22 (RootShield) and Pseudomonas chlororaphis MA 342 (Cedomon) were also evaluated. Different treatment strategies including soil
application (10(7) and 10(8) cfu ml(-1)) were adopted in different glasshouse trials (Trial I to VI) to test the efficacy of the bacterial strains against Fusarium wilt. Root dipping was used in Trial VII
(10(8) and 10(9) cfu ml(-1)). The lowest: disease incidence (3.3) was recorded with a single application of P. putida FC-6B at 10(8) cfu ml(-1). Similar results were obtained with the same bacteria when
the concentration was decreased to 10(7) cfu ml(-1) but an increasing number of applications was required. The highest plant biomass (50.3 g/plant) was recorded in the P. putida FC-8B treatment (Trial
III). In conclusion, the current study showed the potential biocontrol activity of bacterial strains FC-6B, FC-7B, FC-8B, FC-9B and FC-24B isolated from re-used rockwool soilless substrates against
Fusarium wilt disease, and the growth promoting activity of these strains on tomato plants.
Srivastava, D. K., A. K. Singh, et al. (2009). "Efficacy of bio-control agents and seed dressing fungicides against damping off of tomato." Annals of Plant Protection Sciences 17(1): 257-258.
in Unao, Madhya Pradesh, India, during 2005-06 yielded associated pathogen on PDA medium. The antagonistic activity of biological control agents against Fusarium oxysporum f.sp. lycopersici was
determined using dual culture method. All the antagonists and fungicide inhibited the mycelial growth of Fusarium, however, Trichoderma viride caused maximum inhibition of mycelial growth.
Trichoderma viride, Trichoderma harzianum, Gliocladium virens, carbendazim and thiram, which showed significant in vitro inhibition of Fusarium were tested in the field. Maximum increase in seed
germination (83.4%), seedling survival (79.0) and plant height (6.32 cm) over the control was observed when treated with Trichoderma viride followed by Trichoderma harzianum, carbendazim, thiram,
and Gliocladium virens.
Thanh, D. T., L. T. T. Tarn, et al. (2009). "Biological Control of Soilborne Diseases on Tomato, Potato and Black Pepper by Selected PGPR in the Greenhouse and Field in Vietnam." Plant Pathology Journal
25(3): 263-269.
Bacterial wilt, Fusarium wilt and Foot rot caused by Ralstonia solanacearum, Fusarium oxysporum, and Phytophthora capsici respectively, continue to be severe problems to tomato, potato and black
pepper growers in Vietnam. Three bio-products, Bacillus vallismortis EXTN-1 (EXTN-1), Bacillus sp. and Puenibacillus sp. (ESSC) and Bacillus substilis (MFMF) were examined in greenhouse
bioassay for the ability to reduce bacterial wilt, fusarium wilt and foot rot disease severity. While these bio-products significantly reduced disease severities, EXTN-1 was the most effective, providing a
mean level of disease reduction 80.0 to 90.0% against bacterial wilt, fusarium wilt and foot rot diseases under greenhouse conditions. ESSC and MFMF also significantly reduced fusarium wilt, bacterial
wilt and foot rot severity under greenhouse conditions. Bio-product, EXTN-1 with the greatest efficacy under greenhouse condition was tested for the ability to reduce bacterial wilt, fusarium wilt and
foot rot under field condition at Song Phuong and Thuong Tin locations in Ha Tay province, Vietnam. Under field condition, EXTN-1 provided a mean level of disease reduction more than 45.0%
against all three diseases compared to water treated control. Besides, EXTN-1 treatment increased the yield in tomato fruits 17.3% than water treated control plants.
Wu, H., X. Yang, et al. (2009). "Suppression of Fusarium wilt of watermelon by a bio-organic fertilizer containing combinations of antagonistic microorganisms." BioControl 54(2): 287-300.
the crop has been grown for many seasons. Its occurrence results in a severely decreased watermelon crop. The goal of this study was to assess the capability of a new product (bio-organic fertilizer) to
control the wilt in Fusarium-infested soil. Pot experiments were conducted under growth chamber and greenhouse conditions. The results showed that the fertilizer controlled the wilt disease. Compared
with control pots, the incidence rates of Fusarium wilt at 27 and 63 days following treatment of the plants with the bio-organic fertilizer at a rate of 0.5% (organic fertilizer+antagonistic microorganisms,
including 3*109 CFU g-1 respectively, in both the growth chamber and greenhouse settings. The activities of antioxidases (catalase, superoxide dismutase and peroxidase) in watermelon leaves increased
by 38.9, 150 and 250%, respectively. In the roots, stems and leaves, the activity of beta-1,3-glucanase (pathogenesis-related proteins) increased by 80, 1140 and 100% and that of chitinase increased by
240, 80, and 20%, respectively, while the contents of malondialdehyde fell by 56.8, 42.1 and 45.9%, respectively. These results indicate that this new fertilizer formula is capable of protecting
watermelon from Fusarium oxysporum f.sp. niveum. The elevated levels of defense-related enzymes are consistent with the induction and enhancement of systemic acquired resistance of plant.
137
Nicot et al. (Appendix for Chapter 1)
Wu, Q., H. Zeng, et al. (2009). "Stability of fermentation broth of actinomycete strain WZ162 resistance to Fusarium oxysporum f.sp. cubense of banana." Guangxi Agricultural Sciences 40(4): 366-369.
The fermentation broth of actinomycete strain WZ162 has strong inhibiting effect against Fusarium oxysporum f.sp. cubense of banana. Under different conditions, the stabilities of fermentation broth of
WZ162 were detected. The results showed that the fermentation broth of WZ162 had better heat stability when temperature of water bath was below 80C. The antibiotics ingredient of fermentation broth
would not be changed and can maintain the antifungal activity under conditions of sun light and ultraviolet rays. Under acid and neutrality conditions, the inhibition rate of fermentation broth against
Focr4 was 24.92%-34.73% and 11.21%-25.39%, respectively. Therefore, the stability of fermentation broth in acid was better than that of neutrality. When the fermentation broth with pH 1-12 were
treated with different time in 100C water bath, the inhibition rate was obviously lower than that of the treatments without water bath, and the stability of fermentation broth with pH 1 was the best.
Yin, X., D. Chen, et al. (2009). "An endophytic Erwinia chrysanthemi strain antagonistic against banana fusarium wilt disease." Chinese Journal of Biological Control 25(1): 60-65.
An endophytic strain E353 was obtained from the pseudostem of healthy banana plant in a field heavily infected with Fusarium oxysporum f. sp. cubense (FOC). Antagonism of the strain against FOC
was tested via dual-culture, inhibition test on conidia germination, and pot trials. Results showed that E353 effectively inhibited mycelium growth and conidia germination. Efficacy of strain E353 to
control the wilt disease was 60.67% in pot trials. Strain E353 was identified as Erwinia chrysanthemi according to its characteristics in morphology, physiology, biochemistry and 16S rDNA sequence.
Zhong, X., M. Liang, et al. (2009). "Study on the inhibition of Trichoderma sp. against Fusarium oxysporum f. sp. cubense in banana." Journal of Fruit Science 26(2): 186-189.
effective antagonist against Fusarium oxysporum f. sp. cubens, was isolated and identified as Trichoderma sp. based upon 18S rDNA gene analysis. With solid and liquid cultures, the inhibitive efficacy
to the growth of Fusarium oxysporum f. sp. cubens was primarily studied. The experimental results showed that the cells of Fusarium oxysporum f. sp. cubens were completely covered by short fiber-like
hyphace and spore stem of G2 within 7 days in the dual culture plate, and in the antagonist plate, the average rate of inhibitory by the culture solution of G2 was about 90.4%, the average rate of the
inhibitory by volatile substance reached 68.3%. After 10 days' incubation with 20% (v/v) fungal strain G2, the melt of the pathogenic mycel and spore were observed in the liquid culture containing
1.0*107 cfu . L-1 G2 can strongly inhibit the growth of Fusarium oxysporum f. sp. cubens.
Zhu, H., Y. Ma, et al. (2009). "Control effect of combining biocontrol strains against Fusarium oxysporium f. sp. niveum and Verticillium dahliae." Journal of Northwest A & F University - Natural Science
Edition 37(7): 152-156.
Objective: Five actinomycetes strains having certain inhibiting capability were screened as material to study the control effect of the actinomycetes and five combinations on watermelon Fusarium wilt
and Eggplant Verticillium wilt, and to filter the combining biocontrol strains which have better biocontrol efficacy and growth promotion. Method: The biocontrol efficacy and growth promotion of
single and combining strains were analyzed by antagonistic activity in vitro and manual inoculation in vivo. Result: Strain SC11 and SE2 had significant inhibiting effect on Fusarium oxysporium f. sp.
niveum and Verticillium dahliae in vitro. Inhibiting rate on conidia germination was also high; in greenhouse experiment, 84.93% control ratio to Fusarium oxysporium f. sp. niveum and 71. 48% to
Verticillium dahliae were found by C2; The fermentation broth of C3 had the most significant effect for every index of watermelon. The effect on reduction intensity of watermelon rootage was obvious.
For eggplant, the growth promotion was only inferior to strain SF6. Conclusion: These results suggested that the control effect and growth promotion of combining biocontrol strains are significantly
higher than individual, and combining strains express complementary biocontrol activities by collaboration. There is no correlation between the number of strains and control effect, only proper
combinations of biocontrol strains can enhance disease control effect.
138
Appendix 7. Number of references retrieved by using the CAB Abstracts database in
order to review scientific literatures on augmentative biological control in
selected crops for Chapter 2.
GRAPEVINE*
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
1644
7
10
4
7
773
320
607
1998-2008
6
6
1
3
373
190
579
APPLE
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
3971
13
18
5
10
2310
981
1145
1998-2008
10
9
3
2
817
258
1099
PEAR
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
1270
3
2
1
3
756
174
400
1998-2008
2
1
1
1
325
61
391
* Survey includes records for grapevine, grape and vineyard.
139
140
Nicot et al. (Appendix for Chapter 1)
CORN*
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
6828
19
38
18
39
4293
250
1919
1998-2008
14
18
8
17
1682
66
1805
WHEAT
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
5250
9
13
1
8
2307
157
980
1998-2008
7
6
1
3
866
66
949
CARROT
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
360
1
1
1
0
179
20
76
1998-2008
1
1
1
0
62
8
73
ONION
Key words
Biological control
Augmentative biological control
Augmentation biological control
Inoculative biological control
Inundative biological control
Insects biological control
Mites biological control
Total references dealing with
augmentative biocontrol to be examined
1973-2008
810
2
3
3
1
532
187
313
1998-2008
2
3
3
1
233
62
304
* Survey include records for corn and maize.
140
Appendix 8. Collection of data on augmentative biological control of pests in grapevine. Each table refers to a group of biocontrol agents.
8.1 Parasitoid Hymenoptera: Trichogramma spp. (Trichogrammatidae) [10 species]
References
Species of
biocontrol agent
Species of insect pest
Remund & Bigler, 1986
T. dendrolimi
Eupoecilia ambiguella
(grape berry moth)
Taxonomic
category of
pests
Lepidoptera:
Tortricidae
Country
Type of
augmentation
T. maidis
T. semblidis
Glenn & Hoffmann, 1997
T. carverae
Basso et al., 1998
T. pretiosum
T. exiguum
Basso et al., 1999
T. pretiosum
T. exiguum
T. brassicae
Garnier-Geoffroy et al.,
1999
Hommay et al., 2002
Efficacy of
biocontrol
agents*
Lab
Switzerland
Segonca & Leisse, 1989
Type of
test
Switzerland
Ahr Valley,
Germany
Victoria,
Australia
Eupoecilia ambiguella and
Lobesia botrana
Epiphyas postvittana
(light brown apple moth)
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Argyrotaenia sphaleropa
(South American tortricid
moth),
Bonagota cranaodes
(Brasilian apple leafroller)
A. sphaleropa
B. cranaodes
Lobesia botrana
Lepidoptera:
Tortricidae
Uruguay
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Uruguay
Inundative
Inundative
Field
Field
+
+
Inundative
Field
(small
blocks)
Lab
+
Field
+
Lab
-
Field
+
-
Evaluation of allelocemical
relations
+ as % parasitization.
- as % grapes attacked.
Lobesia botrana
Endopiza viteana (grape
berry moth)
Lepidoptera:
Tortricidae
Pennsylvania,
USA
Field
+
Thomson & Hoffmann,
2002
Nagargatti et al., 2003
T. carverae
Epiphyas postvittana
(light brown apple moth)
Endopiza viteana
Inundative
+
Trichogramma spp.
Victoria,
Australia
Pennsylvania,
USA
Germany
Lab
Field
Field
Zimmermann, 2004
Inundative
Field
Begum et al., 2006
T. carverae
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
+ as natural parasitism.
Inundative releases of T.
minutum in border rows is
suggested
Assessment of quality indicators
Australia
Inundative
Greenho
use/
Field
Parasitoids released in border
rows
Commercialized to be used in
home garden
Ground-cover plant species
identified to improve performance
of mass released parasitoids.
