Good Neighbours? Determinants of Aggregation and ...

Good Neighbours? Determinants of Aggregation and Segregation among Alpine Herbivores Author(s): Isabel C. Barrio & David S. Hik Source: Ecoscience, 20(3):276-282. 2013. Published By: Centre d'études nordiques, Université Laval DOI: http://dx.doi.org/10.2980/20-3-3595 URL: http://www.bioone.org/doi/full/10.2980/20-3-3595

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Good neighbours? Determinants of aggregation and segregation among alpine herbivores1 Isabel C. BARRIO2,'HSDUWPHQWRI%LRORJLFDO6FLHQFHV8QLYHUVLW\RI$OEHUWD(GPRQWRQ$OEHUWD7*(&DQDGD and Instituto Pirenaico de Ecología (CSIC), Avda Nuestra Señora de la Victoria s/n, PO Box 64, Jaca, 22700 Spain, e-mail: [email protected] David S. HIK,'HSDUWPHQWRI%LRORJLFDO6FLHQFHV8QLYHUVLW\RI$OEHUWD(GPRQWRQ$OEHUWD7*(&DQDGD Abstract: Interspecific interactions often determine the structure and stability of biotic communities. In low-productivity and highly seasonal environments such as the alpine tundra, most interactions occur during a short, snow-free period. The strength and direction of these interactions are likely to be determined by the availability of resources, particularly among species of the same ecological guild. Understanding how species interact in such environments can provide insights into the conditions that facilitate their coexistence. We determined the potential for interspecific interactions among 3 resident medium-sized mammalian herbivores inhabiting the alpine tundra and investigated how they share available space and resources. Overlap in their respective activity areas indicated that these species were aggregated at a landscape scale, but other mechanisms allowed their coexistence at a finer scale. Their distributions were primarily associated with shorter distances to heterospecifics and, secondly, with habitat features related to shelter and escape from predation. Our results suggest that these species can (and do) coexist by partitioning their ecological niches. Competition is likely not a major IDFWRU LQ VWUXFWXULQJ WKHVH FRPPXQLWLHV LQ WXUQ IDFLOLWDWLYH PHFKDQLVPV PD\ DOORZ FRRFFXUUHQFH RI WKHVH V\PSDWULF herbivores in seasonal, low productivity environments. Keywords: alpine tundra, coexistence, facilitation, interspecific interactions, medium-sized mammals. Résumé : Les interactions interspécifiques déterminent souvent la structure et la stabilité des communautés biotiques. Dans des environnements très saisonniers et peu productifs, comme la toundra alpine, la plupart des interactions se produisent durant la courte période sans neige. L'intensité et la direction de ces interactions sont probablement déterminées par la disponibilité des ressources, particulièrement entre les espèces d'une même guilde écologique. La compréhension de la façon dont les espèces interagissent dans de tels environnements peut fournir des indices sur les facteurs qui facilitent leur coexistence. Nous avons déterminé le potentiel d'interactions interspécifiques chez 3 mammifères herbivores de taille moyenne résidants de la toundra alpine et avons examiné comment ils se partagent l'espace disponible et les ressources. Le chevauchement de leurs aires respectives d'activité indiquait que ces espèces étaient regroupées à l'échelle du paysage, mais que d'autres mécanismes rendaient leur coexistence possible à plus fine échelle. Leurs distributions étaient associées en premier lieu à des distances plus courtes entre individus hétérospécifiques et, en second lieu, à des caractéristiques de l'habitat reliées à l'abri et à l’évitement de la prédation. Nos résultats suggèrent que ces espèces peuvent coexister (et le font) en se divisant les niches écologiques. La compétition n'est probablement pas un important facteur structurant ces FRPPXQDXWpV GH SOXV GHV PpFDQLVPHV IDFLOLWDQWV SHUPHWWHQW OD FRRFFXUUHQFH GH FHV KHUELYRUHV V\PSDWULTXHV GDQV GHV environnements saisonniers de faible productivité. Mots-clés : coexistence, facilitation, interactions interspécifiques, mammifères de taille moyenne, toundra alpine. Nomenclature7KHPDPPDOVRI&DQDGD

