Journal of Ecology 2014, 102, 1083–1100
doi: 10.1111/1365-2745.12265
BIOLOGICAL FLORA OF THE BRITISH ISLES*
No. 275
List Vasc. Pl. Br. Isles (1992) no. 158, 35, 1
Biological Flora of the British Isles: Ruscus aculeatus
Peter A. Thomas1† and Tarek A. Mukassabi2
1
School of Life Sciences, Keele University, Staffordshire ST5 5BG, UK; and 2Botany Department, University of
Benghazi, Benghazi, Libya
Summary
1. This account presents information on all aspects of the biology of Ruscus aculeatus L. (Butcher’s
broom) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and
physiology, phenology, floral and seed characters, herbivores and disease, history and conservation.
2. Ruscus aculeatus is a multistemmed monocotyledonous shrub with leaves functionally replaced
by cladodes and photosynthetic stems. It is native to southern England primarily in dry shaded
woodland and hedgerows (but widely planted elsewhere) often, but not exclusively, on base-rich
soil. It is rarely abundant in any habitat, usually forming widely spread discrete clumps.
3. Ruscus aculeatus is remarkably shade tolerant and drought resistant with low water conductance
and transpiration, and water storage in the cladodes. Yet unusually for a drought-tolerant stemphotosynthetic plant, it prefers shady environments.
4. The flowers have few if any pollinating mechanisms, low seed production and fruit/seed dispersal
are largely ineffective, which may be a relict of its evolution in a tropical Tertiary climate. Population survival primarily depends upon vegetative spread from stout rhizomes, aided by the plant’s
general unpalatability.
5. Over-collecting for medicinal steroidal saponins has caused some population declines, particularly
in eastern Europe, but it is otherwise facing few conservation problems.
Key-words: climatic limitation, communities, conservation, diseases, ecophysiology, geographical
and altitudinal distribution, germination, herbivory, mycorrhiza, reproductive biology, soils
Butcher’s broom. Asparagaceae. Ruscus aculeatus L. is a
perennial, evergreen shrub with multiple stems arising from a
creeping, thick, sympodially branched rhizome to form an
oval, pyramidal bush. Stems striate, green, erect, much
branched, 25–80 (100) cm. Leaves reduced to triangular scarious scales < 5 mm long and replaced functionally by rigid
cladodes (1–4 9 0.4–1 cm), each arising from a leaf axil;
cladodes ovate, entire, dark green and spine-pointed. Mostly
dioecious but occasional hermaphrodite or female flowers
have been reported on otherwise male plants which led
Martınez-Palle and Aronne (1999) to classify it as subandroecious. Male and female plants very similar in appearance
(Yeo 1968). Flowers 1–2, arising from the axil of a small
*Nomenclature of vascular plants follows Stace (2010) and, for nonBritish species, Flora Europaea.
†Correspondence author: E-mail: p.a.thomas@keele.ac.uk
scarious bract in the centre of the upper surface of a cladode,
each with a short pedicle. Perianth greenish-white, approximately 3 mm long, in two whorls of three segments, bearing
papillae. Female flowers with a cup formed from fused
stamen filaments around the superior, unilocular ovary, which
has a subsessile capitate stigma. Male flowers with three
stamens, filaments green or violet, fused into a tube around
an undeveloped ovary. Fruit a bright red globose berry, 8–
14 mm with 1–4 large seeds; seed mass 163 mg.
Ruscus has shuttled between various families including
Ruscaceae (Kim et al. 2010), Convallariaceae and Liliaceae
(as recorded in List Vasc. Pl. Br. Isles by Kent 1992), but is
currently in the Asparagaceae (Chase, Reveal & Fay 2009;
Stace 2010). The genus includes approximately 7–10 species
spread throughout Europe across to Iran (Yeo 1968) including the larger ornamental R. hypoglossum introduced into
Britain from south-eastern Europe. There are several
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society
1084 P. A. Thomas & T. A. Mukassabi
ornamental varieties, including var. angustifolius Boiss. with
very narrow cladodes, commonest in the eastern part of its
range, and var. platyphyllus Rouy with cladodes 5 cm long
and up to 2.5 cm wide (Bean 1980). There are also a number
of cultivars including: ‘Lanceolatus’ only female plants with
very narrow cladodes five times longer than wide (Cann
2001); ‘Wheeler’s Variety’ a heavy fruiting hermaphrodite;
and ‘John Redmond’ and ‘Christmas Berry’ both dwarf
hermaphrodites with short intercladode lengths. A yellowfruited form has been recorded in woods at Heckfield,
Hampshire (Anon 1866).
Ruscus aculeatus is the only monocotyledonous shrub
native to the British Isles. It is a slow-growing, shade-tolerant
shrub that occurs naturally in dry shaded woods and hedgerows in southern England, an unusual habitat for a stem-photosynthetic plant (Farmer 1918), as such species normally
grow in arid, high-light environments. However, R. aculeatus
also occurs on walls and cliffs, and rocky ground near the
sea. It is also naturalized in many habitats including churchyards and near habitation, either deliberately planted or as a
garden escape (Preston, Pearman & Dines 2002).
I. Geographical and altitudinal distribution
In Britain, Ruscus aculeatus is native to southern England
(Fig. 1) most widespread in the south-east but local across to
Devon, Cornwall and possibly South Wales, and onto the
Isles of Scilly. It has been much planted within this range and
north of this into Scotland and west into Ireland.
In Europe, R. aculeatus is most widespread around the
Mediterranean (Fig. 2), native to North Africa (Morocco,
Algeria, Tunisia and Libya) across to eastern Europe and central Hungary (Tutin et al. 2002). Northwards it is found in
Transylvania, southern and western Switzerland and
northern France, across into the Azores (Clapham, Tutin &
Moore 1987), reaching its northern European limits between
50 and 55° N (Preston 2007).
Altitudinal limits appear largely unrecorded, but it is known
to reach 300 m in southern Romania (Banciu, Mitoi & Brezeanu 2009), 656 m in the deciduous forests of Southern Italy
(Allen, Watts & Huntley 2000), 930 m in oak–hornbeam
woodland in Slovenia (Dakskobler 2013) and 1000 m in
South Anatolia, Turkey (Davis 1984).
R. aculeatus is found in Britain, Ireland and the Channel
Islands, Hill, Preston and Roy (2004) record that it is found
where the January mean temperature is 4.3 °C, July mean
temperature is 16.4 °C with an annual precipitation of
782 mm. Similarly, Banciu, Mitoi and Brezeanu (2009)
found that R. aculeatus in Romania grows in summer temperatures around 9–10.5 °C and 550–700 mm of precipitation.
Although tolerant of low winter temperature, Salisbury (1926)
found that the northern native distribution in Britain was primarily proscribed by the 8.9 °C March isotherm (except
along the coast of East Anglia where it is within the 8.3 °C
isotherm). Although a somewhat higher temperature than
recorded by Hill, Preston and Roy (2004), Salisbury suggested that this is needed by this winter flowering species to
ensure seed production and long-term success; he noted that
the production of fertile seeds was rare near its northern limit
except in hot summers.
In Britain, these conditions are most frequently met in
woodland openings or at their edges, but in the south of its
range, R. aculeatus tends to be found increasingly in the
humidity and shelter of closed forest (Balica, Tamasß & Deliu
2005b; Banciu & Aiftimie-Paunescu 2012). For example, in
southern Spain, Arista (1995) found R. aculeatus in 21% of
176 plots in closed Abies pinsapo forest and none in forest
gaps. In north-western Spain, it was characterized as requiring
a high minimum temperature, typical of coastal sites, and similar in temperature requirement to Laurus nobilis, Erica cinerea
and Fraxinus excelsior (Retuerto & Carballeira 2004).
(B) SUBSTRATUM
In Britain, Ruscus aculeatus is usually found on soils between
pH 3 and 5, of average moisture retention, but it will grow
on all soil types providing they are not too wet (Kay & Page
1985; Hill, Preston & Roy 2004). This catholic taste is shown
by its ability to grow in the crevices of walls (Rishbeth 1948)
and rocky ground near the sea. Fertility also appears to be
unimportant in Britain and Ireland since it grows equally well
on very fertile and infertile soils, although generally prefers
medium fertility soils (Hill, Preston & Roy 2004). In mainland
Europe, however, R. aculeatus is considered an indicator of
poor soil (Rameau, Mansion & Dume 1989). Ruscus aculeatus
is quite frequent (40–60% frequency) on the serpentine
(ultramafic) soils of Tuscany, Italy (Chiarucci et al. 1998).
