Endozoochory varies with ecological scale and context

Kari Anne Brathen, Victoria T. Gonzalez, Marianne Iversen, Siw Killengreen,Virve T. Ravolainen, Rolf A. Ims and Nigel G. Yoccoz

K. A. Brathen (kari.brathen@ib.uit.no), V. T. Gonzalez, M. Iversen, S. Killengreen, V. T. Ravolainen, R. A. Ims and N. G. Yoccoz,Dept of biology, Univ. of Tromsø, NO-9037 Tromsø, Norway.

Several studies on endozoochory have established large herbivores as important for seed dispersal, yet no studieshave evaluated how endozoochory is dependent on ecological scale and context. Here we address effects ofreindeer density on endozoochory in a hierarchical, multi-scale study, encompassing several ecological contexts.

We found reindeer density effects on endozoochory to vary with spatial scale. Higher reindeer densities at thelevel of landscape areas, as indexed through faeces abundance, were related to both less species and lowerabundance of emerging plants from faeces. In contrast, there was no effect of higher reindeer densities at the levelof herding districts (i.e. large scale assemblages of landscapes). Lack of consistency between scales reflectsecological hierarchy, indicating that reindeer density effects on endozoochory best matches at the scale oflandscapes.

Pasture plant composition was only partly an important ecological factor. That is, ericoid species, thedominating plants in the pastures, were also the most abundant seed plants emerging from the faeces. However,only a small proportion of herbaceous seed plant species found in the pastures were emerging from the faeces,and their emergences were positively related to the site fertility and altitude of the pasture.

Studies addressing endozoochory of ruminants are typically concerned with seed plants. In this study wefound indications of that also diaspores of ferns survive the digestive tract of large herbivores. Vascular sporeplants were even more abundant in the faeces than were vascular seed plants.

Results from this study demonstrate that reindeer may counteract a potentially negative impact on seedlimitation from their grazing by returning viable seeds in their faeces. However, in Finnmark, northern Norway,this effect is only marginal, relates only to a very few species and individuals and shows ecological scale andcontext dependence.

Large herbivores may have profound effects on thecomposition of vegetation depending on the ability ofplants to tolerate or resist grazing (Augustine andMcNaughton 1998), whereas herbivores are also ableto affect vegetation composition through the propagulepressure from endozoochory (Yamashiro and Yamashiro2006). Ungulates and other ruminants are potentiallyvery important seed dispersers via endozoochory (Welch1985, Pakeman et al. 2002, Myers et al. 2004, Changet al. 2005, Cosyns et al. 2005, Yamashiro andYamashiro 2006). Studies on endozoochory have beenmore concerned with what type of seeds that are likely tobe dispersed by endozoochory (Janzen 1984, Pakemanet al. 2002, Myers et al. 2004, Bruun and Poschlod2006), than with the variation of endozoochory in

ecological importance. However, the selective force ofthe gastrointestinal tract of ungulates can only modifywhat is available to the ungulate, which in advance hasbeen shaped by the set of ecological factors, i.e. theecological context, of where the ungulates are grazing.

The plant species pool available to the herbivoreobviously affects what species can potentially occur asseeds in faeces. Moreover, pasture plant species abun-dance correlates with the seed content of large herbivorefaeces (Cosyns and Hoffmann 2005). Still, ecologicalfactors affecting the ability of species to flower and setseed are likely to be more important. Herbivores arethemselves modifiers of flowering abundance (Ericsonand Oksanen 1987, Brathen and Oksanen 2001,Cooper and Wookey 2003) and hence seed abundance.

Ecography 30: 308�320, 2007

doi: 10.1111/j.2007.0906-7590.04976.x

Copyright # Ecography 2007, ISSN 0906-7590

Subject Editor: Kai Norrdahl. Accepted 5 March 2007

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More intense herbivory is likely to have antagonisticeffects on seed dispersal (Vellend et al. 2006) becauseplant investment in seeds is reduced due to resource lossor meristem damage by the grazing activity. Otherecological factors are also modifiers of floweringabundance. Alpine ecosystems often have asynchronousmelting among snow patches causing spatio-temporallyfluctuating flowering phenology (Holway and Ward1965, Kudo 1991, Molau et al. 2005). Moreover, seedproduction can be pollen limited because the pollinationenvironment is not constant (Burd 1994). Finally, intundra areas flowering intensity fluctuates between years(Laine and Henttonen 1983), and hence yearly varia-tions in seed content of faeces are to be expected.However, how endozoochory varies with ecological scaleand context is unknown. Due to variation in ecologicalcontexts for endozoochory, fine spatial scales probablycause low predictability (Noda 2004) on the importanceof large herbivores as plant dispersers. Hence, whenassessing the impacts of wide-ranging, large ungulates,adequate study designs probably require regional extentsincorporating the ability to evaluate ecological hierarchy(Senft et al. 1987, Wiens 1989).

