Population ecology of Allium ursinum, a space-monopolizing clonal plant

Acta Botanica Hungarica 53(3–4), pp. 371–388, 2011DOI: 10.1556/ABot.53.2011.3–4.18

POPULATION ECOLOGY OF ALLIUM URSINUM,A SPACE-MONOPOLIZING CLONAL PLANT

B. OBORNY1, Z. BOTTA-DUKÁT2, K. RUDOLF3 and T. MORSCHHAUSER3

1Department of Plant Taxonomy and Ecology, Eötvös Loránd University (ELTE)H-1117 Budapest, Pázmány P. sétány 1/c, Hungary; E-mail: [email protected]

2Institute of Ecology and Botany, Hungarian Academy of SciencesH-2163 Vácrátót, Alkotmány u. 2–4, Hungary; E-mail: [email protected]

3Department of Plant Taxonomy and Geobotany, University of PécsH-7624 Pécs, Ifjúság u. 6, Hungary; E-mails: [email protected], [email protected]

(Received 24 January, 2011; Accepted 31 May, 2011)

We review the population ecology of Allium ursinum according to its life history, pheno-logy, demography, dispersal, and population dynamics. Spatial distribution is reviewed ontwo spatial scales. First, on a broad scale over Europe, in relation to the habitat requirementof the species. Second, on a fine scale of individual patches, presenting some results aboutthe local processes of density regulation and patch formation. We conclude that A. ursinumhas a distinct, hitherto non-described, strategy for monopolizing space and dominating theforest floor. This Clan-of-Clones strategy has the following attributes. 1) Most of the seedsare dispersed close to the parent. 2) Seedling establishment is facilitated by the surroundingadults. 3) Allocation to vegetative reproduction is relatively small; its main role is to pro-long local persistence. 4) The genet is not integrated physiologically, except for a transientconnection between parent and offspring. An important consequence of the Clan-of-Clonesstrategy is that occupied patches can be fine-grained mosaics in terms of genetic composi-tion and age groups.

Key words: dispersal, plant traits, population dynamics, ramet demography, vegetative re-production, wild garlic

INTRODUCTION

Allium ursinum L. is a widespread species in Europe. Due to its frequentoccurrence and high dominance in the understorey vegetation in various me-sic, deciduous woodlands, several papers have dealt with its life history,phenology, demography, and spatial population dynamics. We organise thesedata in a comprehensive review in order to explore its strategy in space andtime.

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Habitat requirements and geographic distribution

A. ursinum is widely distributed in Europe from the Mediterranean toScandinavia. It is absent from the evergreen region of the Mediterranean, fromthe far North (beyond ca 64° N), and from high altitudes (beyond 1,900 m)(Kevey 1977, Tutin 1957, and the references cited therein). It is frequent inwestern Europe, and becomes scarce towards eastern Europe, as the continen-tal climatic influence is increasing (Kevey 1977). Further to the East, the distri-bution extends to the Caucasus and Asia Minor (Stearn 1947, Tutin 1957). Oc-currences have been recorded in North America (USDA 2009) and Africa (inthe Atlas Mts; Schmid 1975), too. In Europe, it is one of the characteristicunderstorey species in mesic, deciduous woodlands. In North America, how-ever, it is an alien species, and is recorded as a noxious weed (USDA 2009).

The species is divided into two subspecies. A. ursinum subsp. ursinum iswidespread in western and central Europe, while subsp. ucrainicum is distrib-uted in eastern and southeastern Europe (Kevey 1977, Kovács 2007). The oc-currences of the subspecies overlap, and transitional forms have also been re-corded (Kevey and Czimber 1982). The division into subspecies has been de-bated recently (Kovács 2007, and the references cited therein).

In spite of its broad distribution across continents, and its occurrence as aweed, the species cannot be considered as a generalist. Several authors haveclassified it as a habitat specialist, having a rather narrow range of ecologicaltolerance (Grime et al. 1988, Kevey 1977, Rychnovská and Bednář 1998). A.ursinum is particularly sensitive to the availability of water. It requires a mesicsoil, which is well-drained. Both drought and waterlogging are unfavourable(Csiky et al. 1999, Grime et al. 1988, Kevey 1977, Rychnovská and Bednář 1998,Trémolières et al. 2009, Tutin 1957). Sufficient humidity in the air is also crucialfor survival (Kevey 1977, Kovács 2007).

Although this is an understorey species, it requires rather high light, atleast in the first few weeks of its growth season (Grime et al. 1988, Kevey 1977).As an early spring geophyte, it avoids competition for light with the canopy inthese first weeks of its growth (Kevey 1977, Tutin 1957). Later the closure of thecanopy induces a plastic response in the photosynthesis, lowering the lightcompensation point (Kevey 1977). In late spring and in the summer the canopycover has facilitative effects, too, because it protects the plant from direct sun-light and wind, and increases humidity in the topsoil and in the air near theground (Eggert 1992, Kevey 1977). The species strongly prefers the forest floor;it can rarely be found outside of a forest (Grime et al. 1988), only in some placeswith high, evenly distributed precipitation (Tutin 1957) or along rivers orstreams (Kevey 1977).