II. Habitat
III. Communities
(A) CLIMATIC AND TOPOGRAPHICAL LIMITATIONS
Ruscus aculeatus is primarily a Mediterranean species but
with oceanic tendencies giving it a sub-Mediterranean–subAtlantic distribution (Preston & Hill 1997). In north-western
Spain, Retuerto and Carballeira (1992) suggest that R. aculeatus
spans the temperate Mediterranean and into the Mediterranean
maritime group where it is more abundant.
British populations grow mostly in relatively mild maritime
areas (Kay & Page 1985) with warm summers (Perring
1996). Using mean values for all 10-km squares within which
Although found occasionally on walls, and cliffs, Ruscus
aculeatus in Britain tends to be found mainly in open woodlands or scrub dominated by a wide range of tree species,
including oak (Quercus spp.), hornbeam (Carpinus betulus)
and beech (Fagus sylvatica). This varies from sea-cliff scrub
in Guernsey to limestone woodland in the Gower Peninsula,
Glamorgan and beechwood on chalk in southern Oxfordshire
(Kay & Page 1985). Ruscus aculeatus is found primarily in
Fagus sylvatica – Rubus fruticosus woodland (W14), and
even then only as an occasional species (< 20% of samples
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
Ruscus aculeatus 1085
Fig. 1. The distribution of Ruscus aculeatus
in the British Isles. Each dot represents at
least one record in a 10-km square of the
National Grid. (●) Native 1970 onwards; (○)
native pre-1970; (+) non-native 1970
onwards; (9) non-native pre-1970. Mapped
by Colin Harrower, Biological Records
Centre, Centre for Ecology and Hydrology,
mainly from records collected by members of
the Botanical Society of the British Isles,
using Dr A. Morton’s DMAP software.
Fig. 2. The European distribution of Ruscus
aculeatus, modified from de Bolos and Vigo
(2001).
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
1086 P. A. Thomas & T. A. Mukassabi
and 1–4 on the Domin scale) mainly in open areas such as
under canopy gaps and at the edges of stands (Rodwell
1991). It is also found locally, and with varying frequency, in
the very base-poor, infertile soils of Fagus sylvatica –
Deschampsia flexuosa woodland (W15), particularly in the
New Forest.
In mid-Europe, R. aculeatus is found in similar woodlands,
particularly the oak–hornbeam woods and calcicolous beechwoods, and also hedgerows (Burel & Bauldry 1990; Parent
2002) including the Querceto – Carpinetum serbicum aculea cic-Nikolic 2013)
tetosum of Serbia (Ocokoljic, Vilotic & Sija
and the Polygonato multiflori – Quercetum roboris of northwestern Italy (Lonati & Lonati 2002). Further north, it is
commonest in the mild, wet Atlantic oakwoods, particularly
Rusco aculeati – Quercetum roboris (Izco, Amigo & Guitian
1990; Gonzalez-Hernandez & Silva-Pando 1999) and further
south in a number of moist forests in the Pyrenees dominated
by Quercus pyrenaica (Jongman 2000; Silva et al. 2011), the
Endymio – Fagion beech forests of northern Spain (Dierschke
1997), and the moist Fagus sylvatica/Quercus cerris forest in
the uplands of Southern Italy (Martınez-Palle & Aronne
1999). Ruscus aculeatus is also common in the Fraxinus
angustifolia woodlands (Pterocaryo pterocarpae – Fraxinetum
angustifoliae) on moist alluvial soils by the Black Sea
(Kutbay, Kilincß & Kandemir 1998).
In drier and warmer areas around the Mediterranean, such
as Tuscany and Southern Italy, R. aculeatus occurs in the
deep shade of Quercus ilex forests (Quercetea ilicis) sometimes mixed with Pinus pinea and P. pinaster (Debussche &
Isenmann 1994; Grubb 1998; Kutbay, Kilincß & Kandemir
1998; Martınez-Palle & Aronne 1999; Maremmani et al.
2003) often associated with Asparagus acutifolius, Smilax
aspera and Rubia peregrina and in cooler areas by Hedera
helix and Ulex europaeus. In cooler and more humid areas
on calcareous soils, this changes to denser forests of
Q. ilex including Cyclamino hederifolii – Quercetum ilicis
and Festuco exaltatae – Quercetum ilicis (Biondi et al. 2004).
In still drier areas of Portugal and south-eastern Italy,
R. aculeatus occurs in Quercus suber forests in association
with shrubby plants such as Asparagus aphyllus, Myrtus communis, Smilax aspera and Viburnum tinus (Santo, Moreira &
Gonzalez 2005; Barrico et al. 2012). In semi-deciduous and
evergreen woods of south-eastern Italy, R. aculeatus is frequent in a range of woodlands including oak woods on neutral soils (Carici halleranae – Quercetum suberis), Quercus
coccifera scrub on more calcareous soils (Arbuto unedi –
Quercetum calliprini), drier, more acidic Q. trojana woods
(Teucrio siculi – Quercetum trojanae) and the warmer wetter
woods of Q. virgiliana (Irido collinae – Quercetum virgilianae and Cyclamino hederifolii – Quercetum virgilianae;
Biondi et al. 2004).
In Sardinia, R. aculeatus is found in a variety of mixed oak
woodlands including Lonicero implexae – Quercetum virgilianae, Ornithogalo pyrenaici – Quercetum ichnusae and Glechomo sardoae – Quercetum congestae (Bacchetta et al. 2004).
The maquis vegetation west of the Black Sea in Turkey also
contains R. aculeatus, which is notably frequent in two low-
altitude associations: Phillyreo – Lauretum nobilis on coastal
limestone and Lauro – Pinetum brutiae on mixed rock types
up to 220 m, but is absent from the higher altitude deciduous
woodlands (Yurdakulol, Demir€
ors & Yildiz 2002).
IV. Response to biotic factors
Ruscus shoots are eaten by a range of animals when young;
Sack, Grubb and Mara~
n
on (2003) recorded that 10–30% of
juvenile shoots showed sign of herbivore damage in southern
Spain, compared to <10% damaged shoots on other Mediterranean species examined. Mature shoots, however, tend to
escape damage, attributable to the physical defence from the
sharply pointed cladodes but also to the poor nutritional value
of the browse offered. Gonzalez-Hernandez and Silva-Pando
(1999) suggested that the relatively high fibre content (acid
detergent fibre: 57.1 5.5%; SD) and low value of digestible
organic matter (37.3 3.1%) make R. aculeatus low-quality
nutritional forage despite the low silica (1.2 0.6%) and
lignin (14.6 1.8%) content and the higher levels of crude
protein (9.9 1.8%) compared to local grasses. This is
clearly effective in reducing herbivory. Onaindia et al. (2004)
found that R. aculeatus was significantly more abundant in
grazed woodlands in northern Spain, reaching a mean cover
of 15.46 5.00 (SE, n = 32) compared to < 5% cover in
mixed broadleaf woodland left to regenerate after clear-felling
for > 30 years.
Goncßalves, Franco and Romano (2008) investigating allelopathy found that methanolic extracts (50 mg L 1) of
R. aculeatus completely inhibited the germination of Lactuca
sativa (as did similar extracts of Myrtus communis) and that
aqueous extracts (5% and 10% w/v) reduced root growth of
L. sativa by 74% and 78%, respectively. By comparison,
extracts of a number of other Mediterranean plants (such as
Olea europaea, Arbutus unedo and Pistacia lentiscus) had no
allelopathic effect.
V. Response to environment
(A) GREGARIOUSNESS
In Britain, Ruscus aculeatus tends to be locally abundant
but usually of < 5% cover, forming well-spaced individual
bushes that can spread to 2 m or more in diameter (Kay &
Page 1985; Rodrıguez-Loinaz, Amezaga & Onaindia 2012)
but extending up to 25–50% cover (Montagnoli et al. 2012)
or even dense carpets in shady conditions (Peltier et al.
1997; Baini et al. 2012) aided by vegetative spread from
rhizomes.
(B) PERFORMANCE IN VARIOUS HABITATS
Ruscus aculeatus is slow-growing and long-lived (Kay &
Page 1985), performing best in Britain in shaded and undisturbed habitats; it is usually considered a species of ancient
woodland (Peterken 1974; Hermy et al. 1999; Rose 1999).
As such it is not an early successional species, but in
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
Ruscus aculeatus 1087
Mediterranean systems tends to arrive with the mass of other
shrubs (Houssard, Escarre & Bomane 1980). Patzel and Ponge
(2001) noted the dense carpets of R. aculeatus in northern
France growing under the deep shade of beech unmanaged
for at least 400 years. However, even in optimal habitats,
R. aculeatus often has very low biomass; in dense oak woodland in central Italy, Aguilar et al. (2012) recorded
28 kg ha 1 of fresh biomass of R. aculeatus, the lowest mass
of any woody plant they investigated.
