Nigel G. Yoccoz and Rolf A. Ims 37

Home , Collared lemming, Common vole, Field vole

Ecological Bulletins 47: 137-144. Copenhagen1999

Nigel G. Yoccozand Rolf A. Ims

Yoccoz,N. G. and Ims, R. A. 1999.Demography of small mammalsin cold regions:rhe importanceof environmentalvariability. - Ecol. Bull. 47: 137-144.

Environmental variability in arctic and alpine regionsis large,and consistsof predictable (seasonality)as well asless predicrable components (e.g. between-years variability). We comparedemography of alpine and arctic microtinesbased on two long-term studies in the French Alps (snow vole, Chionomysnivalis) and at Svalbard(sibling vole, Microtus rossiaemeridionalis),as well as data from a short-term study on the common vole, M arvalis, in the Alps. While the length of the vegetationperiod is of the same order of magnitude (3-4 months in the Alps, 3 months at Svalbard),the population dynamics and demographyof the snow vole and of the sibling vole population are strikingly different.The alpine snowvole population is very stable,with little variability in survival and reproduction betweenyears, particularly so during the winter. The sibling vole Svalbardpopulation is highly fluctuating, with low variability in summerde- mographicrates and largevariability in winter population rate of change.These different patternsof variability in the dynamicsand demographyof small mammalsare relat- ed to the climatic patternsin both areas,particularly the pronouncedseasonal fIuctua- tion in climatic variability at Svalbard,and the somewhatconstant level of climatic variability in the Alps. We arguethat suchpatterns may be of generalrelevance to arctic environmentson Olle hand and alpine environmentsat middle latitudes on the other hand. We funher discussthe possibleconsequences of changesin variability patternson the demographyof small mammals.

N G. Yoccoz([email protected]), Div. o/Arctic Ecology,Norwegian Insti- tute for Nature Research(NINA), Polar Environmental Centre, N-9296 Ti'omsø,Norway. -R.A. Ims, Div. o/Zoology, Depto/Biology, Univ. o/Oslo, EO.B.I050Blindern, N-O316 Oslo, Norway.

"Environmental variability is a virtual Pandoras box of selec- short distances of very different habitats such as broad- rive forces which can injluence the evolution of life histories, leaved forests, coniferous forests and alpine meadows be- and there is still much we do not understand about the nature cause of steep altitudinal gradients (Gerrard 1990). High of selectionin jluctuating environments" (Boyce 1988: 16). altitude climates generally differ from high latitude cli- Cold regions are found either at high latitudes or at mates, but the variability of mountain climates prevents high altitudes. They share common characteristics, first of any simple comparison (Barry 1992). Climate of the west- all a marked seasonality: short summers favourable to veg- ern European Alps is, for example, wetter as altitude in- etation growth separated by lang winters with a permanent creases(mainly becauseof orographic effects), but is not as snow cover. They also differ by important aspects,such ås severe with respect to temperature as compared to arctic climate, photoperiod and spatial heterogeneity: alpine re- environments: extremely cold temperatures - < -30°C - gions will aften be characterized by a juxtaposition over are rare in the European Alps, while they are common in .

