The European bison as seed dispersers: the effecton the species composition of a disturbed pineforest community

Bogdan Jaroszewicz, Ewa Piroznikow, and Ruth Sagehorn

Abstract: We studied the process of change in plant species composition in a pine–spruce forest influenced by endo-zoochorous seed dispersal by the European bison Bison bonasus L. The intensity of endozoochory was 3.4 times higher inthe open tree stand than in the surrounding undisturbed forest (t = –3.0836, df = 50, P = 0.003). Over 1578 individuals/ramets belonging to 23 vascular plant taxa developed on 114 bison dung piles. The process of colonization includedtwo plant species that have never before been recorded in the studied forest community. Seven out of 14 speciestransferred by bison were small-seeded herbaceous plants without morphological adaptations for long-distance dispersal.The majority of plant species recorded on the bison dung (55.9%) occur in deciduous forests. In contrast, over 50%of the plants surrounding bison faeces represented species of coniferous forests. The PCA analysis revealed the exis-tence of two distinct groups of plant species: within bison faeces and on random systematic samples. The Jaccard co-efficient of species composition similarity between them was 0.28. Our results demonstrate that the European bison isan effective vector of plant propagules between plant communities. This fact could have great importance for the re-storation of degraded habitats, and could also introduce the risk of invasion by alien species.

Key words: Białowieza forest, Bison bonasus, Central Europe, endozoochory, forest clearings, vegetation changes.

Resume : Les auteurs ont etudie le processus du changement de la composition en especes vegetales dans une foret de pinset epinettes, influence par une dispersion endozoochore de graines, par le bison europeen, Bison bonasus L. On observeune intensite de l’endozoochorie 3,4 fois superieure dans les peuplements forestiers ouverts comparativement aux peuple-ments forestiers non perturbes (t = –3,0836; df = 50; p = 0,003). Plus de 1578 individus ou rametes appartenant a 23 taxonsde plantes vasculaires se sont developpes sur 114 bouses de bison. Le processus de colonisation inclut deux especes deplantes jamais observees auparavant dans la communaute forestiere etudiee. Sept des 14 especes transferees par le bison re-presentent des plantes herbacees a petites graines depourvues d’adaptation morphologique pour la dispersion a longue dis-tance. La majorite des especes de plantes retrouvees sur les bouses de bison (55.9 %) se retrouvent dans des foretsdecidues, Reciproquement, plus de 50 % des especes venant sur bouses de bisons representent des especes poussant en fo-rets coniferiennes. L’analyse PCA revele l’existence de deux groupes distincts de plantes : echantillons sur bouses de bisonset echantillons preleves systematiquement au hasard. Entre ces deux groupes, on observe un coefficient de Jacquard de0,28, pour la similarite de la composition en especes. Les resultats demontrent que le bison europeen constitue un vecteurefficace pour les propagules des plantes entre les communautes vegetales. Ceci pourrait avoir beaucoup d’importance pourla restauration des habitats degrades, et pourrait egalement comporter un risque d’invasion par des especes adventices.

Mots-cles : Foret de Bialowieza, Bison bonasus, Europe centrale, endozoochorie, coupes forestieres, changements de vege-tation.

[Traduit par la Redaction]

Introduction

Large herbivorous mammals exert an influence on vegeta-tion as they eat plants; limit their opportunities to regener-ate, and transport their propagules within and between plantcommunities (e.g., Falinski 1986; Olff and Ritchie 1998).The significance of endozoochory for the diversity of flora

and vegetation has been the subject of many studies (e.g.,Welch 1985; Malo and Suarez 1995; Pakeman et al. 2002;Bakker and Olff 2003; Cosyns 2004), but what subsequentlyhappens to the dispersed seeds is rarely addressed. Neverthe-less, the endo- and epi-zoochoric transfer of plant propa-gules is identified as a tool in nature conservation (Fischeret al. 1996; Zobel et al. 1998; Cosyns 2004), and as a poten-tial cause of biological invasions (e.g., Campbell and Gibson2001; Constible et al. 2005; Mouissie et al. 2005). Such in-vasions are considered to be among the most serious threatsto the integrity of natural ecosystems, as incursions by plantspecies not naturally occurring may lead to temporary oreven permanent changes in ecosystem structure and func-tioning (Mack et al. 2000; With 2002).

The European bison Bison bonasus L., the largest of theEuropean hoofed mammals, became extinct in the wild in

Received 30 October 2007. Published on the NRC ResearchPress Web site at botany.nrc.ca on 11 April 2008.

B. Jaroszewicz1 and R. Sagehorn. Białowieza GeobotanicalStation, University of Warsaw, Sportowa 19, 17-230 Białowieza,Poland.E. Piroznikow. Institute of Biology, University of Białystok,Swierkowa 20B, 15-950 Białystok, Poland.

1Corresponding author (e-mail: b.jaroszewicz@uw.edu.pl).

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1919 (Pucek et al. 2002). Today, it inhabits a few sites inCentral and Eastern Europe, where it was reintroduced.Bison feed mostly on grasses and herbs, preferably in forestclearings, while resting in the forests (Gebczynska et al.1991; Krasinska and Krasinski 2004). Studies on their im-pact on vegetation are scarce, but very important, as they in-crease our knowledge of European natural vegetationdynamics. The European bison may have played an impor-tant role in shaping the mosaic of forest and grassland eco-systems in the past.

