UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

Predation risk and the 10-year snowshoe hare cycle Hik, David Sherwood 1994

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Item Metadata

Download

Media
831-ubc_1994-894245.pdf [ 1.81MB ]
Metadata
JSON: 831-1.0088088.json
JSON-LD: 831-1.0088088-ld.json
RDF/XML (Pretty): 831-1.0088088-rdf.xml
RDF/JSON: 831-1.0088088-rdf.json
Turtle: 831-1.0088088-turtle.txt
N-Triples: 831-1.0088088-rdf-ntriples.txt
Original Record: 831-1.0088088-source.json
Full Text
831-1.0088088-fulltext.txt
Citation
831-1.0088088.ris

Full Text

PREDATION RISK AND THE 10-YEAR SNOWSHOE HARE CYCLEbyDAVID SHERWOOD HIKB.Sc. (Hons), Queen’s University, 1986M.Sc., University of Toronto, 1988A THESIS SUBMITTED IN PARTIAL FULFILLMENT OFTHE REQUIREMENTS FOR THE DEGREE OFDOCTOR OF PHILOSOPHYinTHE FACULTY OF GRADUATE STUDIESDEPARTMENT OF ZOOLOGYWe accept this thesis as conformingto the required standardTHE UNIVERSITY OF BRITISH COLUMBIAJanuary 1994© David Sherwood Hik, 1994In presenting this thesis in partial fulfilment of the requirements for an advanceddegree at the University of British Columbia, I agree that the Library shall make itfreely available for reference and study. I further agree that permission for extensivecopying of this thesis for scholarly purposes may be granted by the head of mydepartment or by his or her representatives. It is understood that copying orpublication of this thesis for financial gain shall not be allowed without my writtenpermission.(Signature)___________________Department of_____________The University of British ColumbiaVancouver, CanadaDate 1/DE-6 (2188)IIABSTRACTI examined the effects of predation risk on the behaviour and populationdynamics of snowshoe hares (Lepus americanus) during a cyclic peak anddecline (1989-1993) near Kluane Lake, Yukon. Like most heavily preyed uponanimals, snowshoe hares have to balance conflicting demands of obtaining foodat a high rate and avoiding predators. The consequences of adopting predatoravoidance behaviours under high risk of predation in winter may influencepopulation dynamics of hares.Changes in patterns of winter habitat use, survival, body mass, and femalereproduction were compared on four experimental areas: (I) where predation riskwas reduced by excluding-out terrestrial predators (FENCE), (ii) where foodsupply was supplemented with ad lib rabbit chow (FOOD), (iii) a combination ofthese two treatments (FENCE+FOOD), and (iv) an unmanipulated CONTROL.Three hypotheses were compared. The food hypothesis predicts that hares usehabitats with the highest amounts of food: body mass remains high, but survivalis reduced. The predator avoidance hypothesis predicts that hares use habitatswith the lowest risk: survival is high, but body mass decreases. The predation-sensitive foraging (PSF) hypothesis predicts that both survival and body massdecline because a trade-off exists between predation risk and food availability.At peak densities hares used open habitats where food was readilyavailable. However, as predation risk increased during the population decline,hares increased their use of safer, closed habitat and shifted their diet to includea greater proportion of poorer quality spruce twigs. This change in behaviourresulted in lower female body mass and reduced fecundity on the CONTROLarea, even though sufficient winter forage was available. A similar decrease inbody mass was observed on the FOOD treatment during the third year of theIIIpopulation decline. On FENCE+FOOD, female body mass and fecundityremained high during the decline. Similarly, body mass did not decline on theFENCE treatment. These results supported the PSF hypothesis where terrestrialpredators were present (CONTROL and FOOD), and the food hypothesis whereterrestrial predators were absent (FENCE and FENCE+FOOD).Hares appear to have a limited ability to reduce exposure to predatorsbecause they have no absolutely safe refuge from predators, and they havelimited reserves of energy during winter. Preliminary evidence suggests thatphysiological stress associated with high risk and poor condition is elevatedduring the population decline. I suggest that deleterious maternal effectsmediated by predation risk may introduce a lag of one generation into the 10-year population cycle of snowshoe hares.ivTABLE OF CONTENTSpageAbstract IiTable of Contents ivList of Tables viiList of Figures viiiAcknowledgments xChapter 1: The Predation Risk Hypothesis of the Snowshoe Hare Cycle 1Hypotheses to Explain the Snowshoe Hare Cycle 1The Predation Risk Hypothesis 4Chapter 2: Food, Risk of Predation, and Patterns of Habitat Useby Snowshoe Hares 8Introduction 8Methods 13Study Area 13Habitat Characteristics: Food and Cover 14Hare Survival 15Patterns of Habitat Use based on Live Captures 16Results 17Hare Density 17Ratio of Predators to Hares 17Prediction 1: Forage Availability 22Other Habitat Characteristics 28Prediction 2: Hare Survival 30Predictions 3 and 4: Habitat Use 37Discussion 41Significance of the Wolff Model 41Prediction 1: Winter Forage 41Prediction 2: Predation and Hare Survival 43Predictions 3 and 4: Habitat Use 44Cover and Other Factors Influencing Habitat Use 45Conclusions 47VChapter 3: Behavioural Responses of Snowshoe Hares to Changesin Food and Predation Risk 48Introduction 48Hypotheses and Predictions 49Methods 54Study Area 54Habitat Use 54Movement: Home Range and Distance Between Browse Points 56Diet 57Body Mass, Time-constraints, and Sex 58Results 58Prediction 1: Hares Increase Use of Closed Habitat 58Prediction 2: Movements Decrease 64Prediction 3: Diet Quality Declines 67Prediction 4: Hares Increase Use of Open Habitat in Late Winter 67Prediction 5: Hares in Poor Condition Use More Open Habitats 72Prediction 6: Females Adopt Safer Foraging Strategies 72Discussion 75Prediction 1: Measuring Patterns of Habitat Use 77Prediction 2: Home Range and Movements 78Prediction 3: Diet Composition 79Predictions 4, 5, and 6: Time of Season, Body Mass, and Sex 80How Can Snowshoe Hares Minimize Risk of Predation? 82Conclusions 84Chapter 4: Does Predation Risk Influence Population Dynamics?Evidence from the Cyclic Decline of Snowshoe Hares 86Introduction 86Hypotheses and Predictions 88Methods 91Results 92Winter Survival 92Body Mass 92Reproductive Output of Female Hares 97Discussion 97Evidence Supports the PSF Hypothesis 97Why do Body Mass and Reproduction Decline? 101Reproductive Costs of Predation Risk 103Predation Risk, Stress, and Population Cycles 105Conclusions 107viChapter 5: Population Cycles, Predation Risk, and the Ghostof Predators Past 108What Causes Population Cycles? 108Food 109Predation 109Spacing Behaviour 110Multi-factor Explanations 111The Stress Hypothesis Revisited 112Summary of the Main Results of this Thesis 116Predator Avoidance and Population Dynamics 120Conclusions 122Literature Cited 124vi’LIST OF TABLESpageTable 2.1 Forage availability, distance to cover, and snow depth onCONTROL, FENCE, and FENCE+FOOD 23Table 2.2 Winter browse available to hares in mid-March and May 29Table 2.3 Summary of hare mortalities determined from radio-telemetrydata between January and April 1989-1 993 on CONTROL, FENCE, andFENCE+FOOD 35Table 2.4 Manly’s alpha habitat preference index for hare trapping databetween January and April 1988-1 993 on CONTROL, FENCE, andFENCE+FOOD 40Table 3.1 Habitat use in late winter based on tracking data on CONTROLand FENCE+FOOD, 1990-1992 59Table 3.2 Home Range size of males and females on CONTROL andFENCE+FOOD, 1989-1992 65Table 3.3 Distance between browse stations on CONTROL andFENCE+FOOD, 1990-1992 66Table 3.4 Summary of predictions and results of the food, predatoravoidance, and predation-sensitive foraging hypotheses 76Table 4.1 Mean litter size of hares at Kluane, Yukon, 1989-1992 onCONTROL areas and FENCE+FOOD 98Table 4.2 Changes in body mass and survival on CONTROL, FENCE,FOOD, and FENCE+FOOD grids 1989-1 993, compared to predictionsof food, predator avoidance, and PSF hypotheses 99VIIILIST OF FIGURESpageFigure 2.1 Conceptual model of changing distribution of hares in closed,open, and shrub habitat over the course of the hare cycle (after Wolff 1981) 11Figure 2.2 Hare densities in April 1988-1993 on CONTROL, FENCE, andFENCE+FOOD trapping grids 19Figure 2.3 Ratio of predator abundance to CONTROL hare density atKluane, Yukon, 1988-1993 21Figure 2.4 Browse available in mid-March, 1991-1 993, in shrub, open,and closed habitat on CONTROL, FENCE, and FENCE+FOOD 27Figure 2.5 Survival proportions estimated from radio-collar data betweenJanuary and May, 1989-1 993 on CONTROL, FENCE, and FENCE+FOODtrapping grids 32Figure 2.6 Habitat use by hares based on live-trapping captures duringthe period January to April 1988-1993 on CONTROL, FENCE, andFENCE+FOOD 39Figure 3.1 Predictions of the FOOD, PREDATION RISK, and BALANCEhypotheses to explain foraging behaviour of snowshoe hares duringwinters 1989-1 992 52Figure 3.2 Distance to cover while foraging on CONTROL andFENCE+FOOD, 1990-1992 63Figure 3.3 Diet composition of hares on CONTROL and FENCE+FOOD,1990-1 992 69Figure 3.4 Effect of time of season on use of safer habitat on CONTROLand FENCE+FOOD by males and females, 1990-1992 71Figure 3.5 Effect of body mass on use of closed habitat on CONTROLand FENCE+FOOD, 1990-1992 74ixFigure 4.1 Predicted changes in body mass and winter survival undertwo levels of predation risk and food availability 90Figure 4.2 Estimates of 30-day survival in winter on CONTROL, FENCE,FOOD, and FENCE+FOOD, 1989-1 993 94Figure 4.3 Changes in body mass of female hares during Januaryto May, 1989-1993, on CONTROL, FENCE, and FENCE+FOOD 96Figure 5.1 Summary of key results in support of predictions of thepredation risk hypothesis of the snowshoe hare cycle 118xACKNOWLEDGMENTSI owe substantial intellectual debts to many people who have helped meover the past years. I would especially like to thank everyone who was part ofthe Kluane Project for their suggestions and criticism, companionship, and helpin the field and lab. Tony Sinclair challenged me, encouraged my ideas, andhelped me to understand this fragile green planet we live on. I haven’t figured itout yet, but will keep trying. Rudy Boonstra was a constant source of inspirationabout stress and hormones, and many other things. Charley Krebs was open toall of my crazy ideas and his vision of the Kluane Project was always inspiring.Stan Boutin and Jamie Smith were always available to talk about hares andplants and predators. They, along with the rest of my supervisory committee,Ken Hall and Don Ludwig, offered many valuable suggestions, critically reviewedmy early proposals, and read drafts of this thesis. I am particularly grateful toDennis Chitty for his interest in my work. John Boulanger, Karen Hodges, AlexEnd, Mark O’Donoghue, Don Reid, Christoph Rohner, and Locke Rowe mademany helpful suggestions or read parts of this thesis.A number of people assisted with the field work and in many other ways,including Cathy Doyle, Frank Doyle, Remie Dionne, Judy Graham, Kerry Grisely,Robin McQueen, Ryan Patterson, Alistair Sarre, and Sabine Schweiger. Thanks!Anders Angerbjorn, Vilis Nams, and Os Schmitz provided good advice early on.And I am not sure I can ever express my appreciation to Fritz (‘let’s build asauna’) Mueller and Nic (‘the refrigerator goes’) Larter, who went out of their wayto make my life here and in the North memorable. Scott Gilbert provided me witha sanctuary on the other side of the runway. Andy and Carole Williams, and therest of the Kluane Base crew shared great food, good company, and manyridiculous situations.Funding for this project was provided by the National Scientific andEngineering Research Council (NSERC) of Canada through CSP grants to C.J.Krebs et al., and operating grants to A.R.E. Sinclair. I was supported by anNSERC post-graduate fellowship, a University of British Columbia GraduateFellowship, a Canadian Northern Studies Trust Fellowship, and the Departmentof Indian Affairs and Northern Development. All research was conducted underpermit from the Wildlife Branch, Yukon Territorial Government, and facilities weremaintained at Kluane Lake by the Arctic Institute of North America, University ofCalgary. Most importantly, my parents provided love and encouragementthroughout my studies. Thank you.1CHAPTER 1THE PREDATION RISK HYPOTHESIS OF THE SNOWSHOE HARE CYCLEThe ‘10-year’ population cycle of snowshoe hares (Lepus americanus) andtheir predators across boreal North America is a remarkable naturalphenomenon that has attracted the attention of naturalists and scientists for over300 years (Finerty 1980). Fur return records from the Hudson Bay Companyprovide a long-term chronology of these cyclic fluctuations (MacLulich 1937;Elton and Nicholson 1942; Keith 1963), which appear to persist across thecontinent, with some regional exceptions (Smith 1983; Sinclair eta!. 1993).Many studies have considered the role of winter food, predation, and socialbehaviour as causes of the snowshoe hare cycle. Four major hypotheses basedon these primary factors have been proposed (Keith 1990; Krebs et a!. 1992;Royama 1992), and I outline these below.Hypotheses to Explain the Snowshoe Hare Cycle(1) The prevailing explanation is the winter-food and predation, or Keithhypothesis described by Keith (1974, 1983, 1990), and Keith et al. (1984). Atpeak hare populations the depletion of winter food resources is supposed tolead to poor nutrition, and subsequently reduced fecundity and increasedsusceptibility to predation. Then, according to this model, there is a delayeddensity-dependent increase in predators, which continue to drive the hares tolow numbers before declining themselves. Pease et a!. (1979) documented anabsolute shortage of winter food for hares at the population peak, butnevertheless, body weights are highest at this time (Keith and Windberg 1978;Chilly 1987; Smith et al. 1988; Keith 1990). In a comparison of three cyclic2declines Keith et a!. (1984) concluded that food shortage is probably restricted toa period of a few months during late winter of the hare peak. Some models ofthe hare cycle have suggested that food limitation is a crucial factor (Akcakaya1992), but do not distinguish between absolute food limitation and relative foodlimitation, where hares cannot get access to abundant food resources (Smith eta!. 1988; Royama 1992). It may be important to make this distinction tounderstand the mechanisms of the hare cycle. Relative food limitation impliesthat poor nutrition of hares during the decline is mediated by some factor otherthan direct starvation.(2) The plant chemistry hypothesis (Bryant eta!. 1991a,b) suggests thatqualitative nutritional changes in winter food plants may explain why hares sufferpoor nutrition during the decline in spite of having a surplus of food available.Forage plants are defended by an array of antifeedant secondary compounds(Sinclair and Smith 1984; Sinclair et a!. 1988; Bryant et a!. 1991 a,b; Schmitz etaL 1992) that are known to result in poor nutrition of hares. However, Sinclair eta!. (1988) reported that while some plant defenses increased in forage speciesfollowing the hare decline, there was no evidence that antifeedant chemicalscaused the decline. At best, an increase in chemical defenses of forage plantsmay slow the recovery of hares during the low phase of the cycle.(3) The polymorphic behaviour hypothesis (Chitty 1967; Krebs 1978)suggests that the spacing behaviour of hares themselves is a necessarycondition for the occurrence of cycles. This hypothesis was not supported in anexperimental test of its predictions (de Poorter 1984). Boutin (1980, 1984) alsoclaimed that spacing behaviour was not a potentially limiting factor that couldincrease mortality and cause a decline. Results of behavioural experiments3(Sinclair 1986; Ferron 1993) suggested that hare populations are controlled bysocial behaviour only when food is limiting. Resident hares may limit juvenileimmigration and recruitment (Boutin 1 984a) and react aggressively to unfamiliarconspecifics (Graf and Sinclair 1987), but these interactions appear to be relatedto the local availability of food. Social behaviour does not appear to act as amechanism of self-regulation of hare population size (sensu Caughley andKrebs 1983).(4) The predation hypothesis involves a delayed density-dependent interactionbetween predators and hares, according to which specialist and generalistpredators increase in abundance some years after the hares’ increase becauseof their reproductive time-lags. These predators then face starvation as haresbecome increasingly rare, thereby generating the cycle (Keith et al. 1984;Hanski eta!. 1991; Royama 1992). Support for this hypothesis comes fromrecent modeling (Trostel et a!. 1987) and experimental studies which show thatpredation alone may be sufficient to generate the hare population decline (Krebset a!. 1 986a,b). Winter food is not absolutely limiting for hares at any time duringthe cycle (Sinclair et a!. 1988, Smith et a!. 1988), and most hares died ofpredation rather than starvation (Boutin eta!. 1986).This predation hypothesis appears to be a reasonable explanation for thehare cycle. However, as Krebs et al. (1992) point out, there are two problems.First, Keith et a!. (1977, 1984) concluded that predation alone could not regulatehare numbers because, according to their calculations, predators alone couldnot account for the numerical losses of hares during the peak and decline phaseof the cycle. Direct starvation must therefore be a significant factor in the haredecline. Recently, Boutin (1994) and C.J. Walters etal. (unpublished model)have suggested that predation rates and predator densities estimated in4previous studies may be too low, and consequently predation may play a largerrole than previously postulated.The second argument against the predator hypothesis is that a significantreduction in reproduction during the hare decline (Cary and Keith 1979) cannotbe a direct result of predation. Natality and juvenile survival are the twoparameters most highly correlated with the rate of population change (Greenand Evans 1940, Keith and Windberg 1978, Krebs et a!. 1 986a, Keith 1990,Royama 1992). Reduced fecundity is correlated with low body mass during theprevious winter (Keith and Windberg 1978; Vaughan and Keith 1981), and themajor factor determining winter body mass is the availability and quality of winterfood supply. It has been suggested that predation risk may limit access to foodresources, resulting in relative food shortage during winter (Wolff 1980; Keith eta!. 1984; Sievert and Keith 1985).The Predation Risk HypothesisThe effects of predators on prey populations are usually considered to belethal, involving the removal of individual prey. However, there is increasingevidence that nonlethal effects of predators on the behaviour of prey may alsobe important, since many animals use poorer habitat and reduce their foodintake in the presence of predators (for a review see Lima and Dill 1990). Antipredator behaviour of prey in response to increased predation risk may result indecreased fecundity or increased mortality caused by factors other thanpredation. There is considerable interest in how these predator avoidancebehaviours influence predator-prey population dynamics (Hassell and May 1985;Ives and Dobson 1987; McNamara and Houston 1987, 1990; Abrams 1989,51990, 1991, 1992a,b,c, 1993; Williamson 1993; FitzGibbon and Lazarus 1994),but this effect has been difficult to demonstrate experimentally.In this thesis I formulate and test a cohesive predation risk hypothesis ofthe snowshoe hare cycle. The main elements of this hypothesis have beenanticipated for more than 50 years (MacLu lich 1937; Green and Evans 1940;Adams 1958; Wolff 1980; Keith et al. 1984; Sievert and Keith 1985; Krebs et a!.1986a; Smith eta!. 1988; and others), and recent theoretical advances inunderstanding effects of food and predation on behaviour of prey (Ludwig andRowe 1990; Lima 1992; Clark 1993, 1994) are used to integrate these earlierobservations. Predation is clearly the proximate cause of death of most hares(Keith et a!. 1984; Boutin et a!. 1986). It also seems that observed declines inbody mass and reproduction following the cyclic peak cannot be explained byabsolute food limitation (Pease et a!. 1979; Smith et a!. 1988). The distributionof food and cover offering safety from predators may play an important role indetermining habitat preferences and foraging behaviour of hares (Wolff 1980).There may be a decrease in relative food availability (e.g. a reduction in foodintake or quality) if hare foraging activity is reduced as risk of predation isincreased (Gilbert and Boutin 1990).The essence of the predation risk hypothesis is that those hares whichsurvive the initial population decline or are born and recruited during this time,live in an environment of high predation risk. If hares adopt anti-predatorbehaviours that reduce foraging effort, this change may lead to decreases inbody mass and fecundity even though food is abundant. The adverseconsequences of poor condition may persist for more than one generation.Anti-predator behaviours may be reinforced throughout the life of a harebecause predation rates are high and predator capture success is low.O’Donoghue and Krebs (1992) showed that mortality during the first 40 days of6life was 60-90%, and estimates of 30-day adult mortality rates averaged 10-20%(C.J. Krebs eta!., unpublished data). In addition, most adult hares haveprobably survived one or more encounters with a predator. For example,Murray (1990) reported that the precent of chases that result in a kill was 33-81% for coyote, and 17-38% for lynx.The experiments described in this thesis were conducted as part of theKluane Boreal Forest Ecosystem Project (Krebs et aL 1992), a series ofcommunity-scale, decade-long experiments focused on the effects of predatorson the snowshoe hare cycle, and consequences of the hare cycle on thestructure of northern boreal forest communities. I monitored the behaviour anddemography of hares during the cyclic population decline when hare mortality ishigh (Keith 1990), with emphasis on the late winter (pre-reproductive) period,when a tradeoff between survival and reproduction in hares is expected fortheoretical reasons (McNamara and Houston 1987; Ludwig and Rowe 1990;Clark 1993, 1994).In this thesis the following predictions of the predation risk hypothesis wereexamined:(1) Predation risk is not constant during the 10-year population cycle ofsnowshoe hares, and patterns of winter habitat use by hares reflect changes inpredation risk in addition to the distribution of winter food resources (Chapter 2).