372 OBORNY, B., BOTTA-DUKÁT, Z., RUDOLF, K. and MORSCHHAUSER, T.

Acta Bot. Hung. 53, 2011

Considering its broad distribution in terms of latitude and altitude, thespecies is probably not very sensitive to temperature (Tutin 1957). Neverthe-less, the avoidance of large seasonal and daily fluctuations, especially of heatshock, can be an additional reason for preferring the forest floor (Kevey 1977).

The plant requires a nutrient-rich soil (Tutin 1957). High nitrogen andphosphorus content appear to be particularly important (Kevey 1977, Kovács2007). Trémolières et al. (2009), for example, has demonstrated considerable ni-trogen-limitation in frequently flooded alluvial forests; the availability ofphosphorus proved to be more limiting in the unflooded sites. A. ursinum issensitive to the pH, missing from base-poor sands and mor soils (Tutin 1957).Falkengren-Grerup and Tyler (1993) demonstrated experimentally that mor(pH 3.6) inhibited the production of new roots. Tutin (1957) estimated the tol-erated pH range from 5.5 to 7.9; Grime et al. (1988) narrowed it to 6–7.5. LowpH combined with high aluminium concentration has been reported to be del-eterious, suppressing root extension and biomass production. Seedlings haveproven to be particularly sensitive to aluminium toxicity (Anderson 1993).

Due to its well-defined and rather narrow range of ecological tolerance,Allium ursinum has been suggested to be an indicator species (Kovács 2007,Rychnovská and Bednář 1998). In the phytosociological literature, it is a char-acteristic species in Fagetalia, and an identifier of a facies (alliosum ursini; Ke-vey 1977, Kevey and Czimber 1982, Kovács 2007, Soó 1973).

Within Hungary, A. ursinum lives mainly in the hilly regions (Csiky et al.1999, Kevey 1977, 1979). Its distribution pattern suggests that the species doesnot occur in those regions, which are under a strong continental climatic influ-ence. It is missing from the central part of the Great Hungarian Plain. Its occur-rence is scarce in the Little Hungarian Plain (Kisalföld), and is restricted to forestsclose to rivers (typically hardwood alluvial forests; Kevey and Czimber 1982).

Some of the forthcoming characteristics, especially those that are relatedto phenology or demography, are strongly dependent on the site of the study(geographic region, aspect, soil, etc.). The Appendix briefly describes the siteswhere the authors of the cited studies worked.

Life history

A. ursinum is a bulbiferous clonal plant. Several authors have concludedthat its sexual reproduction is prevalent over clonal reproduction in most nat-ural populations (Bierzychudek 1982, Ernst 1979, Grime et al. 1988, Tutin 1957).Biomass allocation into seeds is extraordinarily high among woodland peren-nials (Bierzychudek 1982; see more later).

ECOLOGY OF ALLIUM URSINUM, A SPACE-MONOPOLIZING CLONAL PLANT 373


(a) Germination

A considerable proportion of the seeds rests in dormancy for more thanone year. Eggert (1992) sowed 100 seeds in each of 8 permanent plots to ob-serve germination. The seeds were placed over a mineral soil surface, and werecovered by leaf litter from the original habitat (beech forest). Seed export andimport was prevented by a fine-meshed nylon net. Only 15.8±0.8% of the seedsgerminated in the year in which they were produced. The majority, 61.3±3.6%germinated in the next year; and 3.3±1.4% was observed one year later.

Temperature is an important factor in germination. Under laboratoryconditions, a rather high rate of germination (up to 63%) could be achieved byincubation at 15–20 °C for four months and then at 5–10 °C for another fourmonths. Constant exposure to low temperature (5 °C) for eight months, how-ever, produced less than 5% germination (Ernst 1979).

Germination starts by a downward growth of the cotyledon, which placesthe shoot apical meristem into relatively deeper soil. First a hyaline sheath-likeleaf, then a foliage leaf develops. The first small renewal bulb is a product ofthe petiole base of this foliage leaf. At this stage, fine additional roots are initi-ated, which pull the seedling downwards, deeper into the soil (Eggert 1992).The seedling is said to be sensitive to desiccation, and the shortage of water hasbeen observed to be the main factor of mortality in this period of life.

(b) Juvenile development

The seedling develops only one foliage leaf in the first year (Fig. 1a). Thisleaf has a rather small area, 65–200 mm2 (Ernst 1979). Those plants that areolder than one year can have multiple leaves from the synpodially organisedbelow-ground shoot system (Eggert 1992).

