Food-niche overlap between arctic and red foxes

1274Food-niche overlap between arctic and red foxesBodil Elmhagen, Magnus Tannerfeldt, and Anders AngerbjörnAbstract: Arctic foxes (Alopex lagopus) in Fennoscandia have retreated to higher altitudes on the mountain tundra,possibly because of increased competition with red foxes (Vulpes vulpes) at lower altitudes. In this study we comparesummer food niches of the two species in mountain tundra habitat. Arctic foxes consumed lemmings more often thanred foxes did, while red foxes consumed field voles and birds more often. Yet despite substantial variation in the dietof each species among summers, food-niche overlaps between the species were consistently high in most summers, asarctic and red foxes responded similarly to temporal changes in prey availability. Occurrences of field voles and birdsin fox scats were negatively correlated with altitude, while the occurrences of lemmings tended to increase with altitude.Since arctic foxes bred at higher altitudes than red foxes, the differences between arctic and red fox diets werebetter explained by altitudinal segregation than by differences between their fundamental food niches. Arctic foxesshould therefore endeavour to use the more productive hunting grounds at the lower altitudes of their former range, butinterference competition with red foxes might decrease their access to these areas, and consequently cause a decreasein the size of in their realised niche.Résumé : En Fennoscandie, les renards arctiques (Alopex lagopus) se sont réfugiés à des altitudes plus élevées dans latoundra de montagne, probablement à cause de la compétition plus grande des renards roux (Vulpes vulpes) aux altitudesplus faibles. Nous comparons ici les niches alimentaires des deux espèces en été dans la toundra montagneuse. Lesrenards arctiques consomment plus de lemmings que les renards roux, alors que les renards roux capturent plus decampagnols des champs et d’oiseaux. Pourtant, en dépit de la variation importante dans le régime alimentaire des deuxespèces d’un été à l’autre, les niches alimentaires des deux espèces se chevauchent considérablement la plupart desétés, alors que les animaux des deux espèces ont des réactions semblables aux variations temporelles dans la disponibilitédes proies. La présence de campagnols des champs ou d’oiseaux dans les fèces des renards est en corrélation négativeavec l’altitude, alors que la présence des lemmings a tendance à augmenter avec l’altitude. Étant donné que lesrenards arctiques se reproduisent à des altitudes plus élevées que les renards roux, les différences entre les régimes alimentairesdes deux espèces s’expliquent plutôt par la ségrégation spatiale que par des différences dans les niches alimentairesfondamentales. Les renards arctiques auraient donc intérêt à chercher à utiliser les zones productives dechasse aux altitudes plus basses qu’ils occupaient auparavant, mais la compétition d’interférence avec les renards rouxpourrait limiter leur accès à ces zones, et conséquemment, causer une diminution de leur niche réalisée.[Traduit par la Rédaction] 1285IntroductionElmhagen et al.Competition is usually classified as either exploitative orinterference (Park 1962). Interspecific competition can influencehabitat use and a superior species may exclude an inferiorone from parts of its fundamental niche or, in extremecases, make it go extinct. The arctic fox (Alopex lagopus)has a circumpolar distribution covering the arctic tundra ofNorth America and Eurasia, the Fennoscandian mountaintundra, Greenland, and Iceland (Macpherson 1969). The redfox (Vulpes vulpes) is distributed through North America,Europe, and Russia, but does not penetrate the High Arctic(Larivière and Pasitschniak-Arts 1996). Consequently, arcticand red foxes are sympatric in a relatively narrow overlapzone in the Low Arctic. The red fox is larger than the arcticReceived 22 January 2002. Accepted 27 June 2002. Publishedon the NRC Research Press Web site at http://cjz.nrc.ca on23 August 2002.B. Elmhagen, 1 M. Tannerfeldt, and A. Angerbjörn.Department of Zoology, Stockholm University, Stockholm,Sweden S-106 91.1 Corresponding author (e-mail: Bodil.Elmhagen@zoologi.su.se).fox and the northern distribution limit of the red fox couldbe determined by resource availability, while the southerndistribution limit of the arctic fox could be determined byinterspecific competition with the red fox (Hersteinsson andMacdonald 1982, 1992).During the last century, the red fox spread northwards inNorth America and Russia (Marsh 1938; Macpherson 1964;Chirkova 1968), and the number of red foxes increased onthe mountain tundra in Fennoscandia (Østbye et al. 1978;Kaikusalo and Angerbjörn 1995). In Fennoscandia there isalso evidence of a concurrent redistribution of the arctic fox.It has retreated to peripheral areas and dens at higher altitudeswithin its former range (Østbye et al. 1978; Linnell etal. 1999; Dalerum et al. 2002; Tannerfeldt et al. 2002). Atthe beginning of the 20th century the Fennoscandian arcticfox population declined drastically as a result of hunting(Lönnberg 1927). The population has not recovered, despitecomplete protection since 1940, and increased competitionwith red foxes might have contributed to the non-recovery(Hersteinsson et al. 1989). However, niche overlap is a prerequisitefor competition. If arctic and red foxes have differenthabitat or prey preferences, the redistribution could haveresulted instead from changes in the distribution of prey orother changes in the environment (Chirkova 1968; Linnell etCan. J. Zool. 80: 1274–1285 (2002) DOI: 10.1139/Z02-108 © 2002 NRC Canada