Dung deposition by animals could be a seed source lead-ing to the establishment of new plant species, as well as newcohorts of species already present in the area (e.g., Welch1985; Malo and Suarez 1995; Stender et al. 1997; Bonn andPoschlod 1998; Dai 2000). It could also create safe germina-tion places for seeds (Cosyns et al. 2006), as well as influ-ence vegetation indirectly by the fertilization of soil (Boniset al. 1997; Dai 2000). Forest ungulates, such as red deerCervus elaphus L. (Europe) or white-tailed deer Odocoileusvirginianus Zimm. (North America) are efficient endo-zoochoric vectors of various plants that are more typical ofopen spaces (e.g., Gill and Beardall 2001; Heinken et al.2002; Myers et al. 2004; Mouissie et al. 2005; von Oheimbet al. 2005). By the same token, the European bison mayplay a major role in endozoochoric plant dispersal withinand between ecosystems. However, while Gebczynska et al.(1991) demonstrated how 376 vascular plant species formpart of the species’ diet, there are no data on how many ofthese the animal disseminates endozoochorically. Europeanbison are known for their selective utilization of forest com-munities in obtaining food during different seasons of theyear (Krasinska et al. 1987). They also require regular ac-cess to water, and so move frequently from grazing sites toareas in which they may drink (Krasinska and Krasinski2004). In so doing, they pass through plant communitiespresent en route, simultaneously engaging in the endo- andepi-zoochoric transport of plant propagules between plantcommunities. The only closely related animals to have beenstudied in Europe, regarding their role in plant dispersal, aredomestic cattle Bos taurus s. str. (L.). Seeds of numerousplant species may germinate after having first passed alongthe gastrointestinal tract of cattle (Cosyns 2004; Cosyns etal. 2005).

Pakeman (2001) and Myers et al. (2004) look upon endo-zoochory mediated by large herbivores as the most likelymechanism accounting for the migrations of herbaceous spe-cies. We took the idea further by envisaging its capacity tochange the species composition of disturbed plant commun-ities. The cyclic disintegration of forest stands is a part ofthe natural pine–spruce forest life cycle. Disturbances wereconsidered the main factor shaping the spatial and age struc-ture of natural forests in the past (Falinski 1986). Ruminantsmay play an important role in changing forest communitiesby transporting propagules of light-demanding plants fromold clearings to sites newly open for colonization.

On the basis of our observations of plant seedlings devel-oping on bison dung left in pine–spruce forest of natural ori-gin, we hypothesized that bison endozoochory can accountfor the presence of plant species that are not normally foundin the forest floor vegetation of this community. This studyaims to extend our knowledge of plant species that can take

advantage of endozoochory by studying (i) the diversity andabundance of plant species developing on bison dung;(ii) new plant species supplied to forest vegetation by theEuropean bison; and (iii) the intensity of the endozoochorycaused by the European bison.

Materials and methods

Study areaWe carried out our study in the central part of Białowieza

National Park (52845’53@N, 23851’39@E in northeast Poland,on the border with Belarus; Fig. 1), which is managedmainly for wilderness protection, and where all elements ofnature are stringently protected: interference in the course ofnatural processes within the protected ecosystems is prohib-ited, and access to the area is limited by National Park regu-lations. The area represents the best-preserved forestecosystem of its kind anywhere in continental Europe.Białowieza’s old growth forests consist of Quercus robur L.,Carpinus betulus L., and Tilia cordata Miller on fertile andmoderately moist soils; Pinus sylvestris L. and Picea abies(L.) Karsten on poorer and drier soils; and Alnus glutinosa(L.) Gaertn. and Fraxinus excelsior L. on wet soils. Theresearch was carried out in a unique relict ecosystem withvery high biodiversity (Gutowski and Jaroszewicz 2001;Falinski 2003) and under conditions of minimal human in-fluence. The vegetation and flora of the study plot — thebackground of our study — have previously been investi-gated by Rijken (1976), and Falinski and Mułenko (1997).

The Polish part of Białowieza Forest (BF) is inhabited bya free-roaming population of 402 European bison. The re-gion of the study plot is utilized on a regular basis by onegroup of bison (10–20 cows and their offspring) and a fewsolitary bulls (Krasinska and Krasinski 1997).

We selected subcontinental pine–spruce forest for thisstudy on account of its being a species-poor yet characteris-tic type of vegetation. This ensures that any intrusion of newplant species into the community is easily detected and pin-pointed. The forest community at the study site consists ofPinus sylvestris and Picea abies, with some Betula pendulaRoth and Betula pubescens Ehrh. in the tree stand. The for-est floor vegetation, according to earlier studies (Rijken1976; Falinski and Mułenko 1997), includes Vaccinium myr-tillus L., Vaccinium vitis-idaea L., and Calluna vulgaris (L.)Hull, with less frequent Chamaecytisus ruthenicus (Fischerex Wołoszczak) A. Klaskova, Orthilia secunda (L.) House,Chimaphila umbellata (L.) W. Barton, Lycopodium clavatumL., and Lycopodium annotinum L. and, very sparsely, Trifo-lium lupinaster L., Goodyera repens (L.) R. Br., Peuceda-num oreoselinum (L.) Moench, Scorzonera humilis L.,Convallaria majalis L., Solidago virgaurea L., Polygonatumodoratum (Miller) Druce, Hieracium pilosella L., Veronicaofficinalis L., Fragaria vesca L., and Calamagrostis arundi-nacea (L.) Roth. The moss layer, which covers the forestfloor, is dominated by Hylocomium splendens (Hedw.)B.S.G., Pleurozium schreberi (Brid.) Mitt., Dicranum poly-setum Sw., and Ptilium crista-castrensis (Hedw.) De Not.with an admixture of some other species (Rijken 1976;Falinski 1986; Falinski and Mułenko 1997).