T. minutum
Lobesia botrana and
Eupoecilia ambiguella
Epiphyas postvittana
Inundative
Evaluation of biological
parameters
T. evanescens and
T. cacoeciae (two
strains)
T. minutum
Nagargatti et al., 2002
France
Evaluation of biological
parameters
Evaluation of biological
parameters
Field
Inundative
Additional information and
results
+
141
Giorgini (Appendix for Chapter 2)
El-Wakeil et al., 2008
T. evanescens
Lobesia botrana (European
grape berry moth)
Lepidoptera:
Tortricidae
Egypt
Inundative
Field
Type of
augmentation
Type of
test
+
Parasitism > 97% and reduction
percents of infestation reached
96.8%
* + means effective, - means not effective biocontrol agent.
8.2 Parasitoid Hymenoptera: Encyrtidae [4 species], Pteromalidae [1 species]
Reference
Species of
biocontrol agent
Species of insect
pest
Taxonomic category of
pests
Cuontry
Walton & Pringle, 1999
Coccidoxenoides
peregrinus
Planococcus ficus
(vine mealybug)
Hemiptera:
Pseudococcidae
South Africa
Planococcus ficus
(vine mealybug)
Hemiptera:
Pseudococcidae
South Africa
Inundative
Field
+
Mass release was at least as
effective as the chemical control
Maconellicoccus
hirsutus
Hemiptera:
Pseudococcidae
Egypt
Inundative
Field
+
Planococcus ficus
Hemiptera:
Pseudococcidae
California
Inoculative
Field
+
It is concluded that the releases of
parasitoids were suitable for
control.
Promising results. Commercial
products are not yet available.
Planococcus ficus
Hemiptera:
Pseudococcidae
Israel
Inoculative
Field
+
Promising results. Commercial
products are not yet available.
Ceratitis capitata
(Mediterranean fruit
fly)
Diptera: Tephritidae
Canada
Inundative
Field
Lab
cages
+
M. raptor constitutes a promising
biocontrol agent in vineyards.
Efficacy of
biocontrol
agents*
Additional information and
results
Walton & Pringle, 2004
Abd-Rabou, 2005
Daane et al., 2006
Daane et al., 2008
Kapongo et al., 2007
(Encyrtidae)
Coccidoxenoides
perminutus
(Encyrtidae)
Anagyrus kamali
(Encyrtidae)
Anagyrus
pseudococci
(Encyrtidae)
Anagyrus
pseudococci
(Encyrtidae)
Muscidifurax
raptor
(Pteromalidae)
Efficacy of
biocontrol
agents*
Lab
Additional information and
results
Compatibility of fungicides and
incompatibility of insecticides
with augmentative releases
* + means effective, - means not effective biocontrol agent.
8.3 Predators of mites. Acari: Phytoseidae.
References
Boller et al., 1988
Species of biocontrol
agent
Typhlodromus pyri
Species of mite pest
Panonychus ulmi,
Tetranychus urticae
Taxonomic
category of
pests
Acari:
Tetranychidae
Country
Switzerland
Type of
augmentation
Inoculative
Type of
test
Field
Inoculative release of T. pyri
along with the increase of the
internal ecological diversity
achieved by proper management
of the green cover plants will
have a strong influence on
predator densities.
142
Appendix 8
Camporese & Duso, 1996
Typhlodromus pyri,
Amblyseius andersoni,
Kampimodromus aberrans
Panonychus ulmi
Acari:
Tetranychidae
Italy
Inoculative
Field
+
Takahashi et al., 1998
Phytoseiulus persimilis
Tetranychus kanzawai
Acari:
Tetranychidae
Japan
Inundative
+
Duso & Vettorazzo, 1999
Kampimodromus
aberrans, Typhlodromus
pyri
Panonychus ulmi,
Eotetranychus carpini
Acari:
Tetranychidae
Veneto, Italy
Inoculative
Field
(grape in
green
house)
Field (A)
Field (B)
+
+
+
Calepitrimerus vitis
Acari:
Eriophyidae
Marshall & Lester, 2001
Typhlodromus pyri
Panonychus ulmi
Acari:
Tetranychidae
Ontario,
Canada
Inoculative
Field
Duso et al., 2006
Typhlodromus pyri
strain resistant to
organophosphates
Panonychus ulmi,
Eotetranychus carpini
Acari:
Tetranychidae
North-eastern
Italy
Inoculative
Field
Calomerus vitis
Acari:
Eriophyidae
* + means effective, - means not effective biocontrol agent.
Different colonization patterns on
three grape varieties (with
different pubescent leaf
undersurfaces).
The high competitiveness of K.
aberrans over the other 2
phytoseid species is a major
factor in selecting predatory
species for inoculative releases.
Release of P. persimilis onto the
grass ground cover in the spring.
No chemical control was
required.
Releases were successful and the
predators became more abundant
on the variety with pubescent leaf
under-surface.
Native A. andersoni were
displaced by T. pyri.
Two grape varieties with different
leaf hair density.
T. pyri colonization failed; K.
aberrans was more successful on
glabrous varieties. K. aberrans
displaced native P. finitimus.
T. pyri out-competed native
Amblyseius fallacies.
T. pyri is an effective biocontrol
agent and may be introduced by
transferring leaves.
15-years observations. The
predator colonized the vineyard
and competed successfully with
other species.
Role of alternative foods, leaf
morphology and selective
pesticides.
143
Giorgini (Appendix for Chapter 2)
8.4 Predators of insects. Neuroptera: Chrysopidae [3 species] and Coleoptera: Coccinellidae [2 species]
Reference
Daane et al., 1996
Species of biocontrol
agent
NEUROPTERA:
CHRYSOPIDAE
Chrysoperla carnea
(common green
lacewing)
Daane & Yokota, 1997
Chrysoperla carnea,
C. comanche,
C. rufilabris
Wunderlich & Giles,
1999
Chrysoperla rufilabris
Anagnou et al., 2003
COLEOPTERA:
COCCINELLIDAE
Nephus includens
Species of
insect pest
Taxonomic
category of pests
Country
Type of
augmentation
Type of test
Efficacy of
biocontrol
agents*
Additional information and results
Erythroneura
variabilis,
E. elegantula
(leafhoppers)
Hemiptera:
Cicadellidae
California
Inundative
Field
(caged smallplot)
-
Average leafhopper density reduction
29.5%.
Field
(uncaged
small-plot)
Field
(on-farm
trials)
-
-
Release rates reflecting commercial
recommendations.
Average reduction 15.5%.
Average reduction 9.6%
Not sufficient to lower the leafhopper
density below the economic injury
threshold.
Aspects of release strategies evaluated.
High mortality of lacewing eggs and
neonate larvae.
-
Erythroneura
variabilis,
E. elegantula
(leafhoppers)
Erythroneura
variabilis,
E. elegantula
(leafhoppers)
Hemiptera:
Cicadellidae
California
Inundative
Field
Hemiptera:
Cicadellidae
California
Inundative
Field
A mechanical technique was assessed for
releasing eggs in liquid suspensions.
Adhesion of eggs to the canopy was an
issue.
Planococcus
citri
Hemiptera:
Pseudococcidae
Greece
Field
It is suggested, for combined infestation
by L. botrana and mealybugs, the
application of B. thuringiensis and the
releases of the effective predator N.
includens.
Commonly released in vineyards, but
release rates, timing, and expected
outcomes have not been scientifically
evaluated.
It may be best used by releasing at hot
spots where the mealybug density is high.
Daane et al., 2008
Cryptolaemus
montrouzieri
Pseudococcus
maritimus,
P. longispinus
(mealybugs)
Hemiptera:
Pseudococcidae
California
Inoculative
Field
Mani, 2008
Cryptolaemus
montrouzieri
Planococcus
citri
Hemiptera:
Pseudococcidae
India
Inundative
Green
house
* + means effective, - means not effective biocontrol agent.
+
144
Appendix 8
8.5 Fungi [5 species]
Reference
Species of biocontrol
agent
Species of insect pest
Taxonomic
category of pests
Country
Type of
augmentation
Type of
test
Berner &
Schnetter, 2002
Beauveria brongniartii
(in combination with the
nematode H.
bacteriophora)
Beauveria bassiana
Melolontha melolontha
(European cockchafer)
Coleoptera:
Scarabeidae
Germany
Inundative
Field
(soil)
Frankliniella
occidentalis
(western flower thrips)
Thysanoptera:
Thripidae
Greece
Inundative
Field
Tsitsipis et al.,
2003
Efficacy of
biocontrol
agents*
+
+
Al-Jboory et al.,
2006
Lopes et al., 2002
Beauveria bassiana
grape thrips
Thysanoptera:
Thripidae
Thysanoptera:
Thripidae
Iraq
Metarhizium anisopliae
Frankliniella
occidentalis
Laengle et al.,
2004
Metarhizium anisopliae
Kirchmair et al.,
2004
Metarhizium anisopliae
Kirchmair et al.,
2005
Metarhizium anisopliae
Huber &
Kirchmair, 2007
Metarhizium anisopliae
Lab
+
Brazil
Inundative
Field
+
Daktulosphaira
vitifoliae
(grape phylloxera)
Daktulosphaira
vitifoliae
(grape phylloxera)
Daktulosphaira
vitifoliae
(grape phylloxera)
Hemiptera:
Phylloxeridae
Austria
Inundative
Field
Hemiptera:
Phylloxeridae
Austria
Inundative
Lab
+
Hemiptera:
Phylloxeridae
Germany
Inundative
Field
+
Daktulosphaira
vitifoliae
(grape phylloxera)
Hemiptera:
Phylloxeridae
Germany
Inundative
Field
-
Additional information and results
Only under optimum conditions and with
high doses control of the white grubs
could be reached.
B. bassiana in combination with mass
trapping was compared to mass trapping
or insecticides.
Less efficient in the control of insect
population if compared to some
chemicals.
Two isolates of B. bassiana showed
100% mortality after 5 days
The effect of chemicals (thiacloprid and
methiocarb) with or without M.a. was
tested. M.a. in combination with
methiocarb was the best strategy.
Non-target effects on soil fauna: no
negative effects detected.
M.a. was effective in pot experiments.
Potential role of M.a. in grape phylloxera
control.
M.a. was effective.
No target effects on soil fauna (Acari,
Collembola, Lumbricida and the
Carabidae Harpalus affinis) and fungi.
Evaluation of efficacy: more difficulties
arise in testing the efficacy of M.a. under
field conditions because of the uneven
distribution of roots and pest insects in
the soil.
145
Giorgini (Appendix for Chapter 2)
Kirchmair et al.,
2007
Metarhizium anisopliae
Daktulosphaira
vitifoliae
(grape phylloxera)
Hemiptera:
Phylloxeridae
Germany
Inundative
Field
+
MaheshkumarKatke & Balikai,
2008
Metarhizium anisopliae,
Verticillium lecanii,
Clerodendron inerme
Maconellicoccus
hirsutus
(grape mealybug)
Hemiptera:
Pseudococcidae
India
Inundative
Field
+
Taxonomic
category of
pests
Lepidoptera:
Sesiidae
Country
Type of augmentation
Type
of test
Georgia,
USA
Inundative
(soil)
Lab,
Field
Hemiptera:
Phylloxeridae
NY,
USA
3 months after application an increase of
the M.a. density in soil was observed.
Compared with untreated plots a lower
infestation was observed in the M.a.treated plots. Two years after treatment a
control effect was still observed whereas
the density of M.a. in soil decreased.
Three years after treatment no effect on
the pest was detectable and the M.a.
density had decreased to a value similar
to that in the control . A periodically
application is necessary.
* + means effective, - means not effective biocontrol agent.
8.6 Nematodes [5 species]
Reference
Species of biocontrol agent
Species of insect pest
Saunders & All,
1985
Steinernema carpocapsae
Vitacea polistiformis
(grape root borer)
English-Loeb et
al., 1999
Heterorhabditis
bacteriophora
(Oswego strain),
Steinernema glaseri
(isolate 326)
Daktulosphaira vitifolia
(grape phylloxera - root
form)
Lab
Efficacy of
biocontrol
agents*
+
+
-
Additional information and
results
Susceptibility of V.p. 1st-instar
larvae. Augmentation of nematode
populations during the critical
period of V.p. oviposition and
eclosion is suggested as a control
technique.
H. bacteriophora: reduced survival
of attached phylloxera by up to
80%.
S. glaseri had no measurable impact.
No evidence that H.b. could
successfully reproduce within the
bodies of the hosts.
Augmentative use in the field in an
release programme may be
constrained by the need to use high
densities, their dependence on moist
soils, and their inability to propagate
themselves within hosts.