Elmhagen et al. 1275al. 1999). To assess the importance of competition betweenarctic and red foxes, it is therefore necessary to study theirniche overlap, and food niche is one dimension.Arctic foxes in Fennoscandia and other inland habitatstypically use lemmings as their primary prey, but they alsoinclude voles, birds, eggs, hares, insects, berries, and carcassesof reindeer or caribou (Rangifer tarandus) in theirdiet (Macpherson 1969; Angerbjörn et al. 1999; Strand et al.1999; Dalerum and Angerbjörn 2000; Elmhagen et al. 2000).Voles are usually the most important prey for red foxesin Sweden and northern Europe, but birds, eggs, roe deer(Capreolus capreolus), lagomorphs, insects, fruit, and berriesare also fed upon (Englund 1965; Lindström 1989; Goszczynski1974; Leckie et al. 1998; O’Mahony et al. 1999). In a review,Hersteinsson and Macdonald (1982) concluded thatboth arctic and red foxes are highly opportunistic, and suggestedthat the more limited prey base in arctic areas is theonly reason why arctic fox populations often have a less varieddiet than red fox populations. This assumption is supportedby the results of a feeding experiment in which foxescould choose between already dead prey of different species:neither red foxes nor arctic foxes showed a preference forvoles or lemmings (Barth et al. 2000). On the contrary, threedietary studies involving sympatric arctic and red foxes showedthat arctic foxes generally eat more lemmings and fewervoles than red foxes do, and it was suggested that red foxescould be more generalistic feeders (Smits et al. 1989; Frafjord1995; Frafjord 2000). However, the samples in the two earlierstudies were very small and none of the studies providedany data on prey availability. Thus, it is not possible to determinewith certainty what causes the observed dietary differences.Either arctic and red foxes could have differenthunting behaviours that result in different prey preferences,or they could be segregated on a small spatial scale andtherefore have access to different prey bases in areas wherethey are regarded as sympatric. Differences in prey preferencesindicate that there is food-niche separation betweenthe fox species and that competition may be of less importance.However, if there are no fundamental food-niche differences,spatial segregation could result from interspecificcompetition.The best way to determine if two species compete is tocompare “actual” and “virtual” niche overlaps, these beingthe local population equivalents of the realised and fundamentalniches of an entire species (Colwell and Futuyma1970). For example, food competition between mink (Mustelavision) and otter (Lutra lutra) was investigated throughcomparisons of food-niche breadths and food-niche overlapsunder sympatric and allopatric conditions (Clode and Macdonald1995). In Fennoscandia there are no areas of mountaintundra where red foxes are absent to the extent that wecould study the “virtual diet” of the arctic fox. However, wecan test whether there is small-scale spatial segregation betweenthe species with respect to altitude, an important habitatvariable. Further, lemming and vole populations fluctuateover time and relative abundances change from year to yearat all altitudes (Oksanen et al. 1999). Thus, we can alsostudy how arctic and red foxes respond to differences in preyspecies composition. If there are species-specific differencesin prey preferences, i.e., if arctic and red foxes have differenthunting behaviours, they will respond differently to changesin the composition of the prey community. Consequently,the degree of niche overlap will vary between years. If, instead,they use prey similarly, niche overlaps should be relativelyconstant in time. There are four possible scenariosdepending on the existence of spatial segregation and (or)species-specific prey use: (1) No spatial segregation, no differencesin prey preferences: arctic and red foxes have thesame diets, i.e., food-niche overlap is 100%. (2) No spatialsegregation, different prey preferences: arctic and red foxeshave different diets and the degree of food-niche overlapchanges between years. (3) Spatial segregation, no differencesin prey preferences: arctic and red foxes have differentdiets, owing to differences in the composition of the preycommunity at different altitudes, but the degree of foodnicheoverlap is consistent between years. (4) Spatial segregation,different prey preferences: arctic and red foxes havedifferent diets and the degree of food-niche overlap changesbetween years.In this study we investigated the summer diets of sympatricarctic and red foxes over 4 years to find out which scenariois enacted on the Fennoscandian mountain tundra. We testfor dietary differences between arctic and red foxes, foraltitudinal segregation between these species, and for an effectof altitude on the occurrence of different prey species intheir diets. We also study whether food-niche overlap andfood-niche breadth change between years. Finally, we discussthe implications of arctic and red fox food niches forthe degree of interspecific competition.Materials and methodsStudy areaThe study area covered 1300 km 2 of mountain tundra inthe Vindelfjällen Nature Reserve in Swedish Lapland (66°N,16°E). The main vegetation types were dry heath, grass heath,and dry fen. Plant-species diversity was low, except for somerelatively rich patches (Rune 1981). Arctic foxes bred onlyabove the tree line, which was situated at 750 m asl. Mostred foxes breed below the tree line, in birch and coniferousforests, but all red foxes included in this study inhabited formerarctic fox dens on the mountain tundra. These dens arehereinafter referred to as red fox dens. Prey