ECOLOGICAL BULLETINS 47,1999 37 northem Fennoscandia or in the high Arctic. European Alps (snow yale, Chionomys niva/is, and com- The recent focus on clirnatic change have led to detailed mon yale, M arva/År;northern Alps, France). Two of these studies of lang-term trends both in the Alps and in the studies (sibling and snow voles) are based on intensive Arctic. There is now strong evidence for a significant lang-term (7 yr) capture-recapture methods, and allow for warming trend in the Alps, particularly so during the last a detailed analysis of the variability in demographic rates. two decades (e.g., Diaz and Bradley 1997, Sommaruga- aur main objective is to assessif environments with simi- W6grath et al. 1997). The arctic regions on the other hand lar average seasonality, as measured by the length of the show large spatial heterogeneity, with no clear trend (Przy- breeding season,may select for different life-history tactics bylak 1997). The Svalbard area, for example, has not as a consequence of differences in tempora! variability. warmed up since the 1920s (Førland et al. 1997). The climatic variability may also increase as a consequence of glo- bal change (Katt and Brown 1992, Mearns et al. 1997). Material and methods Studies of climatic variability have mainly focused on decadal scale variability (e.g., Beniston 1997, Hurrell and Van Svalbard Loon 1997), but, to aur knowledge, the interannual climatic variability has not been thoroughly studied in arctic The sibling vaie - a sibling speciesof the common vole- and alpine regions. was introduced to Svalbard from Russia between 1930 and Small mammals present good opportunities for study- 1960. It is a relatively small species (adult females: 30 g, ing the effects of environmental fluctuations because they adult males: 35 g). This speciesis the only small mammal have a short generation time (often less than ane year) and speciesin this high arctic archipelago, and there is only ane are amenable to detailed studies based on capture-mark- persistent population (Fredga et al. 1990, Yoccoz et al. recapture methods (e.g., Leslie et al. 1953, Krebs 1966, 1990; seeFig. 1). The Svalbard population probably origi- Yoccoz et al. 1993b, Ims andYoccoz 1997). Most popula- nates from the region around St. Petersburg, and was first tion studies of small mammals have focused on the issue of identified as M arvalis (Nyholm 1966, Alendal 1977). population cycles, with relatively litcle work being done on The difference in behaviour between the two species- M demography (see e.g. Hansson and Henttonen 1988, rossiameridionalis using human dwellings such as barns Stenseth and Ims 1993). Short-term environmental varia- much more than M arvalis - probablyexplains why the bility may have both lang-term effects through the evolu- sibling vaie was introduced to Svalbard. After an initial tion oflife-history traits as well as direct short-term effects survey in 1989, we started in 1990 a capture-mark-recap- through annual changes in demographic rates and conse- ture study of the population found around the ghost min- quencly population sizes. It is for example known that ing town ofGrumantbyen (78°10'N, 15°16'E). We moni- there may be a trade-off between the mean and the vari- tored the population by following selected areaswithin a 1 ance of a trait, an increasing variance having a negative ef- km strip along the shore inhabited by the voles. We cap- fect on the lang-term fitness, everything else being equal tured individual voles three times a year, at the end ofJune, (Orzack and Tuljapurkar 1989, Yoshimura and Clark just after the snow melt, at the beginning of August, and at 1991). Therefore, different patterns in environmental var- the beginning of September, befare the first snowfalls lead- iability and predictability may well select for different de- ing to permanent snow cover. We based aur trapp ing re- mographic tactics (Boyce 1979, 1988). Population dy- gime on the robust design (Pollock 1982) with 7 -10 trap- namics will be ultimately affected through the demograph- ping secondary sessionswithin each of the three primary ic parameters: populations with large potential turnover sessions.This ensured reliable estimates of population sizes rates (early age at first reproduction, high reproductive based on closed population models. Survival rates was esti- rates) might be more variable than populations with in- mated using generalizations ofCormack-Jolly-Seber mod- verse demographic characteristics. els (Yoccoz et al. 1993b, Yoccoz et al. unpubl.). There have been relatively few empirical studies ad- dressing the issue of environmental variability and its impact on demographic tactics, moscly on plants (Carlsson FrenchAlps and Callaghan 1994, Watson et al. 1997; but see, e.g., Benton and Grant 1996, Gaillard et al. 1997). This is is for Three microtine speciespermanently inhabit alpine (above the most due to the lack of detailed lang-term studies the timberline) areasin the western European Alps (Le where demographic parameters have been reliablyestimat- Louarn 1977,Janeau 1980). The snowvole, C niva/is,is a ed (Gaillard et al. 1998). In this paper, we relate demo- middle-sizedvaie (adult females:40 g, adult males:45 g), graphic and population dynamic patterns to patterns in and is restrictedto boulder and rocky areas(Claude 1995, environmental variability. This we do on the basis of field Janeauand Aulagnier 1997), including housesand alpine studies of three small mammal species performed in the huts (it may thereforebe fOWld up to 4000 m, far above high arctic (sibling vaie, Microtus rossiaemeridionalis= M. the snow line). It is also found at the sealevel closeto the epiroticus; Svalbard, Norway) and in the alpine zone of the Mediterraneansea (Jones and Carter 1980), and therefore