The forest stand in the study site experienced disintegra-tion following the infestation of spruce by the bark beetle

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Ips typographus (L.), in the aftermath of the 2000 drought.The result has been the near-total mortality of spruce trees(Keczynski 2002). The dead trees were downed by gales be-tween autumn 2005 and summer 2006.

MethodsWe conducted our study in an approximately 28 ha patch

of subcontinental pine–spruce forest (Fig. 1). Detailed map-ping of faeces distribution, the counting of plants and esti-mation of species abundance were carried out in August2007 in the fragment of forest characterized by the highestrate of spruce mortality. At the chosen study plot (100 m �100 m) we expected to observe the most intensive bison ac-tivity as it had the most open space in this forest fragment.

We counted all individual plants/ramets within the limitsof each faecal pat to check which plant species are endozoo-chorically dispersed by bison. We also counted plantindividuals/ramets within the limits of circular spots thatshowed a species composition different from the surround-ing area. The area of these plant aggregations was roughlythe same as the area of bison faeces (approximately 20–40 cm in diameter), and their species composition was nottypical for pine–spruce forests. We hypothesized that theseplant aggregations are of endozoochorous origin and thatthey are latter developmental stages of plants emergingfrom bison faeces. Plants were classified as developmentalphases of seedling, juvenile, vegetative, or generative, as de-fined by Gatsuk et al. (1980), to estimate which species are

able to pass through the full life cycle in the new habitat andproduce the next generation of propagules. To keep recordsof colonization success, we classified bison faeces and plantaggregations into four classes: a, faeces without any plants;b, faeces with seedlings only; g, faeces with seedlings, juve-nile, vegetative, and (or) generative ramets; d, a compactplant aggregation formed by at least two species not typicalfor pine forests, with no visible traces of dung as a substra-tum.

To discover differences between the vegetation surround-ing the bison faeces and in randomly selected places, wecarried out a floristic survey and estimated plant abundanceusing the Braun-Blanquet scale (Braun-Blanquet 1951; Dier-schke 1994). In the southwestern quarter of the study plot,we set a random sample of 30 pairs of concentric circles ina 10 m � 10 m grid. The radius of each smaller concentriccircle was equal to our measurement of the mean radius ofbison faeces on the study plot (i.e., 29.56 cm). The radiusof the larger concentric circle was 1.00 m. We carried outfloristic surveys and plant abundance estimates within largercircles, as well as within a 1.00 m radius of the centre of 28bison dung piles at the southwestern quarter of the studyplot. Inside each smaller circle we counted and classifiedplants according to the same method as on bison dung. Floraand plant abundance were compared between circles. Floragrowing on bison dung piles were compared to flora insidethe smaller concentric circles.

We counted bison dung piles on 26 subplots (10 m �

Fig. 1. The study plot (filled square) within Białowieza National Park (northeast Poland). Distribution of forest types after Falinski andMułenko (1997).

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10 m) scattered randomly over the whole patch of this pine–spruce forest community (1 subplot /1 ha of the forest onaverage) with the aim of estimating the intensity of endo-zoochory caused by the European bison in the forest sur-rounding the study plot. This intensity of endozoochory wascompared with that at the study plot. Plant nomenclature fol-lows Tutin et al. (1964–1980) for vascular plants and Dier-ßen (2001) for bryophytes.

Statistical analysesWe tested the randomness of the spatial distribution of bi-

son dung piles using the Mann–Whitney Rank Sum Test.The evidence of the samples’ distinction (the bison faecesvs. random sample) was obtained using two different ap-proaches. Principle component analysis (PCA) of thevariance–covariance matrix was performed on the speciescomposition and the abundance in individual samples to in-vestigate the spatial patterns of the species composition var-iation. Because the abundance data included a few verydominant taxa, we log-transformed it using the base-10 log-arithm to downweight those taxa (Hammer et al. 2001). Weused the neighbour-joining cluster analysis to find hierarchi-cal groupings in multivariate data sets of the samples. Thephylogram displaying the similarity between the sampleswas constructed using the matrix of Jaccard similarity meas-ures for presence–absence data. Statistical analyses wereconfined to plants identified to species or genus level, sincethose allocated to higher taxa were of little diagnostic value.We considered the genus name for those plants that couldonly be identified at the genus level as a ‘‘species’’, e.g.,Agrostis spp. and Carex spp. for the calculation of the Jac-card similarity coefficient. We used the PAST program(Hammer et al. 2001), version 1.58 for calculations.

ResultsWe registered 114 bison dung piles and 14 plant aggrega-

tions on the study plot. The spatial distribution of bison pilesdeparted significantly from random, with the fewest occur-ring in areas covered by fallen tree trunks (U = 7200.00;P < 0.001). The majority of these piles (68%) were in bclass, while class a and g had shares of 25% and 7%, re-spectively.