(2) Hares, like other heavily preyed-upon animals, adopt foraging behavioursthat minimize risk of predation (Chapter 3).(3) The adoption of anti-predator behaviours by hares in response to increasedpredation risk results in reduced body mass and fecundity during the decline7phase of the 10-year cycle, and contributes to the persistence of low harenumbers (Chapter 4).In Chapter 5 the evidence in support of the predation risk hypothesis and itsrole in generating population cycles of hares and other small mammals isreviewed. Particular emphasis is placed on the role of physiological stressassociated with predation-sensitive foraging behaviour.8CHAPTER 2FOOD, RISK OF PREDATION, AND PATTERNS OF HABITAT USEBYSNOWSHOE HARESINTRODUCTIONThe availability of food and protective cover often have a strong influenceon the behaviour of vertebrate herbivores. Classical foraging theory suggeststhat animals select habitats that provide the highest rate of energy return (Krebsand Kacelnik 1991). Recent studies of animal foraging behaviour haveemphasized the importance of predation risk in determining patterns of habitatuse (Gilliam and Fraser 1987; Ludwig and Rowe 1990; McNamara and Houston1987, 1990; Clark 1993). Many animals select environments offering protectionfrom predators (e.g. dense vegetation) even if foraging efficiency there (e.g.intake rate) is lower (Lima and Dill 1990; Cassini and Galante 1992; Dickman1992; Hughes et a!. 1993). Patterns of habitat use may reflect behaviouralprocesses that result in reduced predation risk. In this chapter I examinedifferences in food, cover, and predation that may determine the patterns ofhabitat use by snowshoe hares in winter.Populations of snowshoe hares (Lepus americanus) fluctuate in number,with population peaks occurring at periods of 8 to 11 years throughout most oftheir range in the northern boreal forest (Keith 1963, 1990; Krebs eta!. 1986).Keith et a!. (1984) proposed that successive food-hare and hare-predatorinteractions could explain the ‘10-year’ cycle (see Chapter 1). Recentexperimental studies of the snowshoe hare cycle have shown that the majorproximate cause of hare mortality is predation (Keith et as’. 1984; Boutin et a!.1986; Krebs et a!. 1986; Trostel et a!. 1987), and that winter forage is notabsolutely limiting for hares at Kluane (Smith et al. 1988).9In this thesis I propose a mechanism for the interaction between food andpredation based on changes in predation risk and resource distribution amongdifferent habitats. The spatial heterogeneity of habitats utilized by hares mayinfluence the cyclic dynamics of these populations, since the environment oftenconsists of a mosaic of refuges containing little food, surrounded by relativelyunsafe areas where animals feed (Pullianinen 1983; Holmes 1984; Anderson1986; Sih 1987; Lima and Dill 1990; Cassini and Galante 1992). If safe patchesare too small, the herbivore (hares) may go extinct. Buehler and Keith (1982)suggested that large-scale clearing of land in Wisconsin may have caused localextinction of hare populations because patches of dense refuge habitat wereinsufficient to maintain viable populations through the cyclic low. In a furtherstudy, Keith et a!. (1993) suggested that the probability of local extinction infragmented habitat depends on patch size and the number of resident hares.Predation risk has been recognized as an important factor influencinghabitat use by hares (Keith et a!. 1984; Sievert and Keith 1985). Wolff (1980,1981) developed a conceptual model of changing patterns of winter habitat usein which three habitat types were available to hares. In order of decreasingsuitability based on predation risk, these were closed spruce forest, open spruceforest, and open shrub habitat (Fig. 2.1). In this model, utilization of openspruce and shrub habitat increases with hare density, and at peak hare densitiesall habitat is inhabited (darker shading in Fig. 2.1). Predation is highest in openhabitats and hares decline there first. During the decline and low phase of thecycle, hares survive in closed spruce habitat, which provides refuge frompredators.There is some empirical support for the patterns of habitat use describedby Wolff (1980, 1981). First, many studies have found that hares are moreabundant in dense, closed habitat than in more open habitats (Buehler and10Fig. 2.1 Conceptual model of changing distribution of hares in three differenthabitats of decreasing suitability (closed > open > shrub), over the course of thehare cycle (after Wolff 1981). Hare density increases with darker shading.Arrows indicate direction of dispersal movements between habitats.11LOWDECLININGc1osedINCREASINGEARLY PEAK4LATE PEAK12Keith 1982; Orr and Dodds 1982; Wolfe et a!. 1982; Pietz and Tester 1983; Keithet a!. 1984; Litvaitis et a!. 1985a,b; Scott and Yahner 1989; Litvaitis 1991; andothers). Snowshoe hares are found in virtually all woody and brushy habitatsduring cyclic population peaks, but are restricted to densely vegetated habitatduring population lows (MacLulich 1937; Keith and Windberg 1978; Wolff 1980,1981; Litvaitis eta!. 1985; Keith 1990). Second, Sievert and Keith (1985) foundthat mortality due to predation was higher in open habitat. Finally, movementsof marked snowshoe hares into dense cover were recorded during cyclicpopulation declines (Keith 1966; Keith and Windberg 1978; Wolff 1980, 1981;Boutin 1984b).In this Chapter I describe changes in availability of forage and cover indifferent habitats, predation on hares in different habitats, and patterns of habitatuse by hares during a cyclic decline in the southwest Yukon in order to evaluatethree key predictions of the Wolff model.Prediction 1: Closed and open habitats differ in the amounts of forageavailable: more food is available in open habitats.Prediction 2: The survival rate of hares is higher in closed habitats than in openhabitats.Prediction 3: Habitat use is determined by risk of predation rather than forageavailability. Use of open shrub habitat increases at the population peak, but isreduced during the population decline in favour of more closed habitat.Finally, terrestrial predators were excluded from two experimental study siteswhich allowed me to examine a fourth prediction of the effects of predation riskon patterns of habitat use by hares.13Prediction 4: When predation risk is reduced, habitat use by hares reflects theavailability of food more than cover (predation risk). Therefore, hares useopen habitat more often then they would in areas with higher predation risk.METHODSStudy AreaThis study was conducted between 1988 and 1993 as part of the KluaneBoreal Forest Ecosystem Project (Krebs et a!. 1992). This period spanned thepeak (1989/90) and decline years of one hare cycle. Field sites were located inthe Shakwak Trench along the Alaska Highway, east of Kluane Lake, Yukon,Canada (61° N, 138° W; c. 900 m a.s.l). The forest is dominated by whitespruce (Picea glauca) with an understory of grey willow (Salix glauca) and bogbirch (Betula glandulosa). These three plant species are the primary forage ofsnowshoe hares during winter (Smith et a!. 1988). Experimental feeding trialsshowed that hares prefer twigs of 5 mm basal diameter or less of mature Picea,followed by Betula, and then SaIix (Sinclair and Smith 1984).Hares were studied on three 34-ha experimental grids containing 400 gridpoints located in a 20 x 20 array: (i) an unmanipulated CONTROL (Sulphur), (ii)FENCE+FOOD, a 1-km2 area surrounded by an electric fence to deter terrestrialpredators (lynx, Lynx L canadensis, and coyote, Canis latrans), and provisionedweekly with pelleted rabbit chow (16% crude protein). Chow was distributedalong four cut lines spaced evenly across the grid. Avian predators (mainlyGreat Horned Owl, Bubo virginianus, and Northern Goshawk, Accipitergentilis)had unrestricted access to this site, and (iii) FENCE, a 1-km2 area surrounded14by an electric fence as above. Approximately 12-ha of this grid was covered bymonofilament-line in an attempt to deter avian predators; however, much of thiswas buried by snow in late winter and therefore ineffective.Hares were live-trapped (Tomahawk Live Trap Co., Tomahawk, Wis.) onthe three 34-ha trapping grids between January and May, 1988-1993. At least86 traps were placed on four equally spaced rows across the grid. Traps werebaited with alfalfa cubes, and hares were trapped over 1 to 6 days, at 2- to 4-week intervals between January and May. We eartagged (No. 3 monel tags,National Band and Tag Co., Newport, Ky.), weighed, and determined the sex ofall animals trapped. Hare densities were estimated from 5-6 day trappingsessions in April of each year using the mark-recapture estimators for a closedpopulation (Otis et a!. 1978; Boulanger 1993). The effective trapping area wasestimated to be 60 ha which includes a buffer of one home range (about 5 ha)around the edge of the trapping grid.Habitat characteristics: food and coverBetween late February and mid-March 1991, the following habitatcharacteristics were recorded for an area of 15-rn radius centered on the 400grid stations on each of the three grids: (i) habitat type (shrub: < 10% sprucecover; open spruce: 10 to 50% spruce cover; closed spruce: > 50% sprucecover); (ii) distance to nearest cover (places used by hares that provided coveron at least three sides and overhead; e.g. deadfall trees, large spruce trees,snow-burrows); (iii) the number of 5-mm stems of each species of browse(Picea, Salix, and Betula) available in an area of 3 m2, offset from each gridstake by 2-rn, and that were 80-cm or less above snow level; and (iv) snowdepth. Measures of forage availability were repeated at approximately 10015randomly selected sites on each grid in mid-March 1992 and 1993. Differencesbetween grid, habitat type, and year were compared using ANOVA (Wilkinson1988).In order to convert stem density to twig biomass the fresh weight (fwt) anddry weight (dwt) of fifty 5-mm stems of Salix and Betula were determined. Thebiomass of 5-mm stems of Picea was calculated from a relationship betweenstem diameter and stem mass of 86 twigs (r=0.80; C.J. Krebs, unpublisheddata). Biomass of 5-mm stems were 10.1±0.6 g fwt for Salix, 9.8±0.6 g fwt forBetula, and 26.5 g fwt for Picea stems.Hare su,vivalDuring trapping sessions, some hares were fitted with 40-g radio-collarsequipped with mortality sensors (Lotech Inc., Newmarket, ON). Radiofrequencies were monitored daily to determine survivorship of hares. On thedeath of a radio-collared hare, details of the cause of death and the location ofthe kill site were recorded (C. Doyle et a!., unpublished data). The proportion ofhares surviving was calculated for each month (January to May) using thenonparametric Kaplan-Meier maximum likelihood estimator described by Pollocket al. (1 989a,b), which allows for the staggered entry of animals during the studyand censoring of data for lost radios. Usually 25-35 hares were radio-collaredon each grid, but following the decline all hares (as few as 4) were radio-collaredon CONTROL and FENCE. Survival distributions between treatments werecompared using the Wilcoxon signed ranks test (Pollock et a!. 198gb).16Patterns of habitat use based on live-capturesAt least 86 traps on each grid were placed systematically at grid stationsand later assigned to one of the three habitat types (shrub, open spruce, closedspruce). The total number of hares captured during the first night of eachtrapping session during the January to April period was used to determine theproportion of hares utilizing each habitat. Only the first night of a multi-daytrapping session was used in order to minimize problems associated withtrapping hares, such as trap-saturation and increased stress. The number ofhares captured during this period ranged from 7-217 on CONTROL, 10-131 onFENCE, and 47-230 on FENCE+FOOD, depending on hare density and thenumber of trap-nights (Table 2.4).An index of habitat use for each habitat (Pu) was calculated asPu1 = (P1 - Pa1)*P i, where Pa1 is the proportion of habitat i available, and Pc isthe proportion of hares captured in habitat i. A value of Pu1 = 0 indicated thatthere was no difference in the proportion of habitat available and hares capturedthere. Positive values indicated a preference and negative values indicatedavoidance. For comparison, I also calculated Manly’s alpha as an index ofhabitat preference (Krebs 1989). This value was based on the capturefrequency of hares in each habitat. Differences between the number of harescaptured in each habitat in each year and the number of traps available in eachhabitat type were evaluated using the Kolmogorov-Smirnov test statistic(Wilkinson 1988).17RESULTSHare densityPeak hare densities in April 1990 were approximately 1.2 hares ha-1 onCONTROL, 1.6 hares ha-1 on FENCE, and 5.5 hares ha-1 on FENCE+FOOD(Fig. 2.2). Hare densities declined to 0.2, 0.38, and 4.0 hares ha-1, respectively,by April 1992. Peak numbers on FENCE and FENCE+FOOD were reached oneyear after peak numbers on CONTROL.Ratio of predators to preyThe ratio of an index of predator activity in the entire valley to CONTROLhare density increased each year during the increase, peak and decline phaseof the 10-year cycle (Fig. 2.3), indicating that relative risk of predator encountersper individual hare increased over this time. Activity of lynx and coyote wasestimated using the number of tracks observed per 100 km of winter transects(M. O’Donoghue eta!., unpublished data), goshawk activity by the number ofbirds seen in late winter per 1000 hrs of observation (Doyle and Smith 1994),and great horned owl abundance based on the number of resident individuals in100 km2 in spring (Rohner and Krebs 1994). It is possible that this ratiooverestimates predation risk for hares during the late decline if predators searchfor alternative prey species (Stuart-Smith 1992). I have not tried to adjust thepredation risk index to account for this possibility.18Fig. 2.2 Hare densities (number per ha + 95% C.l.) in April 1988-1993 onCONTROL, FENCE and FENCE+FOOD trapping grids.19=UiC,)Ui=217654301988 1989 1990 1991 1992 1993YEAR20Fig. 2.3 Ratio of predator abundance to CONTROL hare density in late winterat Kluane, Yukon (1988-1993). Predator index described in the text.21Uiz>-Ui0.0IUi•0.50040030020010001988 1989 1990 1991 1992 1993YEAR22Prediction 1: Forage availability is higher in open habitatHabitat was classified into three types based on spruce overstory: shrub(<10% spruce cover), open spruce (10%-50%) and closed spruce (>50%).Forage availability (number of 5-mm stems in 3-rn2) in mid-March for each ofthese three habitats was generally highest for Salix, followed by Picea, on allthree grids (Table 2.1). Betula twigs were rare on CONTROL andFENCE+FOOD, but more abundant on FENCE. Salix forage was generally.more abundant in shrub and open habitat than in closed habitat in all threeyears. Results of a three-way ANOVA for Picea twigs, with main effects of grid,habitat type, and year, indicated that only the effect of grid was significant(F2 17421 0.13, P.<0.001). No other main effect and interaction terms weresignificant (P>0.10). For Salix, two of three main effects were significant (grid:F21742=2.98, P=0.051; habitat:F21742=4.04, P=0.018; year:F21742=8.81,P.<0.001). The interaction between grid*habitat and habitat*year were alsosignificant (P<.009), owing to the lower twig biomass on FENCE+FOOD.Forage availability (stem density) of all species decreased in all habitatsbetween 1991 and 1992. In 1993 there was an increase in the number of Piceaand Salix stems on FENCE+FOOD.The biomass of forage available per individual hare was calculated basedon the number of stems available to hares in each habitat in mid-March. Thesebiomass values were calculated for each habitat and summed, then divided byApril hare density (Fig. 2.2). In addition, I also assumed that 60 days of woodybrowse were required to maintain hares until the end of the season, and thathares require about 300 g (fwt) of forage per day to maintain body mass (Peaseet al. 1979). On this basis, the forage available each year was at least ten timesthe amount required on CONTROL for Picea and Salix three times the amount23Table 2.1 Forage availability, distance to cover, and snow depth. Availability of 5-mmstems (in 3 m2) of Picea, Sallx and Betula, distance to cover (m), and snow depth (cm)in shrub, open spruce, and closed spruce habitats in March 1991 to 1993 onCONTROL, FENCE+FOOD, and FENCE grids. Mean values ± 1 S.E. Sample size inbrackets. Approximately 400 quadrats were sampled in 1991, and 100 quadrats in1992/93.CONTROL # stems /3 m2DistanceHabitat N Year Picea Salix Betula to Cover SnowdepthSHRUB (37) 1991 5.8± 2.2 9.8± 2.7 0.4± 0.2 15.0± 1.7 52±2(12) 1992 1.2± 0.7 3.5±0.7 0 48±7(8) 1993 1.5± 0.8 2.5±0.6 0 52±7OPEN (203) 1991 4.4± 0.7 6.9± 1.0 0.1± 0.01 10.2± 0.5 48±1(55) 1992 3.2± 0.8 5.1± 1.2 0.02± 0.02 44±3(60) 1993 2.1±0.4 3.6±0.8 0 49±2CLOSED (160) 1991 3.9± 0.7 3.8± 0.7 0.01± 0.01 10.3±0.6 43±2(35) 1992 1.7±0.5 2.7± 1.1 0 45±5(35) 1993 2.9± 1.0 1.9±0.6 0 43±324Table 2.1 continuedFENCE #stems/3m2DistanceHabitat N Year Picea Salix Betula to Cover SnowdepthSHRUB (154) 1991 0.8± 0.4 4.2± 1.0 2.5± 0.7 16.4± 1.5(37) 1992 0.5±0.5 2.1±0.7 0.1±0.1 71±4(15) 1993 0 3.0± 1.4 2.5± 0.5 87±4OPEN (195) 1991 0.9±0.2 3.3± 0.3 0.9± 0.2 7.6± 0.5(82) 1992 0.7±0.2 1.7±0.3 0 65±3(57) 1993 1.0±0.5 5.4±0.9 1.3±0.6 72±2CLOSED (34) 1991 0.8± 0.4 2.2± 0.5 0.1± 0.1 6.2± 0.6(10) 1992 0.2±0.2 1.1±0.5 0 54±4(28) 1993 0.8± 0.4 2.0± 0.6 2.8± 1.3 68±325Table 2.1 continuedFENCE+FOOD # stems /3 mDistanceHabitat N Year Picea Salix Betula to Cover SnowdepthSHRUB (92) 1991 0.2±0.1 14.1±2.4 0.6±0.3 15.5± 1.5 66±2(35) 1992 0.03±0.03 2.4± 0.5 0 74±3(27) 1993 1.0±0.35 6.3± 1.5 0 80±4OPEN (289) 1991 0.9±0.1 3.3± 0.5 0.5± 0.1 9.8± 0.5 59±2(65) 1992 0.3±0.1 1.5±0.3 0-- 67±3(72) 1993 1.3± 0.4 3.3± 0.5 0 -- 75±2CLOSED (16) 1991 0 2.9± 1.0 0 8.7± 1.7 56±5(5) 1992 0.3±0.3 0.7±0.7 0 -- 47±21(4) 1993 1.0±0.7 0 0-- 64± 1926Fig. 2.4 Browse available (kg hare1 day1) in mid-March 1991-1 993 based onnumber of 5-mm stems of Picea, Salix and Betula in each habitat (shrub (S),open (0), closed (C)), on CONTROL, FENCE and FENCE+FOOD trappinggrids. Dashed line indicates daily requirement of 300 g per hare, and x indicatesno browse available. Bars, from left to right, indicate values for 1991, 1992, and1993.27aF i-ia01:o.olJ0.001 S 0 CPicea10-F 1-2- 0.1-00.01-0.001 S 0 CPicea100a0aFENCE+FOOD100-10—HI- —I 4.