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- Materials and methods
1. The number of breeding dens and litter sizes of arctic foxes Alopex lagopus were recorded and the diet of the foxes was analysed during a ship-based expedition to 17 sites along the Siberian north coast. At the same time the cyclic dynamics of co-existing lemming species were examined.
2. The diet of arctic foxes was dominated by the Siberian lemming Lemmus sibiricus (on one site the Norwegian lemming L. lemmus), followed by the collared lemming Dicrostonyx torquatus.
3. The examined Lemmus sibiricus populations were in different phases of the lemming cycle as determined by age profiles and population densities.
4. The numerical response of arctic foxes to varying densities of Lemmus had a time lag of 1 year, producing a pattern of limit cycles in lemming–arctic fox interactions. Arctic fox litter sizes showed no time lag, but a linear relation to Lemmus densities. We found no evidence for a numerical response to population density changes in Dicrostonyx.
5. The functional or dietary response of arctic foxes followed a type II curve for Lemmus, but a type III response curve for Dicrostonyx.
6. Arctic foxes act as resident specialist for Lemmus and may increase the amplitude and period of their population cycles. For Dicrostonyx, on the other hand, arctic foxes act as generalists which suggests a capacity to dampen oscillations.
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- Materials and methods
The Arctic tundra communities may appear simple due to low diversity and relatively uncomplicated food webs. Nevertheless, the population dynamics of many tundra species and interactions between their determinants are intriguingly complex. One of the major features of these systems are drastic fluctuations of some herbivore populations, which in turn influence a majority of the mammalian and avian species in the community. In boreal forests in North America, snowshoe hares Lepus americanus Erxleben are the pivot of these fluctuations, with a period of roughly 10 years (Elton & Nicholson 1942; Sinclair et al. 1993; Boutin et al. 1995). In Eurasia, the pattern is governed by 3–5 years fluctuations of lemmings (Lemmus and Dicrostonyx spp.) and voles (Clethrionomys and Microtus spp.) (Collett 1911–12; Hansson & Henttonen 1985; Stenseth & Ims 1993). The fluctuations are referred to as cycles, although they may, in fact, be chaotic with a strong periodic element (Oksanen & Oksanen 1992; Hanski et al. 1993). The cause of these hare and lemming cycles are not yet fully understood, but a number of recent studies have suggested that predators play a critical role (e.g. Erlinge et al. 1983, 1984; Erlinge 1987; Tostel et al. 1987; Korpimäki & Norrdahl 1989; Korpimäki, Norrdahl & Rinta-Jaskari 1991; Hanski et al. 1993; Hanski & Henttonen 1994; Hanski & Korpimäki 1995; Krebs et al. 1995). Small mustelids are suggested as the most influential predators ‘in the north’ (Hanski et al. 1993). In models of this predator–prey complex, the least weasel (Mustela nivalis L.) and Microtus voles are the presumed key species (Korpimäki et al. 1991; Hanski & Korpimäki 1995). Most of these studies have concentrated on the boreal taiga zone. On the Arctic tundra, however, the dominant rodents are lemmings and it has not been shown that small mustelids here play the suggested key role. In some areas, as on the Wrangel Island, where lemming numbers fluctuate in a pronounced cyclic pattern (Chernyavskii & Tkachev 1982; Ovsyanikov 1993), small mustelids are absent (Dorogoi 1987). If the suggested predator-generated fluctuations are valid also for lemming cycles, there may be other predators on the tundra that assume a role similar to that of weasels.
