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Nordic Society Oikos Role of Food in Hare Population Cycles Author(s): Lloyd B. Keith Source: Oikos, Vol. 40, No. 3, Herbivore-Plant Interactions at Northern Latitudes. Proceedings of a Symposium Held 14-18 September, 1981, at Kevo, Finland (May, 1983), pp. 385-395 Published by: Blackwell Publishing on behalf of Nordic Society Oikos Stable URL: http://www.jstor.org/stable/3544311 Accessed: 14/04/2009 18:06 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=black. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. Blackwell Publishing and Nordic Society Oikos are collaborating with JSTOR to digitize, preserve and extend access to Oikos. http://www.jstor.org OIKOS 40: 385-395. Copenhagen 1983 Role of food in hare population cycles Lloyd B. Keith Keith, L. B. 1983. Role of food in hare population cycles. - Oikos 40: 385-395. The snowshoe hare has a well-documented 10-yr cycle in North America's Boreal Forest; the Arctic hare probably has cyclic fluctuations of comparable periodicity, amplitude and geographic scope within the taiga of USSR. Arctic hare populations have a 3- to 4-yr cycle in the forests of Norway and Sweden. Fluctuations of black-tailed jackrabbits in Utah, near the species' northern limit, exhibit an approximate 10-yr periodicity. Cyclic declines in snowshoe and Arctic hare populations having 10-yr cycles of abundance are likely initiated by food shortage over winter which lowers reproduction and juvenile survival. Declines in Arctic hares having a 3to 4-yr cycle in Scandinavia appear to be linked to declines in microtine rodents which cause markedly increased predation on hares and other alternative prey. Declines in the cyclic jackrabbit population of northern Utah are allegedly part of a predator-prey oscillation with coyotes. In neither of the latter two fluctuations is food shortage involved. Both cyclic and noncyclic hare populations may become food short at high densities. It is proposed that the 10-yr cycle is dampened or replaced by irregular fluctuations where snowshoe habitat is fragmented and insular because: (1) the greater structural (niche) diversity of fragmented habitats increases prey species diversity, and hence the stability and facultative nature of predator populations; and (2) the resulting sustained predation on dispersing hares blocks potential increases in distribution and density. Thus it may be the character of predation, as molded by habitat factors, that primarily determines the regularity of snowshoe hare fluctuations. This is likely also true for other species of hares. Because snow cover effectively protects vegetation from browsing by snowshoe and Arctic hares, the impact of varying snow depth on overwinter food supplies may be highly significant to hare populations at or near cyclic peaks. L. B. Keith, Dept of Wildlife Ecology, Univ. of Wisconsin, Madison, WI 53706, USA. AMepaHCKIH 3aSnI-6enTMKMeeT Xopano 9OKyMeHTHpOBaHHbit 10--eTHHI LSHKJB ceBepo-arMpmaHcHx 6opeajbtaxX njiecax. rIaq-pHb 3aSaILmeeT CIeBHO UIIKJNHWie KoJne6aHHH CXOQHOt nepHQnOIHOCTH, aMruIHTJyB H reorpa4qtecKHx MaCI- Ta6OB B TaecHOR 30He CCCP. lonyJIHnM noTIHpHoro safLa HMkeoT3-4-neTHne ULUJU B necax HopBer H u lBeiu. >inyxTyatIg qepHoxBocTror 3afla B TOre y ceBepHoro nperena apeana BKsa noKa3saIBaioTrpHMepHO 1O-JTTHKI nepHQeqMHOCTh. Accepted 11 October 1982 ? 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TaK KaK pHKaHcKoro 3aIa CHeBroBO IIOKpOB 39eKTHBHO 3anraeT paCTHTeJ1bHOCTh OT 06'be-aHLqa aMepHKaHcKHM H nIOlHIMpHHM 3aIaMvH, BTIHHFHe pa3aHmIHO rnJy6IHHb CHeroBOro noKpoBa Ha o6ecrleIeHHOCTb e 3HaqeHHe jMZl noHnMek B TeIeHMe 3HMl NocKeT HMeTb 6on B Mae?HT, Koraa wUKI AOcTHraeT 3alteB rInynjT IHKa. 385 1. Introduction 2.2. Arctichares Certain mammals and birds of northern regions exhibit marked multi-annual fluctuations that are both periodic and synchronous over large geographic areas. Increasingly sophisticated analyses (Bulmer 1974, Finerty 1980) of long-available population indices have convincingly affirmed what seemed intuitively evident to many earlier workers - a 3- to 4-yr cycle in microtine rodents and a 10-yr cycle in the snowshoe hare Lepus americanus. Each oscillation is tracked by a number of largely obligate predators, and by tetraonids that are ecologically linked through common predators, food sources, etc. to microtine and hare populations. The snowshoe hare cycle has stimulated discussion and speculation among biologists for approximately 60 yr (Hewitt 1921, Elton 1924), and was recognized by fur traders at least 100 yr earlier (Elton and Nicholson 1942). Numerous theories and hypotheses about the cycle were reviewed by Keith (1963) and Finerty (1980); there is currently no general agreement as to its cause(s). The specific aim of the present paper is to assess whether food plays a role in generating cyclic fluctuations of snowshoe and/or other hare populations. Three species of Arctic hares are currently recognized: L. timidus (Arctic, blue, snow or mountain hare) of northern Europe and Asia; L. othus (tundra hare) of western Alaska; and L. arcticus (Arctic hare) of northern Canada and Greenland. These