——cOF’ffROLELFRrLS 0 CSalix100S 0 CBetulaFENCEaS 0 C S 0 CSalix Betula10-1I0.01-0.001•NH NH ft HSPiceaS 0 CSd&S 0 CBettia28required on FENCE, but less than the amount required on FENCE+FOOD,particularly in 1992 (Table 2.2). Total forage available on each grid (Table 2.2)generally increased as hare numbers declined. Amounts of Picea availablewere lowest on FENCE÷FOOD, but large quantities were available onCONTROL and FENCE. Estimates of forage available on FENCE+FOOD arelower, but this grid was supplied with ad lib rabbit chow (16% crude protein).Forage available in mid-March in each habitat (Fig. 2.4) also appears to besufficient for hares, except for closed habitat on FENCE+FOOD.Forage available in mid-March was sampled only from 1991-1993. Inorder to compare these amounts with forage available during the peak years(1989/90), I calculated amounts of Salix and Betula browse available at the endof each winter. These estimates are based on the dry weight of 5-mm stemsestimated from clip-plots at the end of winter (early May; C.J. Krebs et a!.,unpublished data). The results show that even after the winter of peak haredensity amounts of woody browse available to hares ranged from 68 to 280 kghare-1 on FENCE+FOOD and CONTROL (Table 2.2). Measures were notavailable for FENCE, but the same pattern was apparent (pers. obs). Thebiomass values estimated at the end of winter were higher than in mid-Marchbecause the May values include forage buried under snow and therefore notcontinuously available to hares. In summary, winter forage was not absolutelylimiting for hares at Kluane, a result consistent with that of Smith et a!. (1988).Other habitat characteristics: distance to cover and snow depthThere was no difference in the distance to cover between open andclosed spruce habitats on any of the grids (P>0.83), but these distances weresignificantly less on FENCE, averaging 7 m compared with about 10 m on29Table 2.2 Winter browse (5-mm stems of Salix, Betula, Picea) available to hares(above snow) in mid-March (kg fwt hare-1 day-1), and in May at end of winter (kg dwthare-1).Water content of browse is approximately 50% (i.e. 1 kg dwt 2 kg fwt).SalixMARCH (kg fwt hare1 day) MAY (kg dwt hare-1)CONTROL FENCE+FOOD FENCE CONTROL FENCE+FOOD1989 1841990 280 4381991 3.6 0.6 1.3 280 681992 9.8 0.2 2.5 1304 401993 22.6 1.9 15.0 3929 845BetulaMARCH (kg fwt hare-1 day1) MAY (kg dwt hare-1)CONTROL FENCE+FOOD FENCE CONTROL FENCE+FOOD1989 0.81990 0.8 57.31991 0.05 0.06 0.4 0 20.31992 0 0 0.03 8.7 13.61993 0 0 5.6 71.4 199.1PiceaMARCH (kg fwt hare day’)CONTROL FENCE+FOOD FENCE1991 6.9 0.2 0.91992 15.5 0.1 2.31993 49.8 1.6 6.430CONTROL and FENCE+FOOD (P <0.002). Distance to cover was greatest inshrub habitat, averaging 15-16 m on all grids (Table 2.1). Results of a two-wayANOVA indicated a significant effect of habitat(F21116=53.44, P.<0.001), sincedistance to cover was less in open spruce and closed spruce habitats.Snow depth was lower on CONTROL than on FENCE or FENCE+FOODin all three years (Table 2.1). CONTROL grid is located 5 km east of the othergrids and at slightly lower elevation, therefore local differences in snowfall couldexplain this difference. On CONTROL, snow depth was similar in all years, butwas consistently higher in shrub and open spruce habitat than in closed sprucehabitat (P.<0.001). The same pattern among habitats was observed onFENCE+FOOD and FENCE where snow depth varied by 10 tol5 cm betweenyears.Prediction 2: Hare suiviva! is higher in closed habitatIn 1989, survival between January and May on CONTROL was similar tothat on FENCE (Wilcoxon signed ranks test: P=0.08), but was significantly lowerthan that on FENCE+FOOD (Wilcoxon test: P<0.05), particularly in Februaryand March (Fig. 2.5). However, in 1990 survival on CONTROL was generallysimilar to FENCE and FENCE+FOOD. In 1991, the first year of the decline,survival of hares on the CONTROL grid dropped significantly lower than that onFENCE and FENCE+FOOD (c. 60% on CONTROL compared with 80-90% onthe two fenced grids between January and May; Wilcoxon test, P.<.05). In 1992survival was lower on CONTROL than on FENCE+FOOD, but was similar to thaton FENCE. In 1992, survival on FENCE was also significantly lower than onFENCE+FOOD (P<0.05). In 1993 survival on the three grids was similar(P>0.5).31Fig. 2.5 Hare survival each month estimated from radio-collar data during theperiod January to May, 1989-1993 on CONTROL, FENCE, and FENCE+FOODtrapping grids.30-DAYII\CI)SURVIVAL0.60.5oFENcE+FcDo0.4•cXDNTFOLQFWDE0.3..•.....•••JFMAMJFMAMJFMAMJFMAMJFMAM1989199019911992199333On FENCE+FOOD survival showed a small decline in 1991 and 1992compared with peak years. On FENCE, survival was also lower in 1991 than in1992. In 1993 survival of hares on CONTROL fluctuated widely betweenmonths (1.0 to 0.39), but was higher overall than in 1992. Survival on FENCE in1993 was similar to that in 1992, while survival on FENCE+F000 was lowerthan in 1992. Increased use of the predator reduction grids by avian predatorsmay account for much of the observed decrease in survival on these areas in1993 (Ch. Rohner, pers. comm.). Overall, survival of both sexes was similar.More dead hares located during the January to April period were in shrubor open habitat than in closed habitat (Table 2.3). On CONTROL, the proportionof kills in shrub and open habitat was 50-100%. About 25% of mortalitiesoccurred in closed habitat, except in 1992 when 50% (5/10) occurred there.The increase in the proportion of hares killed in closed habitat in 1992 reflectsincreased use of this habitat by hares (see Fig. 2.6 below). On FENCE÷FOODthe sample of hares killed was small except in winter 1993 when 12 kills wereobserved; 67% of these occurred in shrub habitat. No kills were recorded inclosed habitat. On FENCE the majority of kills also occurred in shrub or openhabitat. No statistical tests were conducted because of small sample sizes.During this winter period of 1989 to 1993, 83% of all recorded radio-collarmortalities were due to predation, 9% were attributed to starvation, and theremaining 8% were due to unknown or accidental causes. Both terrestrial (41%)and avian (49%) predators contributed equally to mortality on CONTROL (Table2.3). On FENCE, there were more kills by great horned owls (61%) than bygoshawks (18%), but on FENCE+FOOD these avian predators accounted for anequal proportion of kills (about 30% each). Most goshawk predations took placeduring the population peak and first year of decline, but were also observed in1992 and 1993 on FENCE+FOOD. The majority of hares suspected of starving34Table 2.3 Summary of hare mortalities determined from radio-telemetry data betweenJanuary and April on CONTROL, FENCE, and FENCE÷FOOD, 1989-1993. Habitatsare shrub (S), open (0), and closed (C). Cause of death was recorded as coyote(CY), lynx (LX), goshawk (GOS), great horned owl (GHO), other AVIAN, unknownpredator (UNK), suspected starvation (STARVE). Sample size (N) is indicated for (a)the total number of hares predated, and (b) the total number of mortalities (includesnumber recorded as starved).CONTROLHABITAT (%) CAUSE (%)Year N S 0 C N CY LX GOS GHO AVIAN UNK STARVE1989 9 33 44 22 9 22 0 56 0 22 0 01990 6 33 50 17 6 0 50 17 33 0 0 01991 25 20 52 28 30 7 27 13 17 20 0 171992 10 10 40 50 10 10 50 10 20 0 10 01993 2 01000 2 01000 00 0 01989-1993 9 32 19 16 14 2 935Table 2.3 continuedFENCEHABITAT (%) CAUSE (%)Year N S 0 C N CY LX G0S GHO AVIAN UNK STARVE1989 3 0 100 0 4 0 0 0 25 0 50 251990 5 20 60 20 5 0 0 20 80 0 0 01991 18 44 50 6 20 0 0 35 45 5 5 101992 11 27 55 18 11 0 0 0 100 0 0 01993 4 75 25 0 4 0 0 0 50 0 25 251989-1993 0 0 18 61 2 9 936Table 2.3 continuedFENCEi-FOODHABITAT (%) CAUSE (%)Year N S 0 C N CY LX GOS GHO AVIAN UNK STARVE1989 3 33 67 0 5 0 0 0 0 0 60 401990 2 50 50 0 2 0 0 50 0 0 50 01991 5 20 80 0 5 0 0 60 0 40 0 01992 6 50 50 0 7 0 0 43 14 14 14 141993 12 67 33 0 12 0 0 17 75 0 8 01989-1993 0 0 29 32 10 19 1037(5/11) occurred on CONTROL during 1991, the first year of the populationdecline. Hares recorded as starved were found dead with no external injuries.Since the cause of death could not be proven conclusively and may actuallyhave been caused by other factors (i.e. disease, other stress), the number ofhares reported starved should be considered a high estimate. It is also possiblethat some of these other factors may be starvation-induced.Predictions 3 and 4: Use of closed habitat increases during the hare declineThere were three general trends in the patterns of habitat use by hares(Fig. 2.6). First, shrub habitat was usually avoided (P1 < 0). Second, aspredation risk increased hares decreased use of open spruce habitat onCONTROL and FENCE. Third, hares used closed spruce habitat increasinglybetween 1988 and 1993. These results are unlikely to be a consequence of trapsaturation as no more than 62% of all available traps were filled on any oneevening, even on FENCE+FOOD where hare densities were highest. Habitatpreferences based on Manly’s alpha (Table 2.4) showed the same pattern asthe index of habitat use (P). Shrub habitat was least preferred on all threegrids, and overall there was a decrease in use of open habitat and aconcomitant increase in use of closed habitat during the decline.The results of Kolmogorov-Smirnov tests comparing patterns of habitatuse and availability based on winter trapping data showed significant differences(P<0.001) in 1988, 1989,1992, and 1993 on FENCE; 1992 and 1993 onCONTROL; and 1992 on FENCE+FOOD. These significant differencesoccurred mostly during the late decline phase of the cycle (1992/93) on all grids.Hares preferred closed habitat to more open habitat on CONTROL, where bothterrestrial and avian predators were present. A similar pattern was observed38Fig. 2.6 Habitat use by hares based on live-trapping captures during the periodJanuary to April, 1988-1993 on CONTROL, FENCE and FENCE+FOODtrapping grids. Shaded bars (1989/90) indicate years of peak hare density onCONTROL. Positive values indicate preference, negative values indicateavoidance.1.0CONTROL1.0FENCE1.0FENCE-i-FOOD0.50.5[]0.511__________ri[fi_______________tL.1fi____SHRUBOPENCLOSEDSHRUBOPENCLOSEDSHRUBOPENCLOSED40Table 2.4 Manly’s alpha habitat preference index based on proportion of harescaptured in each habitat between January and April, 1988-1993, on CONTROL,FENCE, and FENCE+FOOD (N = total number of hares captured). Habitattypes are shrub (S), open spruce (0), and closed spruce (C).CONTROL FENCE FENCE+FOODYear N S 0 C NS 0 C N SO C1988 (21) 0.17 0.44 0.39 (10) 0 0.79 0.21 --- ---1989 (40) 0.08 0.51 0.41 (38) 0.11 0.43 0.46 (51) 0.21 0.79 01990 (217) 0.13 0.41 0.46 (120) 0.19 0.47 0.34 (201) 0.33 0.40 0.271991 (81) 0.21 0.34 0.45 (131) 0.18 0.42 0.40 (230) 0.37 0.05 0.571992 (22) 0.19 0.28 0.47 (42) 0.08 0.30 0.62 (68) 0.09 0.08 0.831993 (7) 0 0.33 0.66 (30) 0.17 0.23 0.60 (47) 0.06 0.75 0.1941inside the fences where only avian predators were present (Fig. 2.6)DISCUSSIONSignificance of the Wolff modelThe results of this study provide evidence that predation risk, rather thanchanges in food availability, can account for observed shifts in habitat use overthe hare cycle. Hares increased their use of habitat with lower food (i.e. stemdensity and biomass) and higher cover during the hare decline. Several authorshave suggested that this sort of habitat heterogeneity may influence populationdynamics (Rosenzweig and Abramsky 1980; Sih 1987; Morris 1988; Oksanen etal. 1992; Ostfeld 1992). The late winter period is perhaps the most critical timeof the year for hares, because female condition at this time is positivelycorrelated with reproductive output. Although the Wolff model makes noquantitative predictions, it allows testable predictions of the mechanisms (i.e.dispersal, predation, food shortage) responsible for this pattern to be examined.Prediction 1: Winter forage is most abundant in open habitatsThe results of this study support the first prediction of the Wolffhypothesis, that winter food is more available in open habitats. It also appearsthat winter forage is not absolutely limiting for snowshoe hares. If forage wereabsolutely limiting, hares would suffer mortality from direct starvation. Relativefood limitation implies that poor nutrition is mediated by some factor other thanoutright food shortage causing starvation.Hares require about 300 g of mixed species forage (fresh wt) per day to42maintain body mass (Pease et a!. 1979), and results in Table 2.2 and Fig. 2.2show that sufficient winter food is available for hares even during the cyclicpeak. These results are consistent with those of Smith et a!. (1988). However,Pease et a!. (1979) and Wolff (1980) suggested that some hares actually ran outof food at the peak. One explanation that could account for their results is thatpeak hare densities were higher at Rochester, Alberta in the 1960’s and 1970’s,than at Kluane, Yukon during the 1980’s and 1990’s (Keith 1990; Fig. 2.2). InFairbanks, Alaska, peak hare densities were similar to those at Kluane, but Wolff(1980) did not include Picea, which is an important component of winter diet(Wolff 1978), in his estimates of forage availability. Experimental studies atKluane suggest that food shortage is not a necessary cause of the cycle (Krebseta!. 1986; Sinclair eta!. 1988). Although it is possible that some hares did runout of food (Sinclair et al. 1988), this was not because food was absolutelylimiting.Even though forage appears to be available (Table 2.2), body mass ofhares decreased during the population decline (Keith et a!. 1984; Smith et a!.1988; Chapter 4). One possible explanation is that forage availability isoverestimated based on the methods described above. Forage quality may bepoor because plants are defended by an array of antifeedant compounds(Sinclair and Smith 1984; Bryant et a!. 1985; Sinclair et a!. 1988; Schmitz et a!.1992). Sinclair et a!. (1988) reported that the amounts of some secondarydefenses increased in forage plants at Kluane following the hare decline, andtherefore may have contributed to poor nutrition at this time. The diet of hareson CONTROL shifted from predominately Sa!ix twigs in 1990, to one dominatedby Picea in 1992 (Chapter 3). In short term feeding trials, captive hares wereunable to maintain body mass on a diet of Picea twigs, and could just maintain iton a diet of Salix twigs (Rogers and Sinclair 1994); the observed shift in diet may43account in part for observed declines of body mass on CONTROL (Chapter 4).If quality and digestibility of twigs change over the hare cycle, estimates offorage biomass may not be the best measure of winter forage availability.Hares may also lose mass during the decline because foraging efficiencyis lower if predation risk reduces time spent foraging. Hares may forage lessefficiently if winter browse is less available during the decline as the spatialpatchiness of browse increases (e.g. twig density declines as shown in Table2.1). The observed decrease in survival on CONTROL during the first year ofthe hare decline (Fig. 2.5) may also, in part, reflect differences in socialdominance of hares interacting with the relative availability of food (Boutin1984b; Sinclair 1986; Ferron 1993). Subordinate individuals may be excludedfrom food and cover, and therefore suffer higher predation (Keith et a!. 1984).Prediction 2: Predation and hare suivivalThe second prediction, that predation is higher in open habitats, was alsosupported. Results showed that 70% of all mortalities occur in open habitats(Table 2.3), suggesting that differences in cover between habitats are importantto survival of hares in winter. Many of the predators at Kluane also showedhabitat use preferences. Rohner and Krebs (1994) found that great horned owlskilled more hares in open habitat types at Kluane. They concluded that owlsavoid, or have less hunting success, in closed forests and shrub with densecover. Longland and Price (1991) also reported that capture success of greathorned owls hunting heteromyid rodents was higher in open habitat than inbrushy, closed habitat. In their study, the proportion of successful attacksranged from 5% to 60%. Similarly, Murray (1990) found that during the harepopulation increase (1 987-1988), coyote and lynx used open habitat significantly44more than closed habitat, but the proportion of chases that resulted in a kill wassimilar in both habitat types. However, hares were also killed in closed habitat,particularly during the late decline. Therefore, closed spruce habitat does notprovide absolute refuge from predators, but use of these areas may increase theprobability of survival. The behavioural mechanisms by which hares might beable to reduce risk of predation are discussed in Chapter 3.Predictions 3 and 4: Habitat useThe third prediction of the Wolff model, that shrub habitat is generallyavoided and use of closed habitat increases when predation risk is higher, issupported by live-trapping data (Fig. 2.6). These results indicate increased useof more closed habitats during the hare decline. Based on the amounts offorage available in each habitat type, classical foraging models (Krebs andKacelnik 1991) suggest that hares might prefer open spruce habitat, whereforaging rates are higher than in shrub or closed spruce habitat. This patterndoes not emerge from the results. Rather, when terrestrial predators werepresent, hares displayed a preference for closed, relatively safe habitat overriskier open habitat. Absolute amounts of available browse appear to besufficient (Smith et a!. 1988, Table 2.2), but relative availability may be reduced ifpredation risk limits access to forage. The spatial distribution of twigs increasedduring the decline and this may result in lower foraging efficiency (e.g. increasedtravel time between browse patches; Chapter 3).Support for the fourth prediction, of increased use of open habitat onFENCE and FENCE+FOOD, was weak. This may be explained in part by theactivity of avian predators on both fenced areas (Table 2.3). Even thoughterrestrial predators were removed from inside the fences, no pattern of habitat45preference or avoidance was detected at peak numbers. As CONTROL densitydropped and the intensity of avian predation increased on the fenced grids(Table 2.3), hares shifted to more closed habitat, as they did in unfenced areas.These results provide additional evidence that hares are influenced by risk ofpredation.There are several problems in interpreting patterns of habitat use basedon trapping data. Alfalfa baits may attract hares to habitats where they wouldnot normally be found, but this problem was minimized by using a large numberof traps and thereby avoiding trap saturation. Trapping may over-estimate useof open habitat by drawing animals into areas they would not normally travel(Kotler 1985; Hughes et a!. 1993); however, Boulanger (1993) found noevidence that snowshoe hares could be drawn off of their normal home rangesinto traps. Despite these potential problems, there is still a strong trend in thedata suggesting that hares increasingly preferred closed habitats as predationrisk increased. In general, shrub habitat is under-represented in the trappedsample, and there is an increase in use of closed habitat. Other methods ofdetermining habitat use confirm this pattern (Chapter 3), and Litvaitis et a!.