Nomadic avian lemming predators can be abundant on the tundra, especially during summers with rodent peaks (Potapov 1997; Wiklund, Kjellén & Isaksson 1997). The most important of these are long-tailed, pomarine and arctic skuas (Stercorarius longicaudus Vieillot, S. pomarinus Temminck, S. parasiticus L.), snowy owls Nyctea scandiaca (L.) and rough-legged buzzards Buteo lagopus Pontoppidan. However, these species lack a number of traits which have been assumed for the dominant predator in the models mentioned above. First, avian predators are not present during the winter season, which means that rodents have a complete refuge from these predators for three-quarters of the year. Secondly, they usually give up breeding and move elsewhere during rodent lows, and hence do not deepen and prolong rodent population crashes in the way mustelids are suggested to do (Hanski & Korpimäki 1995; Potapov 1997). Thirdly, the numerical response of avian lemming predators shows no time lag (Potapov 1997; Wiklund et al. 1997). This is because many have a generalist diet or migrate when food abundance decreases.
Instead, the arctic fox Alopex lagopus (L.) is a strong candidate for being a most influential lemming predator. Due to its habit of food caching and a slightly less specialized diet, adult mortality is not so strongly influenced by rodent crashes as in mustelids (Hiruki & Stirling 1989; Tannerfeldt & Angerbjörn 1996). Also, arctic foxes have the capacity to migrate over vast distances. Arctic fox breeding success and population dynamics are nonetheless strongly influenced by lemming populations in areas where the species co-exist (Macpherson 1969; Ovsyanikov 1993; Angerbjörn et al. 1995; Kaikusalo & Angerbjörn 1995; Tannerfeldt & Angerbjörn 1998). Furthermore, arctic foxes are present on the tundra also in winter and they often stay in an area once they have established a territory (Tannerfeldt & Angerbjörn 1996). All these features are characteristic of the modelled predators. Further investigations of the role of arctic foxes in lemming dynamics are thus warranted. The interaction has so far only been examined from the view-point that lemmings govern fox populations.
The role of predation in intraguild relationships between prey species is little known, but has gained recent attention (Boutin 1995; Schmitz 1995; Abrams & Matsuda 1996; Hanski & Henttonen 1996). In most of the Arctic, lemmings of the genus Lemmus co-exist with Dicrostonyx. These differ in habitat preference and in diet. Lemmus occur preferably in wet grasslands and feed mainly on sedges, grasses and moss (Batzli 1993). Dicrostonyx prefer dry sandy areas and feed primarily on dicotelydones, such as Salix spp. and Dryas spp. (Batzli 1993). Co-existing microtines are exposed to similar variations in predation pressure and their dynamics seem to be linked (Henttonen et al. 1987; but see Pitelka & Batzli 1993).
Arctic fox predation patterns are also interesting in themselves. The foxes show a large intraspecific variation in diet and with this follow striking differences in life history traits and population dynamics (Hersteinsson 1990; Tannerfeldt & Angerbjörn 1998). Furthermore, the arctic fox is a species of significant economic value to the human inhabitants of the Arctic. If we are to evaluate the role of the arctic fox in the tundra community, we must understand its predation patterns. In this study, we examine the predatory relationship, in terms of functional and numerical response, of arctic foxes in relation to changes in lemming densities on the Siberian tundra.
Materials and methods
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- Materials and methods
The study was performed during a ship-based expedition along the north coast of Siberia in the summer of 1994 where we visited 17 sites, from the Kola Peninsula in the west to Wrangel Island in the east (Fig. 1). The sites were not situated in coastal habitat. At each site, Erlinge and co-workers censused lemming populations, focusing on the Siberian lemming Lemmus sibiricus (Kerr) (Erlinge et al. 1995), whereas Angerbjörn and Tannerfeldt surveyed arctic fox dens and collected scats for diet analysis (Angerbjörn et al. 1995). Some of the western sites were visited twice (sites 1–5 and 8–10). For arctic foxes, data collected during the second visit have been pooled with data from the first visit (Table 1). During the 3-month expedition, we covered 1464 km2 and inspected 142 arctic fox dens. Normally, the predatory response to prey population fluctuations are discussed for one population along a time scale. We instead use each population as a data point and construct response curves along a gradient of prey densities.
