Habitat use of small mustelids in north Fennoscandian tundra: a test of the hypothesis of patchy exploitation ecosystems

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1 ECOGRAPHY IS: 237-^244. Copenhagen 1992 Habitat use of small mustelids in north Fennoscandian tundra: a test of the hypothesis of patchy exploitation ecosystems Tarja Oksanen, Lauri Oksanen and Mats Norberg Oksanen, T, Oksanen, L and Norberg, M 1992 Habitat use of small mustelids in north Fennoscandian tundra a test of the hypothesis of patchy exploitation ecosystems - Ecography The habitat use of small mustelids in a tundra area m Norwegian Lapland was studied chiefly by means of snow-tracking Stoats showed strong preference to a habitat complex immediately beneath the thrust line of the Scandes, with exceptional abundance of luxuriant habitats, whereas weasel activity was more evenly spread over the lowland tundra Mustelid activity on the high tundra above the thrust line was consistently low Within each subarea. stoat activity was concentrated to the most luxuriant habitats Similar preferences were shown by weasels on the lowland but not in the vicinity of the thurst cliff Daily movements of both species varied from local (c 200 m) to extensive (up to 4 km), no consistent interspecific differences m travel distances could be observed The results largely conform to the hypothesis of patchy exploitation ecosystems (T Oksanen 1990a), according to which predator activity tends to 'spill over' from luxuriant habitats, capable of supporting predator populations, to adjacent barren ones, due to despotic behavior within and between species and due to opportunistic predation by transient predators However, predator activity in barren habitats during the crash winter could not be explained by these mechanisms alone A third mechanism - breakdown of habitat preferences of predators during crash phases of a cyclic prey population - was thus introduced T Oksanen and M Norberg, Dept of Animal Eeology, Umv of Umed. S Umed, Sweden - L Oksanen, Dept of Ecological Botany. Univ of Umea, S Umed, Sweden more productive patches (Fretwell's three-link ecosysj^^j^^^ ^j^^ banen habitats will be exploited by socially The hypothesis of exploitation ecosystems (Fretwell subordinate and/or transient predators (see Fretwell 1977, 1987, Oksanen et al 1981, Oksanen 1988) was 1972, Domnicki 1978, 1987, Pulham 1988) The intensity recently generalized to include the impact of dispersmg of this 'spillover predation' depends on the spatial scale (T Oksanen 1990a) and transient (T Oksanen and L and on the relative abundance of barren and productive Oksanen, unpubl.) top consumers on population dy- patches An analogous argument should apply to herbnamics at lower trophic levels. The generalized theory, lvores at the transition between moderately barren to be called the hypothesis of patchy exploitation eco- (Fretwells two-link) habitats and extremely barren systems, shares the basic logical structure of the model (Fretwell's one-link) ones of Oksanen et al. (1981) However, relatively barren In order to perform a critical test of the hypothesis of ecosystems (Fretwell's two-link ecosystems, annual pn- patchy exploitation ecosystems, it is useful to work with mary productivity < 700 g m"^ yr"' dry wt) are predicted a habitat complex which offers both large-scale differto be devoid of predators only if they cover vast regions ences between the average primary productivity of dif- When occurring in a local habitat complex together with ferent subareas and small-scale productivity vanation Accepted 23 January 1991 ECOGRAPHY ECOGRAPHY 15 2 (1992) 237

2 30- rihcrotines highland I -mustelids weasels valtey y y Fig 1 Activity indices (ai) for small mustelids collectively and for weasels separately and density indices for voles (udi) withm the four subdivisions of the study area within each subarea This kind of setting is offered by tundra-brushwood complexes along the thrust line of the Scandinavian mountain formations m northernmost Fennoscandia Study area, material and methods The study was chiefly performed in essentially lowarctic terrain east of Joatkanjavri tundra lodge on Finnmarksvidda. Norwegian Lapland The study area of 16.1 km- consisted of four subareas A high-altitude plateau ( m a s 1 ) above the thrust line of the Scandes constituted the 'highland' subarea (4 2 km"), dominated by lichen-moss tundra, snowbeds, and bogs The 'slope' subarea (2 9 km-) was located immediately beneath the thurst cliff (altitude m a s 1) and was characterized by exceptional abundance of productive, herb-rich scrublands and even