(1985a) found that pellet counts, track counts, and live captures provided similarinformation about the use of habitat types by snowshoe hares.Cover and other factors influencing habitat useDensity of understory cover has been shown to be a key componentinfluencing the distribution of snowshoe hares in many studies (Bider 1961;Buehler and Keith 1986; O’Donoghue 1983; Wolfe eta!. 1982; Wolff 1980), andpreference for closed habitat by snowshoe hares appears to be a general result.Litvaitis et a!. (1 985b) and Pietz and Tester (1983) found that patterns of habitat46use by hares were based primarily on the density of understory species ratherthan composition of forage species. Similarly, Buehler and Keith (1982) andRogowitz (1988) reported that the availability of cover influenced habitat usemore significantly than the availability of food. In western New York state, harespreferred sites with a well developed overstory of mature spruce even thoughforage availability was limited (Rogowitz 1988). Scott and Yahner (1989)reported that habitat use by hares was positively correlated with distance tocover and forage availability. Several studies (Litvaitis eta!. 1985; Wolfe etal.1982; Pietz and Tester 1983; Sullivan and Moses 1986; Carreker 1985) havereported that hare population densities were highly correlated with understorycover> 2-m tall providing at least 40% visual obstruction. At Kluane the shrubunderstory rarely provides this amount of cover and therefore overstoryvegetation is a better index of habitat suitability. Understory shrubs provideforage for hares, but overstory spruce provides most cover. Although overallcover was higher in closed habitat (by definition), distance to point cover wassimilar in both closed and open habitat.Several other factors might influence foraging decisions of hares,including snow depth, temperature, and moonlight. Snow accumulation maydecrease forage availability and cover, but snow also facilitates access to foragethat normally would be out of reach (Keith 1990). Snow burrows are also usedextensively by hares for shelter. Kluane is in the rain shadow of the St. EliasMountains and mean snow depth is shallow, averaging 60 cm and rarelyexceeding 1 m. Hares also excavate craters up to 36 cm deep to obtain buriedforage (Gilbert 1990). Deeper snow may also reduce the hunting success ofsome predators (Murray and Boutin 1991; Huggard 1993).Pease et al. (1979) and Keith (1990) reported that mortality ofmalnourished captive and wild hares was significantly related to ambient47temperature. Low temperatures limit foraging and lead to a decrease incondition. Since snowshoe hares cannot maintain reserves of energy for morethan 3-4 days (Whittaker and Thomas 1983), periods of lost foraging due to lowtemperature may require hares to increase risk during subsequent foragingbouts. Gilbert and Boutin (1991) found that snowshoe hares reduced activity inopen areas, away from cover, during bright moonlit nights. This well knownresponse of small mammals to moonlight may modify predator-prey interactionsby increasing prey vulnerability. The combined effects of low temperature andbright moonlight may greatly reduce time spent foraging by hares. This aspectof foraging ecology requires further investigation.CONCLUSIONSThe results presented in this chapter support the conceptual model ofpatterns of habitat use by hares in winter (Wolff 1980, 1981). Habitat use byhares appears to be determined by risk of predation from both terrestrial andavian predators, rather than by availability of winter forage. Boutin et al. (1985)reported that less than 10% of hares dispersed off their home range, thereforedifferential predation pressure between habitat types may generate theobserved pattern. More information is needed about the foraging success ofhares foraging in different habitats, and the capture success of predatorshunting in different habitats. The mechanisms by which hares may be able toavoid predators and the population-level consequences of predation risk arediscussed in the following chapters.48CHAPTER 3BEHAVIOURAL RESPONSES OF SNOWSHOE HARES TOINCREASING RISK OF PREDATIONINTRODUCTIONPredation risk is defined as the probability of being killed during sometime period (Lima and Dill 1990). Predation risk may influence the time of dayanimals feed, the habitat patches utilized for feeding, the composition of the diet,and other aspects of behaviour. When predation risk is high, many prey specieshave been observed to reduce foraging effort and increase use of protectedhabitats (Lima and Dill 1990). The ability of animals to reduce predation riskmay depend upon both their ability to detect predators, and the feasibility ofalternative foraging strategies. Prey species may evaluate predation risk usingcues based on illumination (Gilbert and Boutin 1991), the presence of predatorodours such as faeces or urine (Sullivan et al. 1985; Dickman 1992;Jedrzejewski et aL 1993), observation of a predator, or predator vocalizations(Curio 1993; Kotler 1992), predation on neighbours (Charnov etal. 1976), orwarning by conspecifics (Underwood 1982; Lazarus 1990).Yet, no matter how successful prey species are at assessing predationrisk, their options for mitigating this risk may be limited. Recent theoretical workhas suggested that the range of anti-predator behaviours available to preyspecies will often depend on their own condition, and the time remaining untilreproduction (Ludwig and Rowe 1990; Clark 1993, 1994). Individuals in dangerof starvation, or of not attaining a certain condition (e.g. fat level, body weight)by the end of a fixed period (e.g. end of winter), may incur increased predationrisk in order to obtain sufficient food. Models which incorporate the currentcondition of an animal and the time remaining to achieve a certain minimum49condition (time-constraints) have been used to predict changes in patterns ofhabitat use (McNamara and Houston 1987, 1 990a; Ludwig and Rowe 1990;Clark 1993, 1994; and references therein).Winter food availability and predation may both be important componentsof the ‘10-year’ population cycle of snowshoe hares (Lepus americanus) in thenorthern boreal forest (Keith 1990; Krebs et a!. 1992; Chapter 1). In Chapter 2, Ishowed that there is spatial heterogeneity in winter food availability andpredation risk among habitats used by hares: safer closed habitats contain lessfood than riskier open habitats. This heterogeneity may lead to a trade-offbetween food and predation risk since hares must balance their energy budgeton a short-term (c. 72 hour) basis (Whittaker and Thomas 1983) whilesimultaneously avoiding predation, the proximate cause of most mortality (Keitheta!. 1984; Boutin etal. 1986).In this chapter I describe patterns of foraging behaviour of snowshoehares under different levels of predation risk during the late peak and earlydecline of the 10-year population cycle (1990-1992). During the cyclicpopulation decline, predation risk (i) increased naturally, and (ii) wasexperimentally reduced in one area by excluding terrestrial predators.Supplemental food (rabbit chow) was also provided there.Hypotheses and PredictionsThe predictions of three hypotheses can be used to contrast the foragingbehaviour of hares. The food hypothesis predicts that animals use habitatswith the highest food availability (where energy gain is maximized; Krebs andKacelnik 1991). The predator avoidance (PA) hypothesis predicts thatanimals use habitats with the lowest predation risk (minimize time spent in riskier50habitats). The predation-sensitive foraging (PSF) hypothesis predicts thatanimals balance predation risk and food availability when choosing habitats(McNamara and Houston 1987; Ludwig and Rowe 1990); as predation riskincreases, so does use of safer habitats.Predictions of these three hypotheses are contrasted in Fig. 3.1. If closedhabitat is relatively safe, but has less food or food of lower quality than moreopen habitats (see Chapter 2), then the food hypothesis predicts that closedhabitat is avoided, independent of predation risk. The predator avoidancehypothesis predicts that closed habitat is preferred, independent of predationrisk (i.e. minimize predation at all times). The PSF hypothesis predicts that thereis a trade-off between food and predation, such that hares increase use ofclosed habitat as predation risk increases during the decline. Similar predictionscan be made for distance to cover, movement (based on proxy measures suchas home range and distance between browse points), and diet composition.These components of winter foraging behaviour (habitat use, movements, anddiet) were used to examine the predictions of the PSF hypothesis.Prediction 1: Patterns of habitat use by hares and movement of hares throughthe environment are not random. As risk of predation increases hares reduceexposure to predation by (i) increasing use of closed habitat, and (ii) reducingdistance to protective cover.Prediction 2: Hare movement (based on two proxy measures) decreases aspredation risk increases: (i) home range decreases in size, and (ii) thedistance between browse points decreases.51Fig. 3.1 Predictions for use of safer, closed habitat during the snowshoe harepopulation decline according to the food, predation risk, and predation-sensitiveforaging (PSF) hypotheses.52HIGHPREDATORAVOIDANCEHYPOTHESIS% — PREDA11ON-SENSfl1VECLOSED FORAGINGHABITAT HYPOTHESISFOOD HYPOTHESISLOWPEAK DECUNEHARE DENSITY53Prediction 3: As predation risk increases, the proportion of poorer quality items(Picea twigs) in the diet increases.Additionally, theoretical investigations (McNamara 1987, 1990; Ludwigand Rowe 1990; Clark 1993, 1994) have suggested that an individual willcounteract a decline in body condition (mass) by spending proportionally moretime in open habitat where food is more available, but risk is higher. For hares,use of the riskier habitat may increase at the end of the winter. Theassumptions of time-constraints (reproduction occurs at the end of winter), andcondition-dependence (changes in body mass influence habitat use) which areimplicit in these models may apply to snowshoe hares. In addition, Clark (1994)suggests that animals with a higher reproductive value (i.e. females) will adopt“safer” behaviours by increasing use of closed habitat than animals with a lowerreproductive value (i.e. males). Although I do not have detailed informationabout changes in behaviour of individuals under different conditions, a numberof predictions of these models can be examined by comparing a sample ofhares from the population at different times.Prediction 4: Use of riskier open habitat will be higher in late winter then inearly winter.Prediction 5: Use of riskier open habitat will increase as body mass decreaseswithin a season.Prediction 6: In late winter, female hares will adopt safer foraging behavioursand use a higher proportion of closed habitat then male hares in order toprotect their reproductive investment, since the young are born in May.54METHODSStudy AreaThis study was conducted near Kluane Lake, southwest Yukon (seeKrebs et al. 1992; Chapter 2). The vegetation is a mosaic of open and closedwhite spruce (Picea glauca) forest, with the understory and open clearingsdominated by grey willow (Salixglauca) and bog birch (Betula glandulosa). Twoexperimental hare live-trapping grids (34-ha) were used: (i) an unmanipulatedCONTROL; and (ii) FENCE+FOOD, a 1-km2area surrounded by an electricfence to deter terrestrial predators (lynx, Lynx L canadensis, and coyote, Canislatrans), and provisioned weekly with pelleted rabbit chow (16% crude protein).Avian predators (mainly Great Horned Owl, Bubo virginianus, and NorthernGoshawk, Accipitergentilis) had unrestricted access to this site. Predation risk,calculated as the index of predators to prey, increased significantly over the haredecline (Fig. 2.3).Habitat structure (percent cover of spruce trees), winter forage availability(number of 5-mm stems of Picea, Sallx, and Betula), distance to cover offeringprotection from predators (deadfall trees, dense thickets, snow burrows), andpredation, in open shrub, open spruce, and closed spruce habitats, aredescribed in Chapter 2.Habitat UseHabitat use and movements of foraging snowshoe hares weredetermined using a spool-and-line technique during winters of 1990-92 (Nams1993). This method involved attaching spools of red thread (180-rn quilting55cocoon bobbins; Culver Textile Corp., 525-52nd St., West New York, NJ, U.S.A.,07093) to hares. Spools were tied in series (up to 3 spools) and secured in anenvelope of clear shrink-wrap plastic to prevent thread from catching onvegetation. Spools were attached to a loop of wire on the radio-collar or gluedto fur on the animals back using a non-irritating skin bond adhesive (Skin BondCement, Pfizer Hospital Products, 11775 Starkey Rd., Largo, FL, U.S.A.,33543). Hares were live-trapped in the evening, weighed, and fitted with spoolswere attached prior to release. The thread trail was followed the next day andinformation about patterns of habitat use and distance to cover was recordedevery 10 m and at browse points. The initial 80-1 00 m when hares were fleeingthe trap were disregarded. The mean length of a trail was 390±64 m. Eachtrack was considered to be an independent sample.Hares were tracked in the same 30-ha area during each winter; thereforeavailability of habitats (shrub, open spruce, closed spruce) was similar betweenyears. The results of this study are based on the foraging track of haresobserved on part of a single night. This sample was probably representative offoraging behaviour of hares while active during the night, but I do not know whatproportion of a 24-hr period was spent active. Most hares rest under coverwhen not foraging.The proportion of each habitat utilized by hares in each year wascompared to the distribution of available habitat on the entire trapping grid usingthe log-likelihood ratio test statistic. The effect of year and sex on habitat usewere also compared using G-tests. Manly’s alpha preference index (Krebs1989) was also calculated for each year. Significant differences in distance tocover between habitat and year were compared using ANOVA (Wilkinson 1988).56Movement: Home Range and Distance Between Browse SitesHome range area is weakly but positively correlated with hare movementrate in winter (Boulanger 1993; r=0.46, p=0.07); therefore home range area maybe a useful index of hare movements. Home range was estimated using radio-telemetry data during the period February - April, 1989-1992. Three permanent,3-rn high, null-peak telemetry towers were placed in a triangular array (White1990) on CONTROL and FENCE+FOOD trapping grids. We oriented the towersusing line-of-site triangulation from known grid locations, and by placing 20survey beacon transmitters at known locations on the grid. Tower orientationwas monitored by placing permanent beacons in known locations. During atelemetry session, bearing direction, signal strength, and an estimate of bearingreliability were made. Unreliable bearings were discarded. Bearings wereusually taken by one observer moving between the three towers in rapidsuccession. Consequently all bearings were not taken simultaneously, butusually within a period of <45 minutes. Some hares may have moved betweenthe recording of first and last bearings. This movement likely increased the errorarea of the location estimate, but did not appear to adversely affect locationestimates. In a simulation study, Schmutz and White (1990) showed that whenbearings were not obtained simultaneously, short-distance movements byanimals increased location error estimates by 10-fold, but decreased locationprecision by <10%. Location estimates were made using Program LOCATE(Narns 1990) to estimate the location of the radio-transmitter and 95%confidence ellipse using the MLE procedure of Lenth (1981). Location estimateswith error estimates of greater than 2 ha were eliminated from subsequentanalysis. The mean error estimate of location estimates was 2.8 1±0.83 ha.57Location estimates were made once every 1-2 days during a 60-dayperiod each winter (February-April). This ensured that successive telemetrylocations were independent of each other (Swikhart and Slade 1985; Boulanger1993). Home ranges were estimated using the harmonic mean estimator (Dixonand Chapman 1980), since it is the most accurate and least sensitive todifferences in sample size (Boulanger and White 1990). Animals for which therewere at least 15 independent locations were used to estimate home range areausing Program LOCATE lVm (Kenward 1990). Asymptotic home range areawas obtained after 15-20 fixes, and was calculated for both 95% and 80% (core)areas. Differences in home ranges were compared using ANOVA.The distance between browsing sites along the path of a foraging harewas also recorded and used as an index of movement. Hares were trackedusing spools of thread described above. Longer distances between browsepoints may indicate higher movement rate. Alternatively, a shorter distance mayindicate that hares are moving less.DietDiet composition was determined by counting the number of times haresbrowsed on Salix or Picea along each threaded track. These points could beclearly identified along many trails, particularly after a snowfall. Sometimes, andparticularly in 1992, there were problems with this method of identifying browsepoints because hares dig for food under the snow, climb spruce trees, eat barkof shrubs and trees, and consume bits of twigs discarded by red squirrels andother herbivores. On FENCE+FOOD the amounts of chow consumed could notbe estimated. In addition, prolonged periods without fresh snow made detailedtracking impossible. In practice, therefore, estimation of diet composition is only58possible when conditions are ideal. For this reason, I consider the number oftimes hares were observed to stop and browse each species, rather than thenumber of stems or biomass of each species consumed.Body Mass, Time-Constraints, and SexThe influence of time of season, body mass, and sex on patterns ofhabitat use were examined using the methods described above. Early wirterwas considered to be the period 15 January to 15 March, and late winter wasthe period from 15 March to the end of winter. Different individuals were trackedduring each period. Habitat use was calculated as a proportion, and wasarcsine transformed before analysis by ANOVA (Wilkinson 1988).RESULTSPrediction 1: Hares Increase Use of Closed Habitat During the DeclineTracking data showed that use of exposed, open habitat in late winterdecreased as predation risk increased between 1990 and 1992 on both grids(Table 3.1). In all years, the distribution of habitats used by hares on CONTROLwas significantly different from the habitat available (G=7.9 - 16.2, df=2, P<0.02).In 1990, hares on CONTROL utilized shrub and open habitat more than closedhabitat, and this pattern was similar for both males and females (G=1 .06, df=2,P=0.588). In 1991 (early decline) females shifted use to include more closedhabitat, whereas males did not (G=54.18, df=2, P.