Table 1. Summary of arctic fox inventories. Site numbers and names follow Hedberg (1995). Asterisk (*) denotes data that were excluded from calculations; at site 3 due to absence of rodents, at other sites due to small sample sizes. The summation ‘Total’ is only of scats included in the analyses
|Site no.||Site name||Inv. area (km2)||Fox dens per 100 km2||Breeding foxes per 100 km2||Fox litter size means ± SD||No. fresh fox scats||No. old fox scats|
|1||Kola Peninsula||109||2·50||3·67|| ||48||2*|
|2||Kanin Peninsula||79||1·67||2·53|| ||2*||40|
|3||Kolguyev Island||70||4·44||5·71|| ||19*||22*|
|4||Pechora Bay||84||3·33||7·14||2·50 ± 0·71||62||20|
|5||W Yamal Peninsula||93||3·63||10·75||2·50 ± 2·12||166||30|
|6||N Yamal Peninsula||39||2·56||5·13||1·00 ± 0·00||50||0|
|8||NW Taymyr Peninsula||79||6·67||10·13||2·50 ± 0·71||35||25|
|9||Chelyuskin Peninsula||65||4·00||6·15|| ||25||25|
|10||NE Taymyr Peninsula||104||10·00||9·62|| ||35||15|
|11||Olenëkskiy Bay||90||1·11||2·22|| ||30||20|
|12||Yana Delta||67||13·43||26·87||4·70 ± 2·56||50||20|
|13a||N.S.I. Faadeyevskiy||100||14·00||28·00||3·12 ± 1·55||75||20|
|13b||N.S.I. Kotel’nyy||35||14·29||28·57|| ||40||30|
|14||Indigirka/Lopatka||130||12·31||24·62||3·19 ± 1·52||50||10|
|15||Kolyma Delta||110||2·73||5·45|| ||10||0|
|16||Ayon Island||50||4·00||8·00||2·00 ± 0·00||30||30|
|17||Wrangel Island||160||6·25||12·50||4·00 ± 2·24||45||35|
|Total|| ||1464||5·00||11·59||3·54 ± 2·01||751||320|
Censusing arctic foxes
Arctic fox dens are usually situated in characteristic landforms and have lush vegetation, making them relatively easy to locate (e.g. Smits et al. 1989; Prestrud 1992a; Smith et al. 1992). A single visit at a den was sufficient to detect if it was occupied with a litter or not. We are convinced that we found a similar proportion of dens in all inventoried areas and that this was a majority of all breeding dens in the area. A longer stay was needed at each den to observe the number of adult foxes and to estimate litter size. Litter size estimates were made between June 25 and August 26, i.e. when the cubs were between 3 and 12 weeks old. These estimates must be regarded as minimum numbers (Garrott, Eberhardt & Hanson 1984; Tannerfeldt & Angerbjörn 1998). It should also be noted that the long time span make litter size comparisons between populations uncertain. We have assumed that each breeding den was occupied by two adult foxes. In a total of 85 breeding dens, there was only one observation of three adults at the same den. The number of occupied dens multiplied by two was used as an index of density of breeding arctic foxes (Angerbjörn et al. 1995). The area inventoried at each site varied from 35 to 160 km2 (Table 1), mostly dependent on the number of hours spent at each site.
Examining lemming populations
We follow Jarrell & Fredga (1993) and regard collared lemmings from all visited sites as one species, Dicrostonyx torquatus (Pallas). The Siberian lemming Lemmus sibiricus is the only Lemmus at all sites except no. 1, the Kola Peninsula, where it is replaced by the Norwegian lemming L. lemmus (L.). The brown lemming L. trimucronatus Davis has been reported from site 16, Ayon Island, but is now considered a synonym to L. sibiricus (Corbett & Hill 1991; Wilson & Reeder 1993). When discussing the genera separately, we use the terms ‘Lemmus’ and ‘Dicrostonyx’, respectively, while the term ‘lemmings’ refers to both genera combined.