146
Appendix 8
Berner &
Schnetter, 2002
Heterorhabditis
bacteriophora,
Melolontha melolontha
(European cockchafer)
Coleoptera:
Scarabeidae
Germany
Inundative
(soil)
Field
+
Williams et al.,
2002
H.bacteriophora
+ Beauveria brongniartii
(fungus)
Heterorhabditis
bacteriophora,
H. zealandica,
H. marelata, and
Steinernema carpocapsae
Only under optimum conditions and
with high doses of nematodes
control of grubs could be reached.
New variant for the application of
nematodes proposed.
Vitacea polistiformis
(grape root borer)
Lepidoptera:
Sesiidae
Ohio, USA
Inundative
Lab
+
Greenh
ouse
+
H. bacteriophora strains GPS11 and
Oswego, H. zealandica strain X1,
and H. marelata.
S. carpocapsae strain All less
effective
H. zealandica strain X1
H. bacteriophora strain GPS11
* + means effective, - means not effective biocontrol agent.
8.7 Bacillus thuringiensis
Reference
B. thuringiensis
subspecies
Species of Insect
pest
Caroli et al., 1998
subsp. aizawai
Boselli et al., 2000
Lobesia botrana
(grape berry moth)
L. botrana,
Eupoecilia
ambiguella
(grape berry moths)
L. botrana,
E. ambiguella
L. botrana
Fretay & Quenin, 2000
L. botrana
Keil & Schruft, 1998
Morando et al., 1998
Bagnoli & Lucchi,
2001
subsp. kurstaki
Boselli & Scannavini,
2001
subsp. kurstaki
subsp. aizawai
Neves & Frescata,
2001
kurstaki x aizawai
Cryptoblabes
gnidiella
(honey moth)
L. botrana
L. botrana
Taxonomic
category of
pests
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Country
Type of test
EmiliaRomagna, Italy
Field
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Lepidoptera :
Pyralidae
Piemonte, Italy
Field
EmiliaRomagna, Italy
France
Toscana, Italy
Field
Lepidoptera:
Tortricidae
EmiliaRomagna, Italy
Field
Lepidoptera:
Tortricidae
Bairrada,
Portugal
Field
Efficacy
Additional results and information
+
90-95% reduction in damage against severe pest infestations
comparable to the standard chemical products.
4 Bt products (0.2% Bactospeine FC, 0.1 % Delfin, 0.1% Dipel
ES and 0.1% Thuricide HP) were compared. The influence of
temperature on the efficacy is discussed.
+
Field
The efficacy of Bt was compared to 7 insecticides. All the
tested insecticides had a significantly good efficacy.
Bt compared to insecticides.
Field
Evaluation of new formularions.
Lab
+
+
Treatments included Agree (Bt kurstaki and aizawi),
flufenoxuron, chlorpyrifos, lufenuron, tebufenozide,
methoxyfenozide, indoxacarb and spinosad. The best control
was obtained with methoxyfenozide, indoxacarb, and spinosad.
TUREX was tested to control the L. botrana third generation.
Great interest of this Bt product regarding its efficiency and
persistence based in a correct spray moment determination.
147
Giorgini (Appendix for Chapter 2)
Anagnou et al., 2003
subsp. kurstaki
subsp. aizawai
L. botrana
Lepidoptera:
Tortricidae
Lab
+
Ifoulis & SavopoulouSoultani, 2003
L. botrana
Lepidoptera:
Tortricidae
Greece
Field
+
Roditakis, 2003
L. botrana
Lepidoptera:
Tortricidae
Greece
Field
Samoilov, 2003
Lepidoptera:
Tortricidae
Odessa, Ukraine
Field
+
Lepidoptera:
Tortricidae
Egypt
Field
+
Lepidoptera:
Tortricidae
Lepidoptera:
Arctiidae
France
Field
+
Romania
Field
+
+
Bakr, 2004
subsp. kurstaki
Sparganothis
pilleriana (grape
leafroller)
Lobesia botrana
Besnard et al., 2004
subsp. aizawai
Lobesia botrana
Hera et al., 2004
subsp. kurstaki
Hyphantria cunea
(fall webworm)
Laccone et al., 2004
subsp. kurstaki
Lobesia botrana
Lepidoptera:
Tortricidae
Calabria, Italy
Field
Mazzocchetti et al.,
2004
Lobesia botrana
Lepidoptera:
Tortricidae
Abruzzo, Italy
Field
Moiraghi et al., 2004
L. botrana
E. ambiguella
Lepidoptera:
Tortricidae
Italy
Field
-
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
France
Field
+
Veneto, Italy
Field
+
Molise and
Calabria, Italy
Field
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Trentino, Italy
Field
+
Romania
Field
+
Delbac et al., 2006
Marchesini et al., 2006
Lobesia botrana
subsp. aizawai
subsp. kurstaki
Lobesia botrana
Laccone, 2007
Lobesia botrana
Mescalchin, 2007
Lobesia botrana
Mitrea et al.,
2007
subsp. kurstaki
Lobesia botrana
Several products incorporated into an artificial diet resulted in
>90% larval mortality.
The same formulations did not significantly affect the survival
of Nephus includens.
Two formulations of Bt are significantly more effective than the
control, the dusting being more effective in most cultivars and
the spraying in a few cultivars.
Pest control strategy involves B.t. application, mating
disruption, botanical insecticides and minimal use of
insecticides
The addition of sugar as a feeding stimulant to a 50% reduced
rate of Dipel-2X resulted in higher control rates (80%)
compared to using the recommended field rates of Dipel-2X
alone or Actellic [pirimiphos-methyl].
Xen Tari commercial product.
Dipel 2x WP at 0.075% also showed good protection. The
synergenism of mixtures (50:50) of chemical and biological
insecticides was effective in controlling the pest.
Bt gave satisfactory control if applied at the onset of
ovideposition and provided the canopy was managed in such a
way as to expose the berries.
Mating disruption was compared with the traditional methods
generally used in the area: chemicals (phosphorganic
molecules) and B. thuringiensis.
In four years, trials were carried out using several commercial
products (9 insecticides and Bt). The best control was obtained
using insecticides. Control was lower for azadirachtin and less
constant for etofenprox and B. thuringiensis.
L. botrana was well-controlled by the use of B.t. or IGR’s,
without mating disruption justification
Bta compared to Btk and chemicals.
High efficacy of B.t. aizawai.
Pest control with indoxacarb, spinosad and B. thuringiensis
applied against the 2nd generation of insects parasitizing fruit is
also outlined
5-years study (2000-2005). Formulations based Bt can be used
for controlling tortricids such as L. botrana.
Chemical insecticides followed by Btk to control the second or
the third generation. Efficiency of the control treatments ranged
between 89.4% and 91.4%.
148
Appendix 8
Morandi-Filho et al.,
2007
Pryke & Samways,
2007
subsp. kurstaki
Ruiz-de-Escudero et
al., 2007
Argyrotaenia
sphaleropa (South
American tortricid
moth)
Epichoristodes
acerbella
(South African
carnation tortrix)
Lobesia botrana
Lepidoptera:
Tortricidae
Brazil
Lab
Field
+
+
Lab: reducition of the insect population by more than 90%.
Field: reduced damage between 83.3 and 94.4%. The control
efficacy of B.t was equal to that of chemicals.
Lepidoptera:
Tortricidae
South Africa
Field
+
DiPelReg commercial formulation
Lab
+
Lepidoptera:
Tortricidae
Lepidoptera:
Tortricidae
Croatia
Field
+
The potential of Bt Cry proteins to control L. botrana was
explored.
Either Cry1Ia or Cry9C could be used in combination with
Cry1Ab to control this pest, either as the active components of
Bt sprays or expressed together in transgenic plants.
Over 90% control was achieved.
Puglia, Italy
Field
+
Subic, 2007
subsp. kurstaki
Lobesia botrana
Dongiovanni et al.,
2008
subsp. kurstaki
Lobesia botrana
Lepidoptera:
Tortricidae
References
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Appendix 8
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151
Appendix 9. References on classical biological control against insect pests (cited in Chapter 3)
9.1. Biocontrol agents not precisely known
Type of work
Pest (genus level)
Prospective studies (55%)
Aproaerema
Cameraria
Cryptococcus
Diabrotica
Hypsipyla
Liriomyza
Lymanthria
Scirtothrips
Tetranychus
Retrospective studies (35%)
Chilo
Cinara
Cosmopolites
Maconellicoccus
mealybugs
Mononychellus
Phenacoccus
Other studies (10%)
Pest biology
Enarmonia
* Numbers correspond to refernces presented in section 9.4
References*
(88)
(89)
(61)
(175) (94)
(154)
(141)
(87)
(70)(72)
(45)
(166)
(128)
(56)
(103)
(47)
(191)
(97)
(82)
(88)
152
Appendix 9
9.2. Details on the use of pathogens, nematodes and predators as agents of Classical Biological Control
Pest
BCA lifestyle
BCA
References*
Aceria
Fungus
Hirsutella
(114)
Predatory mite
Neoseiulus
Adelges
Predatory Insect
Laricobius
(119)
Anticarsia
Virus
Nucleopolyhedrovirus
(197)
Aphids
Predatory Insect
Harmonia
(48) (127)
Aphis
Fungus
Neozygites
(19) (90) (91) (137)
Coptotermes
Fungus
Beauvaria & Metarhizium
(168)
Lymantria
Fungus
Microspora
(35)
Virus
Nucleopolyhedrovirus
Maconellicoccus
Predatory Insect
Cryptolaemus
(165)
Scymnus
Mononychellus
Fungus
Neozygites
(16)
Predatory mite
Neosiulus &Typhlodromalus
Oryctes
Virus
_
(51) (86)
Prostephanus
Predatory Insect
Teretrius
(51)
Review
Fungus
_
(14) (39) (42) (43)
Review
Nematode
_
(14) (55) (124) (125) (193) (194)
Sirex
Nematode
Deladenus
(81)
Solenopsis
Fungus
Vairimorpha
(73) (169) (170)
* Numbers correspond to refernces presented in section 9.4
153
Ris & Malausa (Appendix for Chapter 3)
9.3
Categorization of publications related to Insect parasitoids as ClBCA according to the type of work
Pest Biology
Pest rearing : (83, 183)
BCA Biology
BCA inventories : (30, 34, 65) (67) (88) (157) (178)
BCA systematics: (18, 52, 123) (36) (186)
BCA molecular characterization: (121, 132)
BCA rearing: (21, 58, 92, 163) (171)
BCA biology: (6, 10, 37) (74) (77) (85) (98) (100) (102) (104) (105) (158) (159) (160) (172) (190) (195)
BCA Evaluation: (12, 44, 46) (57) (80) (108) (151)
BCA Field Implications
Pre-release survey: (9, 60, 66) (122) (140) (166)
BCA introduction : see table 1
Post-release survey : (20, 22, 32) (33) (36) (50) (54) (64) (68) (76) (78) (106) (107) (113) (109) (135) (142) (145) (146) (148) (150) (162) (179)
Non-intended effects
(24, 29, 38) (58) (71) (84) (92) (65) (101) (129) (149) (155) (184) (189)
Biocontrol disruption
(17, 27, 69) (95) (130) (147) (180)
Miscellaneous
Economic valuation: (23)
Review: (75, 112, 152) (153)
Miscellaneous: (111, 115, 116) (139) (176)
“Conservation BC-like” : (173)
154
Appendix 9
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Quilici S, Duyck PF, Rousse P, Gourdon F, Simiand C, Franck A. 2005. Bactrocera zonata in La Reunion island. Phytoma
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Rauf A, Shepard BM, Johnson MW. 2000. Leafminers in vegetables, ornamental plants and weeds in Indonesia: surveys of host crops, species composition and parasitoids. International
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Rizqi A, Nia M, Abbassi M, Rochd A. 2003. Establishment of exotic parasites of citrus leaf miner, Phyllocnistis citrella, in citrus groves in Morocco. Bulletin OILB/SROP 26: 1-6
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Roltsch WJ. 2000. Establishment of silverleaf whitefly parasitoids in Imperial Valley. California Conference on Biological Control II, The Historic Mission Inn Riverside, California, USA,
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160
Appendix 9
146.
147.
148.
149.
150.
151.
152.
153.
154.
155.
156.
157.
158.
159.
160.
161.
162.
163.
164.
165.
166.
167.
168.
169.
170.
171.
172.
Roltsch WJ, Meyerdirk DE, Warkentin R, Andress ER, Carrera K. 2006. Classical biological control of the pink hibiscus mealybug, Maconellicoccus hirsutus (Green), in southern California.
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Rousse P, Harris EJ, Quilici S. 2005. Fopius arisanus, an egg-pupal parasitoid of Tephritidae. Overview. Biocontrol News and Information 26: 59N-69N
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Ris & Malausa (Appendix for Chapter 3)
173.
174.
175.
176.
177.
178.
179.
180.
181.
182.
183.
184.
185.
186.
187.
188.
189.
190.
191.
192.
193.
194.
195.
196.
197.