birch woodlands The 'valley' subarea (5 km-) consisted of a lowland plain (c 400 m a s 1 ) below the slope Barren lichen heaths and open bogs prevailed, but productive habitats were fairly abundant along watercourses The 'divide' subarea (4 1 km-) was essentially an extension of the lowland, with only marginally higher altitudes ( m a s 1) This subarea, however, was devoid of significant watercourses and entirely occupied by barren tundra heaths and bogs During the fieldwork, the study area was divided into 15 habitat types, out of which two ones - alluvial thickets and tall herb habitats (moist woodlands and scrublands rich m tall herbs) - dearly exceed the productivity threshold of Oksanen et al. (1981) for three-link ecosystems (Wielgolaski 1975) Four additional habitats - blueberry heaths, dry meadows, willow mires and blueberry-cloudberry mires - were probably more productive than this threshold level, although hard data are only available for a birch woodland variant of the blueberry heath (Wielgolaski 1975) Three habitats typical for the lowland and the divide - windbarrens, lichen heaths and open palsa bogs - have primary productivities well below 700 g m- yr' (Wielgolaski 1975, Rosswall et al 1975) and were thus barren 'two-link' habitats in the terms of Oksanen et al (1981) The same IS true for all highland habitats (moss-lichen heath, moss-blueberry heath, heath snowbed, meadow snowbed, open bog, see Wielgolaski 1975) Spnng and autumn densities of microtmes have been monitored in all habitats since 1977 by the Small Quadrat Method (see Oksanen and Oksanen 1981) Data for different habitat categories and subareas will be presented in detail by Oksanen and Oksanen (T Oksanen 1990b) Here, we present data for 20 small quadrates that were chosen to represent the four subareas for The highland is represented by 5 quadrates in the northernmost part of the traplme, 1 5 km north of the thrust cliff Their habitat distribution is as follows bog 2, meadow snowbed 2, heath snowbed 1 The slope IS represented by 5 dry meadow quadrates c 200 m from the cliff which were physically m the middle of the subarea and also roughly m the middle of the productivity range of the slope habitats The valley is represented by 2 blueberry heath quadrates, 2 lichen heath quadrates and 1 cloudberry blueberry bog quadrate, chosen on the basis of their central location within the subarea (1-1 5 km south of the cliff) and representativeness for Its habitats The divide is represented by the 5 southernmost quadrates, km south of the cliff (habitat distribution lichen heath 4, open bog 1) The main study method was to map all fresh tracks of small mustelids within the study area during 4-6 consecutive days with good tracking snow in November-December and to make measurements of leap lengths and pit widths m order to allow lndentification of species and sex, as in the tracking study at Pallasjarvi (T Oksanen 1990b) However, m the conditions of the tundra, a much narrower range of weather conditions could be regarded as acceptable than in the taiga at Pallasjarvi. only fairly calm days with fresh snow gave reliable results for all habitats As these cntena gave us only three tracking days in December 1988, a new tracking penod (also yielding three acceptable field days) was allocated to March 1989 As the activity patterns during these two periods turned out to be entirely different, the data were treated separately Tracking data were converted to activity indices of stoats and weasels p)er habitat and subarea as by T. Oksanen (1990b) - by summing up the numbers of grids of 20 X 20 m visited by each individual, dividing by the total number of grids representing the habitat withm the subarea and multiplying by 50(Vn, (n = the number of tracking days) In addition, correspionding activity indices were calculated for entire subareas Statistical treatment of this type of data is problematic Many habitat types occurred as fairly separate and 238 ECOGRAPHY 15 2 (1992)