species availableto the foxes were Norwegian lemming (Lemmus lemmus), fieldvole (Microtus agrestis), bank vole (Clethrionomys glareolus),grey-sided vole (Clethrionomys rufocanus), shrews (Sorex spp.),mountain hare (Lepus timidus), reindeer, rock ptarmigan(Lagopus mutus), willow ptarmigan (Lagopus lagopus), passerines(Passeriformes), ducks (Anseriformes), gulls, and waders(Charadriiformes).Lemming and vole populations are generally cyclic in arcticand mountain tundra areas (Elton 1924; Hanski et al.1991; Angerbjörn et al. 2001), but there have been occasionalprolonged interruptions in the cycle in Fennoscandia(Angerbjörn et al. 2001). During these, lemming populationsfluctuate with a periodicity resembling the normal cycle, butthe amplitude is smaller than usual. The interruptions havetherefore been described as periods without peak years, sincethe highest lemming densities are about 10 times lower thanduring “real” peaks (Angerbjörn et al. 2001; Tannerfeldt etal. 2002). The last lemming peak in Sweden occurred in1982, consequently our study was carried out during one of© 2002 NRC Canada

1276 Can. J. Zool. Vol. 80, 2002these periods. However, trapping data from our study areashowed that lemming abundance fluctuated between yearsand the highest summer density was at least 20 times higherthan during population low phases (Ecke et al. 2001). Theabundance of nesting birds does not change significantly betweenyears, although nesting success can vary (Svensson etal. 1984). We have no information on fluctuations in thereindeer and hare populations. Other predators in the areathat could interact with the fox species were wolverines(Gulo gulo) and golden eagles (Aquila chrysaëtos).Collection of scats and scat analysisWe have surveyed arctic fox dens in our study area since1985. We regard a den as inhabited when we observe foxcubs and (or) adult foxes regularly returning to and stayingat it. We also regard a den as inhabited when the amount offresh scats, prey remains, recently excavated openings, andwear and tear on the vegetation surrounding the openings indicatesthat the den is used to this extent, even though nofoxes are seen. Arctic and red fox families occasionally moveduring summer (Tannerfeldt et al. 2002). In such cases weonly used scats from one of the dens in our analyses. Thus,within the same summer, scats collected at different densrepresent different foxes.In the summers of 1993 and 1996–1998, we collectedscats from all dens inhabited by arctic or red foxes. Lemmingnest counts and snap-trapping data showed that thelemming population was in the low phase in 1993, increasedin 1996, decreased (crashed) in 1997, and remained low in1998 (Ecke et al. 2001; Tannerfeldt et al. 2002). Scats werealso collected in 1994 and 1995, but most were unfortunatelylost during storage, owing to a non-understandingmother. Most of the arctic fox scats collected in 1996 and1997 were also included in an earlier study on arctic fox diet(Elmhagen et al. 2000).We separated fresh scats, i.e., collected during the currentsummer, from older ones by their colour, position in the vegetation,and smell (Macpherson 1969; Birks and Penford1990). We made visual observations of foxes at all arctic foxdens but at only 6 of 10 red fox dens. When we did not seeany foxes, we relied on the presence of tracks and fur andthe size of openings of newly excavated dens to determinewhich species used the den. We collected scats only at inhabiteddens, so there was little risk of confusing arctic andred fox scats. There were cubs in all dens where we sawfoxes, except in 1997, when the lemming population was inthe crash phase. In that year, one cub that died early wasseen at one of three dens inhabited by arctic foxes, whilethere were cubs at one of two dens inhabited by red foxes.There can be differences between the prey eaten by adultfoxes themselves and those they bring to their cubs (Lindström1994). However, Frafjord (2000) found only one significantdifference in foxes’ diets between dens with and withoutcubs: insects occurred more often in scats from red fox denswith cubs, though insects were not an important prey item.We therefore assumed that the scats from each den gave afair representation of the prey caught by the adult foxes, independentlyof the proportion of adult to juvenile scats.Scats were dried at 105°C prior to analysis. Small or fragmentedscats were combined, so the analysed volume ofeach sample was approximately that of one medium-sizedscat. Such samples are hereinafter referred to as single scats.When more than 20 scats had been collected from a den, werandomly picked 20 for analysis. The total sample consistedof 293 arctic fox scats and 177 red fox scats from 15 and 9dens, respectively.We fragmented individual scats by hand under a magnifyingglass. We noted occurrences of different prey items andestimated the percent dry volume of mammal fur and bones,feathers, eggshells, insects, and vegetation by eye. We convertedthese volume estimates to “whole-scat equivalents” asdescribed by Angerbjörn et al. (1999). We summarized thepercent volumes of each food category in the scats collectedat the same den.Fur was identified as reindeer, hare, fox, or small mammalby means of a reference collection and microscopic charactersdescribed by Day (1966). We ignored single fox hairsand small tufts of fox hair that probably resulted from grooming.We determined lemming and vole species using descriptionsof molars in Niethammer and Krapp (1982). We didnot distinguish between bank vole and grey-sided vole, butused the category Clethrionomys spp. Shrews were also identifiedby the presence of teeth, but we did not discriminatebetween