Ernst (1979) planted bulbs of known age to estimate the age-dependentgrowth of different organs. He found that growth was, in general, slow in thefirst two years of life. A sudden, rapid growth started after the second year,and lasted to the fifth year. The biomass of bulbs doubled in every year withinthis period. After the fifth year, the biomass increment slowed down again.

The period around the fifth year brings about important, qualitativechanges: the start of reproduction both vegetatively and sexually at the sametime. Note, however, that the timing of life history events is stage-dependentrather than age-dependent in this species (Eggert 1992, Rychnovská andBednář 1998). Consequently, the years mentioned below are rough estimates;large individual differences are possible according to the local conditions.



(c) Vegetative reproduction

A typical young plant, up to ca the fourth year, produces one foliage leafand one scale leaf per year on a primary shoot. A bulb develops in each yearfrom the basal, swollen part of the petiole of the new foliage leaf; the old bulbdecays, and is reduced to a fibrous mass. This sequential production of bulbson a monopodial axis terminates when an inflorescence develops at the shootapex, usually after the fourth year, typically in the fifth. Termination of apicalgrowth generally results in the initiation of a daughter shoot in the axil of thelast foliage leaf. This sympodial branching is a key to vegetative reproduction.Occasionally, both the foliage and the scale leaf axil participate in shoot initia-tion, thus, the mother produces two daughters. In early summer, the above-ground parts of the mother decay, and the below-ground storage compoundsare translocated to the new daughter bulb(s). Connection between the sistersvanishes as the shoot base decays, usually within 1–5 years (Jitka Klimešová,personal communication; based on Imrisch (1850), Graebner et al. (1934)).

Due to the regular renewal process of the bulb, described above, it is nottrivial how to define a ramet. The age-dependent data available in the litera-ture do not specify this, but it appears from the context that most authors con-sider the old and the new bulb belonging to the same ramet (i.e. the same phys-iological individual; see Harper (1977)). We find this definition reasonable,therefore, we use “ramet” with the same meaning. We note, however, that



Fig. 1. Life cycle and phenology of Allium ursinum. Years and months are rough approxima-tions for a hypothetical healthy individual in central Europe; the data can significantly varywith geographic location, soil, microclimate, and many other external factors. See the text

for further details

other authors consider the renewal process as birth of a new ramet (see, for ex-ample, the literature about pseudoannuals; see a comprehensive review aboutthe longevity of ramets and of the connections between ramets in various spe-cies in Jónsdóttir and Watson (1990); and in the CLO-PLA database in Kli-mešová and Klimeš (2006)).

Ernst (1979) observed that only 0.1–7.2% of the five years old rametsformed any daughter bulb; vegetative reproduction typically becomes vigor-ous in later years. The bulb is formed on a very short rhizome, thus, the daugh-ter is formed adjacent to the mother (Tutin 1957). Repeated bulb productionproduces a set of densely packed bulbs. The lifetime of the connection betweenthe mother and the daughter is short, lasting for less than one year (Imrisch1850). Therefore, the species is a genet splitter (sensu Eriksson and Jerling(1990), see also Jónsdóttir and Watson (1990), Oborny and Kun (2003), Pitelkaand Ashmun (1985)). It is usually hypothesised that a short mother-daughterdistance (i.e. short rhizome length between mother and daughter) coincideswith strong and permanent physiological integration, which would permit thetransport of material between multiple ramet generations. A. ursinum is acounterexample: it has a short-distance, short-duration connection.

During the period of connection, the daughter appears to receive a con-siderable amount of resource from the mother. Ernst (1979) describes thatthose ramets that originate from bulbs can develop two leaves and an inflores-cence already by the second year of life, and the sizes of these are approxi-mately the same as those of the mother. By contrast, those ramets that originatefrom seeds can typically reach the flowering stage only by the fourth or fifthyear of life. Their leaf area is, in average, much smaller than that of a six-yearold ramet, i.e. of a typical mother (less than 10%, estimated from Figure 1 inErnst (1979)). It appears, therefore, that A. ursinum has a short but intensive pe-riod of physiological integration, which gives an advantage to the vegetativeoffspring over the seed-derived offspring in terms of size and stage of devel-opment. The evidence is indirect. A clarification would require direct experi-ments about the time-dependence of resource transport, for example, by ra-dioactively labelled nutrients (see a review by Jónsdóttir and Watson (1990)about the application of this method in other clonal species).

(d) Sexual reproduction

The development of inflorescence starts quite late in life, only from thefourth year; more typically from the fifth year (Ernst 1979). Flowering is inter-mittent: Eggert (1992) observed that 81% of those ramets that had inflores-cence in a year were unable to flower again in the next year. Flowering is oftenfollowed by a recovery period of biomass accumulation (Eggert 1992). Tutin



(1957) remarks, however, that the plant can set seeds in every year under fa-vourable conditions. The flowers are incompletely protandrous, primarilypollinated by insects. Some spontaneous self-pollination has also been ob-served (Hegi 1939).