<0.001). This is consistentwith the PSF hypothesis for females, and the food hypothesis for males. In 1992(late decline) both males and females used closed habitat extensively (69-80%).59Table 3.1 Habitat use based on tracking data on CONTROL andFENCE+FOOD grids during late season. Percent of habitat available and meanpercent (± S.E.) of total distance traveled in each habitat (N = number of harestracked).CONTROL% HabitatYear N Shrub Open ClosedAvailable 9 51 40Males1990 13 32±6 49±6 19±81991 9 51±13 36±11 13±81992 6 1± 0.3 19±3 80±3Females1990 8 29±8 46±9 25±91991 7 15±7 26±8 59± 131992 6 2±1 30±9 69± 1060Table 3.1 continuedFENCE+FOOD% HabitatYear N Shrub Open ClosedAvailable 23 73 4Males1990 5 63± 10 37± 10 01991 5 55±5 42±5 3±21992 4 25±9 70± 12 5±4Females1990 5 58±5 42±5 01991 4 62±6 38±6 01992 5 28±9 69±8 3±261In 1990 and 1991 hares on FENCE+FOOD used more shrub and lessopen spruce habitat compared with the available habitat (G-tests, df=2, P<0.01).In 1992 all habitats were used in approximately the proportion that they wereavailable (G=0.75, df=2, P=0.69). During the winter of 1992 hare densitiesoutside of the fence were low and avian predators frequented the fenced grid.The trend in patterns of habitat use suggest hares have increased sensitivity tohigher predation risk. On FENCE+FOOD (Table 2), I compared use of shruband open spruce habitat, since closed spruce habitat was uncommon. In 1991and 1992 shrub habitat (higher food) was preferred to open spruce, but in 1992both males and females changed patterns of use to include predominately openspruce habitat (lower stem density). Both sexes behaved similarly in all threeyears on FENCE+FOOD (G-tests, df=1, P>0.440). Habitat selection based onManly’s alpha showed the same pattern: preference for closed spruce habitatincreased during the population decline on both CONTROL and FENCE+FOOD.Distance to cover while traveling and browsing may also indicatesensitivity of hares to risk of predation (Fig. 3.2). Average distance to cover oneach grid was discussed in Chapter 2 (Table 2.1). On CONTROL, harestraveled closer to cover than expected by chance (P<0.05) in shrub habitat, butnot in open or closed habitat. However, distance to cover at browse sites wassignificantly less than at random for all three habitats, and was occasionally lessthan at random points along the track. This suggests that hares avoided browsefar from cover. However, there was no difference in the distance to cover alonga track or at browse points between years (P>0.80). Therefore, the predictionthat distance to cover decreases as predation risk increases was not supported.Instead, it appears that hares consistently tried to minimize distance to cover inall years.62Fig. 3.2 Distance to cover (± S.E.) at random (squares), along foraging paths(circles), and at browse points (triangles) for male and female snowshoe hareson CONTROL and FENCE+FOOD, 1990-1992.6315-DISTANCE TOCOVER(M) 10DISTANCE TOCOVER CM)5-02015-10 -5-A-RANDOM++CONTROLOicco•199101992TRACKBROWSE— I ISHRUB OPEN CLOSEDHABITATRANDOM+FENCE+FOODOl9co•199101992TRACKBROWSEI ISHRUB OPEN CLOSEDHABITAT64On FENCE+FOOD distance to cover was not different from random whenhares were traveling in shrub, open, and closed spruce habitat (Fig. 3.2).Distance to cover was only slightly less than along a track, except in 1992 inopen habitat. Generally, there was no indication that hares traveled or browsedcloser to cover on FENCE+FOOD than expected in 1990 or 1991. In 1992browse sites were closer to cover than expected.Prediction 2: Movements DecreaseHome range area during the period February to April was lowest for bothmale and female hares at peak density (1989/90), and then gradually increasedon CONTROL (Table 3.2). Male home ranges were consistently larger thanfemale ranges, but the difference between the sexes was not significant (2-wayANOVA of 80% core areas comparing sex and year: Fsex = 0.014, df = 1,35,P=0.90). Similarly, the difference between years was not significant (Fyear =1.633, df=3,35, P=0.21). On FENCE+FOOD there was a significant differencebetween male and female home ranges (Fsex=0.45, df=1 ,29, P= 0.045), but thedifference between years was not significant (P=0.09). Female home rangeswere significantly larger in 1990 than in 1991 or 1992, but male home rangeswere similar in all three years (Table 3.2). These results were not consistentwith the prediction that home range would decrease as predation risk increased.The distances between browsing sites were also considered as an indexof movement while foraging. These distances are minimum estimates becauseonly paths with at least two browse sites were included. The distance betweenbrowsing sites was not significantly different between years on CONTROL(Table 3.3); mean.distances ranged from 32 to 53 m (P>0.40). On65Table 3.2 Home range area (ha ± S.E.) of male and female hares during theperiod February to April on CONTROL and FENCE+FOOD, 1989-1992. Homerange areas shown for 95% and 80% areas (harmonic mean method).CONTROL FENCE+FOODYear N 95% 80% N 95% 80%Male1989 6 2.05±0.68 1.23±0.47 --1990 7 4.99±1.10 3.07±0.79 10 3.86±0.34 1.86±0.251991 8 6.13±3.69 2.95±1.17 4 3.93±0.34 2.17±0.331992 3 5.88±1.90 2.50±1.01 5 3.66±0.52 1.98±0.30Female1989 3 0.98±0.48 0.50±0.15 -- ---1990 4 0.69±0.01 0.49±0.04 6 9.27±1.87 4.80±0.911991 7 4.65±1.86 2.22±0.38 6 2.33±0.64 1.33±0.291992 3 4.52±2.11 2.08±0.41 4 2.61±0.80 1.45±0.3966Table 3.3 Distance between browse sites (± S.E.) on CONTROL andFENCE÷FOOD, winter 1990-1992. Values for male and female hares pooled. Nis the number of browse sites recorded in each year.YearCONTROLN distance (m)1990 49 41.0±7.71991 37 52.7±9.7FENCE+FOODN distance (m)31 32.8±9.129 36.1±1 0.01992 32 31.6±7.9 16 23.7±5.867FENCE+FOOD these distances were lower than on CONTROL, but were alsosimilar between years. There is an indication on both grids that this distancedecreased in 1992, but the difference was not significant (P>0.40).Prediction 3: Diet Quality DeclinesDiet composition was based on the number of times each browse specieswas consumed by hares along foraging tracks (Fig. 3.3). On CONTROL theproportion of Picea increased from 58% (29/50 sites) in 1990 to 91% (30/33) in1992. The proportion of Salix browse sites decreased from 42% to 8% duringthe same period. On FENCE+FOOD SaIix dominated the diet in all three years(55-80%), but consumption of bark increased between 1990 and 1992 (5-25%;Fig. 3.3). The proportion of rabbit chow consumed could not be accuratelycalculated, but higher body mass of FENCE+FOOD hares compared toCONTROL hares (Chapter 4) suggests that all animals had access to thesupplemental chow.Prediction 4: Hares Increase Use of Open Habitat in Late WinterThe PSF model predicted that use of closed habitat would decrease latein the winter season. On CONTROL a decrease in use of closed habitat wasobserved for males in 1991 (Fig. 3.4), but the difference from early season wasnot significant (Fi,i5 = 0.451, P=0.114). A small decrease was also observed forfemales in 1992 but this was not significant. In 1991 females increased use ofclosed habitat between early and late season but this difference was also notsignificant (Ft,io = 0.756, P = 0.41). On FENCE+FOOD, there were no68Fig. 3.3 Estimated diet composition (mean % ± S.E.) of hares based on numberof browse stations for each species. Species eaten in winter are twigs and barkof Picea (spruce), and Salix (willow).69% BROWSESITES% BROWSESITES100806040200•1008060’40200YEARFENCEi-FOOD C PICEAIWGSSALJX1WGS• SAUX BARKYEAR70Fig. 3.4 Proportion (± S.E.) of closed spruce habitat on CONTROL and openspruce habitat on FENCE+FOOD, used by female and male hares early and latein the winter, 1990-1992.71100-75-% CLOSEDSPRUCE .HABITAT% OPENSPRUCEHABITAT25-0-SEASONCONTROL92d92991991 dI IEARLY LATE100EARLY LATESEASON72differences observed between early and late season use of the safer openspruce habitat (which was the only closed habitat available on this grid).Prediction 5: Hares in Poor Condition Use More Open HabitatsBody mass was not correlated with use of closed habitat within a givenyear on CONTROL or FENCE+FOOD (Fig. 3.5). Over all three winter seasonsthere was a strong negative relationship between use of closed spruce habitatand body mass on CONTROL, but there was no indication that individualsincreased use of open habitat as body mass declined within a season. OnFENCE+FOOD there was no relationship between body mass and use of openspruce habitat, even over all seasons (Fig. 3.5). These results do not appear tosupport the prediction that use of open habitat increases as body mass declines.Prediction 6: Females Adopt Safer Foraging Strategies than MalesFigure 3.4 indicates differences in the use of closed habitat betweenmales and females in 1991 on CONTROL grid: females used closed habitatmore than males late in the season. This shift is consistent with the hypothesisthat females may reduce predation risk in order to protect their reproductivevalue (Prediction 6; Clark 1994), but this result was observed in one year onlyand the overall change in patterns of habitat use between males and femaleswas not significant in 1991 (two-way ANOVA; sex: F1,25 = 2.686, P = 0.114;season: F1,25 = 0.013, P= 0.91). However, in the late winter season femalesused closed habitat significantly more than did males (Ft,14 = 10.981, P< 0.005).There were no differences between males and females on FENCE+FOOD. Insummary, 1991 on CONTROL is the only year that a difference in use of closed73Fig. 3.5 Relationship between body mass of male and female hares and theproportion of closed habitat used on CONTROL or open spruce habitat used onFENCE+FOOD, 1990-1992.74100--- •CONTROLd9DOl9cojE •1991I80 J.. Q19920060 I%CLOSEDSPRUCEHABITAT40Doii C20 CC 0.C • 0•D•Do• •..O- .ii I — I I I1100 1200 1300 1400 ‘1500 1600 1700 1800 1900 2000BODY MASS (g)100FENCE÷FOODI9ID 0 iccol0 ••i99i800• 09c2060 I% OPENSPRUCE 1 0HABITAT40 00•0.20 0.C0 I I I I I I1100 1200 1300 1400 1500 1600 1700 1800 1900 2000BODY MASS (g)75habitat was observed between males and females. No other differences inpatterns of habitat use between males and females were observed.DISCUSSIONThe results suggest that the foraging behaviour of hares changed frombeing primarily influenced by the availability of food at the peak, to a strategy ofpredator avoidance during the decline (Table 3.4). On CONTROL, two of theresults are consistent with the predation-sensitive foraging (PSF) hypothesis (%closed habitat used and diet composition). However, distance to cover was lowin all years, suggesting that hares are always sensitive to predation risk.Conversely, home range size generally increased during the decline andpossibly hares were moving more. Since I have no detailed information abouthow hares were using their home range, this may not be a good index ofmovement. Distance between browse points was also similar in all years,suggesting no differences in behaviour at this scale. The main differencesbetween years were increased use of closed habitat and increased use of Piceabrowse.On FENCE+FOOD the changes in diet composition between 1990 and1992 were consistent with the food hypothesis, but the other results support thepredator avoidance and PSF hypotheses (Table 3.4). It is possible that hareshave more alternative foraging strategies available when predation risk is loweror when supplemental rabbit chow is provided. Similar to results on CONTROLthere was no change in distance to cover between years suggesting that haresminimize this distance most of the time. The main difference between years isan increase in use of safer habitat in 1992.76Table 3.4 Summary of predictions of the food, predator avoidance (PA), andpredation sensitive foraging (PSF) hypotheses, for (a) use of closed habitat, (b)distance to cover relative to the peak, (c) home range size, and (d) % spruce inthe diet. Changes in patterns of use relative to the peak are indicated as low ordecrease (ii.), high or increase (U), or no change (=). Observed trends onCONTROL and FENCE+FOOD are shown and the hypothesis predicted (FOOD,PA, PSF) is indicated in bold type.(a) (b) (c) (d)% use distance to home range % spruceclosed cover relative relative to in diethabitat to peak peakPeak Decline Peak DeclineFOOD U U [ UPredictions PA U U U UPSF U U U U U UMale FemaleCONTROL U U UU U UPSF PA Food PSFObservedFENCE+ U U U U UFOODPSF PA PA - PSF Food77The observed changes in patterns of habitat use within a seasongenerally do not support predictions 4, 5, and 6, relating to the effects of bodymass, time constraints, and sex. Only the change in patterns of habitat use onCONTROL during 1991 support the PSF hypothesis. Further testing of thesepredictions will require observation of individual changes over time. This isdifficult with hares when winter survival is so low.Prediction 1: Measuring Patterns of Habitat UseAs predation risk increased during the population decline, the use ofclosed and safer habitat increased (Table 3.1). This result was also obtainedfrom hare live-trapping data (Fig. 2.6). In addition, hares on CONTROL oftentraveled and browsed closer to cover in shrub habitat than expected if haresmoved randomly (Fig. 3.2). This pattern was similar in all years suggesting thathares have a limited ability to reduce this distance as predation risk increases.Several studies have found that the distance from cover that animals will travelto forage depends on predation risk (e.g. Anderson 1986; Hughes and Ward1993). It seems that hares are more likely to switch to safer, closed habitat asrisk increases, rather than reduce distance to cover. This may indicate theimportance of dense closed forest as refuge areas for hares (Wolff 1980).One assumption of the spool-and-line technique is that behavior of hareswas not influenced by trapping or application of spools. Mikesic and Drickamer(1992) have reported that both radio-collaring and application of fluorescentpowders result in a short-term reduction in the activity of wild house mice (Musmusculus). In my study I attempted to minimize disturbance associated withtrapping by only tracking hares that had been previously captured. These hareswere often more calm in traps than individuals captured for the first time. In78addition, traps were checked at hourly intervals during the evening so that hareswould not have time to consume alfalfa bait, which could modify theirsubsequent behavior. Boonstra and Singleton (1993) suggested that handlingand trap confinement of hares lead to increased blood glucose levels and stress.It is possible, therefore, that trapping could have affected the results reportedhere.Prediction 2: Home Range and MovementsHome range area of hares tended to increase as hare density declined(Table 3.2). These results are consistent with those of Boutin (1984c), whofound that summer home range area decreased with increasing populationdensity. However, it seems likely that home range is related to food availabilityand predation risk, as well as hare density. Increases in home range size onCONTROL and FENCE+FOOD during the population decline do not support thePSF hypothesis, but without knowing more about how hares use the spacewithin their home range I cannot conclude that larger home ranges arecorrelated with higher movement rates. It is possible that hares increase homerange size during the population decline in order to have access to additionalcover, or to dilute their own scent, to reduce predator attraction. Larger homeranges may also be required to locate mates at low population density. Also, onFENCE+FOOD hares traveled between the four rows where rabbit chow wasdistributed. Therefore home range size could be increased by the experimentaldesign.The distance between browse sites was similar in all years an CONTROL.There was a small decline in 1992, but this distance was not significantlydifferent from previous years. On FENCE+FOOD distance between foraging79sites was slightly less than on CONTROL, but overall the pattern was similarbetween years. The results are inconclusive, but suggest that hares mayreduce foraging activity during the decline. The development of more sensitiveactivity radio-collars may permit activity of hares to be measured in the future.Prediction 3: Diet CompositionIncreased use of Picea browse is known to lead to a loss of body mass insnowshoe hares (Rogers and Sinclair 1994). There was a major shift in dietcomposition (based on the number of browse sites for each species) between1990 and 1992 on CONTROL: Salix was replaced by Picea as the dominantwinter forage (Fig. 3.3). Increased use of Picea twigs during the hare declinewas also noted by Smith et a!. (1988; Table 4). Wolff (1978) reported that Piceastems and needles were found in 90-100% of all stomachs, and comprised thelargest proportion of the winter diet of hares in central Alaska; however, heprovided no information about changes in use over the cycle. OnFENCE+FOOD, Picea comprised a smaller proportion of the diet than onCONTROL, but there was also higher consumption of Salix bark (Fig. 3.3). Thismay reflect a dietary requirement for increased fibre when supplemental rabbitchow is provided (Cheeke 1983; J. P. Bryant, pers. comm.).The shift from Salixto Picea forage may also be related to the density ofstems of each species (Table 2.1). Based on stem density in mid-March, theamount of Salix browse in closed spruce habitat is less than that of Picea (Table2.1). As a result hares may be selecting the more available forage in thishabitat, because the biomass of 5-mm stems of Picea are 2-3 times higher thanfor Salix (Chapter 2). If the intake rate of Picea stems is higher than that ofSalix, then the amount of time spent foraging and exposed to predation would80decrease as consumption of Picea twigs increased. This would be particularlytrue if handling time is similar in each habitat and travel time between browsesites increased during the decline.Shipley and Spalinger (1992) tested the hypothesis that food intake rateof herbivores is limited by bite size rather than plant density. They found thatbite size explained 40-90% of the variation in intake rate of moose, caribou, andwhite-tailed deer. However, intake rate was not a function of increasing bite sizein snowshoe hares. In a similar experiment with captive lemmings (Dicrostonyxgroenlandicus), Gross et a!. (1993) concluded that bite size had a larger effecton intake rate did than plant biomass or density. The time needed to process abite in the mouth exceeded that necessary to travel between plants. However,they assumed that herbivores are able to process food while moving betweenbrowse sites. If hares are unable to do this easily, then stem density may havea significant effect on forage intake rate of hares, particularly during the declinephase of the cycle. Foraging on stems of Picea in closed habitat may reduceoverall feeding time for hares and thereby reduce risk of predation. Thishypothesis needs further testing.Predictions 4, 5, and 6: Time of Season, Body Mass, and SexBody mass, time of season, and sex generally did not appear to influenceforaging behaviour within a given year. One explanation for this is thatdifferences in foraging strategies may not be detectable over the short periodthat hares were tracked on a single evening. It is also possible that changes inthese behaviours are not apparent at the population level. Nevertheless,differences in habitat use between each year were significantly correlated withbody mass in mid-April (Chapter 4). Hares did not show changes in habitat use81between early and late winter (Fig. 3.4), although there were differencesbetween years. In 1991 on CONTROL there were also differences betweenmales and females. Sex, body condition, and season are factors which, tovarying degrees, may influence anti-predator behaviours of snowshoe hares,despite equivocal evidence (Litvaitis 1990, 1991).Other experimental studies may provide some clues about where to lookfor these behaviours in snowshoe hares. Recently, Pettersson and Brön mark(1993) reported that crucian carp (Carassius carassius) spent less time in openhabitat when there was a predator present, and when not hungry. There was asignificant interaction between predation and hunger level. Abrahams and Dill(1989) have reported similar results with guppies (Poecilia reticulata). Saarikko(1992) observed that the response of shrews (Sorex araneus) to the presence ofa potential predator (weasel) was positively correlated with body mass. Underrisk of predation, large shrews could decease foraging activity (at the cost ofmass loss), but smaller individuals with lower energy reserves could not.Theoretically there are reasons to expect differences in the behaviour of animalsas their condition changes, or the time to reproduction approaches (Ludwig andRowe 1990; Houston et al. 1993; Clark 1994). There is clearly a need to findbetter indices of condition for hares (e.g. Boonstra and Singleton 1994), and formonitoring detailed individual behaviour in winter over a longer period.Sinclair and Arcese (1994) have suggested that predators affectwildebeest (Connochaetes taurinus) populations through food supply byinfluencing behaviour. They reported that the condition of predator-killedwildebeest was poorer than that of the general population, but better than innon-predator mortality, results which support the PSF hypothesis. Keith et a!.