alleged species are very closely related (Howell 1936, Ognev 1940) and are here simply called Arctic hares. An important ecological distinction, however, is that timidus occupies both tundra and forest habitats, whereas othus and arcticus are restricted to tundra. L. timidus is thus the ecological counterpart of North America's Arctic and snowshoe hares. There are no long-term indices to fluctuations of L. timidus in Eurasia that compare with those available for L. americanus in North America. Nevertheless, a multitude of field observations and some short-term indices of abundance led Formozov (1935) to conclude that L. timidus populations exhibit an approximate 9- to 10-yr cycle in northern regions, but a shorter cycle of about 6 220 0 34 - LEPUS TIMIDUS (NORTHWESTERN U.S.S.R.) U) I 2. Occurrence of cyclic and noncyclic hare populations Implicit in the term "cycle", as applied to wildlife populations, is the idea of regularity. While such cycles are never perfectly regular, they are significantly more so than are other fluctuations. In this section I attempt to identify cyclic hare populations, and briefly describe their periodicity, amplitude and synchrony. 180 > ca: I 140 , 26 - 0 100 18 1 60 1o- oZ Z U 20 2 1876 I I 1886 1896 1920 1930 1940 100 0) 80 Ui 2.1. Snowshoehare The snowshoe hare inhabits the Boreal Forest of North America, and has long been considered a classic cyclic species. Its periodicity is mainly 8 to 11 yr (Keith 1963); measured amplitudes of change have exceeded 100-fold within good habitat, and 10- to 30-fold changes are common (Keith 1981). The cycle is broadly synchronized over a vast area from Alaska to Newfoundland, with regional peaks or lows rarely differing by more than 3 yr (Keith 1963). Cyclic fluctuations are dampened or disappear where snowshoe habitat becomes fragmented through plant succession or agricultural clearing (Buehler and Keith 1982). The fragmented habitats of mountainous regions have apparently never supported cyclic populations (Keith 1963). 386 60 F 40 I 20 1 0 cn u. I z 0 I 1856 1866 1876 1886 1896 1906 Fig. 1. Fluctuationsof Arctichares(Lepustimidus)withinthe taigaof the Soviet Union as depictedby annualharvests(Formozov 1935, Naumov1947, 1960); and fluctuationsof snowshoe hares(L. americanus)in the Boreal Forestnear Hudson Bay, Canada(MacLulich1957). OIKOS 40:3 (1983) yr further south. Naumov (1947) supported this conclusion with additional population indices, and noted that the shorter-term fluctuations to the south were much less regular. He associated 8- to 12-yr fluctuations with ". . . the taiga zones of Europe, Siberia, and the Siberian forest-steppe . . .", and 4- to 9-yr fluctuations with ". .. regions of the mixed and insular forest zones and the European forest-steppe". I have compared (Fig. 1) the 3 longest sets of population indices that are available for L. timidus (Formozov 1935, Naumov 1947, 1960) with those for L. americanus (MacLulich 1957). The periodicity and regularity of these major fluctuations appear similar, and strongly suggest that timidus, like americanus, has a "10-yr cycle". The indices for L. timidus depict fluctuations that occurred within the taiga zone of northwestern and northeastern USSR. This apparent cycle of L. timidus resembles that of L. americanus in two other respects: the amplitude of change is reportedly marked (20- to 50-fold, Formozov 1935); and population peaks occur synchronously over large areas (Naumov 1947). The long-term cycle of L. timidus contrasts sharply with fluctuations recorded in the northern forests of Scandinavia (Fig. 2). These peak at mostly 3- to 4-yr intervals and, as discussed later, seem to be linked to the existing microtine cycle. The 2- to 7-fold amplitudes of change are probably less than for timidus in the USSR, but neither this aspect nor the degree of inter-area synchrony is well documented (Hornfeldt 1978, Lindlof and Lemnell 1981). Indices to Arctic hare fluctuations elsewhere provide little evidence of cyclic changes. Hunting-kill estimates from two estates in Finland spanned about 80 yr, and depicted irregular short-term fluctuations with mean intervals between all apparent peaks of approximately 3 yr (Siivonen 1948). On the other hand, kill data from Scotland (Middleton 1934, Hewson 1955, 1965, 1976) showed major long-term fluctuations with little sugges250 25 200 20 . Co w UlJ rcc < I 150 15 U u a w 100 10 < Co tion of regularity or inter-area synchrony. Measured amplitudes of fluctuation, 2 to 10-fold, were comparable to those in Scandinavia (Watson and Hewson 1973, Hewson 1976). Characteristics of Arctic hare fluctuations in North America and Greenland are virtually unknown. A 42-yr record of pelt shipments from Alaska (L. othus) suggests long-term fluctuations of high amplitude (Buckley 1954). General observations of L. arcticus point to large annual variations in density on Canada's Arctic islands (Howell 1936, Bonnyman 1975). 