Introduction Understanding the structure of biotic communities and how different species coexist is one of the main challenges of community ecology (Agrawal et al., 2007). Mechanisms that allow for coexistence depend on the strength and direction of the interactions among the co-occurring VSHFLHV 7UDYLV   EXW PHDVXULQJ DQG LQWHUSUHWLQJ VSHFLHV LQWHUDFWLRQV LV QRW DOZD\V VLPSOH *URVV   Manipulative experiments are required to infer mechanLVWLF PRGHOV 1RYDN  :RRWWRQ   XQIRUWXQDWHO\ manipulation is not always feasible for some study organisms or broader scale studies, so alternative approaches are 5HFDFF

Associate Editor: Daniel Fortin. for correspondence. '2,

2Author

needed. Studies of community structure and species interactions often involve identifying and quantifying patterns RI FRRFFXUUHQFH 0DF.HQ]LH %DLOH\  1LFKROV  Darmon et al.   EHFDXVH RYHUODS LQ WKH VSDWLDO GLVWULbution of organisms is a prerequisite for the occurrence of interactions among them. In this context, null model analyses can provide a means to study mechanisms where experiPHQWDO VWXGLHV DUH QRW SRVVLEOH *RWHOOL  *UDYHV   Such analyses are becoming increasingly popular among population ecologists to investigate interactions among animals (Richard et al. 5HFHQWVWXGLHVKDYHKLJKOLJKWHG the need to jointly study both spatial structures and biotic interactions (Ritchie et al.  'DUPRQ et al.   WR obtain a comprehensive understanding of the mechanisms of coexistence. In this sense, determining the relative role of environmental (habitat) variables and interspecific

ÉCOSCIENCE, VOL. 20 (3), 2013

interactions in shaping species’ spatial distribution can provide insights into such mechanisms (Azeria, Ibarzabal & +pEHUW  Interactions among co-occurring organisms may show considerable plasticity depending on the local biotic and DELRWLF FRQGLWLRQV $JUDZDO   )RU H[DPSOH IDFLOLWDtive interactions prevail over competition in determining the structure of plant communities in harsh environments (Callaway et al., 2002). However, for herbivores inhabiting less productive ecosystems, competition is thought to be the dominant form of interaction (e.g., Mishra et al.  Cheng & Ritchie, 2006), although positive interactions may also play an important role in their coexistence (Gross,  ,QGHHGGHVSLWHWKHLUORZQXWULHQWVRLOVORZWHPSHUatures, and low net primary production, tundra ecosystems can support a high biomass of herbivores, among which mammalian herbivores are often abundant (Jefferies, Klein  6KDYHU   7KH VKRUW JURZLQJ VHDVRQ LV WKH PRVW critical period for herbivores to accrue energetic reserves QHFHVVDU\ IRU RYHUZLQWHU VXUYLYDO WKHUHIRUH LQWHQVH FRPpetition for resources might be highly localized in time (Xi, *ULIILQ  6XQ   &RQVHTXHQWO\ VSHFLHV LQWHUDFWLRQV may be crucial in determining the structure and stability of these herbivore communities and how they respond to environmental changes. We analyzed the potential for (positive or negative) biotic interactions among 3 alpine mammalian herbivores: hoary marmots (Marmota caligata), arctic ground squirrels (Urocitellus parryii), and collared pikas (Ochotona collaris). Broadly, these species have similar diets, are territorial, and can be considered central place foragers, but some differences in their life strategies and behaviour allow them to cope with harsh environmental conditions. Marmots DQG VTXLUUHOV KLEHUQDWH IRU DSSUR[LPDWHO\ ± PRQWKV while pikas remain active in winter below the snow cover. In contrast to marmots, pikas and (to a lesser extent) ground squirrels cache food for over-winter survival and emergence from hibernation, respectively. Following the approach proposed by Darmon et al. ZHILUVWDQDO\]HGWKHGLVWULbution and co-occurrence of the 3 species. Specifically, we used null models to determine if the overlap between their spatial distribution was random (neutral interaction), larger than expected by chance (positive association), or smaller than expected by chance (avoidance). Then, we analyzed the habitat selection of each species in the presence of the other 2, to determine the extent to which the aggregation or segregation of their distribution patterns could be attributed to environmental factors or to biotic interactions with sympatric herbivores. Given the low productivity of alpine tundra ecosystems, we predicted all 3 species to be aggregated in space as a result of similar diet and habitat requirements. However, we also predicted segregation at a finer scale in order to reduce competition for essential resources, particularly access to foraging areas and refuges from predation or perceived predation risk.