38 it is not a species restricted to the high altitude roDe. It is more common in mountain habitats because rocky areas are more frequent at high altitudes. The common vaie is on the other hand an inhabitant of alpine meadows up to the snow line (Spitz 1977, Meylan 1995). It is not found in the subalpine roDe, and the "alpine" common vaie has sometimes been distinguished from its lowland conspecific under the Dame M incertus (Le Louarn et al. 1970). The lowland M arva/is has a very wide geographic range in Europe (Fig. 1). The common vaie is the smallest rodent speciesin the alpine zone (adult females: 20 g, adult males: 25 g). The third species, the fossorial form of the water vaie, Arvicola terrestrissche1man, is for the most part found at lower altitudes (600-1800 m a.sl. in the areas studied here), and is usually cyclic with a 5-6 yr periodicity (Saucy 1994). It was uncommon or absent at the altitudes consid- ered hete (2200-2700 m), and is much larger (80-100 g) than the two other microtines. ane population of snow vaie located in the Seez mu- nicipality, Savoie, France (45°40'N, 6°50'W), at an altitude of2200-2450 m under the Clapey summit (thereaf- Fig. 1. Oistribution map of the snow vaie, Chionomysnivalis ter called Clapey population). This population has been (dotted line), common vaie, Microtus arvalis, (continuous line) and the sibling vaie, M rossiaemeridionalis(shaded area) in Eu- followed since 1991 by capture-recapture methods. The rope. Arrows show the study sitesat Svalbardand in the French Clapey population inhabits a large boulder field (6 ha) sur- Alps. rounded by alpine meadows used for pasture by cows during the summer. Trapping was done during the summer, irrespectiveof altitude. A more detailedanalysis of weather from snow melt usually in June to first snow falls in Octo- and climatic patterns is clearly warranted in the Alps. ber-November. We had between three and eight primary However, there are rather few high altitude weather sta- trapp ing sessionseach summer, with two to seven second- tions, and theseare situated on mountain tops. Neverthe- ary sessionswithin each primary session.Another popula- less,available data from high altitude weatherstations (sit- tion of snow vaIe was studied in the Mont -Blanc range, 15 uated, however,in eastemparts of the Alps; Barry 1992) km north of the previous site, at an altitude of2500-2700 gavesimilar valuesfor averagetemperature as mose pre- m, in a highly giaciated area close to the Couvercle hut. A dicted using a uniform gradient.The useof monthly val- small population of common vaIe was also studied in the uesis alsosomewhat arbitrary, and patternsof weathervar- same area in 1996-1997 (both populations are refered be- iability at different temporal scalesshould also be focused low as Couvercle populations). Trapping occurred only upon in future studies. during the summer, and was done in two sessionsduring the first half ofJuly and the second half of August. Resultsand discussion Meteorological data Population dynamics of the sibling vaie and snow vaie populations showed relatively similar seasonalpatterns, Svalbard climatic patterns were recently summarised in but were quite different with respectto the multiannual Førland et al. (1997). Monthlyaveragesand standardde- fluctuation patterns(Fig. 2). The snowvaie population in viations were given from the Svalbardairport for the pe- the Alps had very stablepopulation sizes,probably Olle of riDd 1961-1990. The meteorologicalstation is along the the most stableknown among microtine populations (see seashoreand ca 7 km from aur study site. Differencesbe- Henttonen et al. 1985, Ostfeid 1988, Stenseth et al. tween the study site and the meteorologicalstation should 1996).The number ofbreeding adults at the beginning of thereforebe small. the breedingseason did not vary by more than a factor of We used the meteorological station of Bourg Saint two along the courseof the study,staying between 30 and Maurice (altitude 865 m; period 1946-1997) and Cha- 60. The samewas true of the population size in the au- monix (altitude 1040 m; 1951-1980) as referencevalues tumn. The snow vaIe and common vaIe Couverclepopu- for the Clapey and Couverclepopulations, respectively. To lation sizeswere nearly identical in 1996 and 1997. On the correct for the differencein temperaturewith altitude!,we other hand, the Svalbardsibling vaIe population showed used a temperature gradient of 0.6°C 100 m-l (Barry dramatic multiannual fluctuations, by a factor > 20 (Fig. 1992). We assumedthe monthlv variabilitv to be the same 2). This was mainly due to large fluctuations in winter females)on average,and relatively high summer survival rates (Yoccozet al. 1993b), the population is able to in- '" N creasequite fast during the summer,relatively much faster in c O than the snow yale (seeFig. 