species. When teeth from more than one smallmammalspecies were found in the same scat, we used thenumber of teeth from each species to partition the volumesof fur and small-mammal bones among them. When therewere no teeth in a scat, small-mammal fur was classified as“unidentified small mammals” (Tables 1 and 3). For estimatingvolume, calculating niche overlap and niche breadth, andcorrelating the frequencies of occurrence of different preyitems with altitude, we assumed that the total volumes ofunidentified small mammals in the scats were in the sameproportions as the total volumes of small-mammal specieswhich had been identified at each den (Figs. 1 and 2, Table4). Consequently, unidentified small mammals were distributedin these categories accordingly.During the analyses we noted that teeth from small mammalsoccurred less frequently relative to the presence ofsmall-mammal fur in some years, and generally less often inred fox scats than in arctic fox scats (Tables 1 and 3). Thisappeared to be related to the proportion of voles to lemmings.If foxes handle lemmings differently from voles, theuse of teeth for estimating proportions of different smallmammals in the scats could result in a bias. However, if it isappropriate to use this method, the estimated proportions oflemmings, voles, and shrews should be approximately thesame if fur is used for identification. The fur of the Norwegianlemming is largely black and yellow, while the fur ofvoles and shrews is brown or greyish. We made coarse estimatesof the proportions of lemming and vole/shrew fur in25% steps from 0 to 100% for each scat. We compared theresults obtained through identifying teeth (where unidentifiedsmall mammals were distributed in the categories ofidentified small-mammal species) with the estimates obtainedfrom fur using Spearman’s rank-correlation tests, where eachden was treated as one unit. The two methods gave very similarresults, with significant correlations for both arctic foxes(lemmings: p < 0.001, r S = 0.85, n = 15; voles/shrews: p

Elmhagen et al. 1277Table 1. The diets of arctic foxes (Alopex lagopus) and red foxes (Vulpes vulpes) in the Vindelfjällen Nature Reserve in different years.Arctic foxes Red foxes1993(n = 15, 1 den)1996(n = 139, 7 dens)1997(n = 60, 3 dens)1998(n = 79, 4 dens)1993(n = 20, 1 den)1996(n = 18, 1 den)1997(n = 40, 2 dens)1998(n = 99, 5 dens)WSE Frequency WSE Frequency WSE Frequency WSE Frequency WSE Frequency WSE Frequency WSE Frequency WSE FrequencySmall mammals 66.7 86.7 92.8 98.6 88.3 100 87.3 88.6 50.0 80.0 94.4 100 92.5 100 82.8 99.0Lemmus lemmus 13.3 20.0 83.5 91.4 83.3 90.0 31.6 51.9 15.0 20.0 50.0 72.2 30.0 40.0 12.1 24.2Microtus agrestis 6.7 6.7 1.4 3.6 — — 29.1 44.3 5.0 5.0 11.1 22.2 35.0 42.5 29.3 49.5Clethrionomys spp. — — — — — — 2.5 5.1 — — 5.6 11.1 — 2.5 3.0 9.1Sorex spp. — 6.7 — — — — 2.5 5.1 — — — — — — — —Unidentified 46.7 66.7 7.9 10.8 5.0 10.0 21.5 34.2 30.0 60.0 27.8 44.4 27.5 32.5 38.4 60.6Birds 13.3 66.7 1.4 27.3 3.3 26.7 12.7 65.8 10.0 35.0 5.6 83.3 5.0 60.0 11.1 76.8Passeriformes 13.3 53.3 1.4 12.9 3.3 8.3 5.1 32.9 10.0 20.0 5.6 66.7 2.5 17.5 3.0 22.2Galliformes — 13.3 — — — 1.7 1.3 8.9 — 5.0 — 5.6 — 10.0 3.0 13.1Anseriformes — — — — — — 1.3 1.3 — — — — — 5.0 — —Unidentified — 6.7 — 13.7 — 16.7 3.8 19.0 — 15.0 — 16.7 2.5 27.5 5.1 32.3Reindeer (R. tarandus) 20.0 46.7 0.7 7.2 1.7 23.3 — 19.0 40.0 65.0 — 11.1 2.5 15.0 2.0 14.1Other mammals — — 2.2 2.9 — — — — — 5.0 — — — 5.0 3.0 4.0Lepus timidus — — — — — — — — — 5.0 — — — — 1,0 1.0Red fox or arctic fox* — — 2.2 2.9 — — — — — — — — — — 2,0 3.0Unidentified — — — — — — — — — — — — — 5.0 — —Eggshells — — — 0.7 — 3.3 — 2.5 — — — — — — — 1.0Insects — 13.3 — 13.7 1.7 18.3 — 15.2 — 5.0 — 16.7 — 12.5 — 10.1Vegetation — 73.3 2.9 76.3 5.0 70.0 — 70.9 — 70.0 — 66.7 — 77.5 — 76.8Note: Values shown are percent whole-scat equivalents (WSE) and percent frequency of occurrence. WSE is a measure that takes the volume of prey remains from each fox species into account. InFigs. 1 and 2, unidentified small mammals are distributed among categories of small-mammal species in the proportions suggested by the identified material.*We ignored single fox hairs or small tufts of fox hair that probably resulted from grooming. The larger quantities of fox hairs included in the table occurred once for each fox species. In both yearsthe fur appeared to be from cubs and the colours indicated that it resulted from cannibalism.© 2002 NRC Canada

1278 Can. J. Zool. Vol. 80, 2002Table 2. Food-niche overlaps and food-niche breadths for 1993and 1996–1998, calculated from the volumes of prey items in thescats (see Fig. 1).1993 1996 1997 1998Food-niche overlapPercent overlap 79.6 79.6 44.2 75.1Horn’s index 0.93 0.92 0.63 0.93Food-niche breadthArctic fox 0.41 0.026 0.023 0.33Red fox 0.33 0.12 0.20 0.29Lemming phase Low Increase Crash LowLemming index — 0.94 0.25 0.01Field vole index — 0.88 0.41 0.22Note: Lemming and vole indices show the number of animals trappedper 100 trap-nights in our study area (data from Ecke et al. 2001).are eaten in the same way by the foxes and that the numbersof teeth in the scats are proportional to the ingested proportionsof voles and lemmings. This assumption is also supportedby Lockie’s (1959) feeding experiment with redfoxes, where the number of teeth of different small-mammalspecies in the scats was proportional to the ingested proportionof each species. Thus, the method described above shouldnot yield a biased result.We identified bird feathers to the orders Passeriformes,Galliformes, and Anseriformes using the keys of Brom (1986)and Day (1966). According to these keys, Charadriiformescan be identified through the absence