The population densities of lemmings were estimated by trapping. We concentrated our trapping effort on the Siberian lemming. Relative density estimates of Siberian lemmings were obtained according to a standardized grid snap-trapping program, the ‘small quadrate method’ (Myllimäki et al. 1971). On each locality generally 20 quadrates (15 × 15 m) were set out, each with 12 traps (three in each corner of the quadrate). The site of a trap was carefully chosen and if possible the traps were set at the entrance of a nest or across a lemming runway. We placed the quadrates about 50 m apart on representative and suitable habitat for the Siberian lemming (wet grasslands). The traps were checked every 8 h and trapping was carried out for 24 h on each locality. Site 16 was an exception with only 50 trap-nights (Table 2). In this trapping programme, the number of captured Lemmus per 100 trap-nights was used as an index of their population density. To obtain further information on the demography of Siberian lemming populations we placed additional traps at selected places where there were signs of recent lemming activity.
Table 2. Relative density of Lemmus spp. and Dicrostonyx torquatus populations, with age profile and phase of examined Lemmus sibiricus populations. Density of Lemmus is measured as number of animals captured per 100 trap-nights with the small quadrate method, whereas for Dicrostonyx and total lemming density it is number of animals captured per 24 h with selectively set traps (see text for details). n is the number of examined L sibiricus for age and phase determination. Age profile is based on weight of eye-lenses; the figures are the average of the lens-weights of each population. Note that the lens-weights are not comparable for mainland and island populations (lemmings on islands were about 40% heavier). Phase determination is based on information on age profile of the population, captures and estimated density during previous season (indicated by the frequency of old lemming faeces, winter nests and lemming runways). During the second visit to some sites (2nd) additional captures were made of L sibiricusfor population phase analyses. Lemming trapping at site 4 was insufficient for analysis. Asterisk (*) denotes Lemmus indices not used in comparisons with arctic fox data
Body weight and sex of captured Siberian lemmings were determined. We removed eye-lenses to be used for age determination according to Hagen et al. (1980). The weight of eye-lenses made it possible to separate five cohorts: juveniles and sub-adults (less than 2 and 4 months old, respectively), and three categories of adults, adult 1 (4–8 months and born in preceding winter), adult 2 (9–14 months and born in previous summer), and adult 3 (more than 14 months old). The detailed data on age determination will be published separately (Sam Erlinge et al. unpublished data). The data on Siberian lemmings permitted us to determine in which phase the examined population was. In doing so, we used information on present and previous densities together with information on the age profile of the population. Estimates on previous densities were based on the amount and frequency of old lemming faeces and earlier used runways in typical Siberian lemming habitats. A population in the increase phase is expected to have medium present density and indications of low past density; typically, the age profile should be dominated by younger age categories. A population in the peak phase, on the other hand, is expected to have a high density, both in the preceding and present season. Furthermore, the population should have a relatively high frequency of older individuals. A population in the decline phase should have a moderate present density and high past density, and an age profile dominated by older cohorts. The low phase is characterized by very low present density and indications of higher previous density.
As discussed earlier, Lemmus and Dicrostonyx have different habitat preferences (Rodgers & Lewis 1986; Batzli 1993). The grids were set to trap Lemmus, but Dicrostonyx were also trapped to some extent. However, we do not consider this trapping efficient for estimates on Dicrostonyx density. Other scientists on the expedition trapped lemmings, especially Dicrostonyx, for genetic and taxonomic analyses (Fredga et al. 1995). They used a constant number of 200 Sherman live traps and 50 snap-traps, set selectively at active Dicrostonyx holes at each site (Vadim Fedorov, personal communication). We have used the number of Dicrostonyx trapped by Fredga and co-workers divided by the time the 250 traps were active, i.e. number of trapped animals per 24 h (per 250 traps). We call this estimate ‘Dicrostonyx index’ (Table 2). It is important to note that this index has a different scale than the number of Lemmus per 100 trap-nights. For an estimate on both species together, we have therefore calculated a ‘total lemming index’. It is derived in the same way as the Dicrostonyx index, but also includes total captures of Lemmus by selective and grid trapping, again per 24 h (Table 2). We have used the most reliable index type for each category of lemmings and the indices cannot be compared directly. However, testing for Lemmus, the two types of trapping indices were highly correlated (r = 0·85, P = 0·0001, n = 15).