The intensity of the endozoochory caused by the Euro-pean bison on the study plot was 3.4 times higher than inthe surrounding pine–spruce forest (0.35 ± 0.6288 dung pilesper 100 m2 versus 1.20 ± 1.2583 dung piles per 100 m2).The differences were statistically significant (t = –3.0836,df = 50, P = 0.003).

Within the 29 taxa recorded on the bison dung, and withinthe limits of plant aggregations, 17 were of endozoochorousorigin and five could be of anemochorous origin. The originof the rest of the taxa is uncertain as they had no adaptationsfor anemochoric dispersal but were recorded only on plantaggregations (Table 1). Six out of nine endozoochorous spe-cies common for bison dung and plant aggregations devel-oped generative ramets on the aggregations. These arepotential colonizers. Amongst them Poa nemoralis L. andVeronica chamaedrys L. had not been recorded previouslyin the study area. The Jaccard similarity of plant speciescomposition within the limits of plant aggregations and

within bison dung was 0.42 and 0.27 in the case of plant ag-gregations compared to the surrounding vegetation (Fig. 2).

We noted 1578 plant individuals/ramets belonging to 23taxa, and one ‘‘dicotyledonous seedling group’’ (seedlingswith two visible cotyledons) within 114 bison dung piles.The majority of the plants (1425) were in the seedlingphase, compared with 147 and 6 in the juvenile and vegeta-tive phases, respectively (Table 1; Fig. 2). Only 42 plant in-dividuals out of 779 recorded within 14 plant aggregationswere in the seedling phase, while the majority (413) werein the vegetative phase (Table 1; Fig. 2).

The most abundant species occurring on bison dung wasUrtica dioica L. — represented by 659 ramets. Between 1and 72 ramets of this species were noted for each dung pile,with the majority being seedlings (542 individuals). Therewas also an abundance of Betula sp. seedlings (461), whichwere probably of anemochorous origin. The seeds of fivetaxa found on bison dung show morphologic adaptations al-lowing airborne transport over long distances. As we are un-able to prove their endozoochoric origin, they wereclassified as anemochorous (Table 1).

We identified, at species level, 836 individuals/ramets of17 species growing on bison dung. Two of these specieshad not been recorded previously in the whole patch of thepine–spruce forest, and another four had previously been re-corded in fewer than five locations (Table 1). Four speciesrepresented by 11.9% of individuals/ramets identified at spe-cies level belonged to the vegetation of the surrounding sub-continental pine–spruce forest: Calamagrostis arundinacea,Luzula pilosa (L.) Willd., Vaccinium myrtillus, and V. vitis-idaea. Six species were characteristic of broadleaved forestson mineral soils: Geranium robertianum L., Lamiastrum ga-leobdolon (L.) Ehrend. Polatschek, Milium effusum L., Poanemoralis, Stellaria nemorum (L.), and Urtica dioica. Theseaccounted for 80.51% of the individuals/ramets identified atspecies level. Other species reported in the samples weretypical of nonforest plant communities, clear-cut forestareas, and clearings in tree stands (Fig. 2). Seven out of 14species transferred by bison were small-seeded herbaceousplants without any specific adaptations for long-distance dis-persal (Table 1).

The floristic survey in the southwestern quarter of thestudy plot recorded 24 taxa of vascular plants within circles(radius of 1 m) with bison faeces in the centre, and 37 taxawithin larger circles of the random sample. The principlecomponent analysis (PCA) of data collected within thesecircles did not result in a significant difference. This indi-cates that plant species composition and abundance betweenthe random samples and in the immediate vicinity of the bi-son faeces are similar.

Plants assigned to 14 taxa were growing within the limitsof the bison faeces at the southwestern quarter of the studyplot, and only 9 taxa grew within the smaller circles of therandom sample. Five taxa were common for both series(Table 2). The Jaccard similarity coefficient of the plant spe-cies composition was 0.28. All but one species, (Galiumodoratum (L.) Scop.), growing within the random sampleswere typical of pine–spruce forest communities or were typ-ical colonizers of clear-cut forest areas. Species adapted toanemochorous (four) and epizoochorous (three) seed disper-sal dominated in the random sample. In contrast, 5 out of 10

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Table 1. Plant species recorded on the dung of European bison and within plant aggregations, breakdown by classes of faeces (b, with seedlings only; g, with plants in various devel-opmental stages; d, aggregation of plants without traces of dung) and developmental stages (S, seedlings; J, juveniles; V, vegetative; G, generative).

b g d

Species S J V G S J V G S J V G Total

On bison dung, endozoochorous originRubus idaeus 42 0 0 0 0 0 0 0 0 0 0 0 42Luzula pilosa 3 0 0 0 0 0 0 0 0 0 0 0 3Geranium robertianum 3 0 0 0 0 0 0 0 0 0 0 0 3Lamiastrum galeobdolonb,c 1 0 0 0 0 0 0 0 0 0 0 0 1Vaccinium vitis-idaea 4 0 0 0 79 0 0 0 0 0 0 0 83Stellaria mediab,c 2 0 0 0 4 8 0 0 0 0 0 0 14Ranunculus sp. 3 0 0 0 1 1 0 0 0 0 0 0 5Agrostis sp. 0 0 0 0 0 2 0 0 0 0 0 0 2