2). The alpine common yale t hasa smallerlitter size(4.02 on averageagainst> 5 in the -:; D- O plains; Le Louarn et al. 1970), and the Couverclepopula- Q.. -O tion clearlyshows high summersurvival (Yoccozunpubl.). '" Winter reproduction neveroccurred in the alpine populations, but in two yearsout of sevenat Svalbard.The main demographiccharacteristics of the three populations are summarizedin T able 1. The demographictraits found in the snowyale and sibling yale populationsare among the most extremewithin microtines(e.g., Innes and Millar 1994).They are,however, both found in environments characterisedby very strong seasonality:the snow-freeor vegetativeseason in both casesdid not last much more than three months. None of the two populationsstudied could unambiguous- ly be claimedto haveevolved traits selectedby the specific characteristicsof their environment: the sibling yale was introduced to Svalbardfrom Russia,and the snowyale is a speciesrestricted to rocky habitats at all altitudes.Regard- ing the latter species,a few mammal populationsinhabit- ing rocky habitatsare indeedknown to havelow turnover 1.06.90 1.0691 1.06.92 1.06.93 1.06.94 1.06.95 1.06.96 comparedto congenersor conspecificsliving in apen hab- 1.1290 1.12.91 1.12.92 1.12.93 1.12.94 1.12.95 itats (e.g. pika, Ochotonaprinceps, Smith 1988; deer mouse,Peromyscus maniculatus, Millar and Teferi 1993). Fig. 2. Population dynamicsof the snow vole in the Alps, 1991- Microtine speciesrelated to the snow yale, and living in 1997 and the sibling vole at Svalbardin 1990-1996. Estimated similar habitats (suchas the Balkan snow yale, Dinaromys population sizesbased on closedpopulation models (open cir- bogdanovz)have also been reported to havesmalllitter size, cles), with population sizesat the beginning of the breedingsea- but very littie is actually known. It is thereforelikely that son indicated with stars. the demographictactic of the snow yale is at least partly associatedwith its rocky habitat preferences.With respect breedingand survival at Svalbard,bur also,bur to a lesser to the sibling yale, the fact mat this population hasappar- extent, to density-dependenteffects on summer survival ently not changedwith respectto reproductiveparameters and reproduction (Yoccozet al. unpubl.). As we trapped sinceit wasinttoduced (Yoccozet al. 1993a)despite that at most of the areawhere the population was found in low least 100 generationselapsed since Russiansleft the area, abundanceyears, bur only a small proportion of the area show that the selectionpressures have not beenfor a lower occupied by the population in high abundanceyears, the turn over rate. It could be that litter sizeis a trait showing actualfluctuations of the whole population arelikely to be slow evolutionary response(e.g. because of conflicting ge- an order of magnitude higher.The alpine common yale is netic and maternal effects:Bernardo 1996). Other arctic not known to exhibit large multiannual fluctuations such microtines have,however, similar traits such as high litter as the anes found in lowland Europe (Le Louarn 1977, sizesand early ageat first reproduction (e.g.,Wildhagen Jobsen1988, Mackin-Rogalskaand Nabaglo 1990). 1953, Krebs 1964, Batzli and Henttonen 1993). Finally, The populations differed also with respectto demo- observationsmade on alpine common volespoint to the graphic tactics.The snow yale is a specieswith very low samedemographic tactic as found in the snow yale: low turnover: young usually did not reproducein their yearof reproductiverates and high survival rates.Note that the birth, litter sizewas low (3 on average;Frank 1953,Janeau bank yale, Clethrionomysglareolus in subalpineforests also and Aulagnier 1997) and survivalwas high, particularly so presentstraits characteristicof specieswith low turnover, during the winter (Yoccozunpubl.). Very similar valuesfor with high survivalrate and relativelyshort breedingseason survivalwere estimated for the Clapeyand Couverclepop- (Yoccozand Mesnager1998). Sucha pattern hasalso been ulations. On the other hand, the sibling yale at Svalbardis suggestedfor the deermouse along an altitudinal gradient Olle of the fastestreproducing mammal in the world, fe- (Ounmire 1960). However, the lack of detailed demo- malesgiving birth for the first time when barelymore than graphicstudies in the alpine zone in, e.g.,North America, Olle month old (Yoccozet al. 1993a). With a litter size preventsus to conclude whether this demographic syn- equal to 4.5 (nulliparous females)and 6.5 (multiparous drome is generallyselected for in alpine environmentsor