Methods SITE AND STUDY SPECIES The study was conducted in the Ruby Range ƒ N  ƒ W ), southwest Yukon, Canada, in a

valley (about 7.2 km2  ZLWK HOHYDWLRQV UDQJLQJ IURP  to 2000 m, where 3 main herbivore species coexist at relatively high densities. Landscapes are composed of a mosaic of alpine meadows and tundra vegetation (Hik, McColl  %RRQVWUD  0F,QWLUH  +LN   LQWHUVSHUVHG with boulder fields (i.e., talus patches), which represent XS WR  RI WKH VXUIDFH$QQXDO DERYHJURXQG SULPDU\ SURGXFWLYLW\ LV ORZ PHDQ “ 6'  “  JāP –2 David S. Hik, unpubl. data). Three species of medium-sized herbivores, ranging in PDVV IURP  WR  J SHUPDQHQWO\ UHVLGH LQ WKH DUHD and are the dominant herbivores: hoary marmots, arctic ground squirrels, and collared pikas. All 3 species have been the subjects of extensive study at this site over the past  \ 2WKHU KHUELYRUHV LQ WKH DUHD RFFXU RQO\ VSRUDGLFDOO\ (caribou, Rangifer tarandus'DOOVKHHSOvis dalli) or more locally (voles, Clethrionomys spp. and Microtus spp.) or exploit other feeding resources (ptarmigan, Lagopus spp.). Predators are relatively low in abundance (Hik, McColl & %RRQVWUD  SURVEY Signs of active presence of the 3 herbivores were FHQVXVHG LQ -XO\  ZKHQ DOO  KHUELYRUH VSHFLHV ZHUH active. One observer (ICB) slowly walked the whole study area inspecting for presence signs everywhere. Signs of SUHVHQFH DW OHDVW  P DSDUW DQG VLJKWLQJV RI LQGLYLGXDOV were recorded and geo-referenced using a hand-held GPS receiver. Active burrows were considered to be signs of SUHVHQFH RI DUFWLF JURXQG VTXLUUHOV DFWLYH EXUURZV DQG ODWULQHVZHUHFRQVLGHUHGVLJQVRISUHVHQFHRIPDUPRWVDQG the presence of active haypiles (over-winter food stores) were considered signs of presence of pikas. Active burrows of marmots and ground squirrels had fresh pellets or recent GLJJLQJDFWLYLW\ODWULQHVZHUHDFWLYHLIWKH\FRQWDLQHGIUHVK pellets. Activity of haypiles was assessed by the presence of IUHVK YHJHWDWLRQ WKHVH DVVHVVPHQWV ZHUH XSGDWHG LQ HDUO\ August, as some pikas may only collect vegetation later in the season (Morrison et al.  Since all 3 species are central place foragers, “high use areas” were defined as those within a certain distance of each species’ respective signs of active presence, according to the literature available from the study area and NQRZOHGJHRQWKHELRORJ\RIHDFKVSHFLHVPIRUSLNDV )UDQNHQ   P IRU PDUPRWV DQG JURXQG VTXLUUHOV *LOOLV.DUHOV.RSSHO +LN 2YHUOD\LQJWKH maps of the 3 species yielded a map of herbivore activity )LJXUH   DQG GHILQHG  SRVVLEOH LQWHUVHFWLRQ FDWHJRULHV (Table I). To correlate our map to the actual presence of animals we generated a set of random observation points within each intersection category sufficiently represented in WKHPDS!RIWKHVXUIDFHSLNDRQO\SLND±PDUPRWDQG SLND±VTXLUUHO FDWHJRULHV ZHUH H[FOXGHG $W OHDVW  SRLQWV DQG WKHLU VXUURXQGLQJ PUDGLXV DUHDV ZHUH VXUYH\HG in each category, and the effort was increased in the marPRW±VTXLUUHODUHDVZKLFKDFFRXQWHGIRURIWKHVXUIDFH Occurrence of the 3 species was assessed by checking points for signs of recent activity (see above) and conGXFWLQJ GLUHFW REVHUYDWLRQ ± K $OWKRXJK WKLV SURFHGure cannot be considered a true validation of the map, 277