of some characters thatdistinguish Passeriformes. However, the number of feathersin the scats was generally low and the feathers were in poorcondition. Absence of characters could be caused by degradationof the feathers during digestion, therefore we did notattempt to identify Charadriiformes. We did not include microscopicfragments when we estimated percent dry volumefor each prey category, but we sometimes used them to identifybird orders when macroscopic remains were present. Wedid not attempt to further classify eggshells, insects, or plantmaterial.We used log-linear likelihood tests on frequency of occurrencedata to test for dietary differences between arctic andred foxes, as recommended by Reynolds and Aebischer (1991).We could test thereby the separate effects of fox species andyear on each dietary category. Owing to the large number ofcomparisons (12 dietary categories), we adjusted the level ofsignificance to 0.0042 with a Bonferroni correction. We pooledthe scats from each species and year. In years when morethan one den was represented in the sample, there were always19 or 20 scats from each den. Thus, there was no biastowards any particular den.Food-niche overlap and food-niche breadthThere has been much controversy over how to measureniche overlap (Abrams 1980; Krebs 1989). Percent overlap(Schoener’s measure) is the most commonly used (Schoener1970; Krebs 1989) and is recommended by Abrams (1980).However, Schoener’s measure is sensitive to unequal samplesizes and Horn’s index may be a better alternative in suchcases (Krebs 1989). To estimate food-niche overlap, we thereforecalculated both percent overlap (p jk ), and Horn’s index(R 0 ), i.e., the overlaps between species j and k, where p ij andp ik are the proportions of resource i in the diets of the species,and there are n different resources.R0=∑⎡ n⎤p jk = ⎢pij p ⎥ik⎣⎢∑ ( minimum , ) 100⎦⎥( p + p ) log( p + p ) −∑p log p −∑ p log p2 log 2ij ik ij ik ij ij ik ikFor each year we calculated food-niche overlap from theaverage volumes of prey remains in the scats. Three preycategories, eggs, insects, and vegetation, were present onlyin trace amounts and other studies have shown that they areof negligible importance in fox diets in this area (Elmhagenet al. 2000; Frafjord 2000). If there are many resource states,niche overlaps become biased (Smith and Zaret 1982). Forthese two reasons we excluded eggs, insects, and vegetationfrom the calculations. Fox was also excluded. Large volumesof fox hairs were found in scats at one red and one arctic foxden, but the hair colours indicated that they had resultedfrom cannibalism. Consumption of already dead cubs hasbeen observed earlier in arctic foxes (Frafjord 1993; Dalerumand Angerbjörn 2000). Dead cubs are a food resource forsurviving siblings and their parents, but they are not prey inthe same sense as other species are.To compare the dietary variation between species with thevariation within species each summer, we did pairwise calculationsof food-niche overlap between dens inhabited byarctic and red foxes. Only years with more than one den inthe sample could be included. Because sample sizes werethe same at each den, we calculated only percent overlap.We then calculated the average food-niche overlap withineach species each year. We also did pairwise calculations offood-niche overlap between years within and between species.Sample sizes varied among years, so we calculatedboth percent overlap and Horn’s index.Niche breadth is a measure of the degree of specializationof a species, and to estimate food-niche breadth, we usedLevin’s measure, B A , standardized on a scale from 0 to 1,where p i is the proportion of resource i in a diet consistingof n resources (Hurlbert 1978; Krebs 1989):BA =⎡⎢⎛ ⎢⎜⎣⎝∑1p2i⎞ ⎤n⎟ − 1⎥( − 1)⎠ ⎥⎦For each year we calculated food-niche breadth from theaverage volumes of prey remains in the scats. We includedthe same prey categories as for calculations of food-nicheoverlap.Effect of altitudeWe tested for a difference in altitude between the arcticand red fox dens included in this study (logistic regression).We also performed Spearman’s rank-correlation tests to comparethe frequencies of occurrence of the most importantprey species with altitude.ResultsSmall mammals, particularly lemmings and field voles,were the most important prey of both arctic and red foxes,© 2002 NRC Canada

Elmhagen et al. 1279Table 3. The separate effects (partial associations) of fox species and year on the occurrenceof different prey categories in a log-linear likelihood test.Prey category Effect df χ 2 pSmall mammals (total) Year 3 21.7

1280 Can. J. Zool. Vol. 80, 2002Fig. 1. The diets of arctic foxes (Alopex lagopus) (a) and red foxes (Vulpes vulpes) (b) in different summers. Unidentified remains ofsmall mammals (see Table 1) are distributed among categories of identified small-mammal species according to the distribution ofthose species in the scats.often in arctic fox scats than in red fox scats in 1993, whilethe reverse was true in other years (Tables 1 and 3). Passerines,ptarmigans, and ducks were all utilized by both foxspecies. Passerines were consumed most often, while duckswere eaten on only a few occasions. On average, red andarctic foxes ate passerines equally often. However, red foxesate passerines more often than arctic foxes did in 2 years,while the reverse was true in the other 2 years. Therefore,the three-way interaction between year, species, and passerineswas significant, although there were no significant twowayinteractions. There were no effects of fox species oryear on the occurrence of ptarmigan and ducks in the scats(Tables 1 and 3).There were no effects of