Tansi, Karaman and Toncer (2009) found that R. aculeatus
in Turkish oak/pine woodland (species not stated but most
likely dominated by Quercus coccifera/Q. cerris and Pinus
brutia) was almost twice the height (45.2 4.69 cm; SD)
compared to plants in deforested, open former pine areas
(26.4 1.73 cm). This was matched by plants in woodland
areas having more cladodes per stem (19.8 12.11 compared
to 9.3 1.26 in the deforested area) and a very much larger
combined rhizome and root dry mass (30.6 8.35 g compared to 2.2 0.47 g). Above-ground dry mass was not
significantly different, but the data had high standard deviations so it is likely that with more sampling, the aboveground dry mass would have been higher in the woodland;
certainly, the fresh mass was significantly larger in the
woodland (10.4 3.07 g) compared to the cleared area
(2.8 0.41 g). The shade appears to be more important than
lack of disturbance since in southern France the cover of
R. aculeatus in 5- to 7-m-high Quercus ilex was 27%, but in
nearby, more open shrublands was just 3% and completely
absent in open fields (Debussche & Isenmann 1994). Similarly, in more marginal habitats such as open Mediterranean
shrublands in southern Spain, Herrera (1984) recorded
< 0.1% cover of R. aculeatus.
The apparent need for shade may also explain the differing
response to grazing in different habitats. Thus, in dry, open
Quercus pubescens forest, Debussche, Debussche and Lepart
(2001) noted that R. aculeatus had increased in abundance in
areas where coppicing or grazing and burning had been abandoned 18 years previously, presumably due to a beneficial
increase in shade. By contrast, Onaindia et al. (2004) found
that in Atlantic oak forest in northern Spain, R. aculeatus had
its highest cover in woods clear cut approximately 30 years
ago and in woodland grazed by cattle compared to older
woods; presumably, the reduction in shade by cutting and
grazing is outweighed by reduction in competition.
The ability to produce new shoots from large rhizomes is
sometimes assumed to give R. aculeatus a distinct advantage
in recovering from fire (Onaindia et al. 2004). And, indeed,
there are records of it being abundant after a fire: Elia et al.
(2012) stated that after an intense fire in oak forest in central
Italy, killing 95% of canopy trees, R. aculeatus was amongst
the ‘herbs and seedlings’ covering the ground in open spaces,
but no specific data were given. However, detailed studies
have shown that it is usually absent from immediate post-fire
habitats despite being present beforehand (Schaffhauser et al.
2012). Ruscus aculeatus was present in open Pinus halepensis
woodland in northern Greece before a fire in 1994, but did
not reappear on the site for 5 months (Ganatsas et al. 2004).
At the end of the first growing season, the new shoots were
at most 4 cm tall. Ten years after the fire, the dominant
woody species had a higher shoot density than before the fire
while R. aculeatus went from a mean stem density of
1.1 stems m 2 pre-fire, to 0.2 m 2 after 10 years. Similarly,
dominant species were taller after 10 years than they were
before the fire, whereas R. aculeatus was not significantly different before the fire (33.1 0.04 cm tall and 1.7 0.05 cm
diameter, SE, n unstated) compared to afterwards. Ubeda,
Outeiro and Sala (2006) observed that R. aculeatus ‘disappeared completely after the fire’ in Pinus pinaster/Quercus
suber woodland in north-eastern Spain and after 2 years was
still sparse (0.45% cover compared to 1.9% pre-fire) and then
only in areas burnt at a medium intensity where the soil had
least cover of litter after the fire (perhaps aiding seed germination).
The drought resistance of R. aculeatus does allow it to
inhabit dry marginal habitats. Thus, in north-western France,
it performs better in urban hedgerows than in rural woodlands
and is significantly associated with the arid, impervious surfaces of urban areas (Vallet et al. 2008).
Ruscus aculeatus has been seen to affect directly the heterogeneity of both litter and earthworm populations in beech
woodland (Campana, Gauvin & Ponge 2002). The stiff, spiny
nature of the plant prevents beech leaf litter from reaching the
ground, which in turn deprives earthworms of food, and possibly creates conditions chemically repellent to most earthworm species. This also has the probable effect of reducing
carbon and nutrient availability beneath the plants.
(C) EFFECT OF FROST, DROUGHT, ETC
The degree of frost tolerance is largely unknown. The very
cold year of 1956 led to Ruscus aculeatus loosing half of its
cladodes at an altitude of 450 m at Olot, northern Spain,
while still surviving (de Bol
os 1956). This response was similar to other Mediterranean species.
Ruscus aculeatus is able to cope with a combination of
extreme drought and deep shade (Grubb 1998; Pivovaroff
et al. 2013) and is similar to Buxus sempervirens and Hedera
helix in this respect (Sack 2004). Coping with shade and
drought is partly due to physiological mechanisms, discussed
under VI (E), and partly morphological, discussed under VI
(A). Using 13 species from across northern to Mediterranean
Europe in a common garden experiment in Cambridge, Sack
(2004) investigated growth and survival under a 20-day
drought with soils reaching 18% of field capacity, at which
point soils were brought back to 49% field capacity before
the drought cycle began again. Drought decreased the relative
growth rate of all species except for R. aculeatus, and it was
concluded that it performed as effectively in both drying and
ever-moist soil. The survival time of first year seedlings under
drought was also tested; seedlings were hardened by reducing
soil capacity to 37%, rewatered and then left to dry indefinitely, repeated under 3% and 30% full sunlight. Survival
time of R. aculeatus seedlings was the highest of all 13 species tested: 65 days under 3% daylight, 59 days under 30%
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
1088 P. A. Thomas & T. A. Mukassabi
daylight compared to a norm of 48 days in the others. Sack
(2004) concluded that this ability to tolerate drought was
attributable to water-use efficiency rather than tolerance of
water loss. This fits with the findings of de Lillis and Fontanella (1992) that R. aculeatus in Mediterranean climates tends
to limit growth to the period when water is available and
stops growth once summer drought reduces water availability.
Ruscus aculeatus often only produces flowers and fruits in
deep shade (Sack, Grubb & Mara~non 2003; Sack 2004), but
it will grow in less shady conditions and so has an Ellenberg
indicator value for light of 4 – a semi-shade plant (Hill, Preston & Roy 2004). Despite this tolerance, Sack (2004) found
that of the 13 European species tested, the growth rate of
R. aculeatus was the most affected by shade; the relative
growth rate under 3% full sunlight was 0.23 that at 30% sunlight (compared, for example, to 0.76 for Sambucus nigra).
Yet the reduction in final mass due to shading at the end of
the growing season was least in R. aculeatus (0.48 of the
mass in 3% compared to 30% sunlight, compared to 0.05 in
Rubia peregrina), attributed to the slow growth in both
shaded and less shaded environments.
Antonellini and Mollema (2010) observed R. aculeatus
growing in dune slacks with shrubs such as Juniperus
communis and Amorpha fruticosa along the Adriatic coast of
Italy. The water-table 0.45 m below the slack surface had a
salinity of 16 g L 1 (approximately half the salinity of sea
water). However, the soil electrical conductivity below
R. aculeatus was between 0 and 6 dS m 1; by comparison,
Pinus pinea could tolerate 12 dS m 1 and salt-tolerant plants
up to 25 dS m 1, so it was concluded that R. aculeatus is not
salt tolerant (agreeing with Hill, Preston & Roy 2004).
VI. Structure and physiology
(A) MORPHOLOGY
There has been argument as to whether the cladodes are
derived from a branch (explaining its axillary nature and the
bearing of flowers) or from a leaf on an aborted shoot, as suggested by its determinate growth and the venation (Hirsch
1977). Hirayama et al. (2007) looked for the expression of
genes normally associated with leaf (YAB2: RaYAB2) and
shoot (STM: RaSTM) growth and found both expressed in the
cladode suggesting that it is a double organ derived from both.
Cooney-Sovetts and Sattler (2008) agree with this dual origin.
All parts of the cladodes and stem are photosynthetic. The
shoots live for several years but do not grow after the first
year. New shoots are produced annually from the underground rhizome (D’Antuono & Lovato 2003; Balica, Tamasß
& Deliu 2005b). The wood is typical of monocotyledons with
the vascular bundles scattered through the sclerenchyma cylinder (Schweingruber 1990). Morphology of the cladodes and
stem is further discussed by Arber (1924), Gilliland (1931)
and Balica, Tamasß & Deliu (2005b).