2.3. Black-tailedjackrabbit The black-tailed jackrabbit occupies arid and semi-arid deserts and grasslands of the western United States and Mexico. Its fluctuations have often been marked (Palmer 1897, Nelson 1909), and recent studies indicate a regularity within northern sections of its range. Thus Gross et al. (1974) concluded: "... there is variationin synchronybetweenlocalizedareas ... yet, there has been sufficientsimilarityover this broad region[UtahandsouthernIdaho]to stampthe early1950's, the late 1950's, and the late 1960's or early 1970's as the highdensityyears.The amplitudeof variation[9-fold]during our study has evidentlybeen less than that commonly reportedfor the snowshoehare." I have compared jackrabbit population trends on an intensive study area in Utah during 1963-1980 with those of a cyclic snowshoe hare population in Alberta during 1961-77 (Fig. 3). This comparison, together with the general historical trend cited above, suggests that the Utah jackrabbit population is also cyclic. 2.4. Otherhares The European hare (L. europaeus) is the only other species for which indices are adequate to classify fluctuations. These were reviewed by Keith (1981) and interpreted as indicating irregular and short-term (2-4 yr) changes in numbers. The white-tailed jackrabbit occupies much of the northern prairies of the United States and Canada. Nothing is known of its population fluctuations, and very little of other aspects of demography. 2.5. Synopsis 0 I Cyclic fluctuations of mainly 8 to 11 yr occur among snowshoe hares occupying more or less continuous (nonfragmented) habitat within the Boreal Forest , I I 1945 1950 1955 960 1965 1 1 (taiga) of North America. A cycle of similar length 1945 1950 1955 1960 1965 1970 1975 probably occurs among Arctic hares in the taiga of the Fig. 2. Fluctuationsof Arctic hares (Lepus timidus) in the Soviet Union. In each case fluctuations are of high northerntaigaof Norway(solidline) andSweden(dashedline) as depicted by annual harvests (Moksnes 1972, Hornfeldt amplitude (> 10-fold) and broadly synchronized within 1978). Arrowsindicatereportedyearsof peak microtinenum- large geographic regions. In the northern forests of bers. Norway and Sweden, Arctic hare fluctuations are much z 50 OIKOS 40:3 (1983) 387 Vaughan and Keith 1981), together with other field studies of shorter duration (see Keith and Windberg 1978: 50-52, Wolff 1980), disclosed that the cyclic pattern is generated by a predictable sequence of birthand survival-rate changes. The decline from peak autumn densities is initiated by sharply lower overwinter survival of juveniles; adult survival is not notably reduced until 1 or 2 yr later. A major decrease in the birth rate immediately precedes and/or follows that in juvenile survival, and accentuates the population decline. Both juvenile survival and reproductive rates remain low for 2 or 3 yr, then recover over a period of 2 or 3 yr; reproduction improves more rapidly than juvenile survival. Onset of the next cyclic increase in numbers is evoked by marked rises in both juvenile and adult survival, reproduction having already fully recovered. 600 LEPUS AMERICANUS 500 : z y 400 UJ L 300 I , a 0 n 200 100 o z 0 1960 1965 1970 1975 300 I a: | LEPUS CALIFORNICUS 250 3.1.2. A conceptual model In 1971 I presented a conceptual model of the snowshoe hare cycle which was later summarized by Keith and Windberg (1978): z x o 200 z Q 150 Z < 100 oc y II 50 0 1965 1970 1975 1980 "... the cycleis repeatedlygeneratedintrinsicallythrougha hare-vegetationinteraction(dominantherbivorevs. winter food supply)that triggersthe populationdecline.This elevates the predator-hareratio,therebyintensifyinga second interactionthat extendsthe periodof declineanddrivesthe hare populationstill lower. The grouse are cyclic due to varyingratesof predatorinducedmortality- a spin-offfrom the hare-predatorinteraction.Interregionalsynchronyis causedbasicallyby mildwintersthat moderatemortalityin peakharepopulations,andpermitothersthatarelaggingto attainpeakdensities.Suchsynchronyis reinforcedby highly mobile predatorpopulations." Fig. 3. Fluctuationsof snowshoehares(Lepusamericanus)on intensivestudy areasnear Rochester,Alberta,Canada(Keith et al. 1977, L. B. Keith, unpubl.)and black-tailedjackrabbits (L. californicus)in CurlewValley,Utah, USA (L. C. Stoddart, unpubl.). Both the hare-vegetation and predator-hare interactions have the strong delayed-density-dependent attributes that can promote and sustain oscillations. The shorter-termed and of lower amplitude: prominent cyc- successive population changes and the relative biolic peaks occur at chiefly 3- to 4-yr intervals, as do those masses involved are outlined in Fig. 4. in associated microtine populations. Black-tailed jackrabbits probably have a cycle of around 7 to 10 yr in 3.1.3. Role of food The cornerstone of the foregoing model is a hare-winter Utah near the northern limit of their range. in marked food interaction, evidence of which will now be fluctuations sometimes be may Although other hare species, and in other populations of the examined. In this and later sections I use the term "food" in a strictly quantitative sense - as something above-mentioned cyclic species, they are either noncyclic (e.g. European hare, Arctic hare in Scotland) or providing hares with energy. The overwinter (6-8 month) diet of cyclic snowshoe there are insufficient data on which to