BARRIO & HIK: SPATIAL DISTRIBUTION OF ALPINE HERBIVORES

because different methods were used, it provides an estimate of the map’s reliability. Overall, the agreement between the activity at observation points and predictions EDVHGRQWKHPDSZDVFRQVLGHULQJWKHVKRUWSHULRG of direct observations compared to the cumulative activity recorded for the map, we consider this agreement to be very good. To further evaluate potential direct behavLRXUDO LQWHUDFWLRQV ZH GHSOR\HG  PRWLRQWULJJHUHG FDPHUDV GXULQJ -XO\  WRWDO  FDPHUD KRXUV  LQ DUHDV where the mapped distributions of the 3 species overlapped. ,Q WRWDO  LPDJHV FRQWDLQHG DQLPDOV DQG DOO  VSHFLHVZHUHGHWHFWHGDWHDFKRIWKHVDPSOLQJSRLQWV2QO\ LPDJHVFDSWXUHGPRUHWKDQVSHFLHVLQWKHVDPHIUDPH (e.g. ZLWKLQ  P RI HDFK RWKHU  DQG LQ  RI WKHVH FDVHV marmots and pikas were together. We interpreted these cases as “potential direct interactions”. STATISTICAL ANALYSES To test the overlap between the areas of activity of the herbivore species we used a null model (Gotelli & *UDYHV :HUDQGRPL]HGWKHVSDWLDOGLVWULEXWLRQRIWKH

3 species by generating a number of random points equal to the number of locations recorded in the field (npikas = 206, nmarmots   nsquirrels = 746). In the case of pikas, random points were restricted to talus patches, because the distribution of haypiles is a priori known to be limited to WKLV KDELWDW W\SH VXFK D FRQVWUDLQW HQVXUHV WKDW WKH UDQdomly generated points for pikas lie within a biologically meaningful habitat type. Based on the randomly generated points and the buffer distances considered for each species (see above), we then calculated the randomized high-use areas for each species and their overlap and compared the observed area for each category with the distribution of VLPXODWHGDUHDVWRFRPSXWHDP-value for this test. To determine habitat selection of each species we combined our map of species activity with maps of potentially relevant habitat and interspecific variables (distances to locations for the other 2 species). Habitat variables included topographic characteristics (elevation, slope, and aspect at  P UHVROXWLRQ  DQG WKH GLVWDQFH WR WDOXV SDWFKHV 8VLQJ distances rather than the presence/absence of talus enabled us to account for potential edge effects (Conner, Smith & N

All 3 herbivores Marmots and squirrels Ground squirrel only Marmot only No herbivores 0

250

500

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FIGURE +HUELYRUHDFWLYLW\ORFDWLRQVLQWKHVWXG\DUHDGXULQJVXPPHU+LJKXVHDUHDVIRUDOSLQHKHUELYRUHVFROODUHGSLNDKRDU\PDUPRWDUFWLF JURXQGVTXLUUHO ZHUHGHILQHGDVWKRVHZLWKLQDFHUWDLQGLVWDQFHRIUHVSHFWLYHVLJQVRIWKHLUSUHVHQFHPIRUSLNDVPIRUPDUPRWVDQGJURXQGVTXLUUHOV )URPWKHFDWHJRULHVUHVXOWLQJIURPWKHLQWHUVHFWLRQRIWKHDUHDVXVHGE\WKHVSHFLHVRQO\WKRVHUHSUHVHQWLQJ!RIWKHWRWDOVXUIDFHDUHVKRZQ 

ÉCOSCIENCE, VOL. 20 (3), 2013

Burger, 2003). Aspect was linearized using a sine transIRUPDWLRQ VHWWLQJ VRXWKZHVWIDFLQJ VORSHV WR  )UDQNHQ & Hik, 2004). No detailed vegetation map was available at this fine scale, but plant communities are closely determined by local topography in this area (Danby et al. +RUQ PRVWSURGXFWLYHDUHDVLQWKHYDOOH\FRUUHVSRQG to low-elevation, southwest-facing gentle slopes. We used variance partitioning to decompose the variation in the occurrence of each species among 2 blocks of predictors, habitat and interspecific variables, resulting in 3 fractions: the pure effects of habitat alone, those of interspecific variables alone, and the joint effects of both (Figure 2). We used Generalized Additive Models (GAM) with binomial errors and a logit link to calculate the deviance of the general and partial models (Legendre  /HJHQGUH   7KH UHVSRQVH YDULDEOHV LQFOXGHG WKH locations where signs of activity were found and an equal number of random absence points. As the whole area was censused for presence signs, these points can be safely considered true absences. Within each block of predictors TABLE I. Intersection categories of activity areas of the 3 alpine herbivores. Null model comparison indicates whether the obVHUYHGYDOXHVZHUHVLJQL¿FDQWO\P ODUJHU VLJQL¿FDQWO\ VPDOOHU± RUQRQVLJQL¿FDQWO\GLIIHUHQWQV IURPUDQGRPVLPXODWLRQV 2QO\ FDWHJRULHV UHSUHVHQWLQJ ! RI WKH VWXG\ DUHD ZHUH FRQVLGHUHG IRU VHWWLQJ REVHUYDWLRQ SRLQWV LQ WKH ¿HOG WR FRUUHODWH our map of herbivore activity to the actual presence of herbivores. Absence of values are noted with (.)  Category