3 r luxuriant meadow k dry meadow» blueberry heath stoats ai 50-1 ai V moss-blueberry heath A open bog o lichen heath weasels results by comparing them to those of a 5-d pilot study performed m March 1985 (l e during a crash winter, Oksanen and Encson T Oksanen 1990b) at Mollisjok, 30 km southeast of our present study area The basic habitat setting was rather similar to that at Joatkanjavri There was a small subarea (the bottom of a river valley), where productive habitats abounded, an intermediate zone (the slope), where barren habitats prevailed but a significant part of the landscape consisted of productive habitats and an upland area where only c 1% of the landscapie consisted of productive habitats In addition to the snow-tracking study, also live-trapping of small mustelids was carried out However, livetrapping was exclusively conducted m the best habitats of the slope and recaptures were only common during years of low microtine density (1986 and 1989) Thus, the relevance of the live-trapping data in the present context IS limited to studying movements of small mustelids during microtine lows within the slope subarea Data on numerical trends will be presented by Oksanen and Oksanen (MS, see T Oksanen 1990b) Fig 2 Activity indices for stoats and weasels within the six major habitat types of the 'slope" subarea well-dispersed patches which could have been treated as independent replicates withm the scale of the study area However, within this scale, there is no point for computing any statistics We did not limit the trackmg study to some samples but performed snow-tracking within the entire area Between-habitat differences in our data are thus automatically real and cannot be attributed to sampling error The interesting statistical questions are whether our observations reflect habitat use pattems during a longer period (e g early winter) and whether they are representative for a broader area, such as inland tundra in northern Fennoscandia To answer the former question, we looked whether the exclusion of the last tracking day of each period substantially changed the data It never did; the general pattern of habitat use usually emerged dunng the first tracking day and always dunng the two first ones (Notice that reliance on 1-2 d IS also a tacit premise of standard line transect techniques ) In order to answer the latter question m a statistically appropriate way, habitat patches should be randomly sampled from the entire statistical population to be investigated (e g continental tundra in Finnmarken), the use of adjacent patches would be pseudoreplication As the statistically correct sampling exceeded our logistical capacity, we refrained from computing any statistics at all, according to the recommendation of Hurlbert (1985) We could get a rough idea of the repeatability of our Results Changes in microtine numbers, in the activity of small mustelids collectively and in the activity of weasels withm the four subareas at Joatka are presented in Fig 1 The four subareas showed major differences both in fluctuation patterns of microtmes and in their use by 'Willow mire A dry meadow blueberry heath stoats ai open bog lichen heath windbarren weasels Fig 3 Activity indices for stoats and weasels within the six major habitat types of the 'valley' subarea ECOGRAPHY 152 (1992) 239

4 ai 60, blueberry heath T cloudberry bog stoats 1 L / ai ^ open bog :> lichen heath 7 windbarren weasels /I \\ Fig 4 Activity indices for stoats and weasels within the five major habitat types of the "divide' subarea small mustelids In the highland, microtine density peaked in autumn 1988 and crashed immediately thereafter Mustelid activity was restricted to December 1988 and was modest even then On the slope subarea, microtine densities peaked in autumn 1987, reaching a clearly higher level than in other subareas Thereafter, a continuous decline took place Intense mustelid activity was observed in November 1987 and December 1988 TTie stoat was always the predominating species Also in the valley, highest microtine densities were reached in autumn 1987 However, after a seasonal decline in , there were indications of recovery in 1988, followed by a collapse in The activity of small mustelids culminated during this crash, the weasel being the dominating species In the divide, microtine numbers behaved basically as in the highland, with a peak in autumn 1988 and a crash in Mustelid activity culminated late in the crash winter, again with heavy prevalence of weasels Mustelid activity on the highland in December 1988 was concentrated to heath snowbeds: their mustelid activity index was 14 4, whereas activity indices of other habitats were negligible (3.1 for snowbed meadows, < 1 for all remaining habitats). The pet habitat activity indices of the three most abundant productive and barren habitats for the slope, valley and divide are presented in Figs 2, 3 and 4, resfjectively On the slope, the stoat indices obtained maximal values in the most productive habitats and low values in lichen heaths and open bogs (Fig 2) For the weasel, however, lichen heaths and open bogs seemed to be as interesting as the most luxuriant meadow forests and willow thickets In the valley, both species seemed about equally