Reindeer/caribou select for flowers and fruits (Skjen-neberg and Slagsvold 1968, Batzli et al. 1980, Klein1990, Cooper and Wookey 2003). Heintze foundreindeer faces to return viable seeds nine decades ago(Heintze 1915), whereas since then no known literatureabout endozoochory by reindeer have been presented.Also, whereas most literature on endozoochory isconcerned with seed plants, several herbivores also grazevascular spore plants, bryophytes and fungi. Hence,large herbivores can potentially also be dispersers ofspores via endozoochory. Several species of vascularspore plants are known to be grazed by reindeer(Skjenneberg and Slagsvold 1968), and Heintze(1915) reported the bryophyte Polytrichum communefrom his observations. Reindeer have long gastrointest-inal tracts inhabited by large microfloras that makethem able to digest a span of different forage plantqualities, including even birds and lemmings (Skjenne-berg and Slagsvold 1968). However, few propagules areexpected to survive when eaten because of the heavyacidic content in parts of the gastrointestinal tract andthe potential damage from the chewing (Gardener et al.1993, Cosyns et al. 2005). Consequently, reindeer areprimarily expected to be a plant propagule predator.

The low alpine region of Finnmark, northern Nor-way, holds dense reindeer populations. Sites of highfertility are associated with higher abundance of flowers,but only where reindeer densities are relatively low(Brathen et al. unpubl.). Such difference in flowering isexpected to mirror a similar difference in seed abun-dance and hence seed content of faeces. However,because the passage through the gastrointestinal tract ofthe herbivore may take up to 72 h, seeds may be

transported over long distances (Cosyns et al. 2005).Within the region of Finnmark, the close proximitybetween salt marshes, forests, meadows and alpine areasmay cause reindeer to act as important vectors for seedflux, potentially counteracting such seed limitation. Forinstance, seed flux from areas below the tree line to thealpine areas could be common because reindeer oftenmigrate between these habitats. Hence we also expectthe landscapes through which reindeer migrate to haveimportance for seed content of faeces.

In the present study we evaluate if reindeer disperseviable seeds and plant spores, and if reindeer endo-zoochory is affected by ecological scale and context. Toevaluate this, we have sampled ten replicated pairs ofdistricts with contrasting reindeer stocking densities inFinnmark, northern Norway, covering an area of18 003 km2. Within these districts, reindeer faeceswere collected in landscape areas where also a range ofecological factors was identified. We ask if the reindeerfaeces contain emerging plants, and if so, whether theseplants belong to certain plant propagule types. Next, weask whether reindeer endozoochory is important forlong distance and between habitat seed dispersal.Finally, we ask if the abundance of plants emergingfrom the reindeer faeces is affected by reindeer density,whether there is consistency in the effect of reindeerdensity at different hierarchical scales, and whetherother ecological factors of the pastures affects theabundance and type of plants emerging from the faeces.

Methods

General characteristics of focal ecosystem

Finnmark County in Norway forms the northernfrontier of the European continent, delineated by theBarents Sea towards the north and by birch forests andcontinuous, coniferous taiga towards the south. In itswestern parts Finnmark is topographically characterizedby steep hills running from peaks around 800�1200 ma.s.l., often surrounded by glaciers, deep valleys andnarrow fjords or the open sea. Towards the eastern part ofFinnmark the mountain ranges gradually lower towardsplateaus of 300�500 m a.s.l. with abrupt edges towardsthe Barents Sea interspersed with moderately sloped hills.The relief-gradient from west to east has effects on thevariability of the local climate (Kruckeberg 2002).Moreover, in this region there are climatically steepgradients from west to east as well as from coast to inland(Hanssen-Bauer 1999), caused by the NE AtlanticCurrent that gradually declines from west to east.

Coastal Finnmark forms the traditional summerpastures for reindeer and contains patches of forestswhere mountain birch Betula pubescens predominates(Oksanen and Virtanen 1995). These patches are

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typically located in a narrow belt along the coast, andespecially in valleys extending into the mountain ranges.Coastal eastern Finnmark has either no forests (exposedsites) or a forest limit at 100�150 m a.s.l. (moresheltered sites), while the forest line in the western partsis at 300�500 m a.s.l. (Oksanen and Virtanen 1995).The bio-geographical classification of areas beyond thetree-line varies, but generally grades from northernboreal in the west to hemiarctic in the east (Moen 1998,Virtanen et al. 1999). The zonal vegetation focused onin the present study, i.e. the low alpine, is dominated bylow shrub tundra (Anon. 2003a), where heaths domi-nated by Empetrum nigrum ssp. hermaphroditum,Betula nana and species of Vaccinium are interspersedby patches of mesic and wet vegetation where dicoty-ledons such as Bistorta vivipara , Alchemilla alpina ,Thalictrum alpinum and Viola biflora and graminoidssuch as Deschampsia flexuosa , Nardus stricta , Carexbigelowii , Eriophorum angustifolium , Agrostis capillarisand Deschampsia cespitosa are dominating along withSalix herbacea (nomenclature follows Lid and Lid1994). Common herbivores in the low alpine zoneapart from reindeer are ptarmigan (Lagopus lagopus andL. mutus ), hare Lepus timidus and small rodents such asNorwegian lemmings Lemmus lemmus and grey sidedvoles Clethrionomys rufocanus . Large herbivores otherthan reindeer include moose Alces alces and domesticsheep Ovis aries that reach high abundances onlylocally.