140 ~ICAL BULLEllNS 47. 1999 Table 1. Main demographiccharacteriscics of the three populations. Overwinter survivalis given from Septemberto lune. Summer survival is given per 28 d.

Demographic trair Sibling vaIe (Svalbard) Snow vole (Alps) Common vole (Alps)

Overwinter survival (average) 10% 45% - Overwinter survival (variability) high low Summer survival (average) 80-90% 85% 90% Summer survival (variability) moderate moderate moderate Litter size 5.5 3.0 a 4.0 b Litters/season 4 2 3 Winter reproduction Yes No No Age at first reproduction 1 month 1 year l year

a data from Frank 1953,Janeau and Aulagnier 1997, b data from Le Louarn et al. 1970. whether it derivesinstead from same specificcharacteris- bility is much larger during the winter at Svalbard,and tics of the EuropeanAlps, such asdifferent predator com- much smallerduring the summer,as comparedto OUTal- munities (Yoccozand Mesnager1998). It should be noted, pine sites (Fig. 4; Førland et al. 1997). Precipitationsare however,that specialistpredators are absent from Svalbard, very reducedin the arctic, particularly in the winter period but presentin the alpine zone (stoat,Muste/a erminea, and (on average,precipitations in November-April amount to kestrel,Palco tinnunculus). Therefore, the selectionfor low 99 mm at Svalbardairport (Førland et al. 1997) against vs high turnover rate doesnot seemto be relatedto preda- 520 mm in Bourg Saint Maurice - and the precipitations tion pressure. on the alpine field sitesare likely to be evenhigher because There is, however,a climatic differencebetween Sval- of orographiceffects). This resultsin a shallowand unsta- bard and European Alps which may be relevant for ex- ble winter snow larer at Svalbard,as opposed to a well in- plaining the evolution of different life history tactics.Tem- sulating coverin the Alps. In fact, the snow larer at Sval- peraturesare on averagesomewhat lower at Svalbardthan bard can completelydisappear in the middle of the winter at the Clapey alpine site (seeFig. 3), but this difference as a consequenceof freezingrain (unpubl.). The impor- nearly vanishesfor the Couverclesite in the Mont-Blanc tanceof a stablesnow larer for small mammal winter sur- range(Fig. 3). On the other hand, the between-yearvaria- vival and reproduction in the arctic has been repeatedly