On bison dung and within plant aggregations, endozoochorous originUrtica dioicac 435 0 0 0 107 114 3 0 12 87 43 7 808Milium effusumc 2 0 0 0 0 1 0 0 0 14 154 20 191Deschampsia flexuosa 4 0 0 0 0 1 0 0 0 6 73 0 84Carex sp. 2 0 0 0 5 1 0 0 0 12 17 0 37Vaccinium myrtillus 7 0 0 0 3 3 0 0 2 15 6 0 36Stellaria nemorumb,c 1 0 0 0 0 0 1 0 0 0 0 3 5Poa nemoralisa,c 0 0 0 0 0 1 0 0 0 0 50 34 85Calamagrostis arundinacea 0 0 0 0 0 0 1 0 0 3 14 5 23Veronica chamaedrysa,c 0 0 0 0 0 1 0 0 0 2 11 1 15

On plant aggregations, origin uncertainLapsana communisa 0 0 0 0 0 0 0 0 0 91 9 0 100Veronica officinalisc 0 0 0 0 0 0 0 0 0 8 6 1 15Deschampsia cespitosab 0 0 0 0 0 0 0 0 0 0 12 1 13Festuca giganteab 0 0 0 0 0 0 0 0 0 0 5 2 7Carex remotab 0 0 0 0 0 0 0 0 0 0 3 0 3Cerastium fontanuma,c 0 0 0 0 0 0 0 0 0 0 1 0 1Myosotis scorpioidesa,c 0 0 0 0 0 0 0 0 0 0 1 0 1

On bison dung, anemochorous originTaraxacum officinaleb 0 0 0 0 0 1 0 0 0 0 0 0 1Mycelis muralis 0 0 0 0 1 1 1 0 0 0 0 0 3Epilobium angustifolium 0 0 0 0 0 1 0 0 1 0 0 0 2Epilobium sp. 3 0 0 0 0 0 0 0 0 12 0 0 15Betula sp. 261 0 0 0 200 0 0 0 27 0 0 0 488

Not classifiedPoaceae 155 0 0 0 72 5 0 0 0 0 8 0 240Dicotyledonous seedlings 23 0 0 0 2 6 0 0 0 0 0 0 31Total 951 0 0 0 474 147 6 0 42 250 413 74 2357

aNot recorded previously at the studied 28 ha patch of pine–spruce forest.bRecorded previously on less than five spots at the studied patch of pine–spruce forest.cHerbaceous plants without morphologic adaptations for long-distance dispersal.

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species recorded on the bison faeces were those with smallseeds and no specific adaptations for long-distance dispersal(Table 2). The PCA of data collected within smaller circlesand on bison dung showed a clear separation of both serieson PC1 with two principle components explaining 47.73%of the total species diversity (Fig. 3). Axis 1 was highly neg-atively correlated (loading: –0.78) with an abundance ofVaccinium myrtillus, a species typical of poor coniferousforests on acid soils, and positively (0.41) with Urtica dio-ica, a species typical of fertile deciduous forests and ruderalsites. The presence of V. myrtillus is the main factor causingthe separation of samples on PCA axis1. This result wassupported by the phylogram showing the clustering of thewhole data into two clearly separated branches: the one de-rived almost exclusively from bison faeces, and the secondalmost exclusively from random samples (Fig. 4). Bisondung piles of a class and the random samples with no plantsgrowing on them were excluded from this analysis.

DiscussionThe European bison is an able propagule vector of 17

plant taxa. The PCA analysis revealed the existence of twodistinct groups of plant species: (i) within the bison faecesand (ii) on the random, systematic samples of forest floorvegetation. The species composition of plants growing onbison faeces was significantly different from the surroundingvegetation of the pine–spruce forest, while vegetation inclose proximity to the faeces did not differ significantlyfrom the surrounding forest vegetation. Dung deposition re-sulted in an increase of species richness over the wholepatch of the pine–spruce forest by introducing new speciesnot recorded previously at the site. Close to 25% of all plantspecies recorded on bison dung piles had not been previ-ously registered at all in this plant community, or registeredwithin its limits on fewer than five spots (Table 1; Falinskiand Mułenko 1997). Three anemochorous species had not

been registered previously at the site. However, their originis uncertain. It is possible that they use the surface of bisonfaeces as microdisturbances of ground vegetation, allowingtheir establishment, as was shown for the faeces of domesticcattle by Cosyns (2004). Large and small scale disturbancessupply uncolonized ecological niches that plants may oc-cupy (Masters and Sheley 2001).

Germination of seeds does not denote permanent coloni-zation, which depends on various local environmental fac-tors, such as the number of available seeds, changes in thechemical properties of soil as dung decomposes, tree standregeneration, and competition with plants residing in thecommunity. Campbell and Gibson (2001) reported thatwhile numerous species native and alien to Illinois (USA)germinate in situ in horse dung, only a few of these alsogrow in the immediate vicinity. We observed that individu-als of 43% of the species growing on bison dung producedgenerative stems in multispecies plant aggregations growingat the study plot. Out of these, three species were not plantstypical of the surrounding forest and were rare or absentfrom the area prior to forest disintegration. There is no proofthat the observed plant aggregations resulted from seeds dis-persed in bison dung, although their species composition issimilar to plant species composition growing within the lim-its of the bison dung, and both are different from the sur-rounding vegetation. The success of plants transferred bybison can be checked by studying the relative contributionto later generations of the plants developing on the bisonfaeces compared to the contribution of the plants from seedsdispersed by other natural modes in this habitat. Thus farthere are no long-term data permitting an assessment of thepersistence of the observed process in situ. It may be anephemeral phenomenon, curtailed inevitably by changesconnected with the forest stand life-cycle or the initiation oflong-term change in forest vegetation.