 Area (km2)

1RKHUELYRUHV +RDU\PDUPRWRQO\ $UFWLFJURXQGVTXLUUHORQO\ 3LNDRQO\ 3LNDKRDU\PDUPRW 3LNDDUFWLFJURXQGVTXLUUHO +RDU\PDUPRW arctic ground squirrel $OOKHUELYRUHV

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we excluded variables that did not contribute significantly (P! WRWKHH[SODLQHGGHYLDQFHIROORZLQJDEDFNZDUG stepwise procedure. We corrected for spatial autocorrelation in all models by including a non-linear spatial term (Bivand, 3HEHVPD  *yPH]5XELR   FRQVLVWLQJ RI D WZR dimensional smoother of the spatial coordinates. Including the smoother removed spatial trends from the residuals of the model, as assessed by visually inspecting spatial correlograms, making the assumption of spatial independence VDIH$QDO\VHVZHUHSHUIRUPHGXVLQJ$UF*,6(65,,QF 5HGODQGV &$ 86$  DQG 5  5 'HYHORSPHQW &RUH 7HDP   VSHFLILFDOO\ WKH PJFY OLEUDU\ :RRG   IRU*$0DQGWKHQFIOLEUDU\%MRUQVWDG IRUEXLOGLQJ spatial correlograms.

Results The presence of alpine herbivores was aggregated at a broader scale, occurring over smaller areas than expected at random (P DUHODWLYHO\ODUJHDUHDZDVQRWXVHG E\DQ\RIWKHKHUELYRUHV7DEOH, +RZHYHUZLWKLQ the area occupied by herbivores, areas where more than  VSHFLHV RFFXUUHG ZHUH VPDOOHU WKDQ H[SHFWHG E\ FKDQFH suggesting some avoidance mechanisms, such as direct avoidance of heterospecifics or segregation among species at a finer scale. Conversely, areas occupied by each species alone were larger than expected at random except for pikaonly areas, which did not show a clear trend (P    The main part of the study area was shared by marmots DQG JURXQG VTXLUUHOV   SLNDV QHDUO\ DOZD\V RFFXUUHG ZLWKLQDUHDVXVHGE\DWOHDVWRWKHUKHUELYRUHVSHFLHVEXW mainly where the 3 species overlapped (Table I). This spatial pattern was further supported by the habitat selection of each species. Interspecific variables accounted for the highest proportion of the variance in the occurrence of the 3 herbivores (Figure 2), while habitat variables DORQHUHSUHVHQWHGWKHVPDOOHVWFRQWULEXWLRQPDUPRWV VTXLUUHOV  SLNDV   ,QWHUHVWLQJO\ WKH FRQWULEXWLRQ of pure interspecific variables was similar across species PDUPRWV  VTXLUUHOV  SLNDV  )LJXUH   Variance partitioning

Collared pika

Arctic ground squirrel

Hoary marmot

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0.40

0.60

0.80

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Proportion of explained variance Unexplained variance

Habitat

Interspecific

Shared

FIGURE 2. Variance partitioning of the factors determining the distribution of 3 mammalian herbivores in the alpine tundra of southwest Yukon. The bars show the contribution of each block to the variance explained for each herbivore, when spatial structures were taken into account. 

BARRIO & HIK: SPATIAL DISTRIBUTION OF ALPINE HERBIVORES

The occurrence of all species was related to shortest distances to heterospecifics and talus patches (Table II). In the case of arctic ground squirrels, within the interspecific YDULDEOHVRQO\GLVWDQFHVWRPDUPRWVKDGDQHIIHFWGLVWULEXtion of arctic ground squirrels was also positively linked to southwest-facing slopes.