Biomass investment into reproduction has been characterised in variousways in this species. Let us denote the dry weight of the reproductive organsby r, and that of the seeds by s. The total dry weight of the above-ground or-gans is A, and the total dry weight by the whole plant, including theperennating storage organ, is T. Ernst (1979) estimated that reproductive allo-cation (r/A) ranges from 0.47 to 0.70. Eggert (1992) measured reproductive ef-fort as r/T = 0.35. He noted that this value was extraordinarily high comparedwith other woodland perennials, and also relative to other members of theLiliales with similar life histories (where this value was typically < 0.2; see ref-erences in Eggert (1992)). In accordance with this, allocation to seeds, esti-mated by Ernst (1979), was also high: s/A was between 0.19–0.58. Reproduc-tive allocation increases with age (Ernst 1979).

Producing a vegetative daughter ramet consumes approximately thesame amount of carbon as producing two inflorescences and scapes (Eggert1992). Considering that vegetative reproduction spares the 4–5 years waitingtime before flowering, and also the interval for subsequent biomass accumula-tion (recovery after flowering), it appears to be more profitable than sexual re-production (calculated by Eggert (1992)). Therefore, the outstandingly high in-vestment into sexual reproduction is surprising. On the population level, inexperimental plots in a beech forest, Eggert (1992) observed nearly twice asmuch dry matter investment into sexual reproduction (25 g/m2) than into veg-etative reproduction (14 g/m2). Naturally, not only the number but also thespatial placement of the offspring is an important matter of consideration. Thedaughter bulb is close to the mother, touching it physically. Seed dispersalprovides some space, although the mother-daughter distance is usually notvery large (see more about dispersal below).

(e) Specificities of development in the root system

Beside the presence/absence of an inflorescence, the number of coarseroots is also an important indicator of the stage of the plant (Eggert 1992).Coarse roots are contractile, enabling the plant move downward in the soil inthe time of drought. In contrast with those species in which root contractionplays an important role from an early stage of life on (see examples in Pütz(2006), and Pütz and Sukkau (2002)), A. ursinum starts this process rather lateafter establishment. One-year old individuals do not have any contractileroots. The root system of young individuals is restricted mostly to the L and A1



layers of the soil. Development of contractile roots starts approximately fromthe third year of life (Ernst 1979). Due to contraction, the bulb can move down-ward significantly, depending on the resistance of the soil. Eggert (1992) foundthat the depth of the bulb, measured as the distance between the shoot apicalmeristem and the soil surface, strongly depended on the size of the bulb (dryweight). The dependence can be described by a saturation curve. In the soil inthe plots studied by Eggert, the saturation value was approximately 8 cmdepth. Tutin observed 8.5–11.5 cm maximum depths in a woodland and in ahedgerow in Britain. The largest depth published is 27 cm (Ernst 1979). Thedownward movement can shift the root system from the L and A1 to the A2and B soil horizons. Therefore, limiting factors change considerably during alifetime. Before the third year, in the shallower soil layers, the main challengeis desiccation. In deeper layers, desiccation is less likely, while a decline in theconcentration of macronutrients (potassium, phosphorus, and nitrate-nitro-gen) has been measured in A. ursinum habitats (Ernst 1979).

(f) Senescence and death

After a vigorous period of reproduction, senescence starts in 7–8 years oldramets (Ernst 1979). The estimated maximum longevity is 8–10 years (Ernst1979, Klimešová and Klimeš 2006).

Phenology

This section is about the timing of life history events within the year (Fig.1b). Germination occurs in late winter and early spring, from January to April,depending on the place and weather (Ernst 1979).

The emergence of new individuals from the bulbs may start before Janu-ary, but in that case, only a colourless, sheath-like leaf emerges, and remainsunder the soil surface until warming starts (NW Germany: Eggert (1992)). Thenew leaves appear above the soil surface in around February–March (Hungary:Kevey (1977), NW Germany: Ernst (1979)). This process strongly depends onthe temperature during the winter dormancy. In experimental temperaturetreatments, only those individuals developed normal leaves and inflorescen-ces, which were exposed to a cold treatment (4 °C) for three months. Furtherleaf growth was facilitated by a higher temperature (10 °C) (Ernst, 1979).

There is some seasonal mortality between February and mid-April, butthis seems to concern only the young stage groups. Eggert (1992) observed asignificant decline in the density of ramets belonging to Stage I (decreasingfrom February to March) and to Stage II (decreasing from February to mid-



April). Stage I denotes juvenile ramets that do not have any coarse root. StageII refers to those ramets that have only one coarse root.