(1984) observed a similar relationship for snowshoe hares. Overall, there isconsiderable evidence that condition of animals influences foraging decisions82under risk of predation, but a great deal probably depends on the feasibility ofalternative foraging strategies. Hares appear to have few options.How Can Snowshoe Hares Minimize Risk of Predation?Previous studies have suggested that patterns of habitat use bysnowshoe hares in winter may be influenced by risk of predation (Wolff 1980,1981; Keith et al. 1984; Sievert and Keith 1985). Results of my study supportthese observations, and also suggest that hares have a limited ability to reduceexposure to predators. There are two main ways in which hares may be able tominimize predation risk: (1) increase use of safer closed habitat, and (2)decrease time spent foraging. Opportunities to shift to safer habitats are limited,in part because winter forage in closed habitat is less available than in openhabitats. Opportunities to decrease foraging effort or time are equally limited:hares are physiologically constrained by their poor ability to maintain reserves offat or protein (Whittaker and Thomas 1983). Hares also have no absoluterefuge from predators and are at risk in all habitat types (Table 2.3). Theevidence suggests that the alternative anti-predator behaviours available tohares result in reduced foraging effort or a shift to a poorer diet. In each casethis may lead to increased loss of body mass during winter. Indeed, if predatorsshow adaptive behaviour (Abrams 1989) and follow hares into closed habitat(see Chapter 2), the most reasonable option for hares may be to reduceforaging activity or move.At a broader evolutionary level, snowshoe hares appear to be welladapted to minimize risk of predation. Hares undergo a seasonal pelagechange from white in winter to brown in summer. In winter, white pelage hasbeen associated with both improved thermal insulation (Hart and Pohl 1965) and83predator avoidance (Grange 1932; Litvaitis 1991). Other factors which mightinfluence predator avoidance behaviours include bright moonlight (Gilbert andBoutin 1991), low temperature (Pease and Keith 1979; Keith 1990), and highwind (Bider 1961). I did not consider these factors explicitly, although they areprobably important at certain times, and hares do change their foragingbehaviour in response to environmental conditions (e.g. Gilbert and Boutin1991).The mechanisms by which hares detect predators are not wellunderstood, but I suspect that it is probably much easier for hares to detect thevarious faecal, urine, scent gland, and body odours of terrestrial predators, thanof avian predators. Jedrzejewski et aL (1993) have recently shown this to betrue for bank voles (Clethrionomys glareolus). Studies by Sullivan and hiscolleagues (Sullivan and Crump 1984, 1986; Sullivan et al. 1985) demonstratedthat some volatile methyl sulfide constituents of canid, feline, and mustelid urinesuppress feeding activity of snowshoe hares. They suggested that these odoursinduce a fear or avoidance response in hares.Perception of predation risk by individual prey is behaviourally complex,and predator avoidance behaviours may exist even in the absence of any overtpredator cues (Curio 1993). Dickman (1992) found that the survival of predator-experienced house mice (Mus domesticus) was 2.5 times higher than predator-naive mice, because predator-experienced mice used sites with greatervegetation cover. In a recent theoretical study, Bouskila and Blumstein (1992)showed that animals may overestimate predation risk if cues used to indicaterisk are inaccurate or diffuse. The use of conservative “rules of thumb” bysnowshoe hares to assess predation risk would tend to reduce foraging effort ina manner consistent with the observation that hares lose body mass aspredation risk increases, even though food is apparently available.84It is also possible that hares over-estimate risk of predation wheninformation about absolute predation risk is uncertain, or if hares are searchingfor both avian and terrestrial predators simultaneously. The presence of multiplepredators can theoretically increase vigilance of animals, and thereforedecrease time spent foraging (Lima 1992). Kotler et a!. (1992) have shown thatgerbils (Gerbillus spp.) are unable to forage and remain safe from snakes andowls simultaneously. Like hares, gerbils appear to have few options available toreduce risk of predation when several types of predators are present.CONCLUSIONSSnowshoe hares act to minimize risk of predation during the snowshoehare decline by reducing use of open habitats in favour of more closed habitatsas predation risk increases, but finer scale changes were not apparent in thisstudy. Distance to cover while foraging was not different from random in openand closed spruce habitat, and did not decrease as predation risk increased. Inopen shrub habitat hares traveled closer to cover than expected at random, butagain, this did not change between years. The evidence that hares reducedforaging effort (movements) as predation risk increased was inconclusive.There was a marked shift in diet to include more lower quality Picea twigs eventhough hares seem to lose mass on this diet. There also seemed to be nodifference in patterns of habitat use associated with body mass. Differencesbetween males and females, and early and late winter were apparent only onthe CONTROL grid in 1991. Females reduced use of open habitats, while malesincreased use of open habitats in late winter. Overall the results suggest thathares have limited options available to reduce risk of predation in winter. Sincehares have no absolute refuge from predators, increased use of more closed85habitat, decreased foraging effort, and selection of poorer quality browse leadsto loss of body mass. The consequences of this winter mass loss are discussedin the following chapter.86CHAPTER 4DOES RISK OF PREDATION INFLUENCE POPULATION DYNAMICS?EVIDENCE FROM THE CYCLIC DECLINE OF SNOWSHOE HARESINTRODUCTIONAnti-predator behaviour of prey in response to increased predation riskmay result in decreased fecundity or increased mortality caused by factors otherthan predation. The influence of short-term behavioural decisions by individualanimals (e.g. tradeoffs between maximizing foraging rate and minimizing risk ofpredation), on their longer-term survival and reproduction have been consideredin a number of models (McNamara and Houston 1987, 1990a; Mangel and Clark1988; Ludwig and Rowe 1990; McNamara 1990; Clark 1993, 1994), andempirical studies (Lima and Dill 1990; Peckarsky eta!. 1993). Individuals indanger of starvation may accept increased predation risk in order to obtainsufficient food. However, if predation risk is high and individuals have only afinite amount of energy available, investment in present reproduction may bereduced in order to increase future growth, reproductive capacity, or survival(Partridge and Harvey 1985; Sibly and Calow 1986).There is considerable interest in determining how predator avoidancebehaviours influence predator-prey population dynamics (Hassell and May 1985;Ives and Dobson 1987; McNamara and Houston 1987, 1990; Abrams 1989,1990, 1991, 1992a,b,c; Williamson 1993; FitzGibbon and Lazarus 1994).Several authors (Wolff 1980; Keith et a!. 1984; Smith et a!. 1988) havesuggested that predation risk may influence habitat use of snowshoe hares(Lepus americanus), but whether predation risk is a necessary component of the10-year population cycle has not been considered. There are several alternativehypotheses involving food, predation, and behaviour of hares to explain the 10-87year cycle in North America (Sinclair et al. 1988; Keith 1990; Krebs et a!. 1992;Royama 1992; Chapter 1). Recent experimental studies have suggested thatpredation alone may be sufficient to generate the hare population decline (Krebset a!. 1 986a,b), and that winter food is not absolutely limiting for hares at anytime during the cycle (Sinclair et a!. 1988, Smith et a!. 1988). Most hares die ofpredation (Boutin et al. 1986; Trostel et a!. 1987), although relative winter foodshortage may contribute to the hare decline (Pease et a!. 1979; Smith et a!.1988; Royama 1992). Summer food appears to be plentiful (Keith 1990; D. Hiket a!., unpublished data).Previous studies have observed a significant reduction in femalefecundity during the population decline and this demographic characteristic isclosely linked to the cyclic dynamics (Cary and Keith 1979). Reproduction iscorrelated with female body mass at the end of the previous winter (Keith andWindberg 1978; Keith 1990; Royama 1992). Body mass at the end of winter islowest during the population decline, and this reduction may result in smallerlitters. However, poor female condition does not appear to affect all litter groupsequally: the size of the first litter remains fairly constant, but the size ofsubsequent litters declines significantly.In the previous chapters I showed that predation risk is not constantduring the 10-year population cycle of snowshoe hares, and that changingpatterns of habitat use by hares are a behavioural response to minimizepredation risk. In this Chapter the effects of increased predation risk on survival,body mass, and fecundity during the decline phase of the 10-year cycle areconsidered. Results reported here are compared with those from earlier studiesof Lloyd Keith and his associates (see Keith 1990) and interpreted in light of theeffects of poor nutrition on the physiology of snowshoe hares (Whittaker andThomas 1983; Boonstra and Singleton 1993).88Hypotheses and PredictionsThe interaction between food and predation risk has several possibleoutcomes. In Figure 4.1 changes in condition (body mass) and survival duringwinter predicted under each of three hypotheses are outlined. The predictionsof these hypotheses were examined by manipulating food and predation risk onfour experimental hare-trapping grids at Kluane, Yukon, during a hare populationdecline (1 991-1 993).When food is readily available and predators are scarce (conditionscharacteristic of the hare increase and peak, 1989/90), body mass (condition)and survival of hares should be high (initial state (+,+) in Fig. 4.1). As predationrisk increases the food hypothesis (+,-) predicts that hares maintain body mass(maximized intake rate), but survive less well, relative to the initial state. Thepredator avoidance (PA) hypothesis (-,+) predicts that hares lose body mass,but still survive well (minimize predation). The predation-sensitive foraging(PSF) hypothesis (-,-) predicts that there is a tradeoff between foraging andpredation, such that predation risk restricts access to food. Both survival andcondition will decrease. Specific predictions of PSF (McNamara and Houston1987; Ludwig and Rowe 1990) are (I) increased predation risk leads todecreased body mass (hence fecundity), and (ii) decreased food levels lead toincreased mortality. Two further predictions that can be tested indirectly are, (iii)decreased food will have the greatest effect on condition when predation risk ishighest, and (iv) increased predation risk will have the greatest effect onmortality when food level is lowest.89Fig 4.1. Predicted changes in condition (body mass) and winter survival (- =low, + = high), under two levels of predation risk and food availability. Thearrows indicate the direction of change which supports each hypothesis: food,predator avoidance (PA), or predation sensitive foraging (PSF).90FOODHIGH LOWcondition +FOOD PSFHIGHsurvival-RISK Icondition + -PALOWsurvival +INALSTATE91METHODSThis study area is described in Chapter 2. Experiments were conductedon four 34-ha trapping grids between January and May of 1989-1993. Sulphurgrid was an unmanipulated CONTROL; Beaver Pond (FENCE) was surroundedby an electric fence to deter terrestrial predators (lynx, Lynx L canadénsis, andcoyote, Canis latrans); Hungry Lake (FENCE+FOOD) was surrounded by afence, and provisioned weekly with pelleted rabbit chow (16% crude protein).Avian predators (mainly Great Horned Owl, Bubo virginianus, and NorthernGoshawk, Accipiter gentilis) had unrestricted access to both fenced grids.Gravel Pit (FOOD) was provisioned weekly with pelleted rabbit chow, butpredators had free access to this site. Peak hare densities on CONTROL werereached in 1989 and 1990 (Chapter 2), while peak densities were observed oneyear later on the other three trapping grids.Snowshoe hares were live-trapped at monthly or bimonthly intervalsbetween January and May as described in Chapter 2. Body mass wasdetermined at each capture, but only mass recorded at the first capture during amulti-day trapping session is used in this analysis. The deaths of radio-collaredhares were used to calculate over-winter survival from the Kaplan-Meierestimator (Pollock 1 989a,b), as described in Chapter 2. Female mass in earlyApril and 30-day survival (January to April) in 1990 were compared tocorresponding values in each year of the decline (1991-1993), and significantdifferences are reported in Table 4.2.Mean size of each litter was determined from pregnant females placed inmaternity cages 2-3 days prior to parturition (see O’Donoghue and Krebs 1992for description of methods), on CONTROL grid and adjacent areas (1 989-92),FOOD (1989/90) and FENCE+FOOD (1 991/92) grids (O’Donoghue and Krebs921992; Sovell 1993; C.J. Krebs eta!., unpublished data). I assumed thatreproduction on FENCE+FOOD was similar to that on FOOD in 1989 and 1990.Reproductive output was not measured on FENCE or FOOD during the decline.RESULTSWinter Su,vivalEstimates of 30-day survival in winter (January to April) were highest onFENCE, FOOD, and FENCE+FOOD grids in 1989 and 1990, and weresomewhat lower on CONTROL, particularly in 1989 (Fig. 4.2). In 1991, the firstyear of the decline, survival was highest on FENCE+FOOD (0.92), followed byFOOD (0.86), FENCE (0.76), and then CONTROL (0.64). In 1992 survival onFOOD and CONTROL was lower than on FENCE and FENCE+FOOD. In 1993,survival on FENCE+FOOD decreased significantly, but was similar to the othertreatments (about 0.8).Body MassFemale hares generally maintained body mass throughout the winter andthen increased rapidly in mass following conception in mid-April (Fig. 4.3),except on CONTROL after 1990, and FOOD after 1991. On CONTROL, femalehares were significantly lighter in each winter during the decline than at thepeak, and weighed less than 1400 g at the end of winter in 1991, 1992, and1993. On FENCE grid, body mass did not decline, and values were consistently93Fig. 4.2 Winter (January to April) 30-day survival (± 95% C.L.) of hares onCONTROL, FENCE, FOOD, and FENCE+FOOD, 1989-1993. The number ofradio-collared hares monitored during each sampling period is indicated for eachsample.1.0MEAN30-DAYSURVIVAL(JAN-APRIL)0.9 0.7 0.60.5CD0.419891990199119921993YEAR95Fig. 4.3 Mean body mass of female hares during the period January to May1989-1993 on CONTROL, FENCE, FOOD, and FENCE+FOOD. Solid line joinsestimates of mean mass in early April. Sample size for each mean value variedfrom 2 to 130 individuals depending on the year, and ±1 S.E. is less than thesize of the symbol unless otherwise indicated. Dotted line at 1400 g is areference for comparison between treatments.C66166[[661.0661.•696[c66[66[166[066[6961OOLLOOLOOgL‘OOPL009L009LCOIL‘0091•006L.0O..++.4C00i66[66[COOd-’-33N3J[6610661.6961.66[661[661.0661.6961.+OOLL0OL009LOOPLOOQL00910011009L006L00&OOLL00L009LCOPI009L0091OOLL00910061,0OO•OOL.0091COPL009L0091COIL0091006133N31tVV7••:1OI1NOD97between 1500-1 600 g. On FENCE+FOOD body mass was about 1600 g in allyears. On FOOD, body mass was similar to that on CONTROL during the peak.During the decline body mass remained high, but decreased to about 1350 g in1993.Reproductive Output of Female HaresMean litter sizes (Table 4.1) showed that hares on CONTROL andadjacent unmanipulated areas were much less fecund during the decline thanon FENCE+FOOD. These values are not adjusted for stillborn rates whichranged from 0 to 45% and were highest for third litters (mean 15%;O’Donoghue and Krebs 1992). On CONTROL, the size of the first litter wassimilar in all four years in 1989 and 1990, but no third litter was produced in1991. In 1992 neither second nor third litters were produced. This reduction inreproductive effort on the CONTROL areas suggests that body mass of lessthan 1400 g at the end of winter may contribute to reduced female fecundity.DISCUSSIONEvidence Supports the PSF HypothesisThe observed changes in winter survival (Fig. 4.2) and April body mass(Fig. 4.3) during the hare decline, relative to the population peak, are comparedwith predictions of the food, predator avoidance (PA), and predation sensitiveforaging (PSF) hypotheses in Table 4.2. On CONTROL, the reduction incondition and survival during the hare decline supports the PSF hypothesis. In1993, survival improved while body mass continued to decline, a result98Table 4.1 Mean litter size (± S.D. (sample size)) of hares at Kluane, Yukon onCONTROL and FENCE+FOOD (or FOOD in 1989/90) grids, during thepopulation peak and decline. Data for 1989 and 1990 from O’Donoghue andKrebs (1992). Data from 1991 and 1992 from C.J. Krebs et a!. (unpublisheddata) and Sovell (1993).CONTROLLitterYear First Second Third1989 3.6± 0.7 (8) 5.9± 1.6 (8) 4.2± 0.4 (5)1990 3.9± 0.9 (7) 5.7± 1.4 (14) 4.1± 1.6 (12)1991 3.9± 0.7 (8) 3.9± 1.4 (10) 01992 3.3± 0.5 (4) 0 0FENCE+FOODLitterYear First Second Third1989 3.8±1.2(9) 5.6±1.7(9) 4.6± 1.1 (9)1990 3.8± 0.7 (15) 5.5± 2.2 (11) 5.8± 1.2 (10)1991 7.8± 1.3 (9) 4.7± 2.3 (6)1992 4.2± 1.1 (13) 7.0± 0.9 (18) 5.9± 1.7 (19)99Table 4.2 Observed changes in body mass and survival (+ = high; conditionsduring the peak; - = low; significant decline from peak conditions, P <0.05) onCONTROL, FENCE, FOOD, and FENCE+FOOD grids during the snowshoehare decline (1991-1993), relative to the peak years (1989/90). The hypothesissupported on each grid is indicated as FOOD (food hypothesis), PA (predatoravoidance hypothesis), and PSF (predation-sensitive foraging hypothesis).Treatment Year Condition Survival Hypothesis(body mass) SupportedCONTROL 1989 + +1990 + +1991 - PSF1992 - PSF1993 + PAFENCE 1989 + +1990 + +1991 + - FOOD1992 + - FOOD1993 + - FOODFOOD 1989 + +1990 + +1991 + - FOOD1992 - - PSF1993 - PSFFENCE+FOOD 1989 + +1990 + +1991 + +1992 + +1993 + - FOOD100consistent with the PA hypothesis. On FOOD, the results support the PSFhypothesis, suggesting that predation risk restricted