Discussion The 3 alpine mammalian herbivores were aggregated at a broad scale but segregated at a finer scale, and their distribution was mainly determined by interspecific variables. This scale dependence is not surprising, since processes determining co-occurrence depend on the spatial scale at which species associations are analyzed (Redfern, Ryan & Getz, 2006). Co-occurrence at a coarse habitat scale may result from abiotic constraints on herbivore distribution (Redfern, Ryan & Getz, 2006) and does not necessarily imply sympatry at the smaller patch scale, because patches can be exploited differently by each species (Martin  7KLEDXOW   ,QGHHG WKH EURDGHU VFDOH DJJUHJDtion of marmots, pikas, and squirrels may suggest similar ecological requirements, and might be related to environmental variables not accounted for in the present study. The distribution of these species overlaps in different parts of their ranges, and similar associations have been described IRU HFRORJLFDOO\ HTXLYDOHQW VSHFLHV %DUDVK DE  )RU H[DPSOH %DUDVK D  UHSRUWHG WKH FRRFFXUUHQFH RI American pikas (Ochotona princeps), hoary marmots, and Columbian ground squirrels (Urocitellus columbianus) in talus slopes of Glacier National Park (Montana, USA). He hypothesized that, despite their similarities, these species were able to coexist due to differences in their spatial and TABLE II. Variables explaining the distribution of hoary marmot (a), arctic ground squirrel (b), and collared pika (c) in southwest Yukon, as assessed with Generalized Additive Models. The non-linear terms (s[x,y]) account for the spatial trends in the data. a) Hoary marmot ,QWHUFHSW 'LVWDQFHWRWDOXV 'LVWDQFHWRVTXLUUHOV 'LVWDQFHWRSLNDV s(x,y  b) Arctic ground squirrel

Estimate (± SE) “ ௅“ ௅“ ௅“ edf a  Estimate (± SE)

,QWHUFHSW “ $VSHFW “ 'LVWDQFHWRWDOXV ௅“ 'LVWDQFHWRPDUPRWV ௅“  HGI s(x,y   c) Collared pika

Estimate (± SE)

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WHPSRUDOXVHRIWDOXV%DUDVKD 3LNDVZHUHWKHPRVW GHSHQGHQWRQWDOXVDQGWUDYHOOHGVKRUWHUGLVWDQFHVWRIRUDJH although the foraging areas of marmots and squirrels overlapped, marmots tended to forage closer to boulder fields %DUDVK D  'HVSLWH KDYLQJ VLPLODU GDLO\ DFWLYLW\ SHUiods (Morrison et al.   WKHLU VHDVRQDO DFWLYLW\ DQG WKH timing of their energetic requirements suggests differences in the intensity and timing of use of certain areas. Being obligate hibernators, ground squirrels and hoary marmots need to maximize fat gain, and their activity peaks in WKH HDUO\ JURZLQJ VHDVRQ %XFN  %DUQHV   3LNDV increase their foraging behaviour later in the season, as they can rely on dry vegetation to store in their haypiles (Morrison et al.   ,QWHUVSHFLILF VHJUHJDWLRQ RI DOSLQH herbivores at a local scale seems then to be a result of ecological differences among species, rather than territorial competition for space, as has been described for other taxa 0DUWLQ 7KLEDXOW)LUWK &URZH  According to niche theory, coexistence requires some form of differentiation or partitioning between species, which might be allowed by neutral relationships, facilitation processes, or segregation at finer scales of the species’ ecological niche (e.g. %HKPHU  -RHUQ   1HXWUDO relationships may result from the exploitation of different resources, when species share non-limiting resources or when other mechanisms (e.g., disturbance) prevent comSHWLWLYHH[FOXVLRQIDFLOLWDWLRQRFFXUVZKHQVSHFLHVDPHOLRUate the habitat for other co-occurring species (Stachowicz,   ,QGHHG DOWKRXJK SRWHQWLDO FRPSHWLWLRQ DPRQJ WKH 3 species has been suggested, it has not been clearly demonstrated and no (direct) behavioural interactions have been described (Morrison et al.  WKLV VWXG\  2Q WKH contrary, it has been hypothesized that these species may KHOS UDWKHU WKDQ KLQGHU HDFK RWKHU %URDGERRNV   For example, pikas are known to respond to sympatric heterospecific calls from hoary marmots and arctic ground VTXLUUHOV E\ LQFUHDVLQJ YLJLODQFH 7UHIU\  +LN   which may help them to escape from shared predators. Ground squirrels seem to respond as well to such calls, but PDUPRWVGRWKDWPRUHUDUHO\7\VHUEXWVHH6KULQHU  IRU Marmota flaviventris). Other mechanisms by which these species may facilitate each other are habitat modification, through sharing burrows (Karels, Koppel & Hik, 2004), and feeding facilitation (Arsenault & OwenSmith, 2002). For example, pika herbivory dramatically alters plant community composition along the edges of WDOXV0F,QWLUH +LN DQGFRXOGHQKDQFHIRRGDYDLOability to the other herbivore species, as has been shown for other grazers (Mysterud et al.   ,QWHUHVWLQJO\ WKH strength and direction of the interactions among these species does not need to be symmetrical, especially among KHUELYRUHV RI GLIIHUHQW VL]HV =DPRUD  *yPH]   For example, in our study pikas were positively associated to shorter distances to arctic ground squirrels, but ground squirrels were not affected by the presence of pikas. Further studies identifying the mechanisms by which these species interact will help understand how biotic interactions structure alpine herbivore communities. Habitat selection by the 3 herbivore species was mainly determined by interspecific variables and to a lesser extent by abiotic habitat variables. In all cases, spatial distribution