The intensity of the endozoochory measured by the num-ber of bison dung piles per hectare was several times higherin the strongly disturbed area (the study plot) in comparisonwith the surrounding forest with lower tree mortality. A sim-ilar direct correlation between the appearance of open spacesin the middle of the forest (due to logging) and red deermediated dispersal of plants was reported by Gill and Beard-all (2001). As such habitats are comparatively small andephemeral, colonizing plants need a vector allowing disper-sal: via wind, water, or animal. In our opinion, the prefer-ence for open areas as feeding sites shown by bison(Krasinska et al. 1987; Krasinska and Krasinski 1997, 2004)provides additional support for the hypothesis that they playan important role in plant dispersal, as they not only fre-quent such sites, but they also enrich their flora by zoochoryand maintain plant habitat, moderating forest succession bygrazing, trampling, wallowing and other behavioral activ-ities.

The results obtained here show that European bison trans-fer the seeds of numerous plant species within and betweenforest ecosystems. The highest intensity of this transfer wasobserved at a site newly opened for plant colonization — atarget habitat for light-demanding plants. This process par-ticularly included herbaceous plants with no specific disper-sal adaptations except the small size of their seeds. The onlyway to account for their capacity to rapidly recolonize

Fig. 2. The percentage share of plant individuals/ramets in the de-velopmental phases registered within the limits of (a) bison dung,(b) plant aggregations, and (c) random samples on the study plot inBiałowieza National Park, northeast Poland.

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Table 2. Plant species recorded on European bison faeces (mean diameter 29.56 ± 9. 17 cm)and random samples (circles with diameter 29.56 cm) at the southwestern quarter of thestudy plot in Białowieza National Park, northeast Poland.

Plant species

Found in random samplesFound in random samplesand bison faeces Found in bison faeces

Lack of dispersal mechanisms— — Milium effusum— — Poa nemoralis— — Stellaria media— — Urtica dioica— — Veronica chamaedrys

Endozoochorous— Rubus idaeus —— Vaccinium myrtillus —

EpizoochorousCalamagrostis arundinacea Deschampsia flexuosa Agrostis spp.Galium odoratum — —

AnemochorousEpilobium angustifolium Betula sp. Mycelis muralisPicea abies Epilobium sp. —

Autochorous— — Geranium robertianum

Not classified— — Carex sp.

Total no. of taxa:4 5 9

Note: Species are grouped according to morphological traits.

Fig. 3. The PCA plot showing the differences in the species composition of plants among two groups of samples: within bison faeces (tri-angles) and within the random sample – circles with radius of 29.56 cm (squares). The two principal components used in this plot (PC1 andPC2) account for 47.73% of the total species diversity.

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niches that arise locally (such as newly created open spacein old-growth forests) is by reference to animal-mediateddispersal (Janzen 1984; Pakeman 2001). Consumption ofseeds and their subsequent deposition in the faeces of bisonoffers such a mechanism for many plant species that areclassically recognized as lacking specific dispersal agents.They have nothing to offer potential consumers except theirfoliage, which plays the role of attractive fruit as hypothe-sized by Janzen (1984). The observed phenomenon is thusone of the fundamental ecological processes ensuring thetemporal and spatial persistence of the plant species in a di-verse forest ecosystem. It illustrates the importance of openareas for the conservation of the European bison and the im-portance of the European bison for maintaining high plantspecies diversity at the open areas inside the forest.

The process of the long-distance transfer of plant propa-gules is favoured by the considerable amount of time re-quired for matter to pass along the species’ entiregastrointestinal tract. An experiment by Gill (1967) con-firmed that dye added to food only finally disappeared frombison dung some 8–14 d after that food had been provided.In effect, bison wandering within the home range of theirsocial group and (or) towards drinking places transfer seedsover distances of many kilometres.

Ecosystem management implicationsWe found the European bison to be an important factor

influencing plant species composition in disturbed foresthabitats. Bison-mediated seed dispersal led to the establish-ment of plant species not recorded at the site previously, aswell as to the increase of some other species’ abundance.According to Willems and Huijsmans (1994), Pakeman et

al. (1998) and Dai (2000) up to 90% of viable seeds fromdung serves to replenish the soil seed bank, extending theinfluence of endozoochorous seed dispersal for the future.This could play an important role in the restoration of de-graded habitats.

In our opinion, endozoochory by the European bison alsorisks causing the dissemination of alien species. In Biało-wieza Forest, bison are fed during winter on hay broughtfrom outside the forest complex. Further studies on speciescomposition, and the rates of plant establishment from seedscontained in bisons’ dung in winter will estimate the riskposed by this process. However, it is recommended that forthe feeding of animals in protected areas, only fodder pre-pared within the area or in the immediate proximity of thearea is used. Alternatively, forest administrators may be in-terested in introducing species from outside the forest, andthis process could be used as a way of plant reintroductionthrough fodder given to animals.

AcknowledgementsWe thank Alicja Wiktoruk for help in preparing materials

for publication. The manuscript was constructively criticizedby Anna J. Kwiatkowska-Falinska, Matt Hayward, EricCosyns, and an anonymous reviewer. The scientific work re-ceived support from the 2006/2008 Polish science budgetwithin the framework of project no. 2 P04F 035 30.