selective, with clear preference for productive habitats and low activity levels on open bogs and lichen heaths (Fig 3) A basically similar situation seemed to prevail m the divide (Fig 4) A comparison between Figs 1^ shows that there were no systematical differences in the level of mustelid activity between the productive habitats of each study area during microtine declines However, mustelid activity in barren lichen heaths and bogs was much higher on the slope than in the valley and divide subareas. When interpreting the above summarized data, it is helpful to look at sizes and distributions of individual home ranges or terntones (Fig 5) We see that, in November 1986 and 1987, stoats mainly moved along the longitudinal axis of the slope subarea and along the main creek of the valley By and large, this was the situation in December 1988, too Weasels, m turn, did not have equally clear axes of territory orientation Observed territory sizes were variable in both species, but there were no consistent interspecific or lntersexual differences m mobility During the three tracking days in March 1989, however, only local movements were observed Also the two stoats recurrently trapped m August 1989 were very stationary, with extreme trapping fioints <300 m from each other The stoats and weasels at Mollisjok m March 1985 showed a corresponding dichotomy m space (Fig 6) two stoats stayed within a small area at the main river, dominated by productive habitats, whereas weasels moved extensively over the entire study area and beyond It, with maximum distances between the extreme points of daily tracks approaching 10 km, utihzing small patches of productive habitat within the matrix of lichen heaths and open bogs Mustelid activity m barren habitats in the valley bottom (zone III) exceeded the corresponding value for typical upland tundra (zone I) by a factor of 10, whereas the corresponding difference for mustelid activity in productive habitats the was only 4-fold (Fig 7). Thus, activity in barren habitats was strongly dependent on the vicinity of productive source habitats, whereas activity in productive habitats was less sensitive to the over-all habitat distnbution Discussion In many respects, the results reported above conform with those obtained in a taiga complex at Pallasjarvi (T Oksanen 199(HJ). The winter terntones or home ranges of stoats and especially those of weasels were usually considerably larger than reported in hterature (Lockie 240 ECOGRAmY 15 2 (1992)

5 Fig 5 Activity areas of stoats (thick lines) and weasels (dashed lines) during the snow-tracking periods Hatched productive habitats, crosshatched luxuriant habitats A key to the location of the four subareas in the bottom of the figure XI 86 XI ECOORAPHY 15 2 (1992)

6 N productive habitats o barren habitats 1km Fig 6 Activity areas of stoats (thick, entire lines) and movements of weasels (thin entire lines cf, dashed lines $) in the Mollisjok study area, March 1985 Oblique hatching productive habitats, cross-hatching watercourses The circled numbers refer to distances (in km) from the edge of the study area to the furthest point of the weasel track in question The latin numbers refer to the three major subareas 1966, Erlinge 1974, 1977, King 1975, Simms 1979, Debrot and Mermond 1983, Erlinge and Sandell 1986) During vole crashes, however, stoats seemed to change their strategy of habitat use by establishing a small territory on an exceptionally favourable patch Also some weasels seemed to apply this strategy, whereas others retained the strategy of extensive movements Pre-emptition of localized high-quality patches by stoats seems a likely reason for the difference (King and Moors 1979, Erhnge and Sandell 1988), although different abilities to exploit alternative prey (e g. the grouses of willow thickets) may be involved (Myrberget 1974, Erhnge 1983, Debrot and Mermond 1983) TTie role of despotic behavior is supported by the fact that a clear interspecific difference in habitat use existed even when vole densities in the most productive habitats were high ( ). weasels moved frequently in the lowermost parts of the slope, where open bogs and lichen heaths prevailed, and had low activities in the strand of luxuriant meadows and in the blueberry heath zone between the meadow strand and the thrust cliff As weasels preferred herb-nch habitats and blueberry heaths m other subareas, the situation on the slope can be attributed to the intense stoat activity in the meadow strand (foraging areas) and on the stony heaths at the thrust chff (denning areas) When mustelid activity spread from the slope to the