ÉCOSCIENCE, VOL. 20 (3), 2013

was associated with closer distances to other herbivores, suggesting a positive effect of the presence of heterospecifics. For example, when sharing predators, less preferred prey might select habitats supporting high densities of competitors that are a preferred prey because of reduced predaWLRQ ULVN 9LMD\DQ 0RUULV  0F/DUHQ   %HVLGHV WKH mere presence of heterospecifics can also provide valuable information to animals, providing them with cues to habitat TXDOLW\)RUVPDQ6HSSlQHQ 0|QNN|QHQ WKXVWKH presence of heterospecifics could reflect other habitat variables not accounted for in the present study. In our study, habitat variables mostly reflected areas maximizing shelter from predators and weather extremes, i.e. FORVHU WR WDOXV in the case of ground squirrels, distribution was also related to more productive southwest-facing slopes. Predation risk is a main constraint for the foraging activities of these herbivores (Morrison et al., 2004) even if predator pressure might not be as high as in other habitats (Hik, McColl & %RRQVWUD  Describing the spatial associations and ecological requirements of coexisting species is a first step to understanding the potential mechanisms involved (Darmon et al.,   DQG QXOO PRGHO DQDO\VHV SURYLGH D VXLWDEOH ZD\ RI studying interactions when experimental studies are not an option (Richard et al.   ,Q WKLV VHQVH RXU VWXG\ VXJgests that these 3 alpine herbivores can (and do) coexist, by partitioning their ecological niches at a finer scale. Their aggregated pattern, together with other lines of evidence, may imply that competition is not playing a major role in VWUXFWXULQJWKHVHFRPPXQLWLHVLQWXUQSRVLWLYHDQGQHXWUDO interactions may play an important role in allowing the coexistence of herbivores inhabiting stressful, less productive ecosystems (Barrio et al.   DV SUHGLFWHG E\ WKH ³VWUHVVJUDGLHQW K\SRWKHVLV´ %HUWQHVV  &DOODZD\   /LIHKLVWRULHVRIWKHVHVSHFLHVKLEHUQDWRUVDQGDFWLYH year-round) restrict their direct interactions to the summer, when resources are most abundant in the tundra and competition might be less important. Our work represents a snapshot of a dynamic picture, and changing environmental conditions can reverse the strength and direction of interspecific interactions (Dunson 7UDYLV $OSLQHHFRV\VWHPVDUHSDUWLFXODUO\YXOQHUable to ongoing climate change (Post et al. VRXQGHUstanding these interactions and how they may change will help anticipate the potential responses of alpine herbivore guilds and their cascading effects on ecosystem functioning (Jefferies et al.  Acknowledgements Special thanks are due to F. C. Hik, A. Kolar, and R. Mitten for their invaluable help in the field, to S. Williamson for assistance with GIS, C. Calenge for statistical advice, and C. G. Bueno for helping with the modeling. T. Bao, E. Cameron, S. Nyanumba, K. Peck, A. Shaw, and H. Wheeler provided useful comments on an earlier draft. Funding was provided by the Natural Sciences and Engineering Research Council (Canada). I. C. Barrio was supported by a postdoctoral fellowship provided by the Consejería de Educación, Ciencia y Cultura (JCCM, Spain) and the European Social Fund. We thank Kluane First Nation for permission to conduct this research on their traditional lands.