'" o I , , , , , , , , , ,---,- ~ .~ -~ ... ~ --" .~ -, ( ~ ;$'~ ~~ ~CI t-~ \1"" ")~~ ")~,#"' ~ QQ"'~-o«" ~-o«" A."<>~ «v :o~ ~ '" ~of' oCJ" ~ti (,ti G.,~~ ~O ~q;

Fig. 3. Temperaturemonthly averagesat the Clapeyand Couver- Fig. 4. Standarddeviation of monthly averagetemperature at cle study sites(estimates based on the nearestmeteorological sta- Svalbard(squares) and at Bourg Saint Maurice (circles). tions and an altitudinal gradient ofo.6°C 100 m-I; seetext) and the Svalbardstudy site. Averagevalues for two high altitude alpine meteorological stations (Zugspitze and Sonnblick; data from Barry 1992) are alsoshown.

ECOLOGICAL BULLETINS 47.1999 emphasized(e.g., Krebs 1964, Fuller et al. 1969, Chappell able to escapepredation pressureand reachvery high den- 1980, Hyvarinen 1984, Scott 1993, Reid and Krebs sities.The absenceof cyclesin alpine regionswould there- 1996). Reid and Krebs (1996), for example,showed that fore be an indirect consequenceof selectionin stableenvi- both the cold intensity in the autumn (i.e.,befare a perma- ronments.Clearly, we needmuch more empirical work in nent snow cover), and the insulativepotential of the snow other alpine regionsto assessif environmentalvariability is (i.e., the snow coverdivided by the number of degree-days one of the ultimate causesof population cycles. of frost) wereimportant determinantsof the winter surviv- It is surprisingthat the sibling vole population at Sval- al in the collared lemming, Dicrostonyx kilangmiutak. bard did not becomeextinct given the huge fluctuationsin However, their study site, as aur Svalbardstudy site, is numbers,and the associatedvery low numbersafter winter characterisedby a very shallowsnow cover,25 cm on aver- crashes.aur observationsshowed that the spatialvariabil- age in the end of January.Clearly, alpine environments irr, and in particular the relatively large altitudinal spread have much more stable and predictable snow cover than of the population after one or two yearsofincrease (ca 300 arctic environments, as a consequenceof higher winter m), rescuethe population by alwaysleading to SOfiein- precipitations and a lower climatic variability. Snow depth habitedpatches staying ice-free during the winter (Ims and on aur alpine study sitesis at its maximum in April varied Yoccozunpubl.). However, any increasein the extent of between 2 m (in 1994, a snow-poor winter) and 5 m freezing rain events, either in intensity or in frequency (1995, a snow-rich winter) (seeMartin et al. 1994). Most would lead this population to extinction. SOfie climatic importantly, freezing raiD is extremely rare in the alpine modelspredict an increasein the varianceof temperature roDe,and ice coveron the ground is exceptional(unpubl.). and precipitation (e.g.Mearns et al. 1997),and this would Winter survival is thereforeexpected to be higher on aver- probably havesevere consequences for speciessuch as arc- ageand more stable in alpine areasas comparedto arctic tic small mammals.An increasein precipitation is alsoex- enVlronments. pected(Houghton et al. 1996), and this may counterbal- It remains to be shown that thesedifferent patterns in ancethe previousnegative effects by providing a more sta- environmentalvariability may be responsiblefor the evolu- ble snow cover. More researchis neededto understand tion of the observeddifferent demographic tactics. The how the stability and insulating propertiesof the snow lay- stablepopulation siles observedin the Alps may result in er arelikely to be affectedby climatic changes,both in arc- strongerdensity-dependent selection, and thereforelower tic and alpine areas. investrnent in reproduction and higher survival (MacArthur 1962, Boyce 1984, MuelIer 1997). In the Arctic, extreme population fluctuations causedby unfa- Conclusion vourablewinter conditions may resultin frequent local ex- tinctions (Framstad et al. 1993, Yoccozet al. unpubl.). Studiesof small mammalsin cold regionshave mainly This will favour a demographictactic leadingto fast recol- focusedon boreal and {sub)arcticpopulations, emphasiz- onization of habitat patches,that is, high intrinsic rate of ing the occurrenceof dramatic multiannual fluctuations tncrease. (cycles).Less studied havebeen the consequencesin terms The importance of snow cover has also been empha- of demographyof the strong seasonalityand largeinteran- sizedwith respectto patternsof small mammal population nual environmentalvariability, particularly with respectto dynamics.The lack of snow cover in low altitude!middle winter conditions. Here we compare demographicpat- latitude environments (e.g., southem Sweden:Hansson terns of alpine and arctic populations of small mammals, 1971) togetherwith the existenceof a diversecommunity and suggestthat opposite demographictactics have been of generalist predators would prevent the occurrenceof selectedfor: low turn over rate in alpine, stable environ- multiannual fluctuations, i.e., cycles.In northem environments,high turnover rate in arctic, unpredictableenviron- ments, specialist predators may constitute with small ments. mammals a predator-prey oscillating system,where seasonality may furthermore be an important component Acknowledgements- The Svalbardstudy was supported by the (Hanssonand Henttonen 1985, 1988, Hanski et al. 1991, Norwegian PolarInstitute, the French PolarInstitute (I.F.R.T.P.) 1993, Hanski and Korpimaki 1995, Stensethet al. 1996). and the Norwegian Programmefor TerrestrialEcology at Sval- However, as pointed out abovewith respectto demogra- bard (TERRØK). The Alps studieshave been supportedby the CNRS - Univ. Lyon 1, the Ministere de l'Environnement and phy, this claesnot seemto apply to the Svalbard!Alps mi- the National Geographic Society (Grant 5541-95). We thank crotines.The snow yale and the alpine common yale are Meteo Francefor providing the Bourg Saint Maurice and Cha- indeed not known to exhibit large multiannual fluctua- monix meteorologicaldata. Jean,Regina Croz and Michel Tav- tions suchas the anesfound in lowland Europe (Le Louarn ernier providedwelcome support in the field. JepAgrell and Len- 1977,Jobsen 1988, Mackin-Rogalskaand Nabaglo 1990), nart Hanssonprovided useful commentson the manuscript. whereasthe Svalbardpopulation showslarge multiannual fluctuations. It; however,low turnover ratesare selected for in alpine environments, then small mammalsmay not be