fox species or year on the occurrenceof eggshells, insects, or vegetation in the scats (p >0.28). Eggshells and insects occurred infrequently and innegligible volumes. Vegetation occurred frequently in thescats, but only in trace amounts (Table 1).To summarize, there were three important differences betweenarctic and red fox diets: lemmings occurred more oftenin the diet of arctic foxes, while field voles and birdsoccurred more often in the diet of red foxes. However, thesummer diets of both species varied over time and the frequenciesof occurrence of lemmings, field voles, reindeer,and birds in the diets varied significantly among years.Food-niche breadth and food-niche overlapThe diets of both fox species varied considerably amongyears and this was reflected by large variations in food-nicheoverlap within species among years. The average percent© 2002 NRC Canada

Elmhagen et al. 1281Fig. 2. Frequencies of occurrence of different prey species atarctic and red fox dens at different altitudes. Solid symbols denotedens inhabited by arctic foxes and open symbols denotedens inhabited by red foxes. For the two species and all yearscombined, there was a tendency towards a positive correlationbetween altitude and occurrence of lemmings (a), but there weresignificant negative correlations between altitude and occurrenceof field voles (b) and birds (c).100806040200100806040200100806040200(a)199319961997800 850 900 950 1000 1050 1100(b)199319961997800 850 900 950 1000 1050 1100(c)199319961997800 850 900 950 1000 1050 1100overlap between summers was 60.8% for arctic foxes and58.5% for red foxes (Table 4). Using Horn’s index, the averagefor arctic foxes was 0.79 (range 0.68–0.98). The averagefor red foxes was also 0.79 (range 0.68–0.93). Nevertheless,food-niche overlap between arctic and red foxes was consistentlyhigh in three out of four summers (percent overlap75.1–79.6%; Horn’s index 0.92–0.93), with a smaller overlapin 1997 (44.2% and 0.63, respectively; Fig. 1, Tables 2and 4). In 1997, however, food-niche overlap was smallerwithin red foxes than between arctic and red foxes. Theoverlap within arctic foxes seemed to be higher than betweenspecies when the lemming population was in the increaseand crash phases, while overlaps within and betweenspecies were similar during the lemming low phase in 1998(Table 4).Arctic foxes had narrower food-niche breadths than redfoxes during the lemming increase and crash phases (1996–1997), while both fox species were relatively generalisticwhen the lemming population was in the low phase (1993,1998; Fig. 1, Table 2).Effect of altitudeWe found small-scale spatial segregation between the foxspecies. Dens inhabited by arctic foxes were situated at higheraltitudes than those inhabited by red foxes (logistic regression,p < 0.001, χ 2 = 18.7, df = 1, n = 24). Dens used exclusivelyby red foxes were found between 800 and 900 m asl,while those used solely by arctic foxes were found at 880–1100 m asl. Two dens situated at 900 and 920 m asl wereused alternately by both fox species. However, red foxeswere never found at higher altitudes than arctic foxes duringthe same summer (Fig. 2).For arctic and red foxes combined, there were significantnegative relationships between altitude and the occurrence offield voles (p = 0.013, r S = –0.50, Fig. 2b) and birds (p =0.024, r S = –0.57; Fig. 2c) in the diets. There was also a tendencytowards a positive relationship between the occurrenceof lemmings and altitude (p = 0.057, r S = 0.39; Fig. 2a).None of the relationships were significant if the fox specieswere treated separately. There was no relationship betweenthe occurrence of reindeer in the diets and altitude (p = 0.41,r S = 0.18).DiscussionLemmings, field voles, birds, and reindeer were the essentialprey species for both arctic and red foxes in the VindelfjällenNature Reserve. However, lemmings occurred more frequentlyin arctic fox scats than in red fox scats, while field voles andbirds occurred more often in red fox scats than in arctic foxscats. Reindeer occurred equally often in the scats of bothfox species. Other prey items, i.e., Clethrionomys spp., shrews,mountain hare, eggs, and insects, occurred infrequently andwere probably of little importance to either fox species. Shrewsoccurred only in the scats of arctic foxes, but both arctic andred foxes generally dislike and avoid eating shrews (Lockie1959; Chesemore 1968; Barth et al. 2000). Hares occurredonly in the scats of red foxes, but other studies have shownthat arctic foxes sometimes include hares in their diet(Macpherson 1969; Birks and Penford 1990; Strand et al.1999; Frafjord 2000). Thus, the absence of shrews in red foxscats and hares in arctic fox scats may not be related to foxspecies, but to random occurrences of rare prey.© 2002 NRC Canada

1282 Can. J. Zool. Vol. 80, 2002Table 4. Percent overlaps between and within fox species in different summers.Within speciesYearLemmingphase Between species Arctic fox Red fox1993 Low 79.6 — —1996 Increase 79.6 91.9 (83–100) —1997 Crash 44.2 90.6 (88–94) 28.71998 Low 75.1 79.3 (71–85) 75.9 (54–92)Between summers 54.7 (28.8–84.2) 60.8 (46–97) 58.5 (45–83)Note: For years when there were scats from more than one den, food-niche overlaps within speciesare shown as the average from pairwise calculations of overlap between the dens. The last row showsthe average of pairwise calculations of overlap between summers. Numbers in parentheses are ranges.There was spatial segregation between the fox specieswith respect to altitude. Our dataset is therefore representativeof what appears to be the general pattern on the mountaintundra in Fennoscandia: arctic foxes use dens at relativelyhigh