Seedlings initially have a single thick root, which readily
bifurcates. By the third growing season, the rhizome (up to
5 mm in diameter) develops together with coarsely branched
roots radiating out both vertically downwards and horizontally (Sack, Grubb & Mara~
n
on 2003). Rooting depth was
modelled for theoretical standardized plants of 100 mg and
1 g total dry mass by Sack, Grubb and Mara~
n
on (2003) and
found to be 9.6 cm (9.1–10.2 cm 95% CI) and 16.1 cm
(15.0–17.2 cm 95% CI), respectively, for the two plant
masses. The fine roots 5 mm from the tip have been measured at 0.71 0.034 mm (SE, n = 10), the widest of any
of the Mediterranean species tested by Sack, Grubb and
Mara~
n
on (2003) which, other than R. aculeatus, ranged from
0.33 to 0.45 mm in diameter. Ruscus aculeatus had the
highest proportion of its mass in the roots of any of the 13
species tested by Sack (2004), particularly so under 30% full
sunlight (approximately 30% of dry mass in roots) compared
to 3% sunlight (approximately 22%), a reflection of the relatively large fleshy roots and the short but wide (pachycaul)
rhizome (Sack, Grubb & Mara~
n
on 2003). The rhizome can
reach 25 cm in length and 3 cm in diameter. At the end of
the growing season, the rhizome usually produces two lateral
buds in the axils of the rudimentary leaf scales (Hirsch
1977).
Cladodes are 0.2–0.46 mm thick from seedling to adult plant
(Balica, Tamasß & Deliu 2005b). Cladodes vary in size. Cladodes on plants grown in California were measured at
1.8 0.06 cm2 (SE, n = 92) with a specific leaf area (SLA) of
81.4 cm2 g 1 by Pivovaroff et al. (2013), while European
cladodes in full sun were measured by Sack, Grubb and
Mara~
n
on (2003) to have an area of 2.62 0.151 cm2 (SE,
n = 10) and a SLA of 78.5 2.91 cm2 g 1 (SE, n = 10), the
latter similar to Smilax aspera and Rubia peregrina. The SLA
of shade cladodes of R. aculeatus was estimated at
134 cm2 g 1, a plasticity ratio of 1.7. This was considered by
Sack, Grubb and Mara~
n
on (2003) to be very low compared to
other Mediterranean species. The SLA for seedlings was found
to be somewhat higher by Sack (2004) at approximately
200 cm2 g 1 (estimated from a figure). The SLA of R. aculeatus
is much higher than typically found in temperate evergreen
plants,
with
a
concomitant
low
bulk
density
(0.39 0.03 g cm 3 dry mass; SE, n = 10) which Pivovaroff
et al. (2013) attribute to large water storage areas within the
cladodes (10.5 1.38% total leaf air/water space; SE, n = 5),
occupying a third of the cladode thickness, which aid drought
resistance. Cladodes do indeed have a high water content:
approximately 220–300%, estimated from a figure in Sack,
Grubb and Mara~
n
on (2003). Ruscus aculeatus also has a high
leaf water mass concentration (measured as the difference
between the maximum mass of water that can be held by tissue
compared to its dry mass: approximately 275%, estimated from
a figure), similar to that of Smilax aspera and Ceratonia siliqua
and only exceeded by Rubia peregrina at approximately 350%
(Sack, Grubb & Mara~
n
on 2003). As stated in VI (A), the fleshy
roots and rhizome also apparently store water (Antonielli,
Ceccarelli & Pocceschi 1989). Withstanding shade and drought
is also aided by reduced leaves, thick cladodes (278
3.34 lm; SE, n = 5) with a cuticle that is thick
(3.52 0.22 lm; SE, n = 5), but similar to other evergreen
species (Balica, Tamasß & Deliu 2005b; Pivovaroff et al. 2013).
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
Ruscus aculeatus 1089
Cladodes have stomata in equal number on both sides
(Dickson 1886). Stomatal density was measured at
25.8 4.6 mm 2 (SE, n unstated) in southern Spain (Sack,
Grubb & Mara~non 2003) and 40.69 1.21 mm 2 (SE,
n = 18) in Central Italy (Bettarini, Vaccari & Miglietta 1998).
This is very low compared to dicotyledonous plants even if
doubled to account for both surfaces. Stomatal density was
not significantly different in plants growing beside a natural
CO2 spring in Central Italy at double the atmospheric concentration, but 13 other of the 17 species investigated were also
not affected (Bettarini, Vaccari & Miglietta 1998). Ruscus
aculeatus has relatively long stomatal guard cells (approximately 28 lm, estimated from a figure), compared to approximately 8 lm in Phillyrea latifolia and 38 lm in Viburnum
tinus (Bettarini, Vaccari & Miglietta 1998).
(B) MYCORRHIZA
Ruscus aculeatus normally has arbuscular mycorrhiza (Harley
& Harley 1986; Maremmani et al. 2003). Jumpponen and
Trappe (1998) record colonization of roots by dark septate
endophytes (Deuteromycotina, Fungi Imperfecti), which may
have a mycorrhizal function.
(C) PERENNATION: REPRODUCTION
Ruscus aculeatus has geophyte properties in that it readily
produces new shoots from the creeping rhizome, and this
appears to be the main method of spread within a locality.
D’Antuono and Lovato (2003) in Italy found that seedlings
planted out (after germination in climatically controlled chambers) had already produced several new shoots from the roots
when 1 year old.
There has been a lot of research on micropropagation from
rhizome, stem and cladode tissue, particularly in eastern Europe (Balica, Deliu & Tamasß 2005a; Banciu, Mitoi & Brezeanu 2009; Brezeanu & Banciu 2010; Ivanova et al. 2011).
New shoots readily develop from callus tissue (Banciu &
Aiftimie-Paunescu 2012). Moreover, since the rhizomes have
a large number of aerial buds, they are a particularly good
source of vegetative explants for micropropagation. New
plants can be produced in vitro from excised buds in
< 4 months (Moyano et al. 2006) that are physiologically and
structurally similar to normally produced plants except that
the cladode ground parenchyma is less developed and veins
are less prominent (Banciu & Aiftimie-Paunescu 2012).
(D) CHROMOSOMES
Chromosome number in R. aculeatus is 2n = 40 (Maude
1940).
(E) PHYSIOLOGICAL DATA
Ruscus aculeatus can survive readily and grow in as little as
3–5% full sunlight (Sack, Grubb & Mara~non 2003; Pivovaroff
et al. 2013). Concomitantly, it does not appear to be able to
perform well under high-light fluxes; D’Antuono and Lovato
(2003) recorded that R. aculeatus plants in Bologna, Italy,
almost stopped growth when kept in full sunlight during the
summer. Light-saturated rate of photosynthesis is low, measured by Pivovaroff et al. (2013) per unit area as
5.22 1.33 lmol CO2 m 2 s 1 (SE, n = 6) and per unit
mass as 0.043 0.011 nmol CO2 g 1 s 1 (n = 4), associated with low maximum rate of carboxylation
(26.6 3.18 lmol CO2 m 2 s 1, n = 4) and maximum rate
of electron transport (60.1 6.35 lmol e m 2 s 1, n = 5).
Concomitant with withstanding shade and drought, Pivovaroff
et al. (2013) also found very low levels of respiration per unit
area (0.044 0.009 lmol CO2 m 2 s 1, n = 8) and per unit
mass (3.56 0.70 9 10 4 nmol CO2 g 1 s 1, n = 4). Sack,
Grubb and Mara~
n
on (2003) found a strong relationship
between chlorophyll concentration per unit area and SLA so
that shade cladodes had 1.2–2.5 times the amount of chlorophyll per unit mass of cladode than sun cladodes.
The water conductance of R. aculeatus stems has been
found to be very low. Pivovaroff et al. (2013) measured shoot
hydraulic conductance at 2.16 0.10 mmol m 2 s 1 MPa 1
(SE, n = 10). Farmer (1918) gives a figure relative to stem
cross-sectional area of 3.4 mL cm 2 h 1 at 0.04 Mpa; this
compares to figures of 35 and 36 mL cm 2 h 1 in Ilex aquifolium and Ligustrum vulgare, respectively. Similarly, Warne
(1942) using identical conditions measured water conductivity
as 0.172 0.0116 mL 100 cm 2 h 1 of cladodes (SE,
n = 20), which was the lowest of any of the 16 woody plants
tested, and half that of Buxus sempervirens. This matched
with low transpiration rates of 0.208 mL 100 cm 2 h 1 from
cut stems of R. aculeatus placed in water in a laboratory in
bright light with temperatures up to 28 °C (Warne 1942) and
the very low maximum stomatal conductance of
33 0.007 mmol m 2 s 1 (SE, n = 4), cladode cuticular
conductance (0.379 0.082 mmol m 2 s 1, n = 10) and
stem cuticular conductance (0.095 0.025 mmol m 2 s 1,
n = 6; Pivovaroff et al. 2013). Warne (1942) suggested that
the low hydraulic conductivity is compensated for by the
short distances over which this low-stature plant needs to conduct water. Moreover, Pivovaroff et al. (2013) suggested that
the low shoot conductance is aided by low stomatal conductance and the high water storage in the cladodes, enabling
transpiration needs to be met.