Reindeer Rangifer tarandus tarandus has been pre-sent since Finnmark was deglaciated 10 000�15 000 yrBP (Skogland 1994). Herds perform distinct seasonalmigrations between inland winter pastures and coastalsummer pastures. Since the 16th century, reindeer herdsin Finnmark have become semi-domesticated andnowadays are entirely managed by the indigenousSami people, but with the seasonal migration patternmaintained (Muga 1986). However, in contrast to thepristine, unmanaged situation severe range restrictionshave taken place. The summer pastures are naturallydelineated by coastlines into distinct geographic areas,but are now further separated by reindeer fences intodiscrete management districts. These summer pasturedistricts, which constitute the basic political manage-ment unit within the Norwegian husbandry manage-ment regime, vary in terms of pasture area and densityof reindeer. Yearly records of reindeer densities at thisdistrict level are available for the two-three last decades.

Study design

We designed the study so that reindeer density effectscould be assessed along with scale and ecological contexteffects on reindeer endozoochory. We take advantagefrom the fact that separate summer pasture districts

were subject to different management regimes givingrise to persistent differences in reindeer densities andcalf weights (Fauchald et al. 2004, Tveraa et al. 2007).As districts with high (resp. low) density were locatedthroughout Finnmark we could use a paired blockdesign with each pair having neighbouring low- andhigh- density districts. This quasi-experimental design(Shadish et al. 2002) controlled for large scale environ-mental gradients (e.g. east-west climatic gradient). Thecomponent that was not randomized was the allocationof high vs low reindeer density within a pair. To ourknowledge, this difference is mainly due to social andhistorical factors and is not related to systematicenvironmental differences. Neighbouring summer pas-ture districts were paired based on the criteria that ahigh-density district had, consistently over the two lastdecades, lower calf weights and higher reindeer densitythan the neighbouring low-density district with which itwas paired (Fig. 1A). Ten district pairs conformed toboth criteria and were included in the study (Fig. 2),representing 62% of the available summer grazing areasin Finnmark.

The selected summer districts represent large hetero-geneous areas and we aimed for a sampling designwithin districts that would balance unbiasedness, cover-age and a focus on areas of assumed highest importanceas pasture for reindeer. We assured that sampling unitswere drawn from separate siida regions (i.e. areasbelonging to separate cooperative groups of Samiherders within districts) and different geographicregions (i.e. based on topographic features such asvalleys, peninsulas and mountain ranges) within thedistricts. Often such geographical and social regionscoincided. Landscapes practically empty of vegetationwere not included as potential study areas. This wasaccomplished by delineating mesic and wet vegetationstrata based on previous satellite image classifications ofvegetation types in Finnmark (Johansen et al. 1995)using GIS software (Anon. 2003b). The stratificationand selection procedure was as follows: a grid of 2�2 km landscape areas was superimposed on the areas ofthe district situated in the low alpine zone. Next weidentified landscape areas with more than average ofmesic and wet vegetation for the district. Finally, fromthose highly vegetated areas, we discarded landscapeareas that included �50% of forest, lakes, sea orglaciers or included a major road (National LandSurvey), because such factors may influence presenceof reindeer independently of pasture quality. Theremaining landscape areas fulfilling the above criteriawere then subjected to random selection under thecondition that there should be a minimum of two areaswithin each siida/geographic region per district. Abovethis minimum the number of selected landscape areasincreased with the area of the focal stratum of theregion. The number of selected landscape areas per

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district then varied between 6 and 14 depending on thenumber of socio-geographic regions. All landscape areasof a district pair were sampled within the same time-period during July and August 2003.

The selected 2�2 km landscape areas were furthersubdivided in 100 sampling square areas of 200�200 m among which 25 were randomly selected(Fig. 2) and of which in average 10 were analyseddepending on the accessibility of the sampling squares.The centre of a selected area was a start position for asampling line whose direction was given by a randomGPS position on a circle of 50 m radius from thecentre. Criteria for asserting that the majority of asampling line was covering vegetation were followed.The sampling lines were sub-sampled at plots every 5 malong the line with a triangular sampling frame withsides of 40 cm (Fig. 2).