The first leaf in each ramet unfolds by late March – early April (Eggert1992). These young leaves are characterised by an extremely high nitrate con-centration (Ernst 1979). The formation of new bulbs starts from March to April(Ernst 1979).

The peak of dry matter allocation into leaves is from late April to May(Ernst 1979). Then the developing flowers and seeds become the major sinks,and the leaves start to wilt and decompose gradually. Ernst (1979) remarkedthat the time of wilting was the same for seedlings as for adult ramets. Eggert(1992) confirmed the observation that the time difference is not very large,nevertheless, he observed a few days difference, smaller individuals startingsenescence earlier.

The peak of dry matter allocated into reproductive organs is in late June –early July. Cold spring or summer can delay shedding of seeds by 2–3 weeks.North versus south-facing slopes can also differ by 2–3 weeks (Ernst 1979).

Shedding of seeds is rapidly followed by the withdrawal of resourcesfrom all the above-ground organs in around early July. Below the ground, aconsiderable amount of dry matter is allocated for the development of roots atthe expense of allocation into the bulb for storage. This late-season investmentinto the root system is an interesting characteristic of this species (Ernst 1979).

All the leaves are decomposed by August (Ernst 1979). The decomposedleaves form a mat on the soil surface in dense A. ursinum stands. Its thicknesscan reach 1 cm. The mechanical resistance of this mat can be hypothesised toreduce the establishment of other species (Ernst 1979). Beside mechanical re-sistance, allelopathic inhibition may also be considerable. Djurdjevic et al.(2004) extracted phenolic compounds from the soil under an A. ursinum standin a fir-beech forest in western Serbia; a significant allelopathic effect was dem-onstrated on test plants (Lactuca sativa, Triticum aestivum and Amaranthuscaudatus). Ernst (1979) also reviews the subject, mentioning that he productionof isothiocyanates and organic disulphides in A. ursinum leaves was found toinhibit tomato grown in sand. Unfortunately, little is known about the effect ofA. ursinum on those species that co-occur with it in natural habitats. DecayingA. ursinum leaves did not show any inhibitory effect on the growth of two nat-ural cohabitants, Mercurialis perennis and Glechoma hederacea (Ernst (1979), andthe references cited therein). Further studies with more cohabitant specieswould be needed to elucidate the importance of allelopathy.

The bulb is in dormancy until the beginning of October. Then a second,small flush of growth starts: thin roots (so-called autumn roots) develop, andmost importantly, new leaves are formed inside the bulb. These leaves emergeto above-ground only in the next growing season (Eggert 1992, Ernst 1979).



During the winter, bulbs and roots store an exceptionally high concentrationof the reserve carbohydrate fructan (Hendry and Brocklebank unpubl., citedby Grime et al. (1988)).

Demography

Ernst (1979) estimated an average of 20 seeds/year in fertile ramets. Alto-gether, Schmucker and Drude (1934) counted 156 fruiting umbels in a 1 m2

quadrate, which had over 9,000 seeds. A similarly high density of seeds wasobserved by Rychnovská and Bednář (1998): 5,612 seeds/m2. An averagealong a 15 m transect was 2,692 seeds/m2. In the same site, the number of seed-lings was also considerable: 250–300/m2.

Ernst (1979) estimated the survival curve by observing the fates of indi-viduals in permanent plots in a beech wood (Asperulo-Fagetum). The initialnumber of individuals at the beginning of the study was more than 20,000. Theobservations lasted for 6 years. The study revealed four phases of high mortal-ity: (1) at the embryo stage, (2) during dormancy and stratification of the seeds,(3) at reaching maturity, when the adult bulbs start to move into a deeper soillayer by contractile roots, and (4) in 7–8 years old individuals due to ageing.

Mortality peak (1) was rather high: only 54±20% of the ovules could de-velop a viable, fully developed embryo. Peak (2) was also considerable: merely28±6% of the seeds survived to the beginning of the next growth season. Thenthe germinated seeds survived up to the end of the second year in a remark-ably high proportion (79±11%). Peak (3) coincided with reaching maturity,when the bulb started to move down in the soil by contractile roots. The mainreason for death was the consumption by nematodes. Less than 11% of theseedlings could reach reproductive stage (calculated and rounded from thedata published by Ernst (1979)). The reproductive stage proved to be rathersafe in terms of survival. Finally, death due to senescence started to dominateafter 7–8 years.

Demography was found to depend strongly on the local conditions.Asynchronous, local increases and decreases in the population size, and corre-sponding changes in the age structure of the population have been observed inthe permanent plots. For example, the number of individuals increased by afactor of three within 3 years on a southern slope in the beech wood, while de-creased on the plateau and on the northern slope. The sudden increase on thesouthern slope was preceded by an “explosion of seeds” (Ernst 1979).