altitudes, while red foxes occupy dens at lower altitudes(Østbye et al. 1978; Linnell et al. 1999; Dalerum et al. 2002).For the two species combined, consumption of field volesand birds decreased with increasing altitude, while consumptionof lemmings increased with altitude. These results areconsistent with those of Frafjord (2000). Field voles preferproductive tundra habitats and are generally more abundantat lower altitudes, while lemmings are more common in unproductivehabitats and at relatively higher altitudes (Oksanenand Oksanen 1992; Oksanen et al. 1999). Birds are far lessabundant in unproductive than in productive tundra habitat(Svensson et al. 1984). Productivity generally decreases withincreasing altitude, so the observed relationships probablyreflect changes in prey abundance.Two dens were used alternately by arctic and red foxes.Although a small number of individuals were involved, theirdiets are interesting, since the species hunted in approximatelythe same territories, i.e., at the same altitude. Thefirst den, at 900 m asl, was inhabited by arctic foxes duringthe year of the lemming increase phase (1996) and by redfoxes during a lemming low phase (1998). Lemmings occurredmore often in arctic fox scats than in red fox scats,while the reverse was true for field voles and birds (Fig. 2).The second den, at 920 m asl, was inhabited by arctic foxesin 1996–1998 and by red foxes during the lemming lowphase in 1993. Lemmings occurred frequently in arctic foxscats during the lemming increase- and crash-phase years(1996–1997), while occurrences of lemmings dropped markedlyduring the low-phase years, 1998 and 1993, when theden was inhabited by arctic and red foxes, respectively. Fieldvoles rarely occurred in the scats of either species, exceptfor 1998, when there was a marked increase in the occurrenceof field voles in arctic fox scats (Fig. 2).For each year, occurrences of different prey in scats atthese dens were similar to those that would be expectedbased on the general patterns of diet composition and preyavailability in these years. This indicates that interspecificdifferences in diet can be predicted on the basis of preyavailability only, and do not require differences in prey preferenceto explain them.Since arctic and red foxes were spatially segregated, neitherscenario 1 nor 2, described in the Introduction, explainsthe differences between arctic and red fox diets. However,we found significant temporal differences in foxes’ diets andthis variation was reflected in relatively low average foodnicheoverlap between years within each species (60.8 and58.5% for arctic and red foxes, respectively). Despite this,food-niche overlap between the species was consistently highin 3 out of 4 years (75.1–79.6%). During the lemming increasephase, arctic and red foxes mainly consumed lemmings.During lemming low phases, food-niche overlap remainedhigh, owing to increased consumption of the same alternativeprey: reindeer, voles, and birds in 1993 and voles andbirds in 1998. In one year, 1997, foxes deviated from thispattern, but the variation within red foxes was larger thanthe variation between the species. This may indicate that denwas a more important factor for diet than species. Eitherway, the dominant pattern was that arctic and red foxes respondedsimilarly to changes in prey availability, and nicheoverlap was relatively constant between years, which supportsscenario 3. Thus, arctic and red foxes have similarprey preferences, while the spatial segregation between themcould have caused the observed differences in diets.Our samples were larger than that in two earlier comparisonsof arctic and red fox diets (Smits et al. 1989; Frafjord1995), but were still small in some years. There are severalreasons why samples were small despite our large studyarea. The arctic fox in Sweden is threatened with extinction.Further, since arctic foxes’ reproduction depends heavily onlemming availability (Strand et al. 1999; Elmhagen et al.2000), only a few dens were inhabited in years when lemmingdensity was low. On the other hand, the number ofdens inhabited by red foxes on the mountain tundra is independentof lemming phase but positively correlated withvole availability in surrounding forests (unpublished data).This is also reflected in our sample sizes. The numerical responsesof arctic and red foxes to lemming and vole availabilityled to skewed samples between both years and foxspecies. However, since arctic and red fox diets are affectedby temporal variation in lemming and vole availability, thetemporal aspect should be included in comparisons of theirdiets. Frafjord’s (2000) study on arctic and red fox diets inFennoscandia over 5 years involved a large sample but wasskewed between years and fox species. He did not considervariation in prey availability. He concluded that environmentalfactors explained most of the differences between red andarctic fox diets in Fennoscandia, but suggested that arcticfoxes depended more on lemmings than red foxes at thesame altitude did. Thus, he suggested that arctic and redfoxes would use similar prey bases differently. Although our© 2002 NRC Canada