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162
Appendix 10. Substances included in the "EU Pesticides Database" as of April 21 2009
Substance
Cipac
& incl
2008/
127 √
Category
Inclusion
Date
Expiry
Date
Legislation
A4
A4
A4
A4
C
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/04/2005
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/03/2015
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
05/3/EC
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
Botanical
Botanical
Botanical
Botanical
Botanical
Botanical
Botanical
Botanical
Botanical
Botanical
Botanical
Extract from tea tree
Garlic extract
Gibberellic acid
Gibberellin
Laminarin
Pepper
Plant oils / Citronella oil
Plant oils / Clove oil
Plant oils / Rape seed oil
Plant oils / Spearmint oil
Sea-algae extract (formerly seaalgae extract and seaweeds)
Botanical
copied by
synthesis
Carvone
PG
C
01/08/2008
31/07/2018
2008/44/EC
Botanical
copied by
synthesis
Ethylene
PG
A4
01/09/2009
31/08/2019
2008/127
Botanical
but excluded
Pyrethrins
'32
IN
A4
01/09/2009
31/08/2019
2008/127
Chemical
Chemical
Chemical
Chemical
Chemical
2,4-D
2,4-DB
1-Methyl-cyclopropene
Acetamiprid
Acibenzolar-S-methyl
(benzothiadiazole)
'1
'83
HB, PG
HB
PG
IN
PA
A1
A1
C
C
C
01/10/2002
01/01/2004
01/04/2006
01/01/2005
01/11/2001
30/09/2012
31/12/2013
31/03/2016
31/12/2014
31/10/2011
01/103/EC
03/31/EC
06/19/EC
04/99/EC
01/87/EC
Chemical
Chemical
Aclonifen
Alpha-Cypermethrin (aka
alphamethrin)
'498
'454
HB
IN
A3
A1
01/08/2009
01/03/2005
31/07/2019
28/02/2015
2008/116
04/58/EC
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Aluminium ammonium sulfate
Aluminium phosphide
Amidosulfuron
Amitrole (aminotriazole)
Azimsulfuron
Azoxystrobin
Beflubutamid
Benalaxyl
Benfluralin
Bensulfuron
Bentazone
Benthiavalicarb
Beta-Cyfluthrin
Bifenazate
Bifenox
Bordeaux mixture
RE
IN, RO
HB
HB
HB
FU
HB
FU
HB
HB
HB
FU
IN
AC
HB
FU
A4
A3
A3
A1
C
C
C
A1
A3
A3
A1
C
A1
C
A3
A3
01/09/2009
01/09/2009
01/01/2009
01/01/2002
01/10/1999
01/07/1998
01/12/2007
01/03/2005
01/01/2009
01/11/2009
01/08/2001
01/08/2008
01/01/2004
01/12/2005
01/01/2009
01/11/2009
31/08/2019
31/08/2019
31/12/2018
31/12/2012
01/10/2019
01/07/2008
30/11/2017
28/02/2015
31/12/2018
31/10/2019
31/07/2011
31/07/2018
31/12/2013
30/11/2015
31/12/2018
30/11/2016
2008/127
2008/125
2008/40
01/21/EC
99/80/EC
98/47/EC
07/50/EC
04/58/EC
2008/108
2009/11
00/68/EC
08/44/EC
03/31/EC
05/58/EC
2008/66
SCoFCAH
voted
01.2009
Chemical
Chemical
Boscalid
Bromoxynil
FU
HB
C
A1
01/08/2008
01/03/2005
31/07/2018
28/02/2015
08/44/EC
04/58/EC
'307
'227
'515
'90
'416
'285
'502
'366
'482
'413
'87
RE
RE
PG
PG
EL
RE
HB
RE
IN, AC
PG
PG
List
(*)
163
Heilig et al (Appendix for Chapter 4)
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Calcium carbide
Calcium phosphide
Captan
Carbendazim
Carfentrazone-ethyl
Chloridazon (aka pyrazone)
Chlormequat (chloride)
Chlorothalonil
Chlorotoluron
Chlorpropham
Chlorpyrifos
Chlorpyrifos-methyl
Chlorsulfuron
Cinidon ethyl
Clodinafop
Clofentezine
Clomazone
Clopyralid
Clothianidin
Copper compounds
RE
RO
FU
FU
HB
HB
PG
FU
HB
PG, HB
IN, AC
IN, AC
HB
HB
HB
AC
HB
HB
IN
FU
A4
A3
A2
A1
C
A3
A3
A1
A1
A1
A1
A1
A3
C
A2
A3
A3
A2
C
A3
01/09/2009
01/09/2009
01/10/2007
01/01/2007
01/10/2003
01/01/2009
01/12/2009
01/03/2006
01/03/2006
01/02/2005
01/07/2006
01/07/2006
01/09/2009
01/10/2002
01/02/2007
01/01/2009
01/11/2008
01/01/2007
01/08/2006
01/11/2009
31/08/2019
31/08/2019
30/09/2017
31/12/2009
30/09/2013
31/12/2018
30/11/2019
28/02/2016
28/02/2016
31/01/2015
30/06/2016
30/06/2016
31/08/2019
30/09/2012
31/01/2017
31/12/2018
01/11/2018
30/04/2017
31/07/2016
30/11/2016
Chemical
Copper hydroxide
FU
A3
01/11/2009
30/11/2016
Chemical
Copper oxychloride
FU
A3
01/11/2009
30/11/2016
Chemical
Cuprous oxide
FU
A3
01/11/2009
30/11/2016
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Cyazofamid
Cyclanilide
Cyfluthrin
Cyhalofop-butyl
Cymoxanil
Cypermethrin
Cyprodinil
Cyromazine
Daminozide
Deltamethrin
Desmedipham
Dicamba
Dichlorobenzoic acid methylester
Dichlorprop-P
Didecyldimethylammonium
chloride
Difenacoum
Difenoconazole
Diflubenzuron
Diflufenican
Dimethachlor
Dimethenamid ? P
Dimethoate
Dimethomorph
FU
PG
IN, AC
HB
FU
IN, AC
FU
IN
PG
IN
HB
HB
FU, PGR
HB
FU
C
C
A1
C
A3
A1
A2
A3
A1
A1
A1
A3
A3
A2
A4
01/07/2003
01/11/2001
01/01/2004
01/10/2002
01/09/2009
01/03/2006
01/05/2007
01/01/2010
01/03/2006
01/11/2003
01/11/2003
01/01/2009
01/09/2009
01/06/2007
30/06/2013
31/10/2011
31/12/2013
30/09/2012
31/08/2019
28/02/2016
30/04/2017
31/08/2019
28/02/2016
31/10/2013
31/10/2013
31/12/2018
31/08/2019
31/05/2017
RO
FU
IN
HB
HB
HB
IN, AC
FU
A4
A3
A3
A3
A3
C
A2
A2
01/01/2009
01/01/2009
01/01/2009
01/01/2010
01/01/2004
01/10/2007
01/10/2007
31/12/2018
31/12/2018
31/12/2018
31/08/2019
31/12/2013
30/09/2017
30/09/2017
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
'505
'40
'263
'111
'143
'288
'217
'43
'221
'486
'391
'418
'509
'455
'385
'419
'332
'511
'420
'330
'333
'477
'85
'476
'514
'687
'339
'462
'59
'483
164
2008/127
2008/125
07/5/EC
06/135/EC
03/68/EC
2008/41
05/53/EC
05/53/EC
04/20/EC
05/72/EC
05/72/EC
02/64/EC
06/39/EC
2008/69
2007/76
06/64/EC
06/41/EC
SCoFCAH
voted
01.2009
SCoFCAH
voted
01.2009
SCoFCAH
voted
01.2009
SCoFCAH
voted
01.2009
03/23/EC
01/87/EC
03/31/EC
02/64/EC
2008/125
05/53/EC
06/64/EC
05/53/EC
03/5/EC
04/58/EC
2008/69
2008/125
06/74/EC
2008/69
2008/69
2008/66
03/84/EC
07/25/EC
07/25/EC
Appendix 10
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Dimoxystrobin
Dinocap
Diquat (dibromide)
Diuron
Dodemorph
Epoxiconazole
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Esfenvalerate
Ethephon
Ethofumesate
Ethoprophos
Ethoxysulfuron
Etofenprox
Etoxazole
Famoxadone
Fenamidone
Fenamiphos (aka phenamiphos)
Fenhexamid
'481
'373
'233
'218
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Fenoxaprop-P
Fenpropidin
Fenpropimorph
Fenpyroximate
Fipronil
Flazasulfuron
Florasulam
Fluazinam
Fludioxonil
Flufenacet (formerly fluthiamide)
Flumioxazin
Fluoxastrobin
Flupyrsulfuron methyl
'484
'520
'427
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Fluroxypyr
Flurtamone
Flusilazole
Flutolanil
Folpet
Foramsulfuron
'431
Chemical
Forchlorfenuron
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Formetanate
Fosetyl
Fosthiazate
Fuberidazole
Glufosinate
Glyphosate (incl trimesium aka
sulfosate)
Imazalil (aka enilconazole)
Imazamox
Imazaquin
Imazosulfuron
Imidacloprid
Indoxacarb
Iodosulfuron-methyl-sodium
Ioxynil
Iprodione
Iprovalicarb
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
'98
'55
'100
'300
'609
'471
'581
'521
'522
'435
'524
'75
'384
'525
'437
'284
'335
'699
'86
'278
FU
FU, AC
HB
HB
FU
FU
C
A1
A1
A2
A3
A3
01/10/2006
01/01/2007
01/01/2002
01/10/2008
01/09/2009
01/01/2009
30/09/2016
31/12/2009
31/12/2011
30/09/2018
31/08/2019
31/12/2018
06/75/EC
06/136/EC
01/21/EC
08/91/EC
2008/125
2008/107
IN
PG
HB
NE, IN
HB
IN
IN
FU
FU
NE
FU
A1
A2
A1
A2
C
A3
C
C
C
A2
C
01/08/2001
01/08/2007
01/03/2003
01/10/2007
01/07/2003
01/01/2010
01/06/2005
01/10/2002
01/10/2003
01/08/2007
01/06/2001
31/07/2011
31/07/2017
28/02/2013
30/09/2017
30/06/2013
31/12/2019
31/05/2015
30/09/2012
30/09/2013
31/07/2017
31/05/2011
00/67/EC
06/85/EC
02/37/EC
07/52/EC
03/23/EC
HB
FU
FU
AC
IN
HB
HB
FU
FU
HB
HB
FU
HB
A3
A3
A3
A3
A2
C
C
A3
A3
C
C
C
C
01/01/2009
01/01/2009
01/01/2009
01/01/2009
01/10/2007
01/06/2004
01/10/2002
01/01/2009
01/11/2008
01/01/2004
01/01/2003
01/08/2008
01/07/2001
31/12/2018
31/12/2018
31/12/2018
31/12/2018
30/09/2017
31/05/2014
30/09/2012
31/12/2018
01/11/2018
31/12/2013
31/12/2012
31/07/2018
30/06/2011
2008/66
2008/66
2008/107
2008/107
07/52/EC
04/30/EC
02/64/EC
2008/108
2007/76
03/84/EC
02/81/EC
08/44/EC
01/49/EC
HB
HB
FU
FU
FU
HB
A1
C
A1
A3
A2
C
01/12/2000
01/01/2004
01/01/2007
01/01/2009
01/10/2007
01/07/2003
30/11/2010
31/12/2013
30/06/2008
31/12/2018
30/09/2017
30/06/2013
00/10/EC
03/84/EC
06/133/EC
2008/108
07/5/EC
03/23/EC
PG
C
01/04/2006
31/03/2016
06/10/EC
IN, AC
FU
NE
FU
HB
HB
A2
A2
C
A3
A2
A1
01/10/2007
01/05/2007
01/01/2004
01/01/2009
01/10/2007
01/07/2002
30/09/2017
30/04/2017
31/12/2013
31/12/2018
30/09/2017
30/06/2012
07/5/EC
06/64/EC
03/84/EC
2008/108
07/25/EC
01/99/EC
FU
HB
PG
HB
IN
IN
HB
HB
FU
FU
A1
C
A3
C
A3
C
C
A1
A1
C
01/01/1999
01/07/2003
01/01/2009
01/04/2005
01/08/2009
01/04/2006
01/01/2004
01/03/2005
01/01/2004
01/07/2002
31/12/2008
30/06/2013
31/12/2018
31/03/2015
31/07/2019
31/03/2016
31/12/2013