less productive subareas, so did the decline of the microtine populations At least for the productive habitat patches on the lowland and the divide, where predator activity in was high, a causal connection is plausible In the last phase of the decline, weasel activity shifted to the lichen heaths and bogs of the divide and even there, microtine populations collapsed The synchronous decline of both voles and lemmings (Oksaai I subarea Fig 7 Mean activity indices of small mustelids for patches of produetive and barren habitats at MoUisjok in relation to the vicinity of the nver I Upland tundra, II River valley III immediate vicinity of the nver (see Fig. 6) Bars refer to standard errors, indicating the variability of habitat use within the study area. I 242 ECOCmAPHY 15 2 (19»2)

7 nen and Oksanen MS, see T Oksanen 1990b) supports the idea that predation had a role m this dechne On the highland, only modest predator activity was observed The devastation of the moss cover, the observation of numerous intact dead lemmings m the spnng and low incidence of winter nest predation suggests that the lemming-dominated small mammal guild of the highland crashed due to overexploitation of winter food before predation pressure had become substantial The data are supportive to the prediction of T Oksanen (1990a) that pieces of barren land which by themselves could not support predators get 'spillover predation' in the form of aggressively subordinate predators (l e weasels) which have to balance the advantages of high resource supply m the best habitats with the risk of death or injury due to encounters with aggressively dominating predators As predicted by T Oksanen (1990a), the intensity of 'spillover predation' shows strong positively relation to the abundance of productive source habitats m near-by areas The presence of mustelid tracks even on windbarrens (where practically no voles were ever captured) suggests that a part of the predator activity in barren habitats could be regarded as transitory However, also such transitory activity is likely to lead to 'spillover predation', provided that prey items are valuable enough to make opportunistic foraging of encountered prey economical In microtine-mustelid systems, this condition IS obviously satisfied as even a small vole represents the daily energy requirement of the predator Opportunistic foraging of transient predators leads to basically similar relation between the abundance of preferred habitats and the intensity of spillover predation as despotic habitat choise, only in a different spatial scale (Oksanen and Oksanen, unpubl ) In the final phase of the vole decline, even a third mechanism appears to have contnbuted to 'spillover predation' active choise of a barren habitat or an area where barren habitats overwhelmingly prevail The habitat shift between December 1988 and March 1989 is difficult to attribute to desfkjtic behavior, as large parts of the slope were deserted simultaneously as predators appeared on the divide The movement was connected to severe depletion of prey supply in the generally preferred habitat (a typical situation during prey dechnes in predator-prey hmit cycles, see Gilpin 1975) which apparently made even the barren heaths and bogs of the divide attractive, especially for weasels, too small to utilize the alternative resources (hares and willow grouses) present in meadow forests and willow thickets. CondusioBS and perspectives tor future work By and large, the data conformed to the predictions of the model of patchy expltmtation ecosystems of T. Oksanen (1990a) Predator activity in barren habitats was found to vary strongly, depending on the productivity of surrounding areas While little predator activity was discovered within large tracts of barren land, similar habitats received substantial activity m areas where relatively luxuriant habitats abounded The cyclicity of the mustehd-microtine system somewhat confounded the situation. In the final phase of the microtine crash, habitat preferences of small mustelids seemed to disappear or become reversed, apparently due to severe overexploitation of prey in the best habitats The model of patchy exploitation systems does not give full insights in the behavior of cyclic predator-prey systems It does not explain the causes of cyclicity, either Patchy systems tend generally to be more stable than homogenous ones, due to the tilting of the predator isocline m the productive habitat (T Oksanen 1990a, see also Lomnicki 1978) Thus, cycles exist m spite of patchmess, probably because of the destabilizing impact of seasonality of primary production