Analysis of arctic fox scats
We collected arctic fox scats at occupied dens. Fresh scats, from the summer of 1994, were separated from older scats by appearance. Older scats are dry and weathered or overgrown by recent vegetation. Fresh and old scats contained similar proportion of migrating birds, indicating that scats on the dens were from summers only, making age separation easier. We ignored scats that were 2 years or older, as determined by extensive weathering, generally being white and brittle, or overgrowth of vegetation from previous seasons. Scats were dried at 90°C and prey remains were identified using reference material. In the analysis of scats we identified rodent species, reindeer Rangifer tarandus (L.), mountain hare Lepus timidus L., bird groups (ducks and geese, ptarmigan and grouse, waders, passerines), insects and plant material, as far as possible. At site 3, Kolguyev Island, we found rodent remains in one of the arctic fox scats (n = 41). This is the first report of rodents from the island, but the remains were only 20% by volume in the single scat and we were unable to determine the species. Since the amount was negligible, we excluded data from this site from all analyses of predatory response to rodents. The remains of Lemmus in the scats followed known distributions, with the Norwegian lemming Lemmus lemmus only on site 1, the Kola Peninsula, and the Siberian lemming L. sibiricus on all other sites. The collared lemming Dicrostonyx torquatus is not known for sites 1 and 13a (Faadeyevskiy Island). We found remains of Dicrostonyx in five out of 40 arctic fox scats from site 13b (Kotel’nyy Island), where the species previously was unknown.
We used a modified frequency of occurrence measure to estimate the amount of each prey category. When there were remains from more than one species in a single scat, we took into account the proportion of each prey species by dry volume. For example, one scat with 40%Lemmus and 60%Dicrostonyx plus another scat with 60%Lemmus and 40%Dicrostonyx, were considered to be equivalent to one scat with 100%Lemmus and one with 100%Dicrostonyx. We call this semi-quantitative measure ‘percentage whole scat equivalents’ (% WSE). Sample sizes remain the same as for frequency of occurrence. The advantage of this measure is that the relative amount of each prey category in the faeces is taken into account. This is especially important for prey items such as insects, which occur in small quantities in each scat. With a strict frequency of occurrence measure, these will be over-estimated. Very small or broken scats were joined with others from the same sample to form a scat of normal size.
We could not classify all prey items to species level. In some cases, lemming remains could be identified, but not as species (14% WSE in fresh, 9% in old scats). That class of remains was for each site divided into the Lemmus and Dicrostonyx classes, respectively, in the same proportion as the remains identified to species level. We have no reason to believe that there was a bias towards one species in the unidentified lemming class. In the same way we divided the class of unidentified rodents (22% WSE in fresh and 13% in old scats) among all rodents species found at each site. Beside Lemmus and Dicrostonyx, these were Microtus spp. and Clethrionomys spp. We did not identify these voles to species level, but trapped species were M. oeconomus (Pallas) (sites 1, 2, 4), M. gregalis (Pallas) (sites 5, 15), Clethrionomys rufocanus (Sundevall) (site 1) and C. rutilus (Pallas) (site 5) (Fredga et al. 1995).
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V. Fedorov and K. Fredga trapped the collared lemmings and several people, especially E. Isaksson and N. Kjellén, helped us with inventories of fox dens. We are immensely indebted to D. Fucik for his patience and skill in helping us with analyses of fox scats. We thank P. Frodin, D. Hasselquist, P. Nilsson, and M. Svensson for help with lemming trapping and analysing these data, K. Danell for providing unpublished data from his dendrochronological analyses, and L. Baskin for translating Russian papers on lemming studies in Siberia. We are very grateful to the Swedish Polar Secretariat for organizing the Tundra Ecology Expedition 1994. Financial support was obtained from NFR (B–BU 3324–308) to Erlinge and Fredga, and from the Ymer foundation to Angerbjörn.