Osmotic potential at full turgor ( 1.28 0.10 Mpa; SE,
n = 6) and turgor loss point ( 1.84 0.10 MPa; n = 6), measured in shoots progressively dried on a bench, has been found
to be higher (less negative) than comparative evergreen woody
species (Pivovaroff et al. 2013). de Lillis and Fontanella
(1992) found that in plants in high Maquis near Rome, Italy,
water potential decreased through spring and summer reaching
its lowest level (dawn value 1.79 MPa) in July and August
when the plants stopped growing. Water potential increased to
around 0.8 MPa in September (a 50% increase), but no new
growth was observed. These values are comparatively high (i.e.
less negative) compared to trees and shrubs in the same area
where water potentials < 3.5 MPa were common (de Lillis &
Fontanella 1992). This suggests that R. aculeatus is not
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
1090 P. A. Thomas & T. A. Mukassabi
Dro
RWCtlp (+)
Cft (+)
ug
ht
ε (–) gmin (–)
Algs (+)
Dm (–)
Water storage (+)
Nmass (+)
Density (–)
Narea (+)
Lamina
thickness (+)
LMA (–)
Epidermis
thickness (+)
Leaf area (–)
0
50
100
150 200
Rarea (–)
δ13C (+)
Jmax (–)
Rmass (–)
Dro
Vc,max (–)
gs (–)
ht
&
Sh
Kshoot (–) Aarea (–)
LCP (–)
Amass (–)
a
e
ug
ψTLP(–)
Π 0 (–)
de
250
Sh
ad
Fig. 3. Radar graph of shade and drought traits, singularly or in combination, of Ruscus aculeatus expressed as per cent of these traits of
comparative species with similar physiognomy. The inner circle represents the mean for comparative species for given traits, and the values
for R. aculeatus are scaled as a per cent relative to this value, with a
value outside the disc representing greater ability to cope with shade
and/or drought; (+) and ( ) indicate whether the value outside the
inner circle is a higher or lower percentage than the comparative
value. For traits expressed as negative values, (+) and ( ) indicate
more or less negative values, respectively. Symbols: d13C, carbon isotope ratio; Jmax, maximum rate of electron transport; Vc,max, maximum
rate of carboxylation; LCP, light compensation point; Amass, Aarea,
light-saturated rate of photosynthesis per unit mass and per unit area;
Kshoot, shoot hydraulic conductance; po, osmotic potential at full turgor; wTLP, turgor loss point; gs, maximum stomatal conductance per
area; Rmass, Rarea, respiration rate per unit mass and per unit area;
Narea, Nmass, N per unit area and per unit mass; Cft, relative capacitance at full turgor; RWCtlp, relative water content at turgor loss
point; e, modulus of elasticity; gmin, leaf cuticular conductance; A/gs,
intrinsic water-use efficiency; Dm, minimum distance from vein to
epidermis; Water storage, thickness of water storage tissue in cladode;
Density, density of cladodes (g cm 3); LMA, leaf (cladode) mass per
area (g m 2). From: Pivovaroff et al. (2013) courtesy of CSIRO Publishing (www.publish.csiro.au/?paper=FP13047).
drought tolerant since it limits growth to the period in spring
before aridity increases. Instead, the physiology and morphology [VI (A)] of R. aculeatus suggests a higher degree of
drought resistance through water storage. Although the degree
of water storage is small compared to true succulents, since stomatal conductivity is so low, even the modest relative capacitance at full turgor of 0.104 0.015 MPa 1 (SE, n = 6:
Pivovaroff et al. 2013) will enable survival for a number of
weeks (Sack, Grubb & Mara~non 2003; Sack 2004). The combination of traits that contribute to the overall shade tolerance
and drought resistance is given in Fig. 3.
Cladode N concentration has been measured at 1.32–2.04%
dry mass in northern and eastern Spain from herbarium specimens (Pe~nuelas & Filella 2001), 1.94 0.06% (SE, n = 9)
in plants grown in California (Pivovaroff et al. 2013), while
in semi-shaded adults in Central Italy, R. aculeatus N was
notably high in early spring at 3.4% (de Lillis & Fontanella
1992). Some of this variation may be due to variations during
the year; de Lillis and Fontanella (1992) noted that cladode N
concentration peaked in late winter (2.2%) and early spring
(3.4%) before vegetative growth started and reached the lowest level (approximately 1.8%) in July. Sack, Grubb and
Mara~
n
on (2003) also found levels to be higher in sun cladodes (approximately 22 mg g 1) than in shade cladodes
(approximately 16 mg g 1, estimated from a figure). These
values are high compared to comparative broadleaf evergreen
species (Pivovaroff et al. 2013), which they suggest is consistent with adaptation to drought. de Lillis and Fontanella
(1992) also found maximum cladode C concentration in
August (60%) and December (52%), associated with cessation
in growth, and lowest in between in October (40%). Cladode
carbon : nitrogen ratio was found by Pivovaroff et al. (2013)
to be 23.1 0.68 (SE, n = 9), while the carbon isotope ratio
(d13C) was very negative ( 33.32 0.29&; n = 9) and typical of values normal in understorey plants. The non-protein
amino acid azetidine-3-carboxylic acid has been found in
R. aculeatus (Fowden & Steward 1957).
Ruscus aculeatus has no known heavy metal resistance
(Ecological Flora of the British Isles 2013) but was found to
hyperaccumulate iron (up to 1440 mg Fe kg 1 dry plant
mass) on a Portuguese lead mine (Pratas et al. 2013). Other
values for heavy metal content of dried plant material were
(mg kg 1) as follows: Ag, 0.1–0.17; Co, 0.2–0.63; Cr, 0.42–
1.6; Cu, 3.5–6.7; Ni, 0.65–5.2; Pb 3.37–54; and Zn 32–74
(Pratas et al. 2013).
(F) BIOCHEMICAL DATA
There is a very large literature on the medicinal value of
biochemical components of Ruscus aculeatus, including 17
steroidal saponins (characterized by spirostanol or furostanol
aglycones, in particular two from the first group, ruscogenin
and neoruscogenin, but also aculeosides), flavonoids, chrysophanic acid, glycolic acid, phenols and a benzofuran (Capra
1972; Elsohly et al. 1974, 1975; Pedersen 1994; Facino et al.
1995; Dunouau et al. 1996; Mimaki et al. 1998a,b, 1999;
Ali-Shtayeh & Abu Ghdeib 1999; Redman 2000; de Combarieu et al. 2002; Mangas et al. 2006; G€
uvencß, S
ß atır &
Cosßkun 2007; De Marino et al. 2012; Mari et al. 2012;
Barbic et al. 2013). The amount of pharmacologically active
steroid saponins in plants appears to be variable but is usually
highest in the rhizome and root (Longo & Vasapollo 2005).
In wild plants in Romania, Balica et al. (2007) found the
highest concentration of sapogenin in the rhizome (0.17%
neoruscogenin and 0.11% ruscogenin). By contrast, Zistler
et al. (2008) found higher levels of just ruscogenin (0.9–1.8%,
estimated from a figure) in the rhizome of German material,
and the European Pharmacopoeia states that the required
pharmaceutical minimum is 1% (Council of Europe 2011).
Pharmaceutical material is still primarily collected in the wild
since little has been done using tissue culture sources
(Moyano et al. 2006), and the concentration of saponins in such
cultured material is low; Balica et al. (2007) found that in in vi-
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
Ruscus aculeatus 1091
Phylloclade
Scale leaf
Floral bud and its bracts
Shoot apex
Rhizome
Ground
Fig. 4. Phenology of shoot growth of Ruscus
aculeatus. The main shoot system of the
previous year is omitted in stage 0 and I, and
the dashed line in stage II shows the
disintegrated main shoot system of the
previous year. From: Hirayama et al. (2007),
fig. 8, p. 236. With kind permission from
Springer Science and Business Media.
0
tro samples, the highest concentration was found in shoots
but was low (0.075% neoruscogenin and 0.017% ruscogenin).
The Greek philosopher Theophrastus claimed R. aculeatus
extracts stopped swelling and allowed lame people to walk,
and Pliny the Elder described its use in treating varicose veins
(Pedersen 1994), but its medicinal use appears to have
been largely forgotten in Europe until the 1970s (Salzmann,
Ehresmann & Adler 1977). The saponins are a potent venous
vasoconstrictor agent with a diminishing oedema effect, acting
as an agonist on adrenergic receptors of the smooth muscle of
veins and reducing vascular permeability (Bouskela & Cyrino
1994; Mimaki, Kuroda & Kameyama 1998; Parrado & Buzzi
1999; Hexsel, Orlandi & Zechmeister 2005) and have been
used as a diuretic and mild laxative (Berg 1990; Bouskela &
Cyrino 1994; Goncßalves et al. 2013). They have thus been
used in the therapy of cancer, circulatory problems (such as
oedema) and diabetes (Tarayre & Lauressergues 1979; Cluzan
et al. 1996; Anon 2001) since they are effective and have
few side effects (Redman 2000; Sadarmin & Timperley
2013). Flavonoid and phenolic acid extracts have antimicrobial and antioxidant properties (Hadzifejzovic et al. 2013).