make a judgement (e.g. white-tailed jackrabbit, Arctic hares in North hare populations is predominantly woody vegetation the terminal twigs of various shrubs and small trees. In America and Greenland). November 1970, at the outset of a winter of peak hare densities, we began to measure food supplies on study 3. Cause(s) of cyclic fluctuations areas in central Alberta. Food was insufficient to suphare populations in this peak winter and the winter port 3.1. Snowshoe hare following, and there was probably also food shortage 3.1.1. General demography during the third winter (Pease et al. 1979). This was the Cyclic snowshoe hare populations in central Alberta, first quantification of food shortage during a cyclic peak and decline. Subsequently, Wolff (1980) showed that Canada, were studied intensively for 17 yr (1961-77). This work (Keith et al. 1977, Keith and Windberg 1978, snowshoe populations in interior Alaska had also ex388 OIKOS 40:3 (1983) 250 little evidence of a density effect on any demographic attribute of these experimental populations. In summary, there is good evidence - direct, indirect, and experimental - that peak snowshoe hare populations become short of food over winter; and that this produces the characteristic sequence of demographic responses which initiates cyclic declines. 100 3.2. Arctichares 0Sooo 26000 - 25>0 - / WOODYBROWSE (WINTER FOODFOR HARES) 1 ooo 500 -j HARES SNOWSHOE SO 3.2.1. Soviet Union As noted earlier, available indices suggest that Arctic 25 hare populations within the Russian taiga have cyclic RUFFEDGROUSE fluctuations comparable in periodicity, amplitude and synchrony to those of snowshoe hares in Canada. It is thus logical to anticipate that other aspects of their population dynamics are similar, including the role of winter food shortage in triggering cyclic declines. 1.00 Both Formozov (1935) and Naumov (1947) largely PFEDATORS 0.50 discounted the idea that cyclic Arctic hare populations usually declined from food shortage. Instead, they re025 peatedly emphasized the role of "epizootics", especially parasitic, as primary causes of mortality. This seems 6 7 9 10 11 12 4 8 5 1 2 0 3 -1 questionable to me because it is often malnutrition that YEARS predisposes mammals to conspicuous losses from Fig. 4. Fluctuationsin relativebiomassof majorcomponentsof parasitic disease. Furthermore, obvious and widespread the 10-yr cycle as observednear Rochester,Alberta,Canada destruction of woody vegetation by high Arctic hare (Keith et al. 1977, Pease et al. 1979, L. B. Keith, unpubl.). populations is apparently common (Formozov 1935): ceeded their food supplies during 2-3 peak and postpeak winters. Annual midwinter-to-spring weight losses among hares were interpreted as providing strong indirect evidence of periodic food shortage in Alberta (Keith and Windberg 1978). Such weight losses were greater during the 3 successive winters of known food shortage and population decline than during the next 3 winters when food was ample (8.5-10.3% vs. 3.0-5.8%). There was an apparent cyclic trend in such weight losses during 1963-76, and a significant correlation with reproduction and juvenile growth rates. To test the hypothesis that midwinter-to-spring weight losses, reproduction, and juvenile growth reflected overwinter nutrition, Vaughan and Keith (1981) experimentally manipulated winter food supplies of captive snowshoe populations. The results of this experiment were wholly consistent with the above-stated hypothesis: hares in food-scarce treatments exhibited greater overwinter weight loss, and markedly lower reproduction during the subsequent breeding season. Growth rates of young born to parents from food-scarce treatments were also lower. Parameter values in all 3 cases closely approximated those previously observed in declining wild populations. Adult survival was only slightly reduced by food scarcity, but juvenile survival dropped sharply - a situation comparable to that noted during the first year or two of a cyclic decline. There was 24 OIKOS 40:3 (1983) "Therewere so manyof them [hares]that there was not a singlebushwithoutone in it. Aspens,birchesandwillowsup to a centimetreand a half thick have been completelydevoured." "... in years in which the white hare is few in number, willowthickets,youngaspens,aldersand bircheshave time to grow and re-establishthemselves,after being generally completelydestroyedby haresin yearsin whichtheirnumbersare at a maximum(I tracedthis re-establishment of the winter food base of the white hare very thoroughlyin SharinskDistrictoverthe years1930-34, afterall the young shoots of edible specieshad been destroyedby the animals in 1927-28.)." These accounts are reminiscent of early descriptions of severe browsing by peak snowshoe hare populations (Seton 1911, Soper 1921, MacLulich 1937, etc.). But as pointed out by Grange (1965) and Pease et al. (1979), food shortage may exist without such conspicuous damage because it is the most inconspicuous parts of the browsable vegetation that comprise the essential food resource, i.e. the small terminal twigs produced largely during the previous growing season. Popov (1960) measured the quantity of browse available to Arctic hares in Yakutia, and concluded: "A comparisonof food requirementsand reservesshows that at the onset of hare populationdecline in 1954, there was no lack of food, such that would have led directlyto hare deaths due to starvation,but food reserveswere limited, which rendereddifficult any possibilityof further growthof the snow hare population." 