Validating the adequacy of the quasi-experimental study design

Records of presence/absence of reindeer pellets (or pats)were made within triangular sampling frames (Fig. 2) inorder to get a picture of the actual activity of reindeeracross our sampling plots. The records of the frequencyof pellets at the district level conformed to the long-term reindeer density contrasts forming the basis for thequasi-experimental design (Fig. 1B). This confirms thatour sampling design is adequate for assessing the effectsof the prevailing reindeer densities. There was oneapparent discrepancy regarding district pair 6 (Fig. 1B)because the reindeer density contrast for 2003 (Anon.2004a) had flipped over relative to the long-termaverage for this district pair.

We did not expect any consistent differences (i.e.bias) between high and low-density-districts in poten-tially influential ecological factors because the focus ofthe design was on contrasts between neighbouringdistricts, hence controlling for large-scale gradients inenvironmental factors. We validated this presumptionby extracting information about geoedaphic factors(Kruckeberg 2002) such as terrain, parent materialand sediment deposits as well as simple geographicparameters for all sampling squares (Fig. 2) using GIS(Anon. 2004b) and a digital terrain model (DTM) of25�25 m pixels (National Land Survey). Data on themajor category of bedrock types and the major categoryof sediment deposits (Anon. 2004c) were collected persampling square. The bedrock nutrient content wasclassified into three ordinal categories poor, moderateand rich based on Tarbuck and Lutgens (1992). Allecological factors tested for showed a relative differenceof B7.04% between high and low-density-districts andwas therefore considered of low influence on the studydesign.

Quantifying plant abundance and distinction ofplant functional groups

The abundance of vascular plant species and flowers inthe triangular sampling frames was measured using thepoint intercept method (Jonasson 1988, Frank andMcNaughton 1990, Brathen and Hagberg 2004). Tooptimize sampling effort with respect to the trade offbetween within- and between-plot sampling variance(Brathen and Hagberg 2004), we used only three pinsper frame allowing for a larger number of plots persampling line and sampling lines per landscape area.One side (two pins) of the triangle was placed exactly

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Reindeer density (animals per square km) Reindeer density (animals per square km)

Fig. 1. The relationship between reindeer density and weight of slaughtered calves (A) and between reindeer density and meanfrequency of plots with reindeer faeces (B). Lines connect districts within 10 pairs with contrasting densities (Fig. 2). Estimates ofyearly reindeer density and calf weights are averaged over a 23 yr period using the official statistics of the Norwegian ReindeerAdministration, whereas the estimate of faeces frequency was obtained in 2003 by our sampling design (see main text). Districtpair 6 had reversed density of reindeer in 2003 compared to the long term average (Anon. 2004a).

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Fig. 2. (Continued).

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parallel to the left side of the measurement ribbonrunning from the start to the end position of thesampling line (Fig. 2). Reproducing plant structuresand vegetative parts were registered separately.

Sampling of reindeer faeces and analysis ofemerging plants

Throughout each landscape area faeces were collected inthe form of relatively large-sized pellets or pats, of 100to 250 ml volume depending on the size of pats ornumber of pellets. There were no observations of plantsemerging from the faeces upon collection. The collectedfaeces were stored in plastic bags and frozen. Thefreezing treatment was considered a simulation ofnatural winter conditions for faeces pellets (or pats),considering the long, and climatically variable winter ofthe Finnmark alpine coastal region where freezingevents of ground uncovered by snow are not unusual(Norwegian Meteorological Inst.). After ca two monthsthe faeces were spread onto perlite in 15 cm diameterpots at the phytotron at the Univ. of Tromsø, Norway.The faeces were kept moist under a light permeable lid,at 24 h of daylight and within a temperature range of18�218C. Observations for seedlings and vascular sporeplants were conducted twice a week. Seedlings wereobserved to emerge from inside the faeces pellets (orpats), whereas this could not be established for the sporeplants. Emerging plants were replanted onto soil andallowed to grow until species identity could beestablished. After three months the faeces were storedat 0.58C in darkness for one month after which thefaeces were mashed. Observations for emerging plantswere then continued for two more months. From tworandomly chosen landscape areas per district, bryophytespecies that emerged on the sampled faeces wereidentified.

Statistical analysis

The hierarchical structure of the nested factors, i.e.landscape areas within district within district pairs, isproperly taken into account by using linear mixedmodels (Draper 1995, Pinheiro and Bates 2000). Weused the lme function (Pinheiro et al. 2004) in the Renvironment (Anon. 2004d). Primary response vari-ables were seedling or vascular spore plant abundance,

sorted according to common plant functional groups(Chapin et al. 1996), and the total species richnessemerging from the faeces. The empirical distribution ofplant emergence proved often to be inadequate forlinear modelling. However, the response variablesbecame adequate for statistical modelling when omit-ting landscape areas from the analysis that had no plantsemerging from the collected faeces and then transform-ing the data by loge(x�1).