28/02/2015
31/12/2013
30/06/2011
97/73/EC
03/23/EC
2008/69
05/3/EC
2008/116
06/10/EC
03/84/EC
04/58/EC
03/31/EC
02/48/EC
165
05/34/EC
02/64/EC
03/68/EC
06/85/EC
01/28/EC
Heilig et al (Appendix for Chapter 4)
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Iron sulphate
Isoproturon
Isoxaflutole
Kresoxim-methyl
lambda-Cyhalothrin
Lenacil
Linuron
Lufenuron
Magnesium phosphide
Maleic hydrazide
Mancozeb
Maneb
MCPA
MCPB
Mecoprop
Mecoprop-P
Mepanipyrim
Mepiquat
Mesosulfuron
Mesotrione
Metalaxyl-M
Metamitron
Metazachlor
Chemical
Chemical
Metconazole
Methiocarb (aka
mercaptodimethur)
Methoxyfenozide
Metiram
Metrafenone
Metribuzin
Metsulfuron
Molinate
Nicosulfuron
Oxadiargyl
Oxadiazon
Oxamyl
Oxasulfuron
Penconazole
Pendimethalin
Pethoxamid
Phenmedipham
Phosmet
Picloram
Picolinafen
Picoxystrobin
Pirimicarb
Pirimiphos-methyl
Prohexadione-calcium
Propamocarb
Propaquizafop
Propiconazole
Propineb
Propoxycarbazone
Propyzamide
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
A4
A1
C
C
A1
A3
A1
A3
A3
A1
A1
A1
A1
A1
A1
A1
C
A3
C
C
C
A3
A3
01/09/2009
01/01/2003
01/01/2003
01/02/1999
01/01/2002
01/01/2009
01/01/2004
01/01/2010
01/09/2009
01/01/2004
01/07/2006
01/07/2006
01/05/2006
01/05/2006
01/06/2004
01/06/2004
01/10/2004
01/01/2009
01/04/2004
01/10/2003
01/10/2002
01/09/2009
01/08/2009
31/08/2019
31/12/2012
31/12/2012
31/01/2009
31/12/2011
31/12/2018
31/12/2013
31/12/2019
31/08/2019
31/12/2013
30/06/2016
30/06/2016
30/04/2016
30/04/2016
31/05/2014
31/05/2014
30/09/2014
31/12/2018
31/03/2014
30/09/2013
30/09/2012
31/08/2019
31/07/2019
2008/127
02/18/EC
03/68/EC
99/01/EC
00/80/EC
2008/69
03/31/EC
'381
'411
HB
HB
HB
FU
IN
HB
HB
IN
IN, RO
PG
FU
FU
HB
HB
HB
HB
FU
PG
HB
HB
FU
HB
HB
'165
FU
IN, MO, RE
A2
A2
01/06/2007
01/10/2007
31/05/2017
30/09/2017
06/74/EC
07/5/EC
IN
FU
FU
HB
HB
HB
HB
HB
HB
IN, NE
HB
FU
HB
HB
HB
IN
HB
HB
FU
IN
IN
PG
FU
HB
FU
FU
HB
HB
C
A1
C
A2
A1
A1
A3
C
A3
A2
C
A3
A1
C
A1
A2
A3
C
C
A2
A2
C
A2
A3
A1
A1
C
A1
01/04/2005
01/07/2006
01/02/2007
01/10/2007
01/07/2001
01/08/2004
01/01/2009
01/07/2003
01/01/2009
01/08/2006
01/07/2003
01/01/2010
01/01/2004
01/08/2006
01/03/2005
01/10/2007
01/01/2009
01/10/2002
01/01/2004
01/02/2007
01/10/2007
01/10/2000
01/10/2007
01/12/2009
01/06/2004
01/04/2004
01/04/2004
01/04/2004
31/03/2015
30/06/2016
31/01/2017
30/09/2017
30/06/2011
31/07/2014
31/12/2018
30/06/2013
31/12/2018
31/07/2016
30/06/2013
31/08/2019
31/12/2013
31/07/2016
28/02/2015
30/09/2017
31/12/2018
30/09/2012
31/12/2013
31/01/2017
30/09/2017
01/10/2010
30/09/2017
30/11/2019
31/05/2014
30/03/2014
31/03/2014
30/03/2014
05/3/EC
05/72/EC
07/6/EC
07/25/EC
00/49/EC
03/81/EC
2008/40
03/23/EC
2008/69
06/16/EC
03/23/EC
'336
'463
'163
'76
'228
'310
'34
'61
'2
'50
'51
'475
'440
'478
'283
'441
'235
'709
'213
'342
'446
'357
'77
'318
'174
'231
'239
'399
'408
'177
'315
166
2008/125
03/31/EC
05/72/EC
05/72/EC
05/57/EC
05/57/EC
03/70/EC
03/70/EC
04/62/EC
2008/108
03/119/EC
03/68/EC
02/64/EC
2008/125
2008/116
03/31/EC
06/41/EC
04/58/EC
07/25/EC
2008/69
02/64/EC
03/84/EC
06/39/EC
07/52/EC
00/50/EC
07/25/EC
03/70/EC
03/39/EC
03/119/EC
03/39/EC
Appendix 10
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Prosulfocarb
Prosulfuron
Prothioconazole
Pymetrozine
Pyraclostrobin
Pyraflufen-ethyl
Pyridate
Pyrimethanil
Pyriproxyfen
Quinoclamine
Quinoxyfen
Quizalofop-P
'539
HB
HB
FU
IN
FU, PG
HB
HB
FU
IN
HB, AL
FU
HB
A3
C
C
C
C
C
A1
A2
A3
A3
C
A3
01/01/2009
01/07/2002
01/08/2008
01/11/2001
01/06/2004
01/11/2001
01/01/2002
01/06/2007
01/01/2009
01/01/2009
01/09/2004
01/12/2009
31/12/2018
30/06/2011
31/07/2018
31/10/2011
31/05/2014
31/10/2011
31/12/2011
31/05/2017
31/12/2018
31/12/2018
31/08/2014
30/11/2019
Chemical
Chemical
Chemical
Chemical
Quizalofop-P-ethyl
Quizalofop-P-tefuryl
Rimsulfuron (aka renriduron)
Silthiofam
'641
'641
HB
HB
HB
FU
A3
A3
A2
C
01/12/2009
01/12/2009
01/02/2007
01/01/2004
30/11/2019
30/11/2019
31/01/2017
31/12/2013
06/39/EC
03/84/EC
Chemical
Chemical
chemical
S-Metholachlor
Sodium 5-nitroguaiacolate
Sodium hypochlorite
HB
PG
BA
C
A3
A4
01/04/2005
01/11/2009
01/09/2009
31/03/2015
31/10/2019
31/08/2019
05/3/EC
2009/11
2008/127
Chemical
Sodium o-nitrophenolate
PG
A3
01/11/2009
31/10/2019
2009/11
Chemical
Chemical
Chemical
Chemical
Chemical
Sodium p-nitrophenolate
Spiroxamine
Sulcotrione
Sulfosulfuron
Sulphur
A3
C
A3
C
A4
01/11/2009
01/09/1999
01/09/2009
01/07/2002
31/10/2019
01/09/2009
31/08/2019
30/06/2011
'0018
PG
FU
HB
HB
FU, AC, RE
Chemical
Tebuconazole
'494
FU
A3
01/09/2009
31/08/2019
2009/11
99/73/EC
2008/125
02/48/EC
SCoFCAH
voted
03.2009
2008/125
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Chemical
Tebufenpyrad
Teflubenzuron
Tepraloxydim
Thiabendazole
Thiacloprid
Thiamethoxam
Thifensulfuron-methyl
Thiophanate-methyl
Thiram
Tolclofos-methyl
Tolylfluanid
Tralkoxydim
Triadimenol
Tri-allate
Triasulfuron
Tribasic copper sulfate
Tribenuron (aka metometuron)
Triclopyr
Trifloxystrobin
Triflusulfuron
Trinexapac (aka cimetacarb ethyl)
Triticonazole
Tritosulfuron
Warfarin (aka coumaphene)
AC
IN
HB
FU
IN
IN
HB
FU
FU
FU
FU, AC
HB
FU
HB
HB
FU
HB
HB
FU
HB
PG
FU
HB
RO
A3
A3
C
A1
C
C
A1
A1
A1
A2
A2
A3
A3
A3
A1
A3
A2
A2
C
A3
A2
A2
C
A1
01/11/2009
01/12/2009
01/06/2005
01/01/2002
01/01/2005
01/02/2007
01/07/2002
01/03/2006
01/08/2004
01/02/2007
01/10/2006
01/01/2009
01/09/2009
01/01/2010
01/08/2001
31/10/2019
30/11/2019
31/05/2015
31/12/2011
31/12/2014
31/01/2017
30/06/2012
28/02/2016
31/07/2014
31/01/2017
30/09/2016
31/12/2018
31/08/2019
31/12/2019
31/07/2011
2009/11
01/03/2006
01/06/2007
01/10/2003
01/01/2010
01/05/2007
01/02/2007
01/12/2008
01/10/2006
28/02/2016
31/05/2017
30/09/2013
31/12/2019
30/04/2017
31/01/2017
30/11/2018
30/09/2013
05/54/EC
06/74/EC
03/68/EC
'447
'715
'648
'641
'450
'323
'452
'262
'24
'479
'275
'544
'398
'97
'480
'546
'376
'652
'70
167
2007/76
02/48/EC
08/44/EC
01/87/EC
04/30/EC
01/87/EC
01/21/EC
06/74/EC
2008/69
2008/66
04/60/EC
SCoFCAH
voted
01.2009
05/34/EC
01/21/EC
04/99/EC
07/6/EC
01/99/EC
05/53/EC
03/81/EC
06/39/EC
06/06/EC
2008/107
2008/125
00/66/EC
06/64/EC
06/39/EC
08/70/EC
06/05/EC
Heilig et al (Appendix for Chapter 4)
Chemical
Chemical
Chemical
Chemical
repellent
zeta-Cypermethrin
Ziram
Zoxamide
Denathonium benzoate
A3
A1
C
A4
01/12/2009
01/08/2004
01/04/2004
01/09/2009
30/11/2019
31/07/2014
31/03/2014
31/08/2019
03/81/EC
03/119/EC
2008/127
Chemical
repellent
Repellents by smell/ Tall oil crude
(CAS 8002-26-4)
A4
01/09/2009
31/08/2019
2008/127
Chemical
repellent
Repellents by smell/Tall oil pitch
(CAS 8016-81-7)
A4
01/09/2009
31/08/2019
2008/127
Microbial
Ampelomyces quisqualis strain
AQ10
Bacillus subtilis str. QST 713
Bacillus thuringiensis subsp.
aizawai (ABTS-1857 and GC-91)
FU
C
01/04/2005
31/03/2015
05/2/EC
BA, FU
[IN]
C
A4
01/02/2007
01/01/2009
31/01/2017
31/12/2018
07/6/EC
2008/113
Microbial
Bacillus thuringiensis subsp.
israelensis (AM65-52)
[IN]
A4
01/01/2009
31/12/2018
2008/113
Microbial
Bacillus thuringiensis subsp.
kurstaki (ABTS 351, PB 54, SA
11, SA12 and EG 2348)
Bacillus thuringiensis subsp.
tenebrionis (NB 176)
[IN]
A4
01/01/2009
31/12/2018
2008/113
[IN]
A4
01/01/2009
31/12/2018
2008/113
Microbial
Beauveria bassiana (ATCC 74040
and GHA)
IN
A4
01/01/2009
31/12/2018
2008/113
Microbial
Microbial
Coniothyrium minitans
Cydia pomonella granulosis virus
(CpGV)
FU
IN
C
A4
01/01/2004
01/01/2009
31/12/2013
31/12/2018
03/79/EC
2008/113
Microbial
Gliocladium catenulatum strain
J1446
Lecanicillimum muscarium (Ve6)
(former Verticillium lecanii)
FU
C
01/04/2005
31/03/2015
05/2/EC
IN
A4
01/01/2009
31/12/2018
2008/113
Microbial
Metarhizium anisopliae
(BIPESCO 5F/52)
IN
A4
01/01/2009
31/12/2018
2008/113
Microbial
Paecilomyces fumosoroseus
Apopka strain 97
FU
C
01/07/2001
30/06/2011
01/47/EC
Microbial
Microbial
Paecilomyces lilacinus
Phlebiopsis gigantea (several
strains)
Pseudomonas chlororaphis
strain MA342
FU
FU
C
A4
01/08/2008
01/01/2009
31/07/2018
31/12/2018
2008/44/EC
2008/113
FU
C
01/10/2004
30/09/2014
04/71/EC
Microbial
Microbial
Pythium oligandrum (M1)
Spodoptera exigua nuclear
polyhedrosis virus
FU
FU
A4
C
01/01/2009
01/12/2007
31/12/2018
30/11/2017
2008/113
07/50/EC
Microbial
Streptomyces K61 (K61) (formerly
Streptomyces griseoviridis)
FU
A4
01/01/2009
31/12/2018
2008/113
Microbial
Trichoderma aspellerum (ICC012)
(T11) (TV1) (formerly T.
harzianum)
Trichoderma atroviride (IMI
206040) (T 11) (formerly
Trichoderma harzianum)
Trichoderma gamsii (formerly T.