389 Hornfeldt (1978) modified Keith's (1974) conceptual model of the snowshoe hare cycle to fit the Swedish ecosystem: thus voles replaced snowshoes as the dominant herbivore in successive herbivore-winter food and herbivore-predator interactions, and the Arctic hare was added to the tetraonids as a species suffering higher predation rates (predator shift) and hence declining after the dominant herbivore (i.e. voles) had crashed due to food shortage. Field studies at Grims6, which began in 1974, were designed to test this same model of population change. According to Lindlof (1980) amplitudes of change in both vole and hare populations are less pronounced at Grimso than further north in Sweden, and the chronological relationship between their fluctuations was not clear. Angelstam et al. (in press) and Lindstrom et al. (unpubl.) also reported a low-amplitude fluctuation at Grims6, but noted that hare density changes followed the vole cycle with a lag of 1 yr. Lindstrom et "'Everynow and then incursionsof haresoccuron such a al. (unpubl.) further concluded that hare mortality rates large scale that they attractattentionby destroyingshrubs vegetationandeven the grass.Thisoccurred,for instance,in decreased when vole numbers rose, and increased when 1914 when vast tractsof willows,poplarsand aspenswere voles declined. The same 1-yr lag that occurred in the destroyedin VerkhoyanskDistrict ... from the mouth of hare decline likewise occurred among foxes (Vulpes the river Yana to the Aldan [1000 km] I saw trees and shrubsin some placesthat had been strippedby these vor- vulpes) - the hares' chief predator (Lindstrom unpubl.). The credibility of the above model in explaining the aciousrodents."' short-cyclic fluctuations of these hares is further enPredation has likewise been stressed as a mortality fac- hanced by their reported densities of only 1-4 ind km-2 tor by Soviet workers (Formozov 1935, Naumov 1947), (Lindlof and Lemnell 1981, Lindstrom et al. unpubl.), or less than 10 hares per fox (Lindstrom unpubl.). mainly concomitant with epizootics. The delayed-denLindlof and Lemnell (1981) pointed out that hare sity-dependence, or lag, in predator population redensities at Grimso were 1/100 of those on an island off sponse to snowshoe hare declines (Keith et al. 1977) also occurs among the chief predators of Arctic hares the Swedish west coast, where food resources were evi(Labutin 1960, Naumov 1972). dently poorer. They suggested that food was, therefore, The only solid demographic data that I have seen not likely limiting the growth of the hare population at published on Arctic hares in the Soviet Union deal with Grimso. I am inclined to agree with them. reproduction (Naumov 1947). Mean litter size varies with the stage of the cycle, decreasing during the peak 3.3. Black-tailedjackrabbit year or year following, and remaining low throughout most of the period of population decline. This relation- The cyclic black-tailed jackrabbit population in Curlew ship is also typical of snowshoe hares (Keith and Valley, Utah (Fig. 3), has been studied intensively since Windberg 1978: 50-52, Cary and Keith 1979), and has 1962, and much is known of its demography and inbeen interpreted by me as reflecting the food shortage teraction with food and predators. A demographic summary covering the period that besets peak and declining populations. Naumov (1947) likewise ascribed such reproductive variation to 1962-70 (Gross et al. 1974) revealed two characterisnutrition, but in a qualitative (vitamin) rather than tics of this jackrabbit population which indicate to me that food shortage likely played no significant role in its quantitative (energy) sense. The obvious parallels between cyclic fluctuations of population dynamics: (1) annual variations in natality Arctic hares in USSR and snowshoe hares in North were small (< 20% of the 8-year mean); and (2) both America suggest that their cyclic declines have a com- annual survival of juveniles and variation in annual survival were similar to that of adults. As I described earmon basis - food shortage. lier, snowshoe hares respond to food shortage with 3.2.2. Norway and Sweden major decreases in reproduction and highly differential The largely 3- to 4-yr cyclic fluctuations of Arctic hares losses of young. in Norway and Sweden have been investigated at Clark (1981) and Clark and Innis (unpubl.) examined Grimso in central Sweden, but not to my knowledge the interaction between jackrabbits and their food reelsewhere. The most evident ecological correlate with sources in Curlew Valley. The general conclusion from this hare cycle is a periodic fluctuation among mic- a simulation of this interaction (Clark and Innis unrotines occupying these same northern forests (Fig. 2). publ.) was that "... the observed declines