142 ECOWGICALBU l1NS Gaillard,J. M., Festa-Bianchet,M. and Yoccoz,N. G. 1998.Pop- References ulation dynamics of large herbivores:variable recruitment Alendal, E. 1977. Sørlig markmus har att fotfestepå Svalbard. - with constant adult survival. - Trends Ecol. Evol. 13: 58-63. Fauna30: 8-11. Gerrard,A. J. 1990. Mountain environments:an examinationof Barry, R. G. 1992. Mountain weatherand climate. - Routledge, the physicalgeography of mountains.- BelhavenPress, Lon- London. don. Batzli, G. O. and Henttonen, H. 1993. Home rangeand social Hanski, I. and Korpimaki, E. 1995. Microtine rodent dynamics organization of the singingvole (Microtus miurus). - J. Mam- in northem Europe: pararneterizedmodels for the predator- prey interaction. - Ecology76: 840-850. mal. 74: 868-878. Beniston,M. 1997.Variations of snow depth and duranon in the Hanski, I., Hansson, L. and Henttonen, H. 1991. Specialist SwissAlps over the last 50 years:links to changesin large- predators,generalist predators, and the microtine rodent cy- scaleclimatic forcings.- Clim. Change36: 281-300. de. - J. Anim. Ecol. 60: 353-367. Benton, T. G. and Grant, A. 1996. How to keep fit in the real Hanski, I. et al.1993. Population oscillationsof borealrodents: world: elasticityanalyses and selectionpressures on life histo- regulation by mustelid predators leads to chaos. - Nature ries in a variableenvironment. -Am. Nat. 147: 115-139. 364:232-235. Bernardo, J. 1996. Maternal effects in animal ecology.- Am. Hansson,L. 1971. Habitat, food and population dynamicsof the Zool. 36: 83-105. field vole Microtus agrestis(L.) in southem Sweden. - Viltrevy Boyce,M. S. 1979. Seasonalityand patternsof natural selection 8: 267-378. for life histories.- Am. Nat. 114: 569-583. Hansson,L. and Henttonen, H. 1985. Gradienrsin densityvar- Boyce,M. S. 1984. Restitution of r- and K-selectionas a model iations of small rodents:the importanceoflatitude and snow of density dependentnatural selection.- Annu. Rev. Ecol. cover.- Oecologia67: 394-402. Syst. 15: 427-447. Hansson,L. and Henttonen, H. 1988.Rodent dynamics as com- munity processes.- TrendsEcol. Evol. 3: 195-200. Boyce, M. S. 1988. Evolution oflife histories: theoryand patterns from mammals.- In: Boyce,M. S. (ed.), Evolution of Henttonen, H., McGuire, A. D. and Hansson,L. 1985. Com- life-histories of mammals: theory and pattern. Yale Univ. parison of amplitudes and frequencies(spectral analysis) of Press,pr. 3-30. density variations in long-term data sets of Clethrionomys Carlsson, B. A. and Callaghan,T. v: 1994. Impact of climate species.-Ann. Zool. Fenn. 22: 221-227. changefactors on the clonal sedgeCarex bigelowii: implica- Houghton, J. T. et al. (eds) 1996. Climate change 1995. The tions for population growth and vegtativespread. - Ecogra- scienceof climate change.- CambridgeUniv. Press. phy 17: 321-330. Hurrell, J. w: and Van Loon, H. 1997. Decadal variations in Chappell, M. A. 1980.Thermal energeticsand thermoregulatory climate associatedwith the nonh Atlantic oscillation. - costsof small arctic mammals.- J. Mammal. 61: 278-291. Clim. Change36: 301-326. Claude, C. 1995. Chionomysniva/is (Mattins, 1842). - In: Hyvarinen, H. 1984. Wintering strategyof voles and shrewsin Finland. - In: Merritt, J. F. (ed.),Winter ecologyof small Hausser,J. (ed.), Mammiferes de la Suisse.Birkhauser, pr. 339-343. mammals. Spec. Publ. CarnegieMus. Nat. Hist. 10, pp. Diaz, H. F. and Bradley,R. S. 1997.Temperature variations dur- 139-148. ing the last century at high elevationsites. - Clim. Change lms, R. A. and Yoccoz,N. G. 1997.Studying transfer processes in metapopulations:emigration, migration, and colonization.- 36: 253-279. Dunmire, W W 1960.An altitudinal surveyof reproducnon in In: Hanski, I. and Gilpin, M. E. (eds),Metapopulation biol- Peromyscusmanicu/atus. - Ecology41: 174-182. ogy. Ecology, geneticsand evolution. Academic Press,pp. Førland, E. J., Hanssen-Bauer,I. and Nordli, P.ø. 1997. Climate 247-265. statisticsand longterm seriesof temperatureand precipita- Innes, D. G. L. and Millar, J. S. 1994. Life historiesof Clethrion- non at Svalbard and Jan Mayen. - Norwegian Meteorol. omysand Microtus (Microtinae). - Mammal Rev.24: 179- Inst., Oslo. 207. Framstad,E., Stenseth,N. C. and Østbye, E. 1993.1ime series Janeau,G. 1980. Repartition ecologiquedes micromammiferes analysisof population fluctuations of Lemmuslemmus. - In: dansl'etage alpin de la region de Briancon.- Mammalia 44: Stenseth,N. C. and Ims, R. A. (eds),The biology of lem- 1-25. mings. Academic Press,pr. 97-115. Janeau,G. andAulagnier, 5.1997. Snowvole- Chionomysniva/is (Martins 1842). - IBEXJ.M.E. 4: l-Il. Frank, F.)9:53. Beitragelur Biologie, insbesondereJugendent- wicklung der Schneemaus.- Z. Tierpsychol. Il: 1-9. Jobsen, J. A. 1988. Plagues of Microtus arva/is in grassland areas in the Netherlands.- Bull. OEPP 18: 271-276. Fredga,K. et al. 1990.The "common vole" in Spitsbergenidenti- fied as Microtus epiroticusby chromosomeanalysis. - Polar Jones,J. K. and Carter, D. C. 1980. The snow vole, Microtus niva/is,in the lowlandsof westernYugoslavia. - J. Mammal. Res.8: 283-290. Fuller,W A., Stebbins,L. L. and Dyke, G. R. 1969. Overwinter- 61: 572. ing of small mammalsnear Great SlaveLake, Northern Can- . Katz, R. w: and Brown, B. G. 1992. Extremeevents in a chang- ing climate: variability is more important than averages.- ada.-Arctic 22: 34-55. Clim. Change21: 289-302. Gaillard,J .-M. et al. 1997. Early survival in roe deer:causes and consequencesof cohort variation in two contrastedpopula- Krebs,C. J. 1964.The lemming cycleat BakerLake, Northwest Territories, during 19~9-62. - Arct. Inst. North America, tions. -Oecologia 112: 502-513. Tech. rap. 15