on predator-prey systems with rapidly reproducing prey (L Oksanen 1990) Integrating the patch model of T Oksanen (1990a) and the seasonality perspective of L Oksanen (1990) thus seems to be the natural direction to move in the theoretical work On the empirical level the natural next step is to focus on cascading impacts of spillover predation on herbivores and plants What we have at least preliminarily shown IS that predator activity spills over from productive habitats to barren ones This prediction arises from several models of metapopulation dynamics (e g Lomnicki 1978, PuUiam 1988) The salient feature of the model of patchy exploitation systems is that the spillover exploitation has population dynamical impacts on victim populations and, indirectly, even on their resources In order to test these predictions, it is essential to perform comparative and expenmental fkjpulation dynamical studies on herbivores and plants in habitats with different levels of spillover predation Acknowledgments - Sincerest thanks to B and H Romsdal for all they have done to help us to solve all kinds of practical problems and to make our stays at Joatka comfortable Equally valuable help was obtained from A and K -R Johnsen dunng the MoUisjok field penod In the tracking work, we have been helped by A Lukkari and B Romsdal Useful comments on the MS were obtained from C Otto The figures were drawn by G Marklund References Debrot, S and Mermod, C 1983 The spatial and temporal distnbution pattern of the stoat {Mustela ermmea L ) - Oecologia (Berl ) Erlinge, S 1974 Distnbution, temtoriality and numbers of the weasel Mustela ntvalis in relation to prey abundance - Oikos Spacing strategy in stoat Mustela ermmea - Oikos 28' Demography and dynamics of stoat Mustela ermmea W ECOGRAPHY 15 2 (1992) 243

8 in a diverse community of vertebrates - J Anim Ecol and Sandell, M 1986 Seasonal changes in the social organization of male stoats, Mustela erminea an effect of shifts between two decisive resources - Oikos and Sandell, M 1988 Coexistence of stoat, Mustela erminea, and weasel, M nivalis social dominance, scent communication, and reciprocal distribution - Oikos Fretwell, S D 1972 Populations in a seasonal environment - Princeton Umv Press, Pnnceton The regulation of plant communities by food chains exploiting them - Perspect Biol Med Food chain dynamics - the central theory of ecology'' - Oikos Gilpin, M E 1975 Group selection in predator-prey communities - Pnnceton Umv Press, Princeton Hurlbert, S H 1985 Pseudoreplication and the design of ecological field experiments -Ecol Monogr King, C M 1975 Home range of the weasel {Mustela nivalts) m an English woodland - J Anim Ecol and Moors, P J 1979 On co-existence, foraging strategy and biogeography of weasels and stoats - Oecologia (Berl ) Lockie, J D 1966 Territory in small carnivores - Symp Zool Soc Lond Lomnicki, A 1978 Individual differences between animals and the natural regulation of their numbers - J Anim Ecol Population ecology of individuals - Pnnceton Univ Press, Pnnceton NJ Myrberget, S 1974 Variations in the production of the willow grouse Lagopus lagopus (L ) m Norway, Onus Scand Oksanen, L 1988 Ecosystem organization cybernetics and mutuahsm or plain Darwinian struggle for existence'' - Am Nat ^* Exploitation ecosystems in seasonal environments - Oikos and Encson, L 1987 Dynamics of tundra and taiga populations of herbaceous plants in relation to the Tihomirov- Fretwell and Kalela-Tast hypotheses - Oikos and Oksanen, T 1981 Lemmings (Lemmus lemmus) and grey sided voles (Ctethrionomys rufoeanus) in interaction with their resources and predators on Finnmarksvidda, northern Norway -Rep KevoSubarct Res Stn , Fretwell, S D, Arruda, J and Niemela, P 1981 Exploitation ecosystems in gradients of pnmary productivity Am Nat Oksanen, T 1990a Exploitation ecosystems m heterogeneous habitat complexes - Evol Ecology b Predator-prey dynamics in small mammals along gradients of pnmary productivity - Ph D thesis, Univ of UmeS Pulham, H R 1988 Sources, sinks and population regulation Am Nat Rosswall, T, Flower-Elhs, J K G, Johansson, L G, Jonsson, S, Ryden, B E and Sonesson, M 1975 Stordalen, Abisko, Sweden -In Rosswall, T and Heal, O W (eds). Structure and function of tundra ecosystems Ecol Bull NFR 20, Stockholm, pp Simms, D A 1979 North American weasels resource utilization and distnbution - Can J Zool Wielgolaski, F E 1975 Functioning of the Fennoscandian tundra ecosystems - In Wielgolaski, F E (ed ), Fennoscandian tundra ecosystems, part 2 Spnnger, Berlin, pp ECOGRAFHY 15 2 (1992)

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