The skin of the fruit has been found to contain anthocyanins
pelargonidin 3-O-rutinoside (64%), pelargonidin 3-Oglucoside (16%) and pelargonidin 3-O-trans-p-coumaryl-glucoside (13%) (Longo & Vasapollo 2005).
VII. Phenology
Hirayama et al. (2007) investigated the phenology of shoot
growth in cultivated plants grown in Japan. New growth arose
I
II
III
IV
V
from lateral dormant buds formed at the base of the previous
year’s shoots. These began to expand in February and March
(stage 0 in Fig. 4) and produced new shoots in June (stage I).
Over the next 5 months, cladode primordia developed in the
axils of scale leaves on the developing stem (stage II), and in
the following 3 months (December to early February), flower
buds developed on the uppermost cladodes (stage III). From
mid-February to mid-March (stage IV), the developing cladodes became progressively flattened and the next set of dormant buds (stage 0) was initiated at the base of the current
shoot. The shoot appeared above-ground in late March (stage
V), and, in central Italy, reached adult height within a week
but were very thin and pale and continued developing until
mid-July (de Lillis & Fontanella 1992; Martınez-Palle &
Aronne 1999). Cladodes are not shed individually in the
autumn since the shoots grow and die as a whole, with a life
span of 14–26 months (Perez-Latorre & Cabezudo 2006).
As noted by Bennett (1869), the ‘normal time of flowering
is almost the depth of winter’. Flower buds begin to enlarge
in July, all flowers developing male and female parts until
they become functionally either male or female by early
September due to arrestation of either the anthers or pistil
(Martınez-Palle & Aronne 1999). Flower opening usually
begins in September or October and carries on till April in
mainland Europe (Herrera 1981; de Lillis & Fontanella 1992;
Tansi, Karaman & Toncer 2009) sometimes extending to June
in Britain (Hillman 1979). Within this period, the timing of
peak flowering varies widely and has been recorded as October–November in southern Italy (Martınez-Palle & Aronne
1999) and (November) January–April in the British Isles (Kay
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
1092 P. A. Thomas & T. A. Mukassabi
& Page 1985; Clapham, Tutin & Moore 1987). Others have
recorded R. aculeatus flowering twice in the same year (October–December and again from early February/mid-April to
the end of May) in Italy (de Lillis & Fontanella 1992; Aronne
& Wilcock 1997), or even flowering ‘practically all year
round’ (Perez-Latorre & Cabezudo 2006). This variation is
partly due to different flower buds on the same cladode opening at different times. In Central Italy, Martınez-Palle and
Aronne (1999) noted that while many cladodes have no
flower buds, others often have two flower buds. In both male
and female plants, the first bud opened in October–December,
while the second was delayed a number of weeks until after
the main rain period, opening in January–April.
In male flowers, the anthers dehisce within the first day,
and in female flowers, the stigma is receptive from flower
opening. Both male and female flowers remain open for 4–
10 days. Following this, all flowers fall except for a small
number of female flowers that develop fruits (Martınez-Palle
& Aronne 1999).
Despite the long flowering period, fruit development usually
begins only in late April (Martınez-Palle & Aronne 2000),
taking 6–8 months to mature, and so producing mature fruits
usually by the end of October (Fuentes 1992; de Lillis & Fontanella 1992; Aronne & Wilcock 1997). Ripe fruits remain on the
plant for long time, certainly through the winter (Herrera 1981)
and often for 1–2 years (Martınez-Palle & Aronne 1999) so that
plants tend to carry fruits all year round.
VIII. Floral and seed characters
(A) FLORAL BIOLOGY
Flowers are concentrated on a small number of cladodes. In
southern Italy, Martınez-Palle and Aronne (1999) recorded
that on female plants, 54.4% of cladodes had no flower buds,
14.6% had one and 30.9% had two flower buds. Male plants
by contrast had more flower buds: 43.3% of cladodes had no
buds, while 23.9% and 32.7% had one and two flower buds,
respectively. Only 10–15 flowers open simultaneously on a
plant at the peak of flowering (Kay & Page 1985).
Ruscus aculeatus is often assumed to be entomophilous,
offering pollen but no nectar or detectable scent (Kay & Page
1985; Aronne & Wilcock 1994). Indeed, Hillman (1979)
found that fruit set was correlated with the number of sunny
days and so concluded that it is insect-pollinated since insects
are active on sunny days. Yeo (1968) also suggested that
small flies that hover around R. aculeatus bushes might serendipitously land on open flowers. However, there is little direct
evidence that insects visit the flowers. Both Kay and Page
(1985) in the British Isles and Martınez-Palle and Aronne
(2000) in southern Italy made lengthy observations during the
flowering period and recorded no insect visits despite the
plants being covered in spider webs in winter and seeing
small flies and other insects resting on cladodes (but showing
no interest in the flowers). The apparent absence of pollinators in Italy belies the suggestion by Kay and Page (1985)
that pollinators present in the Mediterranean region might be
absent from the British Isles. Pollen has also not been found
in honeybee pollen loads in Spain and Italy, despite the plant
being in the area (Diaz-Losada, Ricciardelli-d’Albore & SaaOtero 1998). Anemophily is possible where male and female
shoots intermingle, but experiments using blown air have
shown that a fairly high wind speed (> 5 m s 1) is needed
for pollen removal (Martınez-Palle & Aronne 2000). Moreover, a number of studies looking at atmospheric pollen loads
near ground level have found no R. aculeatus pollen in samples despite the plant being present in the area (G€
uvensen &
€ urk 2002; Celik et al. 2005; Gucel et al. 2013). It is conOzt€
cluded that low pollen transport is the main reason for low
seed set – see VIII (C).
The quantity of pollen produced per flower appears to be
limited. In southern Italy, the number of pollen grains per
anther ranged from 712 to 1316 with an average of 873
(Martınez-Palle & Aronne 2000). Since each male flower
has three anthers, an estimated 2618 pollen grains were produced per flower. Mean pollen viability was 84.9%, ranging
from 71.1% to 96.3% between flowers (Martınez-Palle &
Aronne 2000). The stigmatic surface is composed of small
papillae (20 9 10 lm) covered by a lipid exudate rich in
calcium ions to create a ‘wet stigma’; this calcium is important in the germination and growth of pollen grains
(Bednarska 1991).
Ruscus aculeatus has been described as dioecious (Hillman
& Warren 1973; Hillman 1979), subdioecious (normally dioecious but with some exceptions) by Tutin et al. (2002), dioecious or andromonoecious (varying between populations) by
Kay and Page (1985) and subandroecious (dioecious with
occasional hermaphrodite flowers on male plants) by
Martınez-Palle and Aronne (1999). Of plants surveyed in
Surrey, 104 plants were dioecious and one other plant was a
male that produced a single berry (Hillman & Warren 1973;
Hillman 1979). Similarly, of 164 plants sampled on the Gower Peninsula, one male plant had a solitary berry, while on
Guernsey, 8.4% of plants (n = 347) had predominantly male
flowers ‘with some female or hermaphrodite flowers’ (Kay &
Page 1985). In Italy, hermaphrodite flowers (4–5 flowers per
plant) were found on two male plants by Martınez-Palle and
Aronne (1999). Given the presence of male flowers with
occasional hermaphrodite flowers, andromonoecious would
appear to be the best description of its floral biology. Being
primarily dioecious, outcrossing is normally obligatory, but
andromonoecious populations are capable of self-pollination
(Martınez-Palle & Aronne 1999). Despite this, neither Kay
and Page (1985) nor Hillman and Warren (1973) found that
andromonoecious plants produced more berries than dioecious
plants, although obviously the sample sizes are small. The
andromonoecious form has been exploited horticulturally to
ensure that solitary plants bear fruits (Bean 1980). Kay and
Page (1985) note the ‘Treseder’s Variety’ (introduced into
Cornwall in the late 1950s) is andromonoecious (although
described in horticultural literature as an hermaphrodite), and
it may produce hermaphrodite flowers in April–May and male
flowers the rest of the flowering season (P. F. Yeo, pers.
comm. quoted in Kay & Page 1985).