ReferencesBakker, E.S., and Olff, H. 2003. The impact of different-sized

herbivores on recruitment opportunities for subordinate herbs ingrasslands. J. Veg. Sci. 14: 465–474. doi:10.1658/1100-9233(2003)014[0465:IODHOR]2.0.CO;2.

Fig. 4. Dendrogram showing the relations of plant species composition among bison dung (s1–s22) and the circles (radius of 29.56 cm) ofthe random sample (r1–r25).

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Bonis, A., Grubb, P.J., and Coomes, D.A. 1997. Requirements ofgap-demanding species in chalk grassland: reduction of rootcompetition versus nutrient enrichment by animals. J. Ecol. 85:625–633. doi:10.2307/2960533.

Bonn, S., and Poschlod, P. 1998. Ausbreitungsbiologie der PflanzenMitteleuropas. Quelle and Meyer Verlag, Wiesbaden, Germany.

Braun-Blanquet, J. 1951. Pflanzensoziologie. Grundzuge derVegetationskunde. Springer, Wien, Austria.

Campbell, J.E., and Gibson, D.J. 2001. The effect of seeds of exoticspecies transported via horse dung on vegetation along trail cor-ridors. Plant Ecol. 157: 23–35. doi:10.1023/A:1013751615636.

Constible, J.M., Sweitzer, R.A., Van Vuren, D.H., Schuyler, P.T.,and Knapp, D.A. 2005. Dispersal of non-native plants by intro-duced bison in an island ecosystem. Biol. Invasions, 7: 699–709.doi:10.1007/s10530-004-5859-x.

Cosyns, E. 2004. Ungulate seed dispersal. Aspects of endozoochoryin a seminatural landscape. Institute of Nature Conservation,Brussels, Belgium.

Cosyns, E., Claerbout, S., Lamoot, I., and Hoffmann, M. 2005.Endozoochorus seed dispersal by cattle and horse in a spatiallyheterogeneous landscape. Plant Ecol. 178: 149–162. doi:10.1007/s11258-004-2846-3.

Cosyns, E., Bossuyt, B., Hoffmann, M., Vervaet, H., and Lens, L.2006. Seedling establishment after endozoochory in disturbedand undisturbed grasslands. Basic Appl. Ecol. 7: 360–369.doi:10.1016/j.baae.2005.08.007.

Dai, X. 2000. Impact of cattle dung deposition on the distributionpattern of plant species in an alvar limestone grassland. J. Veg.Sci. 11: 715–724. doi:10.2307/3236578.

Dierschke, H. 1994. Pflanzensoziologie. Grundlagen und Methoden.Verlag Eugen Ulmer, Stuttgart, Germany.

Dierßen, K. 2001. Distribution, ecological amplitude and phytoso-ciological characterisation of European bryophytes. Bryophyt.Bibl. 56: 1–289.

Falinski, J.B. 1986. Vegetation dynamics in temperate forests(ecological studies in Białowieza forest). W. Junk Publishers,Dordrecht, Netherlands.

Falinski, J.B. 2003. The Białowieza forest, a relict ecosystem inPoland and Belarus. Biodiversity — Journal of Life on Earth,4(1): 18–27.

Falinski, J.B., and Mułenko, W. (Editors). 1997. Cryptogamousplants in the forest communities of Białowieza National Park.Ecological Atlas (Project CRYPTO 4). Phytocoenosis, 9, Suppl.Cart. Geobot. 7.

Fischer, S.F., Poschlod, P., and Beinlich, B. 1996. Experimental stu-dies on the dispersal of plants and animals on sheep in calcareousgrasslands. J. Appl. Ecol. 33: 1206–1222. doi:10.2307/2404699.

Gatsuk, L.E., Smirnova, O.V., Vorontzova, L.I., Zaugolnova, L.B.,and Zhukova, L.A. 1980. Age states of plants of various growthforms: a review. J. Ecol. 68: 675–696. doi:10.2307/2259429.

Gebczynska, Z., Gebczynski, M., and Martynowicz, E. 1991. Foodeaten by free-living European bison in Białowieza Forest. ActaTheriol. 36: 307–313.

Gill, J. 1967. The physiological properties of the European Bison.Acta Theriol. 12: 349–360.

Gill, R.M.A., and Beardall, V. 2001. The impact of deer on wood-lands: The effects of browsing and seed dispersal on vegetationstructure and composition. Forestry, 74: 209–218. doi:10.1093/forestry/74.3.209.

Gutowski, J.M., and Jaroszewicz, B. (Editors). 2001. Catalogue ofthe fauna of Białowieza Primeval Forest. Instytut BadawczyLesnictwa, Warszawa, Poland.

Hammer, Ø., Harper, D.A.T., and Ryan, P.D. 2001. PAST:paleontological statistics software package for education and

data analysis [online]. Palaeontol. Electr. 4(1): 1–9. Availablefrom palaeo-electronica.org/2001_1/past/issue1_01.htm [accessed15 August 2007].

Heinken, T., Hanspach, H., Raudnitschka, D., and Schaumann, F.2002. Dispersal of vascular plants by four species of wild mam-mals in a deciduous forest in NE Germany. Phytocoenologia,32: 627–643. doi:10.1127/0340-269X/2002/0032-0627.