Dispersal

The literature suggests that the dispersal kernel is small. The seeds arequite heavy (5.4±0.7 mg), and most of them fall onto the ground directly be-neath the capsules. Before the seeds ripen, the fruiting stalks are erect; by thetime of ripening, most of them (up to 75%) become prostrate, and thus, in-crease the distance between the mother and the seeds (Ernst 1979). This dis-tance is not very large, however. The mean stalk length was estimated 22.4±5.7cm in four populations in NW Germany (Ernst 1979), up to 45 cm (Grime et al.1988). We can estimate with reasonable confidence that the dispersal kernel iswithin a 50 cm circle around the mother. Due to the weight of the seeds, dis-persal by wind is negligible (Ernst 1979). Heavy rains may significantly con-tribute to dispersal, especially on steep slopes. The seeds have elaiosomes,therefore, it is reasonable to hypothesise myrmecochory. Observations in thefield, however, reject the hypothesis (see Ernst (1979) and the references citedtherein). In an experiment, in which 1000 seeds were placed along ant trails,only 2 seeds were moved, and these were displaced by less than 24 cm. Eggert(1992) did not observe any ant dispersal during his three-year study.

An estimation of spatial spreading by seeds over a 20-year period yieldedonly ≤ 2.5 m (Ernst 1979). This underlines that crowding, and competition be-tween generations can be significant in this species (cf. Eggert 1992). Clonalspreading is even more restricted: the daughter bulb is initiated at the side ofthe mother, touching it physically (Tutin 1957). Therefore, both the sexual andthe asexual offspring are seriously limited in space.

Occasional transfer to a large distance can be imagined by deer or otherlarge mammal (the seed sticking to its leg with mud), but no direct evidencehas been published (Kevey 1977). This kind of occasional zoochory can explainthe colonisation of new areas; nevertheless, the majority of the seeds is aggre-gated in the vicinity of the mother.

Fine-scale patch structure and density regulation

A. ursinum can form monodominant stands (Ernst 1979, Grime et al. 1988,Kevey and Czimber 1982, Kovács 2007, Rychnovská and Bednář 1998). Withinthese, the spatial distribution is remarkably patchy even in the absence of anyidentifiable edaphic or microclimatic patchiness in the background. Gaps be-tween and within the patches vary in size up to several square metres (see a 1 m2

resolution map about the spatial cover in Figure 2 in Morschhauser et al. (2009)).Within high-cover areas, the ramet density can be higher than 900/m2

(Rychnovská and Bednář 1998). Correspondingly, the standing crop has been



found to grow up to 560 g/m2 (Ernst 1979). Several authors have suggestedthat a reason for monodominance in A. ursinum is that adult individuals do notsuppress the development of juveniles (Grime et al. 1988, Kovács 2007, Rych-novská and Bednář 1998).

We tested this hypothesis directly by observing the development of A.ursinum seedlings under various neighbourhood densities (Morschhauser etal. 2009). The seedlings were marked at their natural places of germination in amonodominant stand, in the understorey of an oak-hornbeam forest. We mea-sured the size of the bulbs at the end of the first growing season, and investi-gated how this size depended on the density of neighbouring adult individu-als. The neighbours’ density was estimated in a 25 cm × 25 cm resolution. Theseedlings selected for the study were always in a gap among the adults, withina 25 cm × 25 cm permanent plot from which all the individuals except for theselected seedlings were regularly removed during the three months of obser-vation. The success of establishment of the seedling was characterised by theweight of the bulb at the end of this period, i.e. at the beginning of the summerdormancy. The results showed a peak in the bulb weight at intermediateneighbour density (at approximately 50% cover). This suggests that the pres-ence of adults has a facilitative effect on seedling establishment, provided thatthe density of adults is not too high. At high density, the effect of competitionprevails over facilitation.

This phenomenon, facilitation between different genets, can be inter-preted as a demographic Allee effect (cf. Courchamp et al. 1999). The mechanismis probably protection from desiccation by increasing the water content in thetopsoil and humidity in the air. Decreasing the variation of temperature canalso be an important factor. The results suggest that not only those neighboursthat are in the immediate vicinity (within 25 cm) but also more distant neigh-bours (within 50 cm) can have a facilitative effect (Morschhauser et al. 2009).

High tolerance of the seedlings to the presence of adults has been sup-ported by other observations as well. Ernst (1979) concludes from his observa-tions in beech forests and other mesic woodlands in North Germany that A.ursinum is “exceptional among species forming monospecific stands becausedominance does not result in differential mortality of the smallest individu-als” (Grime et al. 1988, p. 73). Kovács (2007) remarked on the basis of his obser-vations at several places in the Carpathian Basin that “in spite of the very highdomination of adult plants, the seedlings and the juvenile individuals are notsuppressed” (Kovács 2007, p. 67). In accordance with this, in Eggert’s records,260 seedlings occurred in 1 m2, in spite of the fact that the area was shared with679 adults.