We used a common structure in all analysesfollowing the design. The fixed effects were the reindeerdensity-contrast, high vs low reindeer density at thedistrict level, and then at the landscape level thecontinuous variables faeces abundance, site fertility(three levels of bedrock nutrient content on a linearscale), height above sea level and longitude (as climateindicators) along with flower abundance. The abun-dance of faeces and the abundance of flowers were bothsummed per sampling line and then averaged at thelevel of the landscape area.

There was no confounding between continuouspredictor variables. We chose to model the fixedreindeer-density effect as a nominal contrast withinpair because absolute reindeer densities may not have astraightforward quantitative meaning in terms of graz-ing effects due to heterogeneous contingencies in timeand space. The effect size estimates (including theiruncertainties), form the main basis for the presentationof the results (Table 3). The significance of the differentfactors was assessed using the 95% confidence intervals.The size of the random effects was expressed as units ofstandard deviation on the log scale, which correspondsto coefficients of variation (Lande 1977).

Results

Seedlings or vascular spore plants emerged from faecescollected in 65 out of the 150 landscape areas sampled.Thus, germinating plant propagules were lacking fromthe majority of faeces collected. However, seedlings orvascular spore plants emerged from faeces collected inall districts. There was no difference between low andhigh density districts, with faeces from 56 and 57% outof all landscape areas lacking germinating plant propa-gules respectively. Faeces collected later in the summerwere more likely to have plants emerging as opposed tofaeces collected earlier in the season (Fig. 3).

Fig. 2. Location and the hierarchical levels of the study design. The map shows the delineation of the summer pasture districtsforming the 10 pairs with contrasting reindeer densities. An arrow connects the two districts of each pair. Landscape areas of 2�2 km (light grey squares within the map) varied from 6 to 14 per district. Each of the landscape areas was subdivided into100 sampling squares in which a random subsample (dark grey squares) was chosen. Within each selected sampling square asampling line running from the middle of the square towards a random position at 50 m distance was established. The samplingline was analyzed every 5 m with the point intercept method by use of a triangle of 40 cm sides with analysis pins attached ineach corner.

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A total of 732 vascular plant individuals (468 sporeplants and 264 seedlings) emerged from the faeces,corresponding to 22.5 viable propagules per litre of

faeces. These individuals belonged to 20 different plantspecies (Table 1). Most individuals belonged to theferns, followed by, in descending order, woody,

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Table 1. Number of emerging plants from reindeer faeces, their density in faeces and their diaspore characteristics (Berggren 1969,1981, Grime et al. 1988, Anderberg 1994, Biolflor databaseBhttp://www.ufz.de/biolflor/info.version.jsp�). Diaspore size ispresented in italics for species whenever information was only available for a close relative.

No. ofgerminatedpropagules

No. of plantsper faecesvolume (l)

Diaspore sizelength�width (mm)

Diaspore type Fruit type

HerbaceousCerastium alpinum ssp.glabratum

5 0.15 1.1�1.3�0.6�1.0 seed capsule

Sagina saginoides 55 1.69 0.3�0.35�0.35�0.45 seed capsuleEpilobium hornemannii 5 0.15 1.0�1.3�0.3�0.5 seed with hairs capsuleEpilobium lactiflorum 3 0.09 1.2�1.4�0.3�0.5 seed with hairs capsuleRanunculus pygmaeus 1 0.03 0.9�1.5�0.7�1.1 seed nut with

‘‘crooked nose’’Sibbaldia procumbens 6 0.19 1.1�1.5�0.8�1.2 seed nutDicotyledons not identified 3 0.09 seedAgrostis mertensii 1 0.03 1.0�0.2�0.5 seed nutAgrostis capillaris 1 0.03 1.0�0.2�0.5 seed nut with

attached lemmaCarex mackenziei 5 0.15 2�3�1.5�1.7 seed nutCarex canescens 2 0.06 2.3�2.5�1.0�1.3 seed nutLuzula multiflora 1 0.03 1.5�1.9�0.7�0.9 seed with

attachmentcapsule

Graminoid not identified 1 0.03 seedGymnocarpium dryopteris 381 11.73 BB0.1�0.1 sporePhegopteris connectilis 10 0.31 BB0.1�0.1 sporeCystopteris fragilis 22 0.68 BB0.1�0.1 sporeAthyrium distentifolium 3 0.09 BB0.1�0.1 sporeFerns not identified 52 1.60 spore

WoodyVaccinium myrtillus 134 4.13 1.2�1.5�0.5�0.8 seed berryVaccinium uliginosum 8 0.25 1.2�1.7�0.4�0.6 seed berryEmpetrum nigrum ssp.hermaphroditum