Janzen, D.H. 1984. Dispersal of small seeds by big herbivores: fo-liage is the fruit. Am. Nat. 123: 338–353. doi:10.1086/284208.

Keczynski, A. 2002. Wpływ kornika drukarza na drzewostany ob-szaru ochrony scisłej Białowieskiego Parku Narodowego. Kos-mos, 51: 471–474. [The effect of the spruce bark beetle on thetree stand of the strictly protected area of Białowieza NationalPark.]

Krasinska, M., and Krasinski, Z.A. 1997. Utilization of the Biało-wieza National Park by the European bison. Parki Nar. Rez.Przyr. 16: 63–77.

Krasinska, M., and Krasinski, Z.A. 2004. Zubr. Monografiaprzyrodnicza. [The European Bison. Monograph.]. AgencjaFotograficzno-Wydawnicza Hajstra, Warszawa, Poland.

Krasinska, M., Cabon-Raczynska, K., and Krasinski, Z.A. 1987.Strategy of habitat utilization by European bison in the Biało-wieza Forest. Acta Theriol. 32: 147–202.

Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M.,and Bazzaz, F.A. 2000. Biotic invasions: causes, epidemiology,global consequences, and control. Ecol. Appl. 10: 689–710.doi:10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2.

Malo, J.E., and Suarez, F. 1995. Herbivorous mammals as seed dis-persers in a Mediterranean dehesa. Oecologia, 104: 246–255.doi:10.1007/BF00328589.

Masters, R.A., and Sheley, R.L. 2001. Principles and practices formanaging rangeland invasive plants. J. Range Manage. 54: 502–517. doi:10.2307/4003579.

Mouissie, A.M., Vos, P., Verhagen, H.M., and Bakker, J.P. 2005.Endozoochory by free-ranging, large herbivores: Ecological cor-relates and perspectives for restoration. Basic Appl. Ecol. 6:547–558. doi:10.1016/j.baae.2005.03.004.

Myers, J.A., Vellend, M., Gardescu, S., and Marks, P.L. 2004. Seeddispersal by white-tailed deer: Implications for long-distance dis-persal, invasion, and migration of plants in eastern North Amer-ica. Oecologia, 139: 35–44. doi:10.1007/s00442-003-1474-2.PMID:14740288.

Olff, H., and Ritchie, M. 1998. Effects of herbivores on grasslandplant diversity. Trends Ecol. Evol. 13: 261–265. doi:10.1016/S0169-5347(98)01364-0.

Pakeman, R.J. 2001. Plant migration rates and seed dispersal me-chanisms. J. Biogeogr. 28: 795–800. doi:10.1046/j.1365-2699.2001.00581.x.

Pakeman, R.J., Attwood, J.P., and Engelen, J. 1998. Sources ofplants colonizing experimentally disturbed patches in an acidicgrassland in eastern England. J. Ecol. 86: 1032–1041. doi:10.1046/j.1365-2745.1998.00327.x.

Pakeman, R.J., Digneffe, G., and Small, J.L. 2002. Ecological corre-lates of endozoochory by herbivores. Funct. Ecol. 16: 296–304.doi:10.1046/j.1365-2435.2002.00625.x.

Pucek, Z., Belousova, I.P., Krasinska, M., Krasinski, Z.A., andOlech, W. 2002. European bison Bison bonasus: Current stateof the species and an action plan for its protection. MammalResearch Institute Polish Academy of Sciences, Białowieza,Poland.

Rijken, M. 1976. Comparison of three maps of a natural forestvegetation obtained by different methods. Phytocoenosis, 5:109–126.

Stender, S., Poschlod, P., Vauk-Henzelt, E., and Denedde, T. 1997.

Jaroszewicz et al. 483

# 2008 NRC Canada

Die Ausbreitung von Pflanzen durch Galloway-Rinder. Verhan-dlungen der Gesellschaft fur Okologie, 27: 173–180.

Tutin, T.G., Heywood, V.H., Burges, N.A., Moore, D.M., Valentine,D.H., Walters, S.M., and Webb, D.A. (Editors). 1964–1980.Flora Europaea. Vol. 1–V [online]. Cambridge UniversityPress, Cambridge, UK. Available from rbg-web2.rbge.org.uk/FE/fe.html [accessed 20 October 2007].

von Oheimb, G., Schmidt, M., Kriebitzsch, W.U., and Ellenberg,H. 2005. Dispersal of vascular plants by game in northern Ger-many. Part II: Red deer (Cervus elaphus). Eur. J. Forest Res.124: 55–65. doi:10.1007/s10342-005-0053-y.

Welch, D. 1985. Studies in the grazing of heather moorland in

north-east Scotland. IV. Seed dispersal and plant establishmentin dung. J. Appl. Ecol. 22: 416–472.

Willems, J.H., and Huijsmans, K.G.A. 1994. Vertical seed dispersalby earthworms: a quantitative approach. Ecography, 17: 124–130. doi:10.1111/j.1600-0587.1994.tb00084.x.

With, K.A. 2002. The landscape biology of invasive spread.Conserv. Biol. 16: 1192–1203. doi:10.1046/j.1523-1739.2002.01064.x.

Zobel, M., van der Maarel, E., and Dupre, C. 1998. Species pool:the concept, its determination and significance for communityrestoration. Appl. Veg. Sci. 1: 55–66. doi:10.2307/1479085.

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# 2008 NRC Canada