Early literature on clonal plant population dynamics, up to the end of1980s, was dominated by the view that recruitment from seeds was negligible



compared to vegetative recruitment in established clonal plant populations interms of contribution to the number of ramets (see Eriksson 1992, and the ref-erences cited therein). To examine this hypothesis, Eriksson (1989) reviewedthe occurrence of recruitment from seeds in patches of established adults in 68clonal plant species. He concluded that successful recruitment had been ob-served in a rather high percentage, 40%, of the species. Thus, he suggested todistinguish between two categories of recruitment in clonal plants: “repeatedseedling recruitment” (RSR) vs. “initial seedling recruitment” (ISR). In case ofRSR, seedlings can establish and develop into adults among already existingadult plants. In ISR, seedling establishment occurs only at the colonisation ofan empty site (e.g. after disturbance), and later its significance declines. A.ursinum clearly belongs to species with RSR, having successful seedling estab-lishment in old populations, utilising the natural gaps between adults (Morsch-hauser et al. 2009).

Due to the relatively short lifespan of ramets and to the high rate of colo-nisation of new sites, the patches of A. ursinum change dynamically. Rych-novská and Bednář (1998) established three 15 m transects across A. ursinumpatches, and analysed the local demographic patterns in 25 cm × 50 cm sam-ples. The study revealed that the age distribution differed significantly in dif-ferent parts of the patch. In the interior, it was characteristic for a stationarypopulation (occasionally, for a declining population), while in the perimeter, itwas characteristic for an expanding population. Considerable differenceswere found on a fine spatial scale, within 2–3 metres.

In general, the species appears to be a strong interspecific and weakintraspecific competitor (Kovács 2007, Trémolières et al. 2009). The gap patternwithin the stand is dynamic, and is primarily self-organised. The study of thispattern genesis is an exciting subject for future research.

CONCLUSIONS

Allium ursinum is specific compared to most of the dominant clonal plantsin the herb layer of temperate woodlands for three reasons. 1) Its biomass allo-cation into sexual reproduction is unusually high among woodland peren-nials. 2) Vegetative reproduction is subordinate in terms of biomass allocation,and contributes relatively little to recruitment and dispersal. 3) The lifespan ofthe interconnections between ramets is extremely short. Individual ramets canlive up to 8–10 years, while the lifespan of mother-daughter connections is lessthan a year. Therefore, the species is a genet splitter.

This combination of traits is unique among those clonal plants that havebeen described to have a tendency for monodominance. One of the described



strategies is the “consolidation strategy”, which is characterised by extensivelateral spreading by rhizomes or other means of horizontal growth, strong andpermanent physiological integration among the ramets, and consequently, arather strict intraclonal control over the birth of new shoots, and the growth ofexisting shoots (de Kroon and Schieving 1990). Species with this combinationof traits can be found in woodlands as well as in other habitats (e.g. Brachy-podium pinnatum, Solidago canadensis, Urtica dioica). A common feature in thegrowth pattern is monopolizing space by relatively large and even spacingamong the shoots.

Another strategy, which tends to be locally monodominant is character-ised by an extremely dense packing of the shoots. This is the “phalanx” growthstrategy (Lovett Doust and Lovett Doust 1982, Schmid 1986). A necessary con-dition for dense packing is low intra-genet competition, which has been as-sumed to be achieved by a permanent physiological integration among ramets(Klimeš 2008, Pitelka and Ashmun 1985). Tussock-forming grasses are typicalexamples for this strategy, but dicotyledonous species can also be found (e.g.Bellis perennis; Schmid 1986). The patches of these are usually smaller than thepatches of “consolidators” of similar age, because the mother-daughters dis-tances are typically shorter.

Allium ursinum clearly represents a third way of monopolizing space.Physiological integration is neither extensive nor permanent. In contrast withthe aforementioned two strategies, the pattern of space occupancy is notfrozen, but is dynamically changing. Most of the birth events are due to sexualreproduction; vegetative reproduction only complements this. So, the popula-tion dynamics is essentially dominated by local, independent events.

In the other strategies, monodominance was achieved by a genet-levelregulation. Due to a competition between genets, rather low genetic diversitycan be expected on the spatial scale of patches (unless genets can intermingleby long runners; see Whigham 2004). In A. ursinum, the genet-level regulationis insignificant (short-distance and temporary); each patch can be expected tobe a fine-scale mosaic of different genets. Monodominance is achieved by ahigh tolerance of the seedlings to the presence of adults, which permits the co-existence of several generations in high densities. Even a tendency for facilita-tion between genets has been demonstrated. This effect is probably more sig-nificant in drier habitats, where increasing the soil moisture, and protectionfrom direct sunlight are likely to increase the survival rate of seedlings and ju-veniles. Facilitation of a competitor genet is probably disadvantageous for theadult, but most the facilitative effect is a natural concomitant of the plant’spresence (e.g. shading), or physiological functioning (e.g. transpiration), so,the potential for evolutionary changes is probably limited. In addition, a highproportion of the seedlings in the neighbourhood of an adult is likely to be itsown offspring because of the short dispersal distance.