viride) (ICC080)
FU
A4
01/01/2009
31/12/2018
2008/113
FU
A4
01/01/2009
31/12/2018
2008/113
FU
A4
01/01/2009
31/12/2018
2008/113
Trichoderma harzianum Rifai (T22) (ITEM 908)
Trichoderma polysporum (IMI
206039)
Verticillium albo-atrum
(WCS850) (formerly V. dahliae)
FU
A4
01/01/2009
31/12/2018
2008/113
FU
A4
01/01/2009
31/12/2018
2008/113
FU
A4
01/01/2009
31/12/2018
2008/113
Microbial
Microbial
Microbial
Microbial
Microbial
Microbial
Microbial
Microbial
Microbial
Microbial
'31
IN
FU, RE
FU
RE
168
Appendix 10
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
Natural other
by synthesis
Abamectin (aka avermectin)
Acetic acid
Aluminium silicate (aka kaolin)
Blood meal
Carbon dioxide
Fat distilation residues
Ferric phosphate
Kieselguhr (diatomaceous earth)
Milbemectin
Quartz sand
Spinosad
Benzoic acid
Natural other
by synthesis
'495
AC, IN
HB
RE
RE
IN, RO
RE
MO
IN
IN, AC
RE
IN
BA, FU, OT
A3
A4
A4
A4
A4
A4
C
A4
C
A4
C
C
01/01/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/11/2001
01/09/2009
01/12/2005
01/09/2009
01/02/2007
01/06/2004
31/12/2018
31/08/2018
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/10/2011
31/08/2019
30/11/2015
31/08/2019
31/01/2017
31/05/2014
2008/107
2008/127
2008/127
2008/127
2008/127
2008/127
01/87/EC
2008/127
05/58/EC
2008/127
07/6/EC
04/30/EC
Potassium hydrogen carbonate
FU
A4
01/09/2009
31/08/2019
2008/127
Natural other
by synthesis
Urea
IN
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Capric acid (CAS 334-48-5)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Caprylic acid (CAS 124-07-2)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Fatty acids C7 to C20
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Fatty acids C7-C18 and C18
unsaturated potassium salts (CAS
67701-09-1)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Fatty acids C8-C10 methyl esters
(CAS 85566-26-3)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Lauric acid (CAS 143-07-7)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Methyl decanoate (CAS 110-42-9)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Methyl octaonate (CAS 111-11-5)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Oleic acid (CAS 112-80-1)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
fatty acid
Pelargonic acid (CAS 112-05-0)
IN, AC, HB,
PG
A4
01/09/2009
31/08/2019
2008/127
Natural other
repellent
Calcium carbonate
RE
A4
01/09/2009
31/08/2019
2008/127
Natural other
repellent
Limestone
RE
A4
01/09/2009
31/08/2019
2008/127
Natural other
Repellent
Methyl nonyl ketone
RE
A4
01/09/2009
31/08/2019
2008/127
Natural other
repellent
Sodium aluminium silicate
RE
A4
01/09/2009
31/08/2019
2008/127
Natural other
repellent
Repellents by smell/Fish oil
RE
A4
01/09/2009
31/08/2019
2008/127
Natural other
repellent
Repellents by smell/Sheep fat
RE
A4
01/09/2009
31/08/2019
2008/127
√
169
Heilig et al (Appendix for Chapter 4)
Semio
Semio
(Z)-13-Hexadecen-11yn-1-yl
acetate
(Z,Z,Z,Z)-7,13,16,19Docosatetraen-1-yl isobutyrate
2008/127
√
AT
A4
01/09/2009
31/08/2019
√
√
AT
AT
A4
A4
01/09/2009
01/01/2009
31/08/2019
31/12/2018
√
√
√
√
IN
AT
AT
AT
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
Semio
Semio
Ammonium acetate
Hydrolysed proteins
Semio
Semio
Semio
Putrescine (1,4-Diaminobutane)
Trimethylamine hydrochloride
Straight Chain Lepidoptera
Pheromones
Semio/SCLP
(2E, 13Z)-Octadecadien-1-yl
acetate
(7E, 9E)-Dodecadien 1-yl acetate
√
AT
A4
01/09/2009
31/08/2019
2008/127
√
AT
A4
01/09/2009
31/08/2019
2008/127
(7E, 9Z)-Dodecadien 1-yl acetate
(7Z, 11E)-Hexadecadien-1-yl
acetate
(7Z, 11Z)-Hexadecdien-1-yl
acetate
(9Z, 12E)-Tetradecadien-1-yl
acetate
(E)-11-Tetradecen-1-yl acetate
(E)-5-Decen-1-ol
(E)-5-Decen-1-yl-acetate
(E)-8-Dodecen-1-yl acetate
(E,E)-8,10-Dodecadien-1-ol
(E/Z)-8-Dodecen-1-yl acetate
(Z)-11-Hexadecen-1-ol
(Z)-11-Hexadecen-1-yl acetate
(Z)-11-Hexadecenal
(Z)-11-Tetradecen-1-yl acetate
(Z)-13-Octadecenal
(Z)-7-Tetradecenal
(Z)-8-Dodecen-1-ol
(Z)-8-Dodecen-1-yl acetate
(Z)-9-Dodecen-1-yl acetate
√√
√√
AT
AT
A4
A4
01/09/2009
01/09/2009
31/08/2019
31/08/2019
2008/127
2008/127
√
AT
A4
01/09/2009
31/08/2019
2008/127
√
AT
A4
01/09/2009
31/08/2019
2008/127
√
√√
√√
√√
√
√√
√
√√
√√√
√
√√
√
√√
√√√
422 √
√
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
AT
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
A4
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
01/09/2009
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
31/08/2019
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
2008/127
√√
√
√√
√
334
AT
AT
AT
AT
A4
A4
A4
A4
01/09/2009 31/08/2019 2008/127
01/09/2009 31/08/2019 2008/127
01/09/2009 31/08/2019 2008/127
01/09/2009 31/08/2019 2008/127
A: Existing active substances divided into
four lists for phased evaluations
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
Semio/SCLP
(Z)-9-Hexadecenal
(Z)-9-Tetradecen-1-yl acetate
Dodecyl acetate
Tetradecan-1-ol
Official Total Included:
C: New active substances
170
2008/127
2008/127
2008/127
2008/127
2008/127
Appendix 11. Invertebrate beneficials available as biological control agents against
invertebrate pests in five European countries.
11.1.
Invertebrate biocontrol agents used in France
Beneficial
Adalia bipunctata
Taxonomy
coleoptera
Target
aphids on leaves
Adalia bipunctata
coleoptera
aphids on leaves
Delphastus pusillus
coleoptera
whiteflies
Harmonia axyridis
coleoptera
aphids on leaves
Aphidoletes aphidimyza
diptera
aphids on leaves
Feltiella acarisuga
diptera
Tetranychus urticae
Anthocoris nemoralis
heteroptera
Macrolophus
caliginosus
heteroptera
Anagrus atomus
hymenoptera
psylla
Aleurodina (whiteflies),
secondarily against
Tetranychus & aphids
(Macrosiphum euphorbiae,
Aphis gossypii)
Tomato Leaf-hopper
(Hauptidia maroccana)
Aphelinus abdominalis
hymenoptera
aphids: M. euphorbiae
Aphidius colemani
hymenoptera
Aphidius ervi
hymenoptera
Diaeretiella rapae
hymenoptera
Dacnusa sibirica
hymenoptera
Diglyphus isaea
hymenoptera
Encarsia formosa
hymenoptera
Eretmocerus eremicus
(syn. Californicus)
hymenoptera
Eretmocerus mundus
hymenoptera
Orius insidiosus
hymenoptera
Orius laevigatus
hymenoptera
thrips, partial: Tetranychus
Orius majusculus
hymenoptera
thrips, partial: Tetranychus
aphids:
A. gossypii, Myzus persicae
(green peach aphid)
aphids: Aulacorthum solani, M.
euphorbiae, M. persicae
aphids : Brevicoryne brassicae
Agromyzidae (leaf-miner
flies)
Agromyzidae (leaf-miner
flies)
Aleurodina (whiteflies)
Aleurodina (whiteflies):
Bemisia tabaci,
Trialeurodes vaporariorum
Aleurodina (whiteflies):
B. tabaci,
T. vaporariorum
thrips:
Frankliniella occidentalis,
Thrips tabaci
171
Crop
orchards: all
vegetable greenhouse: all
crops
vegetables greenhouse
and covered
Vegetables , orchards
vegetable greenhouse:
tomato,
cucumber, egg plant,
sweet pepper
vegetable greenhouse: all
crops
orchard: pear
vegetable greenhouse: all
crops
vegetables
vegetable greenhouse: all,
tomato,
egg plant, sweet pepper
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
Cabbage, oil-seed rape
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops, orchards
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
Heilig et al (Appendix for Chapter 4)
Trichogramma brassicae
Bezdenko
Trichogramma
evanescens
Amblyseius andersoni
hymenoptera
Amblyseius andersoni
mite
Amblyseius californicus
mite
Ostrinia nubilalis
(European corn borer)
Noctuidae(Owlet moths),
Pyralidae
N. rubi, P. ulmi, T.urticae
Aculops lycopersici,
Tetranychus
Tetranychus, Panonychus
Amblyseius cucumeris
mite
Tetranychus, thrips
Amblyseius degenerans
mite
thrips
Amblyseius swirskii
mite
Hypoaspis aculeifer
mite
thrips, whiteflies
Sciaridae (fungus gnats), bulb
mite (Rhyzogliphus robini)
Hypoaspis miles
mite
Sciaridae (fungus gnats), thrips
Phytoseiulus persimilis
mite
Heterorhabditis
bacteriophora,
nematode
Heterorhabditis megidis
nematode
Tetranychus urticae
Otiorhynchus salicicola,
orchards: crops & nursery
Otiorhynchus sulcatus (vine
weevil), Phyllopertha horticola
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
Vegetables, flowers
weevil)
Phasmarhabditis
hermaphrodita
Steinernema
carpocapsae
nematode
Limacidae (Slugs)
vegetable: general
nematode
Codling moth
pome fruit
Steinernema kraussei
nematode
Steinernema
carpocapsae
nematode
Steinernema feltiae
nematode
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Noctuids,
Gryllotalpa gryllotalpa
(European mole cricket),
Tipula paludosa (March crane
fly )
codling moth, Cydia molesta
Steinernema feltiae
nematode
Sciaridae (fungus gnats)
Chrysoperla carnea
nevroptera
aphids on leaves
Chrysoperla lucasina
nevroptera
Micromus angulatus
Franklinothrips
vespiformis
nevroptera
aphids, thrips, scales,
whiteflies, acarids eggs, leak
moth
scales, aphids
thysanoptera
thrips
hymenoptera
mite
172
maize
vegetable greenhouse: all
crops
orchards: all
Vegetables
vegetables
vegetable covered:
tomato, cucumber,
sweet pepper, all crops
(thrips)
vegetable greenhouse: egg
plant, sweet pepper
vegetables
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetables
vegetable: general
vegetable: general
pome fruit
vegetable: general young
plants
vegetables and ornements
covered
vegetables and ornements
covered
vegetables
vegetable greenhouse: all
crops
Appendix 11
11.2.
Invertebrate biocontrol agents used in Germany
Beneficial
Pest
Entomopathogenic nematodes
Heterorhabditis bacteriophora Poinar
Heterorhabditis megidis Poinar
Steinernema carpocapsae Weiser
Steinernema feltiae Filipjev
Steinernema kraussei Steiner
Gastropod pathogenic nematodes
Phasmarhabditis hermaphrodita A. Schneider
Predatory mites
Amblyseius andersoni Chant
Amblyseius barkeri Hughes
Amblyseius californicus McGregor
Amblyseius cucumeris Oudemans
Amblyseius degenerans Berlese
Amblyseius swirskii Athias-Henriot
Cheyletus eruditus Schrank
Hypoaspis aculeifer Canestrini
Hypoaspis milesBerlese
Phytoseiulus persimilis Athias-Henriot
Typhlodromus pyri Scheuten
Predatory thrips (Thysanoptera)
Franklinothrips vespiformis Crawford
Parasitic wasps (Hymenoptera)
Anagrus atomus Linnaeus
Anagyrus fusciventris Girault
Anisopteromalus calandrae Howard
Aphelinus abdominalis Dalman
Aphelinus mali Haldeman
Aphidius colemani Viereck
Aphidius ervi Haliday
Aphidius matricariae Haliday
Aprostocetus hagenowii Ratzeburg
Cephalonomia tarsalis Ashmead
Coccidoxenoides perminutus Girault
Coccophagus licymnia Walker
Coccophagus rusti Compere
Larvae of vine weevil (Otiorynchus sulcatus), caterpillars
of ghost moths (genus: Hepialus), larvae of garden
chaffer (Phyllopertha horticola) and other insect larvae
feeding on roots
Larvae of vine weevil (Otiorynchus sulcatus) and other
insect larvae feeding on roots
Larvae of vine weevil (Otiorynchus sulcatus) and other
insect larvae feeding on roots, mole cricket
Larvae of fungus gnats (Diptera: Sciaridae) and March
flies (Diptera: Bibionidae)
Insect larvae feeding on roots, e.g. vine weevil
(Otiorynchus sulcatus)
Slugs (Deroceras spp, Agriolimax spp and others)
Spider mites (Tetranychus spp, Panonychus spp), gall
mites (Eriophyidae) u.a.