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
Ruscus aculeatus 1093
In southern Italy, Martınez-Palle and Aronne (2000) found
the sex ratio of plants to be biased towards female plants
(66% female) uniformly mixed through the population. A
similar ratio was found near London (62% female) by (Hillman 1979). However, Kay and Page (1985) found some populations more weighted to males (Gower: 41% female,
n = 164; Guernsey: 41%, n = 347), while other were near
equal (Oxford: 50%, n = 18). Rottenberg (1998) found a ratio
of 49% (n = 90+) in three populations in Israel.
(B) HYBRIDS
No hybrids are recorded. However, closely related species are
known to hybridize (R. hypoglossum 9 R. hypophyllum =
R. 9 microglossum; Pivovaroff et al. 2013) so R. aculeatus
hybrids may be possible.
(C) SEED PRODUCTION AND DISPERSAL
Fruit production within populations tends to be very low,
though variable between plants. Kay and Page (1985) found
that while some plants had up to 10 fruits, many had none.
Mean number of berries per plant has been recorded as 2.87
berries per female (n = 68) on the Gower, 0.5 per female
(n = 9) in Oxfordshire (Kay & Page 1985) and 1.8 berries
per female (n = 43) in Surrey (Hillman & Warren 1973). In
Italy, Martınez-Palle and Aronne (2000) found that only 3%
(one of 38) of marked flowers produced fruits in 1996 and
none produced in 1997 (n = 130) and 1998 (n = 410). Seed
output was between 1 and 5 seeds per female plant (Kay &
Page 1985; Moyano et al. 2006).
This low fruit and seed production is primarily attributable
to poor pollination. Martınez-Palle and Aronne (2000) noted
the absence of R. aculeatus pollen grains on the stigmatic surface of 80 sampled flowers. Moreover, hand pollination has
been seen to dramatically increase fruit production, reaching
73% (n = 36; Kay & Page 1985) and 80% (n = 34) of flowers compared to just 3% (n = 38) of open-pollinated developing fruits and none in unpollinated flowers (n = 52; MartınezPalle & Aronne 2000). Poor pollination appears to be a
mainly due to ineffective pollen movement rather than distance between male and female plants limiting pollen spread.
In the study by Martınez-Palle and Aronne (2000) described
above, neighbouring plants were just 30–90 cm apart. In the
British Isles, Kay and Page (1985) found that fruit number
was highest (14 fruits) in the Gower population despite
female plants being 24 m from the nearest male. Hillman and
Warren (1973) and Hillman (1979) reported similar findings.
However, distance between plants may play a small part in
poor fruit set since Kay and Page (1985) also recorded that a
plant ‘next to male’ in the Oxford population had 13.5%
flowers set seed, while an isolated plant had 0.8% success.
Martınez-Palle and Aronne (2000) also found that no plant
had more than four fruits when further than 130 cm away
from a male plant while those closer had up to 13 fruits.
Other limitations have been postulated. Low fruit number in
Turkey has been attributed to a distorted sex ratio with very
few female plants (Tansi, Karaman & Toncer 2009), and
Salisbury (1926) suggested that R. aculeatus rarely sets seed
near its natural northern limit in Britain except in unusually
hot summers.
Given the red fleshy fruits, it is often supposed that the
seeds are spread by animals, particularly by endozoochorous
animals and possibly by birds (Hermy et al. 1999; Debussche, Debussche & Lepart 2001; Parent 2002; Preston, Pearman & Dines 2002). However, this does not seem to be the
case despite the long time of fruit retention exposing it to a
wide range of fruit-eating birds (Fuentes 1992). The fruits
appear to be unpalatable (Kay & Page 1985) and remain on
the parent plant until they fall or are forced off by stormy
weather, remaining beneath the parent plant until they rot
(Martınez-Palle & Aronne 1999). Jordano (1988) looked
extensively at the diet of the blackcap Sylvia atricapilla (L.)
and garden warbler S. borin (Bodd.) in southern Spain and
found that although R. aculeatus fruit ripened at the same
time as many other fruits of woody plants (including Pistacia
lentiscus, Myrtus communis and Olea europaea), it did not
form part of their diets. Herrera (1984) pointed out that
R. aculeatus fruits, with a mean diameter of 11.9 mm, were
larger than the gape width of the blackcap and garden warbler
(range 7.1–8.6 mm), although this would suggest that they
are capable of taking the smallest of the R. aculeatus fruits
(range 8–14 mm). However, fruits of R. aculeatus were not
detected in faecal samples by Herrera (1984), suggesting there
is an underlying unpalatability.
Low seed production and lack of animal dispersers lead to
poor seed dispersal. Debussche and Isenmann (1994) measured seed rain in Mediterranean France using seed traps with
a combined area of 39.75 m2 (of which 16.65 m2 was in
R. aculeatus habitat) and collected just two seeds over the 17month study out of a total of 20 373 seeds from 38 fleshyfruited species. Debussche and Isenmann (1994) in their survey found just three seedlings of R. aculeatus < 1 year old in
quadrats totalling 9225 m2, and no seedlings 1–2 years old.
Fresh mass of Spanish fruits was recorded as 0.98 and
1.36 g by Herrera (1987, 1981), respectively, with a dry mass
of 0.39 g (Herrera 1987). This is comparatively large compared to 70 other Mediterranean species measured in Israel,
but the fruits were fairly average in their protein and mineral
contents (Izhaki 2002; individual data not given). Seed mass
was measured at 163 mg (n = 15) for British material (of
unknown provenance) and 174 mg for Spanish material
(Herrera 1987).
(D) VIABILITY OF SEEDS: GERMINATION
Germination is usually very slow and often low. Trials have
shown 20–80% germination on artificial media over 4–
6 months or longer (D’Antuono & Lovato 2003; Banciu, Mitoi & Brezeanu 2009; Banciu & Aiftimie-Paunescu 2012).
There is an element of dormancy since D’Antuono and Lovato (2003) found that tetrazolium tests indicated over 50% viable seeds, while in vitro germination was 20–25% despite
prior removal of ‘defective seeds’. Ruscus aculeatus has an
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
1094 P. A. Thomas & T. A. Mukassabi
impervious seed coat, and germination is improved by scarification. Adding 5 ppm of gibberellic acid to artificial media
has been seen to improve germination from 60% to 85%
(Banciu & Aiftimie-Paunescu 2012), but treatment with
500 ppm for 1 h had little effect (D’Antuono & Lovato
2003). A combination treatment for scarification by concentrated sulphuric acid (concentration unknown) and gibberellic
acid (500 ppm for 1 h) resulted in no germination. Ethylene
and potassium nitrate did not affect per cent germination, but
(compared to a mean germination time of 150 days in controls) 1 mM of ethylene decreased germination time to approximately 120 days (estimated from a figure), while 3 mM
increased germination time to approximately 170 days
(D’Antuono & Lovato 2003). Cold stratification (temperature
unknown) for 120 days had little effect on germination and
mean germination time (D’Antuono & Lovato 2003), but it is
possible that germination may be improved by alternating
periods of warm (15 °C) and cold (5 °C) conditions. Seeds
can be stored under orthodox seed storage conditions of
10–15% moisture content at < 0 °C (Gosling 2007).
Martınez-Palle and Aronne (2000) in Spain found no germination in the field over a 3-year study, although germination teats showed that 45% of tested seeds germinated in
11 months. Ruscus aculeatus seeds survive in the soil for
<1 year and so there is no soil seed bank (Thompson, Bakker
& Bekker 1997).
(a)
(b)
(E) SEEDLING MORPHOLOGY
Seedlings germinated on sterile sand and transplanted into
pots rapidly develop a well-established root system and vigorous shoots in the first year. Seedlings produced several new
shoots from the roots in the spring of second year (D’Antuono
& Lovato 2003). Each new shoot produces scale leaves initially, the cladodes developing in their axils and overtaking
the scales in size (Arber 1924). Seedling development is
shown in Fig. 5.
IX. Herbivory and disease
(A) ANIMAL FEEDERS OR PARASITES
Red deer (Cervus elaphus L.) in riparian areas within the
Mediterranean scrub of Sardinia showed a strong preference
for browsing on Ruscus aculeatus and a number of other
shrubs including Quercus ilex, Alnus glutinosa, Salix caprea,
Myrtus communis and Viburnum tinus. More than 25% of
Ruscus individuals were browsed despite it being uncommon
and the availability of other browse (Lovari et al. 2007).
Other deer species ignore R. aculeatus. It was not found in
the rumen contents of fallow deer (Dama dama L.) in the
New Forest despite it being a common plant (Jackson 1977).
Roe deer (Capreolus capreolus L.) have been found to avoid
it even if starved (Pettorelli et al. 2003), and a density of
20 roe deer km 2 in Germany led to an increase in R. aculeatus at the expense of palatable species such as ivy (Hedera
helix; Cibien, Boutin & Maizeret 1988). Ruscus aculeatus is
Fig. 5. Seedling morphology of Ruscus aculeatus. (a) Young subterranean seedlings bearing just scale leaves, viewed from two sides.