Literature cited $JUDZDO$$3KHQRW\SLFSODVWLFLW\LQWKHLQWHUDFWLRQVDQG HYROXWLRQRIVSHFLHV6FLHQFH± Agrawal, A. A., D. D. Ackerly, F. Adler, A. E. Arnold, C. Cáceres, D. F. Doak, E. Post, P. Hudson, J. Maron, K. A. Mooney, M. Power, D. Schemske, J. Stachowica, S. Strauss, M. G. Turner & E. Werner, 2007. Filling key gaps in population and community ecology. Frontiers in Ecology and the (QYLURQPHQW± Arsenault, R. & N. Owen-Smith, 2002. Facilitation versus compeWLWLRQLQJUD]LQJKHUELYRUHDVVHPEODJHV2LNRV± $]HULD ( 7 - ,EDU]DEDO  & +pEHUW  (IIHFWV RI KDELWDW characteristics and interspecific interactions on co-occurrence patterns of saproxylic beetles breeding in tree boles after forest ILUH1XOOPRGHODQDO\VHV2HFRORJLD± %DQILHOG$:) %URRNV$ 7KHPDPPDOVRI&DQDGD Toronto, Ontario, Canada: University of Toronto Press. %DUDVK ' 3 D +DELWDW XWLOL]DWLRQ LQ WKUHH VSHFLHV RI VXEDOSLQHPDPPDOV-RXUQDORI0DPPDORJ\± %DUDVK'3E/DWLWXGLQDOUHSODFHPHQWLQKDELWDWXWLOL]DWLRQ RIPRXQWDLQPDPPDOV-RXUQDORI0DPPDORJ\± %DUULR , & ' 6 +LN & * %XHQR  - ) &DKLOO  Extending the stress-gradient hypothesis: Is competition among animals less common in harsh environments? Oikos, ± %HKPHU67 $-RHUQ&RH[LVWLQJJHQHUDOLVWKHUELYRUHV occupy unique nutritional feeding niches. Proceedings of the 1DWLRQDO$FDGHP\RI6FLHQFHV± %HUWQHVV 0 '  5 &DOODZD\  3RVLWLYH LQWHUDFWLRQV LQ FRPPXQLWLHV7UHQGVLQ(FRORJ\ (YROXWLRQ± %LYDQG 5 6 ( - 3HEHVPD  9 *yPH]5XELR $SSOLHG Spatial Data Analysis with R. Springer, New York, New York. %MRUQVWDG 2 1  QFI 6SDWLDO 1RQSDUDPHWULF &RYDULDQFH )XQFWLRQV 5 SDFNDJH YHUVLRQ  2QOLQH >85/@ KWWS CRAN.R-project.org/package=ncf (Accessed on st6HSWHPEHU  %URDGERRNV + (  (FRORJ\ DQG GLVWULEXWLRQ RI WKH SLNDV of Washington and Alaska. American Midland Naturalist, ± %XFN & /  % 0 %DUQHV $QQXDO F\FOH RI ERG\ FRPposition and hibernation in free-living arctic ground squirrels. -RXUQDORI0DPPDORJ\± Callaway, R. M., R. W. Brooker, P. Choler, Z. Kikvidze, C. J. Lortie, R. Michalet, L. Paolini, F. I. Pugnaire, B. Newingham, E. T. Aschehoug, C. Armas, D. Kikodze & B. J. Cook, 2002. Positive interactions among alpine plants LQFUHDVHZLWKVWUHVV1DWXUH± Cheng, E. & M. E. Ritchie, 2006. Impacts of simulated livestock grazing on Utah prairie dogs (Cynomys parvidens) in a low SURGXFWLYLW\HFRV\VWHP2HFRORJLD± Conner, L. M., M. D. Smith & L. W. Burger,. 2003. A comparison of distance-based and classification-based analyses of habitat XVH(FRORJ\± 'DQE\5.6.RK'6+LN /:3ULFH)RXUGHFDGHV of plant community change in the alpine tundra of southwest