access to food in thesecond and third year of the population decline. Survival did increase in 1993,even though mass declined, suggesting that hares were minimizing risk eventhough ad lib supplement food was available.On FENCE and FENCE+FOOD, body mass remained high even thoughsurvival decreased during the decline. These results support the foodhypothesis. Predation may have increased inside the fences because avianpredators were more active there following the hare decline outside of thefences (Chapter 2). Overall, the results indicate that in the absence of terrestrialpredators hares are able to maintain body mass. If avian predators are moredifficult to detect than mammalian predators (see Jedrzejewski et a!. 1993),hares may still use open habitat inside the fences. In this case, body mass willremain high, but survival will decrease.A comparison of all four treatments supports the third and fourthpredictions of the PSF hypothesis. Where predators were not controlled, lowerfood level led to decreased condition on CONTROL compared with that onFOOD. Similarly, condition was lower on FENCE compared with that onFENCE+FOOD. Higher predation risk on CONTROL also resulted in lowersurvival compared to FOOD (higher food), at least during the first two years ofthe decline. Differences in hare densities among the treatments may have hadsome influence on the results, but I think that these effects were small. Forexample, I would predict that higher density would result in lower survival andpoorer condition because of competition among hares for food or space (Sinclair1986; Ferron 1993), and the observed results are in the opposite direction.The results also indicate a strong correlation between body mass andfemale reproduction, a result consistent with those of Cary and Keith (1979). In1011991 and 1992, body mass and female reproduction declined on CONTROLeven though food was apparently not limiting (Chapter 2). The relationshipbetween total mean reproductive output and mean female body mass (1989-1992) in mid-March (r2=0.53, N=4, P=0.17), and early May (r2=0.71, N=4,P0.10), was not significant, but the trend was stronger late in the season. Insummary, body mass at the end of winter appears to have the largest effect onreproduction (Keith 1990; Royama 1992).Why do Body Mass and Reproduction Decline?The body mass of hares on CONTROL decreased during the populationdecline, even though sufficient forage appeared to be available. It is possiblethat forage availability and quality was overestimated and therefore food mayhave been limited, but this is unlikely (Chapter 2). The observed increase in theproportion of Picea browse in the diet (Chapter 3) may account in part forobserved declines in body mass (Fig. 4.1); captive hares were unable tomaintain mass on a diet of Picea twigs, and could just maintain mass on a diet ofSalix twigs (Rogers and Sinclair 1994). Hares may also lose mass during thedecline if foraging efficiency is lower as the spatial patchiness of browseincreases (Table 2.1).Alternatively, increased risk of predation may have contributed to thedecline in body mass on CONTROL (and FOOD) by restricting access to foodresources. If animals accept a certain probability of predation in order to obtainfood, outright starvation may be uncommon, but effects of food availability onsurvival, body condition, and reproduction are potentially large (McNamara andHouston 1987). At peak densities, snowshoe hares utilized a significantlygreater proportion of open habitat than expected by chance, a result consistent102with the food hypothesis (Chapter 3). However, as risk of predation increasedduring the cyclic population decline, hares increased their use of more closedhabitats where forage was less available, and foraging rates may be lower. Thisswitch in habitat is consistent with the predictions of the PSF hypothesis. OnCONTROL there was a negative linear relationship between the proportion ofclosed habitat used by female hares and total reproductive output between 1990and 1992 (r=0.98, N=3, P=0.066). The results from the FENCE+FOODtreatment show that hares did not increase use of safer habitat until 1992, andthat provisioning with supplemental rabbit chow prevented a decline of bodymass, survival, and fecundity.Higher body mass was also observed on FOOD during the first year ofthe population decline. This result suggests that provisioning with supplementalfood may allow hares to spend less time spent foraging away from cover. OnFENCE body mass did not decline, suggesting that lower risk of predation maypermit hares to forage more in open habitats.Reduction of predation risk seems to be a necessary factor for hares tomaintain high reproductive output during the cyclic decline. Krebs et aL (1 986b)found that extra natural food supplied on a control area during the populationdecline prevented loss of body mass, but did not increase survival. It seems thateven if hares have access to abundant forage, stress associated with higherpredation risk may lead to reduced reproduction. Desy et a!. (1990) found thatthe presence of predators limited access of prairie voles (Microtus ochrogaste,)to food supplies and resulted in decreased body condition and slower rates ofmaturation.Keith and Windberg (1978) and Cary and Keith (1979) showed thatfemale body weight changes during the winter are correlated with litter size andpregnancy rate in summer. When over-winter loss of body mass is high,103fecundity is low. Reproduction remained low for at least three years followingthe hare peak. Their interpretation of these results is that poor winter nutritionduring the decline caused the reproductive decline. However, this does notovercome the problem of why this reproductive decline continues even whenfood increases in late summer. While I agree in general that poor nutritioncontributes to reproductive loss, I suggest that predation risk restricts access tofood resources and so causes physiological stress associated with poorcondition. This results in suppression of hare reproduction over a long period.The results of the experiments reported here are consistent with this hypothesis.Behavioural interactions between hares may also play a role indetermining condition in summer, but given that poor condition is evident whenpopulation density is declining, I think this is unlikely. Even when hares were ingood condition at the population peak, O’Donoghue and Krebs (1992) observedthe highest rate of stillborn young in third litters. They suggested that the costsassociated with nursing two previous litters may contribute to the high loss.Reproductive Costs of Predation RiskMany studies have shown that mating activity increases predation risk(Ryan 1985; Magnhagen 1991). For example, Cushing (1985) found thatestrous female prairie deer mice (Peromyscus maniculatus bairdi) were morevulnerable to predation by weasels (Mustela nivalis) than were diestrous mice.These results indicate increased risk of predation associated with a female’sattempt to reproduce, and are of considerable evolutionary significance(Magnhagen 1991).Increased predation risk has also been shown to reduce reproductiveeffort. Sih eta!. (1990) showed that food deprivation had no effect on the mating104behaviour of water striders (Gerris remigis); however, predation risk decreasedthe number of matings by about 50%. Ylönen et a!. (1992) found that the odourof small mustelids (M. nivalis and M. erminea) delayed sexual maturation ofyoung voles (Clethrionomys spp.) and suppressed female reproduction underlaboratory conditions. They also reported that female red-backed voles exposedto predator odour at the beginning of pregnancy had foetuses which were about25% lighter than those of control females, suggesting that stress associated withhigh predation risk may influence the survival of offspring. These resultssuggest that the consequences of poor condition in one breeding season maycarry over to the next generation. Korpimâki et a!. (1994) recently conducted afield experiment where reproduction of voles was measured at different weaseldensities. Their results suggest that the presence or scent of small mustelidsdecreases the reproductive rate of voles.The mechanisms by which increased predation risk may lead todecreased reproduction have not been studied in detail. Bronson (1984) foundthat if access to food was limited (a common cause of elevated stress),reproduction in female house mice was adversely affected. These results arenot unexpected because, in general, ovulation in mammals is regulatedindirectly by female energy reserves (Bronson and Manning 1991). Bronson(1984) also reported that if the amount of food given to a weanling female wasrestricted, her subsequent reproductive development was inhibited. Mech et aL(1991) showed that the mass and survival of white-tailed deer (Odocoileusvirginianus) fawns was directly related to maternal nutrition during gestation.Similarly, studies by Albon et a!. (1987) suggested that poor maternal conditionin red deer (Genius elaphus) may have permanent repercussions for theiroffspring.105Predation Risk, Stress, and Population CyclesChristian (1980) reviewed the evidence that the environment of cyclicspecies at peak densities may have long-term negative consequences ondemography through impaired reproduction mediated by endocrine responses toelevated stress. Boonstra and Boag (1992) supported one of Christian’spredictions in a field population of meadow voles (Microtus pennsylvanicus) byshowing that stress responses were positively correlated with population density.Although their high density vole population showed a low rate of populationdecline, they suggested that there were long-term consequences for young frombeing exposed to high free-corticosteroid levels at the peak. Under laboratoryconditions, Mihok and Boonstra (1992) showed that the prior experience ofdecline-phase female meadow voles had long-term detrimental consequencesfor the performance of the next two generations. While the mechanism leadingto increased stress in wild populations may vary (Chitty 1987), laboratory studieshave shown that a variety of pre- and post-natal stresses can have long-lastingeffects, and impair reproductive performance for one or two generations (Pollard1986; Boonstra 1994).Reduced fecundity of snowshoe hares during the population decline isapparently not due to food being absolutely limiting, but to poor condition andelevated stress associated with foraging under high risk of predation. Recentexperiments to examine the ability of snowshoe hares to recover from short-termstress in winter (Boonstra and Singleton 1993), suggested that the pituitaryadrenocortical feedback system in hares from a declining population wasoperating normally, but that higher levels of free-cortisol were present in hares inpoorer condition. In 1992 when CONTROL hares were in even poorer condition,the deleterious effects of short-term stress were even more pronounced106(Boonstra and Hik, unpublished data). The cumulative effects of this higherstress (chronic exposure to free-cortisol) may lead to reduced survival orreproduction. The conditions to which hares are exposed during the populationdecline may have long-term population consequences.Establishing the importance of predation risk on the population dynamicsof hares should be a major focus of future research efforts. The predictions ofthe PSF hypothesis, some of which are supported by this study, can be directlytested in four ways. First, female reproduction should decrease on FOOD butnot on FENCE. Second, other indicators of stress (i.e. free-cortisol levels;Boonstra and Singleton 1993), should be lower on FENCE than on FOOD.Third, female reproduction should remain low on CONTROL and FOOD for atleast one year following the decline in predator numbers (and hence predationrisk). This could be tested by monitoring reproduction of FOOD or CONTROLfemales inside one of the fenced treatment areas.Finally, it is not clear why females are unable to use abundant, highquality summer food to improve their condition during the summer to increasereproduction. The absence of second and third litters suggests that chronicstress associated with poor winter condition mediated by predation risk may limitreproductive output. If this is true, then providing high quality food to hares insummer will not increase reproduction in that season. Whittaker and Thomas(1983) showed that the total number of days of potential metabolic supportderived from neutral lipid and protein reserves of hares was significantly higherin summer than winter (6.0 days compared with 3.8 days, respectively), butmuch of this energy may be used for lactation (O’Donoghue and Krebs 1992).In addition, the hares Whittaker and Thomas studied were collected during apopulation peak. During a population decline summer energy reserves may be107less. The allocation of variable resources to reproduction and other activities(i.e. Reznick and Yang 1993), has not been investigated in hares.CONCLUSIONSThese experiments show that snowshoe hares trade-off body mass andsurvival during the population decline. Anti-predator behaviours in response toincreased predation risk may result in reduced body mass and reproduction ofhares. In the absence of terrestrial predators, hares behaved in a mannerconsistent with the predictions of the food hypothesis: body mass wasmaintained at the expense of lower survival. There appears to be a direct linkbetween female body mass at the end of winter and subsequent reproduction.There is a suggestion that conditions of high predation risk during the declinephase have permanent detrimental effects on ability of hares to recover from‘stress’. Hares may not be able to maintain physiological homeostasis in theface of environmental stress (higher predation risk), because of a deteriorationin the endocrine feedback system. This may lead to a delay in the recovery ofpopulations from low numbers if reproduction and offspring fitness are affected.Several ways to test this hypothesis using the ongoing experimentalmanipulations at Kluane are suggested.108CHAPTER 5POPULATION CYCLES, PREDATION RISK, ANDTHE GHOST OF PREDATORS PASTIn this concluding chapter, I describe the major factors thought toinfluence population cycles of small mammals. In particular, I examine thepotential for sublethal effects of predation to influence snowshoe hare populationdynamics, and I reconsider evidence supporting a variation of the stresshypothesis (Christian 1950, 1980). Finally, I summarize the main results of thisthesis and the potential role of predation risk in shaping snowshoe harebehaviour and population dynamics.What Causes Population Cycles?Periodic, multi-annual fluctuations (cycles) in abundance arecharacteristic of a number of species, including some voles, lemmings,snowshoe hares, and their predators (Elton 1924; Krebs and Myers 1974;Finerty 1980; Keith 1990; Batzli 1992; Krebs 1993;). Demographic changesassociated with population declines have been explained by food limitation(Keith 1974), predation (Hanski etal. 1991; Krebs etal. 1992; Korpimâki 1993),changes in spacing behaviour (Chitty 1967; Krebs 1978), or a variety of ‘multi-factor’ interactions (Lidicker 1988; Batzli 1992). No common cause for thesecycles has been discovered so far.A major enigma of these cycles is the failure of low density populations toincrease more quickly. There is a characteristic extended low-phase which maypersist for one generation or more after food has increased and predators havedeclined. In all populations, the decline and low phase are characterized by*see Connell (1980) for more ghosts.109poor juvenile survival and growth, and the length of the breeding season mayalso be shortened.FoodFood was considered to be the cause of density-dependent populationregulation in 5 of 21 small mammal populations reviewed by Sinclair (1989).However, food shortage does not appear to be necessary to explain the declineof cyclic populations. For example, attempts to stop the snowshoe hare declineby adding supplemental food have been unsuccessful (Krebs et a!. 1 986a,b;Krebs et a!., unpublished data). Indeed, of nine studies that have attempted toprevent population declines of fluctuating populations by adding supplementalfood (Boutin 1990), only one succeeded, and it was conducted in a predator-freeenvironment (Ford and Pitelka 1984).PredationSome authors have suggested that predation may be sufficient to explaincycles of microtine rodents (Erlinge et a!. 1984; Hansson and Hettonen 1988;Korpimaki 1993), and snowshoe hares (Trostel et al. 1987). Some of theseinterpretations have been criticized on the basis that delayed density-dependentpredation may be destabilizing (Kidd and Lewis 1987), but there is considerableevidence that predation alone is sufficient to generate cycles (Boutin 1994).Nevertheless, some microtine populations have declined in the absence ofpredators (Chitty 1967; Taitt and Krebs 1985; Krebs 1993; Lambin and Krebs1991a,b; Boonstra 1994).110Spacing BehaviourChitty (1967, 1987), and others, have argued that predators cannotaccount for decreases in body mass and reproductive output characteristic oflow density populations. Rather, changes in the spacing behaviour anddispersal of individuals are necessary to cause cyclic fluctuations of smallmammals (Krebs 1985; Taitt and Krebs 1985; Lambin and Krebs 1991a).Spacing may affect aggression, the number of individuals gaining breedingstatus, and dispersal. In all of these cases, a decrease in resource (food)availability to resident females may result, leading to reduced juvenile survivaland recruitment. In 14 of 21 studies of small mammal populations reviewed bySinclair (1989), spacing behaviour was thought to be the cause of density-dependent population regulation.There are a number of explanations for the role of spacing behaviour ingenerating cyclic fluctuations, including interactions with food supplies andchanges in the behaviour or genetic structure of these populations. There isevidence for changes in social mortality correlated with population density(Krebs 1985) that may explain some cycles. However, attempts to isolate agenetic-polymorphism responsible for cyclic fluctuations have generally beenunsuccessful (Chitty 1987; Boonstra and Boag 1987).In lemmings, social interactions leading to mortality may be responsiblefor the population decline, and may also explain observed decreases inreproduction and juvenile survival (Krebs 1993). Crowding may reduce therelative availability of cover in a territorial system that is saturated at highdensity. However, predation may also play an important role in regulatinglemming populations (Krebs 1993). Reid et a!. (1993) reported that whenpopulations of collared lemmings (Dicrostonyx torquatus) were protected from111predation, survival of litters to weaning and adult survival were significantlyenhanced. However, juveniles were not recruited into the population becausethey dispersed outside of the protected areas. The relative roles of predation,territoriality, and social spacing in regulating these populations is unknown.Multi-factor ExplanationsSince no single factor appears to be sufficient to explain populationcycles, a number of authors have proposed multi-factor explanations (Hestbeck1987; Lidicker 1988; Batzli 1992). Hestbeck (1987) argued that populationdensities can be regulated by predation, emigration, resource depletion, andbehavioral or physiological collapse. He suggested that each of thesemechanisms dominates the regulation process over a range of densities. Batzli(1992) has emphasized the importance of predation in a multi-factor hypothesisfor vole and lemming cycles. According to this view, populations expandexponentially when food is available and predators are at low density. Aspopulations increase, food becomes scarcer and predators increase. Thesefactors lead to poor juvenile