14 0.43 1.6�1.2 seed berry

Betula pubescens 1 0.03 1.5�3.0�0.9�1.8 seed winged nutBetula nana 1 0.03 1.0�1.9�0.8�1.5 seed winged nut

BryophytesBryum sp., Pohlia sp., Ditrichum flexicaule, Ditrichum sp., Marchantia sp., Oncophorus virens, Brachythecium sp., Encalypta sp.,Polytrichum sp., Pleurozium schreberi, Barbilophozia sp., Dicranum sp., Rhytidium rugosum, Aulacomnium palustre, Straminergonstramineum, Philonotis sp., Tayloria lingulata

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dicotyledon and graminoid species. From the selectedsubset of landscape areas, a total of at least 17 genera/species of bryophytes were found on the faecescollected. In general, spore propagules gave rise tomore emerging plants than seed propagules whereas theseed propagules represented higher species richness.

The most abundant seed plant species found toemerge from the faeces were the deciduous ericoidsVaccinium uliginosum and V. myrtillus and the ever-green Empetrum nigrum ssp. hermaphroditum . Thesespecies were also dominant in the alpine reindeerpastures (Table 2). The herbaceous species emergingfrom the faeces had both low abundance and lowspecies richness in the alpine pastures, i.e. theycomprised only a small fraction of the pasture speciespool. No species of Salix and no evergreen species,

apart from E. hermaphroditum , emerged from the faecesalthough these species were present in the pastures. Thevascular spore plants showed an opposite trend,being the most abundant plants emerging from faecesbut having general low abundance in the alpinepastures.

There was no effect of high or low reindeerstocking density at the scale of herding districts, onthe abundance of seedlings or vascular spore plantsemerging from the faeces (Table 3). However, inlandscape areas where the presence of reindeer faeceswas higher there were significantly fewer plant speciesand in total a lower abundance of plants emergingfrom the collected faeces. Hence, reindeer densityeffects on plant emergence from faeces were scale-dependent, having effect at the level of landscape areas

Table 2. Relative importance in vegetation in terms of abundance (total point intercepts) and species richness of all species andplant functional groups emerging from faeces.

Abundance in vegetation Species richness in vegetation

Abundance ofall species(flowers)

Abundance ofspecies present

in faeces

Species presentin faeces in

proportion to allspecies of group

No. ofspecies

No. of speciespresent in

faeces

Species presentin faeces in

proportion to allspecies of group

HerbaceousDicotyledons 3261 (116) 111 3.4% 100 6 6.0%Graminoids 20536 (291) 1198 5.8% 69 5 7.2%Vascular spore plants 566 (�) 160 28.3% 15 4 26.7%

WoodyDeciduous ericoids 7732 (95) 6408 82.9% 8 2 25.0%Empetrum nigrum ssp.hermaphroditum

14851 (215) present present present

Salix 3119 (19) 0 0 10 0 0Betula 7680 (13) 7680 (13) 100% 2 2 100%

Evergreen(apart fromEmpetrum)

4350 (62) 0 0 18 0 0

Table 3. Results from linear mixed model on the effect of reindeer density (measured as stocking density at district level and asfaeces abundance at landscape level), vegetation factors flower abundance and general plant abundance and abiotic factors sitefertility, height above sea level and longitude on faeces content of emerging plants sorted according to functional groups and onspecies richness per faeces litre. The effect size is presented on a backtransformed loge(x�1) scale where significant effects (i.e. 95%CI do not include 1) are indicated in bold. Effect size below 1 indicates a negative effect on plant emergence from faeces whereasabove 1 indicates a positive effect.

Variable Ecological factors Effect (�/�) Effect size (9 95% CI)

AbundanceAll vascular plants

Reindeer density district scale 0.905 (0.471, 1.739)Reindeer density landscape scale � 0.286 (0.126, 0.651)Flower abundance 1.213 (0.769, 1.912)Plant abundance 1.000 (0.999, 1.001)Site fertility 1.238 (0.842, 1.821)Longitude 0.996 (0.990, 1.002)Altitude 1.001 (0.999, 1.003)

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but not at the most extensive scale, i.e. at the level ofreindeer districts.

Of the other ecological factors tested for, only theabiotic factors were important and only on emergence

of certain growth forms. Faeces collected in landscapeareas with higher site fertility or at higher altitudes had ahigher abundance of herbaceous seedlings emergingfrom the faeces (Table 3). The abundance of woody

Table 3. Continued.