Older seedlings (b) bearing the remains of the shrunken seed, several
lateral buds along the stem and with cladodes in the axils of scale
leaves. From: Arber (1924) by permission of Oxford University
Press.
eaten in winter by free-roaming farmed llamas (Lama glama
L.) and alpacas (Vicugna pacos L.) in Italy (Aguilar et al.
2012).
The tortoise Testudo hermanni hermanni Gmelin sought
out and ate the flowers and unripe fruit of R. aculeatus in
Central Italy as they became available despite the rarity of the
fruit (Del Vecchio et al. 2011). The authors considered these
fruits to be particularly important food source for tortoises
about to enter hibernation.
Comparatively, few insect feeders have been recorded on
R. aculeatus; a small number are listed by the Biological
Records Centre (2013). Two scale insects are known to feed
on the cladodes of R. aculeatus as larvae and adults:
Dynaspidiotus britanicus (Newstead) and Parlatoria proteus
(Curtis) (Hemiptera, Diaspididae). The second of these is
introduced. Larvae of the macromoth Alcis repandata (L.)
(Lepidoptera, Geometridae) have been recorded feeding on
R. aculeatus in a glasshouse. The mealybug Ferrisia malvastra
(Hemiptera, Coccoidea) has been found on plants in Israel
(Ben-Dov 2005) along with the scale insects Coccus hes-
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
Ruscus aculeatus 1095
peridum L., Planococcus citri (Risso) and Pseudococcus longispinus (Targioni Tozzetti) (Hemiptera: Coccoidea) (BenDov 2011–2012). Pseudococcus maritimus (Ehrh.) (Hemiptera, Sternorrhyncha) is recorded as covering up to 50% of
cladode surfaces in a Polish glasshouse (Golan & G
orskaDrabik 2006).
The nematode Longidorus helveticus Lamberti et al. (Nematoda, Dorylaimida) has been isolated from R. aculeatus
rhizomes in Serbia (Barsi & De Luca 2005) and Rotylenchus
agnetis Szczygiel (Nematoda, Hoplolaimidae) on Italian
plants (Cantalapiedra-Navarrete et al. 2013).
Two mites (Mesostigmata: Phytosehdae) have been found
on R. aculeatus on Mt Carmel, Israel (Swirski & Amitai
1997): Amblydromella crypta (Athias-Henriot) and Typhlodromus athiasae (Porath & Swirski).
(B) PLANT PARASITES AND EPIPHYTES
Fungi associated with Ruscus aculeatus are given in Table 1.
Ellis and Ellis (1997) record many other fungi found on living and dead R. aculeatus that are not specific to it.
Several authors record foliicolous lichens found on
R. aculeatus in southern France and Spain (De Sloover &
Serusiaux 1984; Bricaud et al. 1993), and in Tuscany and the
humid mountains of southern Italy (Puntillo & Vezda 1994;
Puntillo & Ottonello 1997).
(C) PLANT DISEASES
Paraphaeosphaeria glaucopunctata (Grev.) Shoemaker & C.E.
Babc. [=Phaeosphaeriopsis glaucopunctata (Grev.) C^amara,
Palm & Ramaley] (Ascomycota, Pleosporales) has caused leaf
spot and necrosis of Ruscus aculeatus in Europe and Australia
(Lohwag 1963; C^amara et al. 2001; Golzar & Wang 2012).
X. History
Members of the former Ruscaceae have been reported to occur
in Laurasia in the Cretaceous (Raven & Axelrod 1974). Ruscus
aculeatus itself is considered to be a relict species that evolved
under a warm tropical climate with summer rains in the Tertiary
(Martınez-Palle & Aronne 2000; Kim et al. 2010). This is said
to explain the breeding system of R. aculeatus: dioecy, small
green flowers, long flowering and fruiting period, fleshy fruits
with few seeds and reliance on vegetative sprouting (Aronne &
Wilcock 1994). It is also likely that shade tolerance evolved
before drought resistance. Subsequent climate changes during
the late Pliocene and the Quaternary to the current climate have
Table 1. Fungi (by Order) directly associated with Ruscus aculeatus. Nomenclature follows the British Mycological Society (2013)
Species/classification
Ascomycota
Botryosphaeriales
Guignardia istriaca Bubak
Phyllosticta ruscicola Durieu & Mont.
Phyllostictina hypoglossi (Mont.) Petr. & Syd.
Capnodiales
Mycosphaerella tassiana (De Not.) Johanson
[=Cladosporium herbarum (Pers.) Link]
Chaetosphaeriales
Menispora ciliata Corda
Diaporthales
Phomopsis rusci (Westend.) Grove
Helotiales
Strossmayeria basitricha (Sacc.) Dennis
Hypocreales
Fusarium aquaeductuum (Rabenh. & Radlk.) Sacc.
Fusarium merismoides Corda
Gibberella baccata (Wallr.) Sacc.
Nectria episphaeria (Tode) Fr.
Pycnofusarium rusci D. Hawksw. & Punith.
Volutella rusci Sacc.
Microthyriales
Microthyrium ciliatum var. ciliatum Gremmen & De Kam
Pleosporales
Cytoplea sp. Bizz. & Sacc.
Paraphaeosphaeria glaucopunctata (Grev.) Shoemaker &
C.E. Babc.
Phoma macrostoma Mont.
Ulocladium chartarum (Preuss) E.G. Simmons
Ecological notes
Source
Live, dead and fallen cladodes, twigs and wood; only
recorded UK host
Only recorded UK host
Stems; recorded only on Ruscus spp. in the United Kingdom
1, 3
1, 2
1, 3
Recorded mainly on a wide variety of non-woody hosts
1
Dead stem
1
Dead cladodes and stems; R. aculeatus only British host
1, 3
Dead wood
1, 3
Endophytic on twig
Dead cladodes
Endophytic on twigs and wood; wide range of woody hosts
Dead cladodes; only recorded UK host
Only recorded UK host
1
1
1
1
1, 3
1
Dead stem
1
Dead wood
Live and dead cladodes; most records from R. aculeatus
1
1, 2, 3
Endophytic on twigs
Endophytic on twigs
1
1
Sources: 1, British Mycological Society (2013); 2, Lohwag (1963); 3, Ellis & Ellis (1997).
© 2014 The Authors. Journal of Ecology © 2014 British Ecological Society, Journal of Ecology, 102, 1083–1100
1096 P. A. Thomas & T. A. Mukassabi
resulted in conditions in which the pollination, seed production
and dispersal mechanisms no longer function effectively
(Martınez-Palle & Aronne 1999, 2000).
Subfossil cladodes of R. aculeatus have been found in
Quaternary volcanic deposits in Central Italy dating from
450 000 years ago, in a mixed conifer woodland including
Amentotaxus, Cephalotaxus, Torreya, Abies, Pinus, Cupressus,
Juniperus and Taxus (Tongiorgi 1938; Follieri 2010). More
recently, pollen of R. aculeatus was noticeably abundant in
Moroccan deposits dating from 9000 to 6400 BP (Morales
et al. 2013; Zapata et al. 2013) where it was growing
amongst maquis-type vegetation dominated by Olea europaea
and Pistacia lentiscus. Herb pollen (4.2–8.3% pollen abundance) was dominated by Poaceae (1.8–3.9%) and R. aculeatus
(0.4–1.6%).
The first British record of Ruscus aculeatus was published
by Willian Turner in 1548. He reported ‘Ruscus is called . . .
in english buchers brome or Petigrue. Petigrue groweth in
Kent wilde by hedge sydes, but it beareth no fruite as it doeth
in Italy’ (Britten, Jackson & Stearn 1965).
Kingdom. Across Europe, R. aculeatus is given some protection as a rare and endangered species by the Habitats Directive, listed in Annex V (plant species of community interest
whose taking in the wild and exploitation may be subject to
management measures). A number of eastern European countries, where harvesting is more intense, have put specific conservation measures in place. In Bulgaria, harvesting in under
legal control and in Romania R. aculeatus is protected by law
as a ‘monument of nature’ (Marossy 2006; Banciu & Aiftimie-Paunescu 2012). Climate change and invasive species
may be detrimental to R. aculeatus (Vicente et al. 2011) in
the future, but there is currently little threat to this species
and it is listed as of ‘least concern’ by IUCN (2011).
Acknowledgements
The Libyan Government is gratefully acknowledged for its support of T.M. at
the start of this study. We thank Alexandria Pivovaroff for providing Fig. 3
and the large amount of work that went into its production, and Chris Preston
for providing access to the original of Fig. 2.
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and diverse history of usage in Europe. It has indeed been
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