Thrips (Frankliniella occidentalis and others)
Spider mites
Thrips (Frankliniella occidentalis and others)
Thrips
White flies (e.g. Bemisia tabaci),
spider mites (Tetranychus spp.) and thrips
Stored product mites, booklice (Psocoptera)
Thrips
Thrips
Spider mites (Tetranychus spp)
Spider mites
Thrips (in particular Echinothrips americanus,
Parthenothrips dracaenae, Frankliniella occidentalis)
Cicadidae eggs
Wooly aphids (Eriosomatidae) and mealy bugs
(Pseudococcididae)
Drugstore (Stegobium paniceum), Tobacco (Lasioderma
serricorne)
Aphids (Macrosiphum euphorbiae, Aulacorthum solani)
Wooly aphid (Eriosoma lanigerum)
Aphids (Aphis gossypii, Myzus persicae, M. nicotianae)
Aphids (Macrosiphum euphorbiae)
Aphids (Myzus persicae)
Cockroaches (Blatta orientalis, Periplaneta spp)
Saw-toothed and marchand grain beetles (Oryzaephilus
surinamensis und O. mercator)
Different wooly aphids and mealy bugs
(Pseudococcididae)
Scale insects (Coccidae)
Scale insects (Coccidae)
173
Heilig et al (Appendix for Chapter 4)
Coccophagus scutellaris Dalman
Dacnusa sibirica Telenga
Diglyphus isaea Walker
Diaeretiella rapae M'Intosh
Encarsia citrina Craw
Encarsia formosa Gahan
Encyrtus lecaniorum Mayr
Eretmocerus californicus Howard (= eremicus
Rose & Zolnerowich)
Eretmocerus mundus Mercet
Gyranusoidea litura Prinsloo
Habrobracon hebetor Say
Lariophagus distinguendus Förster
Leptomastidea abnormis Girault
Leptomastix dactylopii Howard
Leptomastix epona
Walker
Lysiphlebus testaceipes Cresson
Metaphycus flavus Howard
Metaphycus helvolus Compere
Metaphycus lounsburyi Howard
Metaphycus stanleyi Compere
Microterys flavus Howard
Pseudaphycus maculipennis Mercet
Theocolax elegans Westwood
Thripobius semiluteus Boucek
Trichogramma brassicae
Bezdenko
Trichogramma cacoeciae Marchal
Trichogramma dendrolimi Matsumura
Trichogramma evanescens Westwood
Trichogramma evanescens Westwood (Stamm
„Lager“)
Venturia canescens Gravenhorst
Predatory midges and syrphids (Diptera)
Aphidoletes aphidimyza Rondani
Diaeretiella rapae DeGeer
Feltiella acarisuga Vallot
Scale insects (Coccidae)
Leaf-miner flies (Agromyzidae: Liriomyza and others
Leaf-miner flies (Agromyzidae: Liriomyza and others
Cabbage aphid (Brevicoryne brassicae)
Diaspididae
White fly (Trialeurodes vaporarium)
Scale insect (Saissetia hemisphaerica)
White flies (Bemisia spp and others)
White flies (Aleyrodidae)
Long-tailed mealy bug (Pseudococcus longispinus)
Stored product moths (Indian Meal moth, Plodia
interpuntella) and (Ephestia spp)
Grain weevils (Sitophilus spp), drugstore beetle
(Stegobium paniceum), tobacco beetle (Lasioderma
serricorne), shiny spider beetle (Gibbium psylloides),
golden spider beetle (Niptus hololeucus)
Wooly aphids and mealy bugs (Pseudococcididae)
Wooly aphids and mealy bugs (Pseudococcididae)
Wooly aphids and mealy bugs (Pseudococcididae)
Apids (Aphis gossypii)
Scale insects (Coccidae: Saissetia oleae, Coccus
hesperidum)
Scale insects (Coccidae: Saissetia oleae,
Coccus hesperidum)
Scale insects (Coccidae: Saissetia oleae)
Scale insects (Coccidae)
Scale insects (Coccidae: Saissetia oleae)
Wooly aphids and mealy bugs (Pseudococcididae)
Lesser grain borer (Rhyzopertha dominica)
Thrips (Hercinothrips femoralis, Heliothrips
haemorrhoidalis, Echinothrips americanus)
Eggs of corn borer (Ostrinia nubilalis) and other moths
Eggs of plum maggot moth (Cydia funebrana) and
codling moth (Cydia pomonella)
Eggs of plum maggot moth (Cydia funebrana) and
codling moth (Cydia pomonella)
Eggs of pest lepidoptera and stored product moths
Eggs of stored product moths
Eggs of stored product mothes (Indian meal moth, Plodia
interpuntella) and (Ephestia spp)
Aphids
Aphids
Spider mites (Tetranychus urticae, T. cinnabarinus,
Panonychus ulmi)
Predatory beetles (Coleoptera)
Adalia bipunctata Linnaeus
Atheta coriaria Kraatz
Chilocorus nigritus Fabricius
Aphids
Parasites of fly pupa
Scale insects
174
Appendix 11
Coccinella septempunctata Linnaeus
Cryptolaemus montrouzieri Mulsant
Exochomus quadripustulatus Linnaeus
Rhyzobius forestieri Mulsant
Rhyzobius lophantae Blaisdell
Rodolia cardinalis Mulsant
Stethorus punctillum Weise
Predatory true bugs (Heteroptera)
Anthocoris nemoralis Fabricius
Dicyphus hesperus Knight
Macrolophus melanotoma Costa(= caliginosus
E. Wagner)
Macrolophus pygmaeus Rambur
Orius insidiosus Say
Orius laevigatus Fieber
Orius majusculus Reuter
Lacewings
Chrysoperla carnea Stephens
Parasites and predators of stable flies
Diaeretiella rapae Girault & Sanders
Muscidifurax zaraptor Kogan & Legner
Nasonia vitripennis Walker
Spalangia cameroni Perkins
Spalangia endius Walker
Spalangia nigroaeneus Curtis
Hydrothaea aenescens Wiedemann
Aphids
Wooly aphids (Eriosomatidae) and mealy bugs
(Pseudococcididae)
Scale insects
Scale insects (Saissetia oleae)
Scale insects (Coccidae), Wooly aphids (Eriosomatidae)
and mealy bugs (Pseudococcididae)
Wooly aphids (Eriosomatidae) and mealy bugs
(Pseudococcididae)
Spider mites
Suckers (Psyllids, Psyllidae)
White fly (Trialeurodes vaporariorum)
White flies (Aleyrodidae)
White flies (Aleyrodidae)
Thrips (Thysanoptera)
Thrips (Thysanoptera)
Thrips (Thysanoptera)
Aphids
Housefly-related flies
Housefly-related flies
Housefly-related flies
Housefly-related flies
Housefly-related flies
Housefly-related flies
Housefly-related flies
Source: http://www.jki.bund.de/
175
Heilig et al (Appendix for Chapter 4)
11.3.
Invertebrate biocontrol agents used in Spain
Beneficial
Adalia bipunctata
Taxonomy
coleoptera
Target
Aphids on leaves
Adalia bipunctata
coleoptera
Aphids on leaves
Delphastus pusillus
coleoptera
Whiteflies
Harmonia axyridis
coleoptera
aphids on leaves
Aphidoletes aphidimyza
diptera
Aphids on leaves
Feltiella acarisuga
diptera
Tetranychus urticae
Anthocoris nemoralis
heteroptera
Macrolophus
caliginosus
heteroptera
Anagrus atomus
hymenoptera
Aphelinus abdominalis
hymenoptera
Psylla
Aleurodina (whiteflies),
secondary vs
Tetranychus &
Aphids: Macrosiphum
euphorbiae, Aphis gossypii
Tomato Leaf-hopper
(Hauptidia maroccana)
Aphids:
Macrosiphum
euphorbiae
Aphids:
Aphis gossypii,
Aphidius colemani
hymenoptera
Aphidius ervi
hymenoptera
Diaeretiella rapae
hymenoptera
Dacnusa sibirica
hymenoptera
Diglyphus isaea
hymenoptera
Encarsia formosa
hymenoptera
Eretmocerus eremicus
(syn. Californicus)
hymenoptera
Eretmocerus mundus
hymenoptera
Orius insidiosus
hymenoptera
Orius laevigatus
hymenoptera
Orius majusculus
hymenoptera
Myzus persicae (green peach
aphid)
Aphids: Aulacorthum solani
Macrosiphum euphorbiae,
myzus persicae
Aphids : Brevicoryne brassicae
Agromyzidae
(leaf-miner flies)
Agromyzidae
(leaf-miner flies)
Aleurodina (whiteflies)
Aleurodina (whiteflies):
Bemisia tabaci,
Trialeurodes vaporariorum
Aleurodina (whiteflies):
Bemisia tabaci,
Trialeurodes vaporariorum
Thrips:
Frankliniella occidentalis,
Thrips tabaci
Thrips,
partial: Tetranychus
Thrips,
partial: Tetranychus
176
Crop
orchards: all
vegetable greenhouse: all
crops
vegetables greenhouse
and covered
Vegetables , orchards
vegetable greenhouse:
tomato,
cucumber, egg plant,
sweet pepper
vegetable greenhouse: all
crops
orchard: pear
vegetable greenhouse: all
crops
vegetables
vegetable greenhouse: all,
tomato,
egg plant, sweet pepper
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
Cabbage, oil-seed rape
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops, orchards
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
Appendix 11
Trichogramma brassicae
Bezdenko
Trichogramma brassicae
Bezdenko
Trichogramma
evanescens
Amblyseius andersoni
hymenoptera
Amblyseius andersoni
mite
Amblyseius californicus
mite
Ostrinia nubilalis
(European corn borer)
Noctuidae(Owlet moths),
Pyralidae
Noctuidae(Owlet moths),
Pyralidae
N. rubi, P. ulmi, T.urticae
Aculops lycopersici,
Tetranychus
Tetranychus, Panonychus
Amblyseius cucumeris
mite
Tetranychus, thrips
Amblyseius degenerans
mite
Thrips
Amblyseius barkeri
(mackenziei)
Amblyseius swirskii
mite
Thrips
vegetables
mite
Hypoaspis aculeifer
mite
Thrips, whiteflies
Sciaridae (fungus gnats), bulb
mite (Rhyzogliphus robini)
Hypoaspis miles
mite
Sciaridae (fungus gnats), thrips
Phytoseiulus persimilis
mite
Heterorhabditis
bacteriophora,
nematode
Heterorhabditis megidis
nematode
Tetranychus urticae
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil),Phyllopertha horticola
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
vegetables
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetables
Phasmarhabditis
hermaphrodita
Steinernema
carpocapsae
nematode
Limacidae (Slugs)
vegetable: general
nematode
Codling moth
Apple, pear
hymenoptera
hymenoptera
mite
Steinernema kraussei
nematode
Steinernema
carpocapsae
nematode
Steinernema feltiae
nematode
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Noctuids,
Gryllotalpa gryllotalpa
(European mole cricket),
Tipula paludosa (March crane
fly )
Codling moth, cydia molesta
Steinernema feltiae
nematode
Sciaridae (fungus gnats)
Chrysoperla carnea
nevroptera
aphids on leaves
Chrysoperla lucasina
nevroptera
Micromus angulatus
Franklinothrips
vespiformis
Adalia bipunctata
Adalia bipunctata
nevroptera
Aphids, thrips, scales,
whiteflies, acarids eggs, leak
moth
Scales, aphids
Thrips
Thrips
coleoptera
coleoptera
Aphids on leaves
Aphids on leaves
177
maize
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
orchards: all
Vegetables
vegetables
vegetable covered:
tomato, cucumber,
sweet pepper, all crops
(thrips)
vegetable greenhouse: egg
plant, sweet pepper
orchards: crops & nursery
Vegetables, flowers
vegetable: general
vegetable: general
Apple, pear
vegetable: general young
plants
vegetables and ornements
covered
vegetables and ornements
covered
vegetables
vegetable greenhouse: all
crops
orchards: all
vegetable greenhouse: all
Heilig et al (Appendix for Chapter 4)
Delphastus pusillus
coleoptera
Whiteflies
Harmonia axyridis
coleoptera
aphids on leaves
Aphidoletes aphidimyza
diptera
Aphids on leaves
Feltiella acarisuga
diptera
Tetranychus urticae
Anthocoris nemoralis
heteroptera
Macrolophus
caliginosus
heteroptera
Anagrus atomus
hymenoptera
Aphelinus abdominalis
hymenoptera
Psylla
Aleurodina (whiteflies),
secondary vs
Tetranychus &
Aphids: Macrosiphum
euphorbiae, Aphis gossypii
Tomato Leaf-hopper
(Hauptidia maroccana)
Aphids:
Macrosiphum
euphorbiae
178
crops
vegetables greenhouse
and covered
Vegetables , orchards
vegetable greenhouse:
tomato, cucumber, egg
plant, sweet pepper
vegetable greenhouse: all
crops
orchard: pear
vegetable greenhouse: all
crops
vegetables
vegetable greenhouse: all,
tomato, egg plant, sweet
pepper
Appendix 11
11.4.