Variable Ecological factors Effect (�/�) Effect size (9 95% CI)

Seed plantsReindeer density district scale 0.731 (0.319, 1.671)Reindeer density landscape scale � 0.331 (0.115, 0.947)Flower abundance 1.325 (0.783, 2.241)Plant abundance 1.000 (0.999, 1.002)Site fertility 1.324 (0.840, 2.088)Longitude 0.998 (0.991, 1.005)Altitude 1.001 (0.998, 1.003)

Herbaceous spore plantsReindeer density district scale 1.580 (0.660, 3.782)Reindeer density landscape scale 0.495 (0.134, 1.834)Vascular spore plant abundance 1.012 (0.981, 1.045)Site fertility 1.189 (0.546, 2.589)Longitude 1.000 (0.991, 1.010)Altitude 1.000 (0.997, 1.003)

Herbaceous seed plantsReindeer density district scale 0.968 (0.569, 1.646)Reindeer density landscape scale 0.775 (0.371, 1.617)Herbaceous seed plant flower abundance 1.215 (0.633, 2.332)Herbaceous seed plant abundance 1.002 (0.999, 1.005)Site fertility � 2.044 (1.427, 2.928)Longitude (�) 1.005 (1.000, 1.010)Altitude � 1.003 (1.001, 1.004)

Woody plantsReindeer density district scale 0.529 (0.162, 1.725)Reindeer density landscape scale 0.354 (0.045, 2.764)Flower abundance woody plants 1.247 (0.181, 8.581)Woody plant abundance 0.999 (0.995, 1.003)Site fertility 0.881 (0.412, 1.884)Longitude 0.994 (0.980, 1.008)Altitude 1.000 (0.997, 1.004)

Species richnessNumber of vascular plantspecies

Reindeer density district scale 1.018 (0.740, 1.402)Reindeer density landscape scale � 0.547 (0.352, 0.849)Flower abundance 1.182 (0.929, 1.503)Plant abundance 0.999 (0.998, 1.001)Site fertility 1.137 (0.923, 1.401)Longitude 0.999 (0.996, 1.002)Altitude 1.001 (1.000, 1.002)

Number of seed plant speciesReindeer density district scale 1.037 (0.699, 1.539)Reindeer density landscape scale 0.689 (0.382, 1.241)Flower abundance 1.178 (0.887, 1.565)Plant abundance 0.999 (0.997, 1.001)Site fertility 1.157 (0.893, 1.499)Longitude 1.000 (0.997, 1.004)Altitude 1.001 (0.999, 1.002)

Number of bryophyte speciesReindeer density district scale 1.198 (0.825, 1.741)Reindeer density landscape scale 1.190 (0.695, 2.038)Site fertility 1.242 (0.922, 1.674)Longitude 1.002 (0.998, 1.006)Altitude 1.000 (0.999, 1.002)

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plants and vascular spore plants were not significantlyaffected by any ecological factors.

The estimated effects of the random factors weredependent on the hierarchical scale (Table 4). Whenthe fixed effects were accounted for, most residualvariance was among landscape areas within districtswhereas considerably smaller residual variance wasamong district pairs or among districts within pairs.

Discussion

We found that reindeer faeces collected in Finnmarkcontained germinating seeds and emerging vascularspore plants. However, more than half of the collectedfaeces contained neither germinating seeds nor spores,and in general few vascular plants emerged, both interms of abundance and number of species. Faecescollected later in the season were found to have moregerminating vascular plants, which is consistent withexpectations given the availability of flowers and fruits(Malo and Suarez 1995). In comparison to the potentialseedling density of 280�525 l�1 of ungulate faeces(Cosyns and Hoffmann 2005), the density of plantsemerging from reindeer faeces was only 22.5 l�1 ofwhich vascular plant seedlings comprised half. Suchseedling density is within the lower range of what haspreviously been reported for reindeer (Heintze 1915).Hence, propagule pressure from reindeer faeces was lowand endozoochory by reindeer may only have limitedimportance for plant dispersal in Finnmark.

The importance of reindeer density on endozooch-ory was scale dependent. That is, higher reindeerdensities at the level of landscape areas, as indexedthrough faeces abundance, were associated with bothless species and lower abundance of emerging plantsfrom the collected faeces. Hence, mature plant propa-gule availability probably could not satiate reindeer athigher reindeer densities at the scale of landscapes. Suchreduced dispersal rate is possibly also an indication thatgrazing reduces plant population growth rate (Vellend

et al. 2006). Yet, the expectation that the abundance ofseeds in faeces should be lower in districts of higherreindeer stocking density was not confirmed. A likelyexplanation for this discrepancy between scales is that,according to theory on ecological hierarchies (Senftet al. 1987), reindeer are selective of their grazinggrounds at the scale of landscapes. Assemblages oflandscapes, i.e. the scale of herding districts, probablymasked effects of such selection.

In this study we found many fern individualsemerging from the faeces, indicating that other diasporetypes than seeds are viable in faeces. Whether spores hadsurvived the digestive tract of reindeer or whether sporeswere on the surface of the faeces upon collection isuncertain. Nevertheless, endozoochory of spores islikely. Although a poor comparative to reindeer, sporesof ferns have been shown to survive through thedigestive tract of earthworms (Schneller 1998). Inaddition, whereas soil seed banks have been acknowl-edged for almost a century, fern spores have only quiterecently been acknowledged to form persistent soilspore banks (Dyer and Lindsay 1992). As seed survivalthrough the digestive tract of ungulates has ecologicalcorrelates to soil seed bank survival (Myerset al. 2004, Pakeman et al. 2002), so could soil sporebank survival. Hence, spores of ferns could be suffi-ciently robust for survival through the digestive tract ofa large herbivore.