from populaPopov's (1960) data indicated that the total biomass of browse available at the hare peak might have barely supported the population if about equally apportioned among all individuals - a highly improbable event. That the interaction between the hare populations and its winter food supply became critical was seen in Popov's report that by spring 1954 90% of the hares were in poor nutritional condition. Over this same winter, the population allegedly declined more than 90% from 60 km-2 in autumn to 5.4 km-2 by spring. Frequent reports of mass movements of Arctic hares during years of high population provide additional evidence of food shortage. This association is well documented among other species (Lack 1954); and in referring to a peak year, Formozov (1935) stated: "In winter when hares are as abundant as this, food begins to get short and the animals begin to move and undertake migrations." He also cited an observer who wrote: 390 OIKOS 40:3 (1983) tion peaks, characteristic of this oscillatory population, must be caused by some ecological mechanism other than food resource depletion." In all but the poorest production years jackrabbits consumed less than 5% of available net primary production (Clark 1981). On the other hand, Wagner and Stoddart (1972) reported that year-to-year changes in mortality (which accounted for 85% of the variation in rates of population growth) were largely a function of coyote (Canis latrans) predation. And, more recently, Stoddart (1978) concluded ". .. with the observed functional and numerical response of the coyote population to jackrabbit density, and with jackrabbit behavioral changes, the general trend of the observed jackrabbit 'cycle' can be accounted for by coyote predation." If Stoddart's appraisal is correct, this jackrabbit-coyote interaction would appear to be the first documented example of a classic predator-prey oscillation in wild vertebrates. 3.4. Synopsis A predictable syndrome of birth- and survival-rate changes, resulting from overwinter food shortage, initiates cyclic declines of snowshow hares in North America. There is strong circumstantial evidence that declines of Arctic hare populations having a 10-yr cycle in the Soviet Union are also triggered by food shortage. Predation becomes the dominant mortality factor among snowshoes only after their initial food-related decline has greatly increased predator-hare ratios; the same is likely also true for Arctic hares. The much shorter 3- to 4-yr cycle of Arctic hares in Norway and Sweden is probably due to varying rates of predator-caused mortality. The short-cyclic fluctuations of microtines control predator numbers and diet, and the relatively low-density hare populations are especially sensitive to such factors. There is no evidence that food shortage plays a significant role in this hare cycle. The approximate 10-yr cycle of black-tailed jackrabbits in northern Utah, USA, is generated demographically by cyclic changes in annual mortality. These changes are not caused by nutrition but allegedly by predation, with coyotes and jackrabbits interacting to produce a predator-prey oscillation. 4. Discussion 4.1. The basis of food shortageamonghares I earlier cited evidence that the quantity or biomass of available browse has been inadequate to support peak populations of snowshoe and Arctic hares overwinter. There are two other aspects of hare browse - species diversity and chemical composition - that must also be considered because they influence hare nutrition and hence conclusions about the adequacy of natural food supplies. Feeding trials have established that neither snowshoe nor Arctic hares can long survive on a single24* OIKOS 40:3 (1983) species diet (Bookhout 1965, Pehrson 1980, J. P. Bryant, pers. comm.). A mix of two or more woody browse species is evidently essential; and a large biomass of browse, if consisting largely of one species, may not indicate food abundance. Thus hares may starve in the midst of apparent plenty if browse-species diversity is lacking. Such diversity tends to be low within extensive willow (Salix) and black spruce (Picea mariana) monotypes in North America, and likewise within birch (Betula) and larch (Larix) forests of Eurasia. Selective feeding by hares during population highs may likewise reduce browse diversity. Chemical responses by woody plants to browsing by both snowshoe and Arctic hares are well documented (Pehrson 1980, Bryant 1981a). Bryant (1981a,b) demonstrated that adventitious shoots produced after severe browsing contain elevated levels of terpene and phenolic resins which make them extremely unpalatable to snowshoe hares. He also suggested that because such resins repel even food-short hares, browsing-induced chemical defenses may play a role in the 10-yr cycle. The most likely effect would be to reduce supplies of usable browse during the population decline (following severe browsing which occurs at cyclic peaks), and thereby extend the period of food shortage. 