Invertebrate biocontrol agents used in Switzerland
Beneficial
Adalia bipunctata
Adalia bipunctata
Taxonomy
coleoptera
coleoptera
Target
Aphids on leaves
Aphids on leaves
Aphidoletes aphidimyza
diptera
Aphids on leaves
Aphidoletes aphidimyza
Feltiella acarisuga
diptera
diptera
Aphids on leaves
Tetranychus urticae
Anthocoris nemoralis
Macrolophus
caliginosus
heteroptera
heteroptera
Aphelinus abdominalis
hymenoptera
Aphidius colemani
hymenoptera
Psylla
Aleurodina (whiteflies),
secondary vs
Tetranychus &
Aphids: Macrosiphum
euphorbiae, Aphis gossypii
Aphids:
Macrosiphum
euphorbiae,
Aulacorthum solani
Myzus persicae (green peach
aphid)
Aphids:
Aphis gossypii,
Aphis fabae,
Myzus persicae (green peach
aphid)
Aphids:
Aulacorthum solani
Macrosiphum euphorbiae
Agromyzidae
(leaf-miner flies)
Agromyzidae
(leaf-miner flies)
Aleurodina (whiteflies)
hymenoptera
Aphidius ervi
hymenoptera
Dacnusa sibirica
hymenoptera
Diglyphus isaea
Encarsia formosa
Eretmocerus eremicus
(syn. Californicus)
Orius insidiosus
hymenoptera
hymenoptera
Aleurodina (whiteflies):
Bemisia tabaci,
Trialeurodes vaporariorum
hymenoptera
Thrips:
Frankliniella occidentalis,
Thrips tabaci
Thrips,
partial: Tetranychus
Thrips,
partial: Tetranychus
Ostrinia nubilalis
(European corn borer)
Noctuidae(Owlet moths),
hymenoptera
Orius laevigatus
hymenoptera
Orius majusculus
Trichogramma brassicae
Bezdenko
Trichogramma brassicae
hymenoptera
hymenoptera
179
Crop
orchards: all
vegetable greenhouse: egg
plant, cucumber, sweet
pepper
vegetable greenhouse:
tomato,
cucumber, egg plant,
sweet pepper
vegetable covered: all
vegetable greenhouse:
cucumber, egg plant,
sweet pepper
orchard: pear
vegetable greenhouse:
tomato,
egg plant, sweet pepper
vegetable greenhouse: all,
tomato,
egg plant, sweet pepper
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse:
tomato,
cucumber, egg plant,
sweet pepper
vegetable greenhouse:
sweet pepper
vegetable greenhouse: all
crops
vegetable greenhouse:
sweet pepper
maize
vegetable greenhouse: all
Heilig et al (Appendix for Chapter 4)
Bezdenko
Amblyseius barkeri
(mackenziei)
mite
Pyralidae
Thrips
Amblyseius californicus
mite
Tetranychus
Amblyseius cucumeris
mite
Tetranychus, thrips
Amblyseius degenerans
mite
Tetranychus, thrips
mite
Sciaridae (fungus gnats)
mite
Sciaridae (fungus gnats)
Hypoaspis aculeifer
Hypoaspis miles
mite
Phytoseiulus persimilis
Heterorhabditis
bacteriophora,
nematode
Heterorhabditis megidis
nematode
Heterorhabditis megidis
nematode
Phasmarhabditis
hermaphrodita
Photorhabdus
luminescens
nematode
Photorhabdus
luminescens
nematode
Steinernema
carpocapsae
nematode
Steinernema
carpocapsae
nematode
Steinernema
carpocapsae
nematode
Steinernema feltidae
nematode
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Noctuids,
Gryllotalpa gryllotalpa
(European mole cricket)
Sciaridae (fungus gnats)
Xenorhabdus bovienii
nematode
Sciaridae (fungus gnats)
nematode
Tetranychus urticae
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Otiorhynchus salicicola,
Otiorhynchus sulcatus (vine
weevil)
Limacidae (Slugs)
180
crops
vegetable greenhouse: all
crops, tomato, cucumber,
egg plant, sweet pepper
vegetable greenhouse:
sweet pepper
vegetable covered:
tomato, cucumber,
sweet pepper, all crops
(thrips)
vegetable greenhouse: egg
plant, sweet pepper
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops
vegetable greenhouse: all
crops, tomato, cucumber,
egg plant, sweet pepper
orchards: nursery
orchards: nursery
vine: young plants
vegetable: general
orchards: nursery
vine: young plants
orchards: all
vine: young plants
vegetable: general
vegetable: general young
plants
vegetable: general young
plants
Appendix 11
11.5.
Invertebrate biocontrol agents used in the United Kingdom
Active Substance
Product Name
Type of product
Entompathogenic
nematode
Entompathogenic
nematode
Entompathogenic
nematode
Entompathogenic
nematode
Entompathogenic
nematode
Entompathogenic
nematode
Target(s)
Sciarids, leafminer,
WFT
Steinernema feltiae
Nemasys
Steinernema kraussei
Nemasys L
Heterorhabditis megidis
Nemasys H
Heterorhabditis megidis
Nemasys H
Steinernema carpocasae
Nemasys C
Steinernema carpocasae
Nemasys C
Phasmarhabditis
hermaphrodita
Adalia bipunctata
Amblyseius californicus
Trichogramma evanescans
Anagrus atomus
Amblyseius cucumeris
Nemaslug
slug parasitic nematode
Slugs
Adalsure
Ambsure
Trichogramma
Anagsure
Ambsure
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Hypoaspis miles
Hyposure
Natural enemy
Orius laevigatus
Aphelinus abdominalis
Aphidius ervi
Aphidius colemani
Aphidoletes aphidimyza
Chilocorus nigritus
Chrysoperla carnea
Cryptolaemus montrouzieiri
Dacnusa sibirica
Diglyphus isaea
Encarsia formosa
Encarsia formosa and
Eretmocerus eremicus
Eretmocerus eremicus
Feltiella acarisuga
Macrolophus caliginosus
Phytoseiulus persimilis
Bombus terrestris
Metaphycus helvolus,
Encarsia citrina,
Coccophagus lycimnia and
Encyrtus infelix
Leptomastix dactilopii
Leptomastix dactylopii,
Anagyrus pseudococci and
Leptomastidea abnormis
Metaphycus helviolus
Encarsia formosa
Encarsia formosa +
Eretmocerus eremicus pupae
Orisure
Aphelsure
Aphissure (e)
Aphisure (c)
Aphidosure
Chilosure(n)
Chrysosure (c )
Cryptosure (m)
Dacsure (si)
Digsure (i)
Encsure
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Aphids
Thrips, rsm
Caterpillars
Leaf hopper
Thrips
Thrips, bulb mite,
sciarids
Thrips
Aphids
Thrips
Thrips
Aphids
Scale insect
Aphids
Mealy bug
Leaf miner
Leaf miner
Whitefly
Enersure
Natural enemy
Whitefly
Eretsure (f)
Felsure (a)
Macsure (c )
Phytosure (p)
Beesure
Natural enemy
Natural enemy
Natural enemy
Natural enemy
Pollinator
Whitefly
rsm
Whitefly
rsm
Pollination
Scalesure
Natural enemy
Scale insect
Leptosure (d)
Natural enemy
Mealy bug
Mealysure
Natural enemy
Mealy bug
Metasure (h)
EN-STRIP
Natural enemy
parasitic wasp
Scale insect
Whitefly
ENERMIX
parasitic wasp
Whitefly
181
vine weevil
vine weevil,
Grubs
codling moth (occasional
cutworms)
Hylobius
Heilig et al (Appendix for Chapter 4)
Eretmocerus eremicus
Macrolophus caliginosus
Macrolophus caliginosus
Feltiella acarisuga
Phytoseiulus persimilis
Amblyseius californicus
Aphidoletes aphidimyza
Aphelinus abdominalis
Aphidius colemani
Chrysoperla carnea
Aphidius ervi
Episyrphus balteatus
Adalia bipunctata
Amblyseius cucumeris
Orius laevigatus
Amblyseius swirski
Dacnusa sibirica +
Diglyphus isaea
Diglyphus isaea
Dacnusa sibirica
Hypoaspis aculeifer
Steinernema feltiae
Steinernema feltiae
Steinernema carpocapsae
Trichogramma sp.
Heterorhabditis megidis
Cryptolaemus montrouzieri
Adalia bipunctata
Amblyseius (Euseius) ovalis
Amblyseius (Iphiseius)
degenerans
Amblyseius (Neoseiulus )
californicus
Amblyseius (Neoseiulus)
cucumeris
Amblyseius (Typhlodromips)
montdorensis
Amblyseius (Typhlodromips)
swirskii
Amblyseius andersoni
Anagrus atomus
Anthocoris nemoralis
Aphelinus abdominalis
Aphidius colemani
Aphidius ervi
Aphidoletes aphidimyza
Atheta coriaria
Bombus terrestris
Chrysoperla carnea
Cryptolaemus montrouzieri
Dacnusa sibirica
ERCAL
MIRICAL
MIRICAL NYMPH
SPIDEND
SPIDEX
SPICAL
APHIDEND
APHILIN
APHIPAR
CHRYSOPA
ERVIPAR
SYRPHIDEND
ADALIA larvae
THRIPEX
THRIPOR
SWIRSKI MITE
parasitic wasp
predatory bug
predatory bug
predatory bug
predatory mite
predatory mite
predatory bug
parasitic wasp
parasitic wasp
predatory bug
parasitic wasp
predatory bug
predatory beetle
predatory mite
predatory bug
predatory mite
Whitefly
Whitefly/spidermite
Whitefly/spidermite
Spidermite
Spidermite
Spidermite
Aphids
Aphids
Aphids
Aphids
Aphids
Aphids
Aphids
Thrips + some mites
Thrips
Thrips and Whiteflies
DIMINEX
parasitic wasp
Leafminers
MIGLYPHUS
MINUSA
ENTOMITE
aculeifer
ENTONEM
SCIA-RID
CAPSANEM 50
million
TRICHO-STRIP
LARVANEM
CRYPTOBUG
Adaline b
Ovaline
parasitic wasp
parasitic wasp
Leafminers
Leafminers
predatory mite
Sciarids
parasitic nematode
parasitic nematode
Sciarids
Mushroom flies
parasitic nematode
Cranefly, Caterpillar
parasitic wasp
parasitic nematode
predatory beetle
Predator
Predator
Caterpillar
Vine Weevil, Chafer
Mealybug
Aphids
Whitefly and thrips
Amblyline d
Predator
Thrips
Amblyline cal
Predator
Spider mites
Amblyline cu
Predator
Thrips
Amblyline m
Predator
Thrips
Swirskiline
Predator
Whitefly and thrips
Anderline aa
Anagline a
Antholine n
Apheline a
Aphiline c
Aphiline e
Aphidoline a
Staphyline c
Beeline Total
System
Chrysoline c
Cryptoline m
Dacline s
Predator
Parasitoid
Predator
Parasitoid
Parasitoid
Parasitoid
Predator
Predator
Spider mites
Leaf Hoppers
Pear Psylla
Aphids
Small aphids
Large aphids
Aphids
Sciarid and Shore Flies
Pollinator
-
Predator
Predator
Parasitoid
Aphids
Mealybugs
Leafminers
182
Appendix 11
Diglyphus isaea
Encarsia formosa
Digline i
Encarline f
Parasitoid
Parasitoid
Eretmocerus eremicus
Eretline e
Parasitoid
Feltiella acarisuga
Feltiline a
Heterorhabditis megidis
Nemasys H
Hypoaspis miles
Macrolophus caliginosus
(also known as M.
pygmaeus)
Orius laevigatus
Orius majusculus
Phasmarhabditis
hermaphrodita
Phytoseiulus persimilis
Hypoline m
Predator
Entomopathogenic
nematode
Predator
Macroline c
Predator
Whiteflies
Oriline l
Oriline m
Predator
Predator
Entomopathogenic
nematode
Predator
Thrips
Thrips
Nemaslug
Phytoline p
183
Leafminers
Trialeurodes
Trialeurodes and
Bemisia
Spider mites
Vine Weevils
Sciarid Flies
Slugs
Spider mites
Nicot, P. C. (Ed)
Classical and augmentative biological control against diseases and pests: critical status analysis and
review of factors influencing their success
1st Edition August 2011
Copyright: IOBC/WPRS 20011
ISBN
978-92-9067-243-2
http://www.iobc-wprs.org