Elmhagen et al. 1283sample was small in some years, the overall pattern indicatesthat arctic and red foxes would use similar prey bases similarly.Differences between the species at the same altitudeswere more likely due to temporal variations in prey availability,since they were never found at the same altitude inthe same year.Food-niche breadths varied substantially among years forboth species. Arctic foxes showed a higher degree of specializationthan red foxes when the lemming population wasin the increase and crash phases. During lemming low phases,both fox species were relatively generalistic. These variationsin food-niche breadth are probably consequences ofopportunistic feeding behaviours. When lemmings are abundant,both species use them to a large extent, but when lemmingdensities are low they find other prey. Since arcticfoxes were found at altitudes where lemmings should makeup a relatively larger proportion of the prey community, theyshowed more pronounced shifts between specialized andgeneralized feeding strategies.The opportunistic feeding behaviour of arctic foxes is welldocumented. Arctic foxes in coastal habitats have access tomore types of prey than inland foxes do, and have a more diversifieddiet (Chesemore 1968; Fay and Stephenson 1989;Birks and Penford 1990; Hersteinsson and Macdonald 1996;Kapel 1999; Anthony et al. 2000). Foxes near bird coloniesincrease their consumption of birds and eggs upon the arrivalof migrating birds (Stickney 1991; Bantle and Alisauskas1998), while foxes in areas where prey are locally abundantadjust their use of habitat according to seasonal changes inprey distribution (Jepsen et al. 2002).Red foxes in southern Sweden have more diversified dietsthan those in northern Sweden (Englund 1965; Lindström1982). Red fox populations are also relatively stable in thesouth. No direct relationship has been demonstrated betweenreproduction and the availability of any particular prey species,and southern red fox populations are likely to be sociallyregulated. In contrast, the sizes of northern populations varymarkedly with the vole cycle (Englund 1970; Lindström 1989).Thus, just as arctic foxes in inland and coastal habitats havedifferent feeding strategies, there appears to be a south–north gradient in the feeding strategies of red foxes. Alongthe gradient of decreasing productivity in Sweden, from northernforests to low-production mountain tundra, red foxesshould have progressively less varied diets. This is supportedby Englund’s (1965) finding that red foxes on the mountaintundra consumed fewer birds than those in the forest.Because of their larger body size, red foxes require higherprey densities to sustain themselves than arctic foxes do(Hersteinsson and Macdonald 1992), and red foxes are usuallyfound in dens at lower altitudes, i.e., in more productiveareas. However, if arctic and red foxes are equally opportunisticand there are no differences between their virtual foodniches, it is difficult to see why arctic foxes would notendeavour to use the lower parts of their former range. Further,avoidance of lower altitudes, which has also been indicatedby radio-tracking of arctic foxes in Fennoscandia (Landa etal. 1998), is the opposite of the behaviour of arctic foxes onSvalbard, where productive habitats are favoured and morebarren areas avoided (Jepsen et al. 2002). Instead, competitionwith red foxes may explain why arctic foxes have retreatedto higher altitudes, and the high degree of food-nicheoverlap indicates that arctic and red foxes should competefor the same areas, as suggested by Hersteinsson and Macdonald(1982, 1992).What competitive mechanisms, then, may be important?Arctic and red foxes are territorial towards each other(Tannerfeldt et al. 2002) and it is unlikely that red foxes severelyreduce prey densities in areas outside their territorialborders. Exploitative competition should therefore be of littleconsequence on a larger scale. Instead, observations inthe wild and experiments involving penned individuals haveshown that red foxes predominate over arctic foxes and cankill both adults and juveniles (Rudzinski et al. 1982; Schameland Tracy 1986; Frafjord et al. 1989; Korhonen et al. 1997;Tannerfeldt et al. 2002). Arctic foxes also seem to avoid reproducingin dens near reproducing red foxes, which indicatesthat there is a competitive mechanism by which redfoxes can influence the distribution pattern of arctic foxes(Tannerfeldt et al. 2002). Interference competition, mediatedthrough territorial and encounter competition (Schoener 1983),could therefore be a mechanism of habitat segregation, withred foxes occupying the more productive habitats. The restrictedprey base in unproductive habitat will make arcticfoxes more dependent on lemmings than red foxes are.Therefore, competition between red and arctic foxes must beconsidered in efforts to conserve the arctic fox population inFennoscandia (Löfgren and Angerbjörn 1998).We conclude that arctic and red foxes on the Swedishmountain tundra have similar virtual food niches. Observeddifferences in arctic and red fox diets appear to be consequencesof spatial segregation that may, in turn, be causedby interference competition. The red fox is the strongercompetitor and might exclude the arctic fox from more productiveareas. Thus, an expansion of the range of the red foxduring the 20th century might have led to a reduction in theactual niche of the arctic fox.AcknowledgementsWe are grateful for funding from Oscar and Lili Lammsstiftelse, Carl Tryggers stiftelse, foundations at the RoyalSwedish Academy of Science, Magnus Bergvalls stiftelse,European Union LIFE-Nature, and World Wildlife Fund Sweden.Fjällräven AB, AB Dogman, Campbell’s, Milko, CloettaFazer, and Tågkompaniet supplied products that were usedin this project. We are also grateful for all the hard work putin by voluntary field workers.ReferencesAbrams, P. 1980. Some comments on measuring niche overlap.Ecology, 61: 44–49.Angerbjörn A., Tannerfeldt, M., and Erlinge, S. 1999. Predator–prey relations: arctic foxes and lemmings. J. Anim. Ecol. 68:34–49.Angerbjörn, A., Tannerfeldt, M., and Lundberg, H. 2001. 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