4.2. The problemof noncyclicfluctuations Noncyclic snowshoe hare populations occur where suitable habitat (i.e. a dense understory of woody shrubs and saplings) is highly fragmented. This fragmentation exists naturally in mountain ranges, and along the southern limit of snowshoe distribution. It may also develop where fire suppression has permitted forests to mature beyond the successional stage at which hare habitat is more or less continuous (Buehler and Keith 1982). Agricultural clearing, which physically fragments habitat, markedly reduces the amplitude of cyclic fluctuations relative to that occurring on adjacent uncleared land (Windberg and Keith 1978). Buehler and Keith (1982) hypothesized that: ". .. cyclicfluctuationsof snowshoeharesarenot generated where forest cover may be extensiveif areas of low dense woody vegetation therein are widely separated and island-like.This is because dispersersfrom these islandsof favorablehabitatareremovedby a relativelystationaryand abundantcomplexof facultativepredators,thus effectively negatingboth expandeddistributionand local increasesin density. Such hare populationsare therebyprimarilyregulatedwithincomparativelynarrowlimitsby the interaction of habitat,dispersalandpredation.On the otherhand,large blocks of favorablehabitatprovide a matrixof food and cover which is more conduciveto survivalof dispersers. This, coupled with recurrentscarcityof predatorswhose markedfluctuationsstem from their dependencyon hares, permitsthe scatteredpocketsof snowshoesremainingafter a cyclic decline to expand and coalesce as numbersbuild towardanotherpeak. The next significanthare-predation interactionoccursonly after food shortagehas greatlyreduced haresfrom peak abundance." 391 Tab. 1. Peakseasonaldensitiesof snowshoeharesin cyclicandnoncyclicpopulationsas determinedfromestimatorsthatrequired trappingand markingof individualson intensivestudyareas. Studyarea location CentralAlberta (continoushabitat) .. InteriorAlaska .................... InteriorAlaska .................... CentralAlberta(fragmentedhabitat) NorthernNew York ............... WesternOregon................... NorthernMinnesota ............... WesternMontana ................. New Brunswick ................... CentralColorado.................. NorthernMichigan ................ NorthernUtah .................... Haresper km2 Type of long-term of habitat fluctuations exhibitedby hare Autumn Spring population* cyclic cyclic cyclic cyclic noncyclic noncyclic cyclic noncyclic noncyclic noncyclic cyclic noncylic 1288 (Nov)** 609 (Aug)** 592 (Oct) 554 (Nov)** 454 (Sep)*** 395 (Oct) 163 (Sep) 479 (Apr) 192 (Apr) 294 (Apr) 230 (Mar) 184 (Feb) 161 (Mar) 159 (Apr) 73 (Apr) 62 (Apr) 46 (Apr) Reference Keith and Windberg(1978) Ernest(1974) Trapp(1962) Windbergand Keith (1978) Crisseyand Darrow(1949) Black (1965) Green and Evans (1940) Adams (1959) Wood and Munroe(1977) Dolbeer and Clark(1975) Bookhout(1965) Dolbeer and Clark(1975) * There are sufficientlong-termindicesto establishthat populationshere designatedas cyclicare, or have been so, up to the time of the study;populationshere designatedas noncycliclack long-termindices,but on the basisof generalobservations, have been long considerednoncyclic. ** Populationknownto have become shortof food overwinter(Pease et al. 1979, Wolff 1980, Windbergand Keith 1978). *** Descriptionof impactof harepopulationon woodyvegetationoverwinter(Cook and Robeson 1945) stronglysuggeststhat food shortagebroughtabout the populationdecline. A similar view of habitat structure, dispersal, and predation interacting to prevent cyclic fluctuations of snowshoe hares was recently outlined by Wolff (1980, 1981), and discussed at length by Finerty (1980). Lidicker's (1975) conception of "presaturation dispersal" and of a "dispersal sink" are obviously highly relevant to this model. Wagner (1981) indicated that fluctuations of blacktailed jackrabbits decrease in amplitude and regularity from northern Utah to southern Arizona. This he ascribed to increased biotic diversity - in particular, a predator complex that has more species, is largely facultative, and fluctuates less. These changes greatly reduce the interdependency between rate of jackrabbit increase and state (level) of predator population, and vice versa, that Wagner believed necessary to generate cycles. The altered character of predation in cyclic vs. noncyclic jackrabbit populations, as described by Wagner, clearly parallels that deemed significant also in dampening snowshoe fluctuations. Although sustained facultative predation seems to be the paramount limitation on noncyclic snowshoe hare populations, one cannot rule out recurrent food shortage within occupied islands of habitat. Field data (Tab. 1) do not, in fact, support the widespread supposition that maximum densities attained by noncyclic populations are well below those at cyclic peaks. There has been, for example, considerable overlap in highest spring densities of noncyclic (46-230 km-2) and cyclic (62-479 km-2) populations; and, the autumn density of at least one noncyclic population (395 km-2) approached that of two cyclic populations (554 and 609 392 km-2) in which overwinter food shortage was measured. Furthermore, snowshoes on Valcour Island, New York, rose to a peak of 454 km-2 in September 1943, following 3 yr of intensive predator control (Tab. 1). Destruction of woody vegetation on Valcour overwinter 1943-44 (Cook and Robeson 1945), and the occurrence of only 17 predator kills among 112 hare carcasses found in spring 1944 (Crissey and Darrow 1949), suggests to me that acute food shortage was responsible for the population crash. The role of food in noncyclic fluctuations of Arctic hares is even more difficult to assess because: (1) density estimates for noncyclic populations are unavailable, other than in Scotland; and (2) evident high-amplitude fluctuations outside the taiga in the Soviet Union and in Alaska may or may not be cyclic - the data are insufficient to be certain. In any case, there are strong indications that where high densities are attained food shortages sometimes occur: Scotland (Hewson 1965, Moss and Miller 1976); Baltic Islands (Hakkinen and Jokinen 1981); Soviet Union (Formozov 1935); and perhaps Alaska (Grauvogel 1981). Weather conditions affecting food quality and accessibility reportedly aggravate or precipitate shortages of food at high densities in Scotland. The above-cited snowshoe and Arctic hare data suggest that noncyclic populations may also suffer densitydependent food shortages; hence, the occurrence of a hare-food interaction does not in itself guarantee cyclic fluctuations. An obvious major difference between cyclic and noncyclic populations lies in the character of predation, as dictated by habitat structure and species diversity. OIKOS 40:3 (1983) Finerty (1980) apparently reached a similar conclusion through loop analysis (italics mine); DEC NOV JAN FEB MAR APR 1963-64 20 "Biological information and community structure ... suggest that the role of predatorsis to create the type of 3 process." zO functional dispersal sink that sets the stage for the cyclic r, mh -- i (0 0 C) 4.3. Significanceof snow to winterfood supply Snow is an integral part of northern environments, and hindfoot size and coat-color change in the snowshoe and Arctic hare are obviously adaptations to snow. In some regions Arctic hares burrow into snow for shelter (Ognev 1940, Flux 1970, Hakkinen and Jokinen 1974); my impression is that this is less common in forest habitats than on the tundra or other open landscapes. Burrowing by snowshoe hares, a forest dweller, is extremely rare. Although Arctic hares may dig and gnaw through crusted snow to obtain food (Manniche 1910), there is a strong inference in the literature that most vegetation covered by snow is largely unavailable to them (Hewson 1965, 1976, Pulliainen 1972, Bonnyman 1975). I have never seen snowshoes dig for food, nor have I encountered reports of such behavior. If Arctic and snowshoe hares are primarily dependent upon exposed browse, it then seems important to examine the impact of snow depth on overwinter food supply. This question becomes especially significant where snowfall varies markedly from year to year, and cyclic declines in hare populations are initiated by winter food shortages - i.e. in the Boreal Forest or taiga. Accounts of snowfall providing new sources of browse by elevating hares or weighing down vegetation are common (Bider 1961, Pruitt 1970, Pulliainen 1972). To assess the net effect of increasing snow depth, however, one must also know how much food becomes buried and hence unavailable. This will depend importantly on the vertical profile of browse biomass. We were able to estimate this variable from field measurements of hare browse in central Alberta, and then model effects of between-year variations in snow depth on relative availability of browse overwinter. In that largely-deciduous sector of the Boreal Forest, typical of prime snowshoe habitat and characterized by strongly cyclic populations, hare browse was so concentrated near ground level that as little as 50 cm of snow reduced available biomass by 60%. According to our model, annual extremes in snow accumulation alone could have produced a 2-fold difference in the amount of browse available to hares overwinter (Fig. 5). Such variation might easily determine the nutritional status of near-peak hare populations and thus whether or not they begin to decline. Where total annual snowfall tends to be similar over large geographic regions, as for example within the Boreal Forest of North America, comparatively snow-free winters occurring during the OIKOS 40:3 (1983) 40 20 0.8- 0.3. W &!'>? 0.5 0.5- o0I cI - i o.4- 0.3 I . 196364 . . . --- I . I. . 196869 . 197374 III . . . Fig. 5. Extremes in winter snow depths observed near Rochester,Alberta,Canada,1961-77; and the calculatedeffect of snow depth on overwinteravailabilityof browse(hare food) presentin autumn(J. R. Cary,unpubl.). increase phase of a hare cycle may promote inter-area synchrony by permitting already high populations to persist while lagging ones continue to grow toward a critical food shortage. There is certainly a need to determine how food availability for hares is affected elsewhere by changing snow depth. Acknowledgements - I am very grateful to those persons who generouslypermittedme to cite their unpublisheddata and manuscripts. Especially notable in this regard were E. 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