ECOLOGICAL BULLE1lNS 47. 199\ 4~ Krebs, C. J. 1966. Demographicchanges in fluctuating popula- Reid, D. G. and Krebs,C. J. 1996. Limitations to collaredlem- tions of Microtus californicus.- &01. Monogr. 36: 239-273. roing population groWth in winter. - Can. J. Zool. 74: Le Louarn, H. 1977. Les micromammifereset les oiseauxdes 1284-1291. Hautes AIpes.Adaptations a la vie en montagne.- Disserta- Saucy, F. 1994. Density dependence in time series of the fossorial tion, Rennes. form of the water vole, Arvico/a terrestris.- Oikos 71: 381- Le Louarn, H., Spitz, F. and Grolleau, G. 1970. Le campagnol 392. des champs Microtus arva/is Pallasdans le Brianconnais.- Scott, P;A 1993. Relationshipbetween the onset of wimer and Ann. Zool. Ecol. Anim. 2: 423-426. collaredlemming abundanceat Churchill, Manitoba, Cana- Leslie,1>;H., Chitty, D. and Chitty, H. 1953.The estimation of da: 1932-90. - Arctic 46: 293-296. population parametersfrom data obtained by meansof the Smith, A T. 1988. Patternsof pika (genusOchotona) life history capture-recapturemethod. Ill. An exampleof the practical variation.- In: Boyce,M. S. (ed.), Evolution oflife histories applicationsof the method. - Biometrika 40: 137-169. of mammals.Yale Univ. Press,pp. 233-256. MacArthur, R H. 1962. Somegeneralized theorems of natural Sommaruga-Wograth, S. et al. 1997.Temperature effects on the selection.- Proc. Nat. Acad. Sci. USA 48: 1893-1897. acidity of remote alpine lakes.- Nature 387: 64-67. Mackin-Rogalska,R and Nabaglo,L. 1990. Geographicalvaria- Spitz, F. 1977. Le Campagnoldes champs (Microtus arva/is [Pal- tion in cyclic periodicity and synchronyin the common vole, las]) en Europe.- Bull. OEP 7: 165-175. Microtus arvalis.- Oikos 59: 343-348. Stenseth,N. C. and Ims, R. A. (eds) 1993. The biology of lem- Martin, E., Brun, E. and Durand, Y. 1994. Sensitivity of the mings. -'- Academic Press. French AIps snow cover to the variation of climatic variables. Stenseth,N. C., Bjørnstad,O. N. and Falck,W 1996. Is spacing -Ann. Geophys. 12: 469-477. behaviour coupled with predation causing the microtine Mearns, L. O., Rosenzweig,C. and Goldberg, R 1997. Mean density cycle?A synthesisof current process-orientedand and variance changein climate scenarios:methods, agricul- pattern-oriented studies. - Proc. R. Soc. Lond. B. 263: tural applications, and measures of uncertainty. - Clim. 1423-1435. Change 35: 367-396. Watson, I. W, Westoby,M. and Holm, A. M. 1997. Demogra- Meylan,A. 1995. Microtusarvalis (Pallas, 1778). - In: Hausser,J. phy of two shrub speciesfrom an arid grazedecosystem in (ed.), Mammiferes de la Suisse.Birkhauser, pr. 328-333. westernAustralia 1983-93. - J. &01. 85: 815-832. Millar, J. S. and Teferi, T. 1993. Winter survival in northern Wildhagen,A 1953. On the reproduction of volesand lemming Peromyscus maniculatus. - Can. J. Zool. 71: 125-129. in Norway. - StatensViltundersøkelser. Muelier, L. D. 1997. Theoretical and empirical examination of Yoccoz,N. G. and Mesnager,S. 1998.Are alpine bank voleslarg- density-dependentselection. - Annu. Rev. Ecol. Syst. 28: er and more sexuallydimorphic becauseadults survive bet- 269-288. ter?- Oikos 82: 85-98. Nyholm, E. S. 1966. Observationson somebirds and mammals Yoccoz,N. G., Steen,H. and Ims, RA 1990. østmarkmus: en of Spitsbergen.-Ann. Zool. Fenn. 3: 173-175. ny pattedyrart for Svalbard. - Fauna 43: 36--42. Orzack, S. H. and Tuljapurkar,S. D. 1989.Population dynamics Yoccoz,N. G., Ims, R. A. and Steen, H. 1993a. GroWth and in a variableenvironment. VII. The demographyand evolu- reproductionin island and mainland populationsof the yale tion ofiteroparity. -Am. Nat. 133: 901-923. Microtusepiroticus. - Can. J. Zool.71: 2518-2527. Ostfeid, R. S. 1988. Fluctuations and constancyin populations Yoccoz,N. G. et al. 1993b. Estimating demographicparameters of small rodents.-Am. Nat. 131: 445-452. and the population size:an updated methodologicalsurvey. Pollock, K. H. 1982. A capture-recapturedesign robust to une- - In: Stenseth,N. C. and Ims, R A. (eds),The biology of qual probability of capture. - J. Wild!. Manage.46: 752- lemmings.Academic Press, pp. 565-587. 757. Yoshimura,J. and Clark, C. W 1991. Individual adaptationsin Przybylak,R 1997. Spatialand temporal changesin extremeair stochasticenvironments. - Evol. &01. 5: 173-192. temperaturesin the Arctic over the period 1951-1990. - Int. T.Climatol. 17: 615-634.

44 '1 RI