Altogether, A. ursinum has a definite, hitherto non-described strategy formonopolizing space. We suggest to call this strategy “Clan-of-Clones” to ex-press the importance of facilitation between kins, which is complemented byan opportunity for clonal reproduction. The Clan-of-Clones strategy has thefollowing attributes. 1) Most of the seeds are dispersed close to the parent. 2)Seedling establishment is facilitated by the surrounding adults. 3) Allocationto vegetative reproduction is relatively small; its main role is to prolong localpersistence. 4) The genet is not integrated physiologically, except for a tran-sient connection between parent and offspring. It would be interesting to findother examples for this strategy, testing the aforementioned traits. Criteria1)–3) are coherent in the sense that their co-occurrence can be hypothesised tofacilitate monodominance. Criterion 4) is certainly applicable to A. ursinum,but its generality is questionable (see a model on the adaptive advantage ofphysiological integration: Oborny and Kun (2003)). If further studies on morespecies do not confirm its correlation with 1)–3), then 4) can be omitted fromthe criteria.

A. ursinum is an important species in the understorey of several mesic for-ests across Europe. Due to its low intraspecific and high interspecific competi-tion, it can reduce plant species diversity over large areas (cf. Grime et al. 1998,Kovács 2007). But some indirect effects, which increase species diversity, havealso been described. Ernst (1979) summarises that A. ursinum can significantlyimprove the soil’s nutrient budget by lessening the run-off in spring, and accu-mulating a nitrate pool, which becomes later available for summer-greenplants (see also Whigham (2004) for a general review about forest understoreyherbs, and Trémolières et al. (2009), for a detailed study in three A. ursinumpopulations). By the time these species become active, A. ursinum starts its dor-mancy. Jandl et al. (1997) adds that decomposing A. ursinum leaves in earlysummer provide nitrogen-rich forage for the grazing mesofauna, especiallyfor collembolas. This accelerates litter fragmentation, and creates favourableconditions for microorganisms, enhancing the rate of mineralisation, and therelease of nutrients. A. ursinum, as a dominant understorey species, is an im-portant factor in the nutrient economy of many forests. Understanding its be-haviour over a range of different spatial and temporal scales is, therefore, achallenging matter of research.

*

Acknowledgements – We are grateful to Gábor Fekete, Attila J. Kovács, and Wilfried H.O. Ernst for reviewing earlier versions of the manuscript. Jitka Klimešová also helped us byvaluable comments and by a summary about the below-ground morphology and develop-ment in this species; we greatly appreciate her contribution to the section “Vegetative re-production”. The research was subsidised by the Hungarian Scientific Research Fund(OTKA grant no. K-61534).



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APPENDIXStudy sites in the references

We briefly describe the sites where the studies cited in this review hadbeen conducted. Many characteristics, especially those that are related tophenology or demography, may strongly depend on the local conditions.

Ernst (1979) conducted his study in a beech wood on calcareous soil andin a mixed Carpinus-Fagus woodland on a pseudo-gley soil in NW Germany. Aplateau, a north-facing, and a south-facing slope were studied. Eggert (1992)also studied the species in a beech wood on calcareous soil in NW Germany.Rychnovská and Bednář (1998) worked in a floodplain forest (Ficario-Ulmetumtypicum) in the Czech Republic. Trémolières et al. (2009) compared populationsin alluvial forests with frequent vs. infrequent flooding in eastern France. Ourstudy (Morschhauser et al. 2009) was conducted in an oak-hornbeam forestgrowing on brown forest soil with clay illuviation in S Hungary. Kevey andCzimber (1982) observed the occurrences of A. ursinum over a broad area, infloodplain forests in NW Hungary. Kovács (2007) also investigated the occur-rence over a broad geographic region, in the nemoral and boreal belt in theEastern Carpathians and in the eastern part of the Transylvanian Basin (inmountain beech forests, hornbeam-beech woods, riparian alder woods, andother forest types). Grime et al. (1988), Kevey (1977), Klimešová and Klimeš(2006), and Tutin (1957) summarised data from the literature from all over Eu-rope. Bierzychudek’s (1982) and Whigham’s (2004) papers are general reviewsabout shade-tolerant forest herbs from various places in the temperate zone ofthe Northern Hemisphere.



Population ecology of Allium ursinum, a space-monopolizing clonal plant

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