The emerging seed plant species mostly had smallseeds (the majority had seeds B2.0 mm length and1.0 mm width) and were assumed hardcoated (major-ity of species had berries or nuts as fruits). Thus,supporting previous studies on typical seed traitssurviving through the digestive system of a largeherbivore (Janzen 1984, Myers et al. 2004, Yamashiroand Yamashiro 2006). However, the small seed sizefound in this study could also reflect seed character-istics of the grazing environment (Bruun and Poschlod2006), that is, in northern and alpine environmentsseed size is generally small (Welling et al. 2005).

Flower abundance was not important for explainingseed plant emergence from reindeer faeces. Reproduc-

Table 4. Standard deviation of the two hierarchical random factors in the mixed model. The response variable is log-transformed.

Response variable DF (pairs,landscape areas)

Between pairs Between districtswithin pairs

Residuals (between landscapeareas within districts)

AbundanceAll vascular plants 9, 39 0.02 0.439 0.962Seed plants 7, 23 0.016 0.529 0.983Herbaceous spore plants 8, 12 0.024 0.013 1.225Herbaceous seed plants 6, 9 0.008 0.006 0.737Woody 5, 6 0.048 0.456 1.012

Species richnessNumber of vascular plant species 9, 37 0.009 0.159 0.536Number of seed plant species 7, 20 0.044 0.013 0.611Number of bryophyte species 9, 12 0.170 0.005 0.537

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tive shoots may have had few or no mature seeds uponbeing grazed given that seed production often is pollenlimited in arctic and alpine environments (Stenstromand Molau 1992). Also, because most seeds cannottolerate the environment of the gastrointestinal tract,they are lost as propagules (Chang et al. 2005, Cosynset al. 2005), and it is therefore likely that propagules ofmost reproductive shoots did not survive the grazing.However, neither did plant abundance in generalexplain faeces content of viable plants in this ecosystem.Also, only a small fraction of the species pool was foundto emerge from faeces.

Among the seedlings found to emerge from thereindeer faeces most belonged to the ericoids. Incomparison, seeds of grass species were found to bethe most abundant seed type in faeces of kerama deer(Yamashiro and Yamashiro 2006). Yamashiro andYamashiro (2006) predicted deer faeces to causeexpansion of grasslands due to the propagule pressureof grass species from faeces. In our study we found veryfew grass and other herbaceous seed plants emergingfrom the reindeer faeces, both in terms of abundanceand in terms of number of species as compared to in thepastures. Moreover, the emerging herbaceous seedplants were more abundant in faeces collected inlandscape areas where site fertility was higher reflectingthat these areas are more abundant in herbaceous seedspecies in alpine areas of Finnmark (Brathen et al.unpubl.). The typical alpine vegetation composition inFinnmark is however dominated by a few species ofericoids (Brathen et al. unpubl.), and hence faeces seedcontent seems to reflect forage availability also in ourstudy. In turn, reindeer faeces contribute to reinforcethese ericoids in the pasture.

In the alpine, coastal parts of Finnmark seed influx isprecluded by mountains and to some extent glaciers tothe south and the vast Barents Sea to the north. In thissystem reindeer do not seem to contribute to majorlong distance dispersal or major dispersal from otherhabitats: we found no species apart from Carexmackenziei , a littoral sedge, that are rare in the alpineenvironment. In general the dispersal rate of plantpropagules in reindeer faeces seemed low, consideringlow abundance of propagules in faeces. Low productiveenvironments (e.g. alpine areas) have often seed limitedvegetation in terms of plant establishment and totalspecies richness (Foster et al. 2004, Eskelinen andVirtanen 2005), and even more seed limited when alsosubjected to grazing (Gonzalez et al. unpubl.). Resultsfrom this study demonstrate that reindeer may counter-act a potentially negative impact on seed limitationfrom their grazing by returning viable seeds in theirfaeces. However, in Finnmark, northern Norway, thiseffect is small.

Acknowledgements � We are grateful to Bernt Johansen forproviding satellite images, Norwegian Coast Guard and JanKare Amundsen for transportation during field work, toSunna Pentha for field assistance, to Torstein Engelskjøn andChristina Wegener for species identification, and to LeidulfLund, Jarle Nilsen and Kjell Nilsen for help with thephytotron studies. This study, which is a contribution fromthe ‘‘Ecosystem Finnmark’’ project, was financed by Norwe-gian Research Council.

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