survival. Recovery from low densities is delayed byinversely density-dependent predation, slow recovery of the food supply, andpossibly maternal effects. Desy and Batzli (1989) and Desy et al. (1990) haveused such an approach to study population regulation of prairie voles.Keith and his colleagues (Keith 1974; Keith and Windberg 1978; Vaughanand Keith 1981) originally argued that the demography of snowshoe harepopulations was primarily a delayed density-dependent nutritional problem.They suggested that food shortage at high or low density resulted in increasedover-winter weight loss, decreased over-winter survival, decreased reproduction,and decreased growth rates. However, evidence that hares actually run short of112food at any time during the cycle is equivocal (Keith et a!. 1984; Smith et a!.1988; Chapter 2). Keith et al. (1984) and Keith (1990) later emphasized theimportance of predation in hare declines: “over-winter food shortage was stillbelieved to trigger the decline, but with starvation deaths predominating over ashorter period and malnutrition markedly increasing hare vulnerability topredators. Such predation was further amplified by severe cold.” (Keith 1990, p.177). Recent studies have also recognized the importance of predation risk onhabitat use by hares (Wolff 1980; Keith et a!. 1984; Sievert and Keith 1985;Smith eta!. 1988). Relative food shortage at high hare numbers may facilitatethe deaths of hares from predation. Furthermore, the consequences of greaterpredation risk on the behaviour and endocrine physiology of hares may providea mechanism to explain the lag in recovery of populations.The Stress Hypothesis RevisitedAs mentioned previously, spacing behaviour or intraspecific competitionfor space has long been recognized as a possible regulatory factor of smallmammal population cycles (Krebs 1985). Chitty (1952) suggested that thecause of the population decline of Microtus agrestis at Lake Vyrnwy (1936-1939)was increased intraspecific aggression, possibly leading to higher physiologicalstress. Juveniles born at the population peak had lower survival and lowerfertility, and were in poor condition. Mechanisms that could account for maternaleffects were poorly understood at the time, but physiological endocrineresponses (stress) were recognized as being potentially important in regulatinganimal populations (Calhoun 1949; Christian 1950). This early stress hypothesisproposed that intraspecific interactions at high density lead to phenotypicphysiological changes that reduce births and increase deaths.113The endocrine stress hypothesis of Christian was abandoned by Chitty(Chitty and Phipps 1966) because it did not explain the sudden decline ofseemingly healthy individuals. Subsequent studies tested the polymorphicbehaviour hypothesis (Chitty 1958, 1967), which postulates that individualdifferences in spacing behaviour have a genetic basis and respond to naturalselection. Yet, despite many attempts to demonstrate a genetic basis forpopulation fluctuations (see Krebs and Myers 1974; Chitty 1987; Spears andClarke 1988), this hypothesis has not been widely supported (Boonstra andBoag 1987). Recent evidence supports a version of the original stresshypothesis (Christian 1980, Boonstra and Boag 1992, Mihok and Boonstra 1992,Boonstra and Singleton 1993). Chilly (1993) also suggests that intergenerational maternal effects, of the type described below, have the potential toprovide a common explanation for vole and snowshoe hare cycles.Nevertheless, some of the evidence supporting the genetic polymorphicbehaviour hypothesis cannot be explained in any other way at present. Thepossibility that there is selection for different behavioural or physiologicalcharacters during population declines should not be abandoned (Pollard 1986).Interactions between individuals may cause population changes byaltering the ability of animals to cope with increased environmental stressassociated with high density. One of the early explanations for the cyclic declineof snowshoe hares was a physiological condition known as ‘shock disease’(Green and Larson 1938), characterized by low levels of blood glucose and liverglycogen. It was suggested that overcrowding of hares at high density mayresult in strong maternal effects (referred to as “physiological derangementsderived in utero”) leading to reduced viability of generations born during thepopulation peak (Chitty 1952). However, this sort of stress was usually114observed only when hares were being trapped, handled, or crowded artificially(Chilly 1959), suggesting that physiological stress was rare in wild populations.The hypothalamo-pituitary-adrenocortical feedback system plays a centralrole in allowing animals to adapt to environmental challenges, or stress (Muncket al. 1984). Increased stress (i.e. poor nutrition, high risk of predation) mayreduce the ability of this feedback system to respond. Adrenal glucocorticoidsplay a crucial role by shunting energy to muscles and away from other tissues,and in allowing animals to return to homeostasis following elevated stress.However, chronic exposure to glucocorticoids has deleterious consequencessuch as steroid diabetes, fatigue, infertility, inhibition of growth, and impairedresistance to disease (Munck et a!. 1984; Boonstra 1994). In the case of thebrown antechinus (Antechinus stuartil), stress induced by aggressiveinteractions at the time of mating resulted in a tripling of plasma freecorticosteriod concentration, which led to total post-mating male mortality(Bradley et a!. 1980). This is an extreme example, but demonstrates thepossible role of increased adrenocortical activity for population regulation.The weight of adrenal glands provides a rough index of adrenocorticalhypertrophy and cortical hormone production. Studies of snowshoe hares atRochester, Alberta, found that mean adrenal weights were not significantlyrelated to population density or levels of nutrition (Keith 1990). Feist (1980) alsoreported no difference in adrenal stress response in decline-phase populations.These studies suggested that hares showed no significant stress response as aresult of high density. Recently, Boonstra and Singleton (1993) and Boonstraand Hik (unpublished data), have used radio-immunoassay techniques tomeasure hormone levels in field populations of hares during a populationdecline, from a control area and an area protected from terrestrial predatorswhere rabbit chow was provided. Their results indicate that although the115pituitary-adrenocortical feedback system seems to be operating normally, haresin poorer condition (control areas) have higher levels of free cortisol. Chronicexposure to high levels of free cortisol may have long-term effects on thebehaviour, growth, and reproductive performance of hares born to stressedmothers (see Pollard 1986).Maternal effects refer to the influence of environmental conditionsexperienced by mothers on the growth, survival, and fitness of offspring. Theimportance of maternal effects in regulating populations has recently beenconsidered for insect (Rossiter 1991; Peckarsky et al. 1993) and mammal (Mecheta!. 1991; Mihok and Boonstra 1992) populations. Albon eta!. (1987) andMech etal. (1991) have suggested that poor maternal condition has negativeconsequences for offspring fitness in wild deer populations.Is a one-generation lag in reproduction generated by maternal conditionsufficient to account for population cycles? May (1974, 1976) used a singlespecies model to predict that a 2-3 year lag-time for population recovery of harepopulations could generate the observed 8 to 11 year cycle. Possibly, maternaleffects lasting one generation may be sufficient to explain snowshoe harepopulation cycles. This potential reproductive lag complements the delayeddensity-dependent predation response suggested by Trostel eta!. (1987).Similarly, a lag of 9-12 months could generate microtine cycles of 3 to 4 years.Boonstra (1994) has suggested that such a lag could be generated by densitydependent inhibition of maturation in peak years of microtine population densityto produce time lags of the correct magnitude.One significant advance in our understanding of hare populationdynamics over the last forty years, and one of the most important behaviouraldifferences between hares and microtine rodents, is that spacing behaviour byitself appears to be relatively unimportant in regulating hare populations (Boutin1161980, 1984a; Krebs 1986). Although adult hares show dominance hierarchies(Graf 1985), and adult residents may exclude immigrant juveniles (Boutin1 984a), they generally do not generally compete for space, unless food islimiting (Sinclair 1986; Ferron 1993). Thus, social interactions betweenindividual hares may be less important than other types of environmental stress,such as risk of predation.Summary of the Main Results of this ThesisPredation seems to be the proximate cause of mortality of snowshoehares and may be sufficient to generate the population decline. In this thesis Iargue that sublethal effects associated with predation risk are the first step in acascade of behavioural and physiological responses leading to a further declineduring the low-phase of the cycle. The sensitivity of snowshoe hares toincreased risk of predation during the cyclic population decline leads to changesin foraging behaviour which result in poor condition and lower reproductiveoutput. Poor female condition during the cyclic population decline may alsoaffect the fitness of juveniles, resulting in a one- or two-generation lag inrecovery of the population. This may explain why the low period of the 10-yearcycle persists when predators are scarce and food is abundant.The main elements of the predation risk hypothesis are shown in Fig. 5.1.During the hare population decline (a) there is an increase in the predator-tohare ratio, and therefore risk of predation (b). Survival of hares declines in theearly decline (c). However, available forage increases during this period (d),and there is no evidence that hares are absolutely food limited. During thisdecline period female body mass (e) and reproduction (f) are reduced, eventhough per-capita food availability is increasing. However, there is a notable117Fig. 5.1 Summary of main results for CONTROL which support the predationrisk hypothesis. (a) hare density (#/ha); (b) predator-prey ratio of terrestrial andavian predators; (c) survival of hares during January-April period based onradio-telemetry; (d) SaIix forage availability per hare at the end of winter(kg/hare), and 5-mm stems of Salix, Picea and Betula browse available in midMarch; (e) body mass of female hares in mid-April; (f) total reproductive outputof female hares; (g) habitat use by female hares during late winter.(a)HAREDENSflY(NO./HA)Cc)MEAN 30-DAYSURVIVAL(JAN - MAY)(d)SALIX FORAGEAVAILABLE ATEND OF WINTER(I(G/HARE) ()Ce)FEMALEBODY MASSIN MID-APRIL(g)118504030 BROWSEAVAILABLE INMID-MARCH(KG/HARE/DAY)100(f)TOTALREPRODUCTIVEOUTPUT(YOUNG/YEAR)(g)LATE-WINTERHABITATUSE (%)(b)PREDATORHARE RAT1O119shift in patterns of winter habitat use by hares (g): hares increase the proportionof closed habitats used. In general hares appear to have few behaviouraloptions available to reduce predation risk. Observations indicate that the qualityof the diet and proportion of time spent foraging may also decline (Chapter 3).These changes in foraging behaviour contribute to poor condition.These observations support the predation risk hypothesis, which is amixture of the four hypotheses of the snowshoe cycle summarized in Chapter 1.There is little evidence that winter food resources are depleted near thepopulation peak. However, relative food shortage appears to lead to poor harenutrition, lower body mass, reduced fecundity, and increased susceptibility topredation. The evidence from Kluane suggests that predators alone aresufficient to initiate the hare decline (Boutin 1994) and drive hare numbersdown. However, hares are in poorest condition 2 or 3 years after the populationpeak, when food is abundant (Chapter 4). Therefore, there appears to be asynergistic interaction between food and predation, but I suspect it operates inthe opposite order to that originally predicted by Keith (1974): predation causesthe initial decline, and then predation-sensitive foraging leads to poor conditionand higher rates of loss.Changes in plant quality (nutrients or defences) do not appear to causethe decline. However, differences in the chemistry of forage twigs may help toexplain why hares lose body mass during this time. The increase in Piceaforage used by hares during the decline may be an important cause of poorcondition at this time.The polymorphic behaviour hypothesis is also relevant. There may notbe a genetic polymorphism responsible for differences in body mass andreproductive output of low-phase hare populations, but there is a suggestion ofphysiological differences between high-phase and low-phase animals. During120the decline, females are exposed to high predation risk, which may result inreduced access to food. This leads to poor condition at the end of winter andmay leave an indelible physiological imprint leading to lower fitness (Boonstraand Singleton 1993). These effects are phenotypic in origin, but may result instrong maternal effects that are passed to the next generation. Predation alonecannot explain why hares suffer a reproductive decline, and why the low-phaseof the cycle persists for as long as it does. Further modelling and field studiesare needed to test the idea that predation is the factor which initiates a cascadeof sublethal effects, mediated by predation-sensitive foraging, which result in aphysiological collapse of the population and lag in the cycle.This result has been anticipated by, and builds on the pioneering studiesof Green and Evans (1940), and the extensive experimental work of Lloyd Keithand his colleagues at Rochester, Alberta (see Keith 1990). Further work byCharles Krebs and his colleagues at Kluane, Yukon (Krebs et a!. 1992) hasrefined these hypotheses of population regulation. Other factors, such asweather, may modify the amplitude and period of the cycle (Finerty 1980;Sinclair et al. 1993). The behavioural and physiological consequences ofelevated predation risk at the cyclic peak provide a potential mechanism for theobserved lag in the recovery of these populations.Predator Avoidance Behaviour and Population DynamicsWhere predation is implicated in the regulation of prey populations, antipredator behaviour will probably play a role in the process. The cumulativeeffects of predation and starvation determine the state of animals, andtheoretical work suggests that predation and starvation interact to causepopulation declines (McNamara and Houston 1987, 1990; Houston eta!. 1993).121The framework for exploring this problem of a trade-off between gaining energyand avoiding predation has developed rapidly in recent years (Ludwig and Rowe1990; Houston etal. 1993; Clark 1993,1994). The foraging behaviour ofindividual animals will often depend on their energetic state and the timing ofreproduction. There have been numerous studies on the effects of increasedpredation risk on foraging behaviour of small mammals (Holmes 1984; Kotler1984; Anderson 1986; Desy eta!. 1990; Kieffer 1991; Cassini and Galante 1992;Dickman 1992; Kotler et a!. 1992; Hughes et a!. 1993), and in most of thesestudies increased risk of predation has resulted in shifts in patterns of habitatuse, diet, and time spent active or foraging. The influence of predation risk onpopulation dynamics has been more difficult to demonstrate (Ives and Dobson1987; FitzGibbon and Lazarus 1994).Recent theoretical work by Abrams (1986, 1989, 1990, 1991, 1 992a,b,c,1993), Abrams and Matsuda (1993), and Matsuda and Abrams (1993) hassuggested that adaptive behaviour of predators and anti-predator behaviour ofprey can have a large impact on predator-prey dynamics. Matsuda and Abrams(1993) emphasize that seemingly adaptive traits, such as anti-predatorbehaviour, do not always increase the mean fitness of a population. Undersome circumstances it is possible that the evolution of anti-predator traits willlead to the extinction of the prey species, particularly if predator populations aremaintained by alternative prey species. Few field tests to examine thesepossibilities have been conducted (Pech eta!. 1994).Our understanding of predator-prey dynamics has been greatly improvedby accurate measurements of mortality in natural populations (e.g. Boutin et at1986; Boutin 1994). The numerical and functional responses of predators havebeen used to interpret the effects of predators on the survival and recruitment ofprey species, and vice versa. Predation plays a large role in generating hare122cycles (Trostel et a!. 1987), but the direct effects of predation seem to beinsufficient to explain the slow recovery of low-phase populations. Directsublethal effects of increased predation risk during the population decline alsoappear to be necessary. A complete understanding of snowshoe hare cyclesrequires an understanding not only of the causes of mortality, but also of thecondition and behaviour of animals surviving or living in the decline. The “ghostof predators past” may have a profound influence on these cycles.Future research efforts should endeavour to see if maternal condition hasan influence on the behaviour, survival, and reproductive success of hares. Thelatency of these effects may affect the population cycle. It will also be importantto understand more about spacing behaviour and the interactions betweenindividual hares at different times of the cycle. Although food does not appear tobe limiting, hares may compete for sites of protective cover which may belimiting in the environment. If these sites of high quality cover are necessary forhares to reduce their risk of predation, then the availability of cover mayinfluence the lower limit of the population size during the decline.CONCLUSIONSThe results of the experiments described in this thesis show that anti-predator behaviours in response to increased predation risk may result inreduced body mass and reproduction of snowshoe hares. Closed spruce forestappears to provide hares with protective cover from most predators during thepopulation decline, but increased survival is achieved at the cost of lowerfecundity. Thus, even though winter food is sufficient, predation risk reinforcesthe decline of hares during the low phase of the 10-year cycle. All individuals ina population will not be affected equally. The relative importance of predation123risk in regulating predator-prey dynamics will depend on the age, sex,reproductive status, and condition of individual prey that survive predator attack(FitzGibbon and Lazarus 1994). Habitat patchiness may also play an importantrole (Wolff 1981; Fig. 2.1). Further experimental work which explores thebalance between conflicting behaviours by expressing them in terms of survivaland future reproductive success will lead to greater understanding of the role ofpredation risk on life history strategies, population dynamics, and communitystructure (Kotler 1984; Abrams 1990, 1992a; Rowe and Ludwig 1991; Suhonen1993). The non-lethal effects of predators are pervasive.124LITERATURE CITEDAbrahams, MN. and Dill, L.M. 1989. A determination of the energeticequivalence of the risk of predation. Ecology 70, 999-1007.Abrams, P.A. 1986. Adaptive responses of predators to prey and prey topredators: the failure of the arms race analogy. Evolution 40, 1229-1247.Abrams, P.A. 1989. Decreasing functional responses as a result of adaptiveconsumer behavior. Evolutionary Ecology 3, 95-114.Abrams, P.A. 1990. The evolution of anti-predator traits in response toevolutionary change in predators. Qikos 59, 147-156.Abrams, P.A. 1991. Strengths of indirect effects generated by optimal foraging.Oikos62, 167-176.Abrams, P.A. 1 992a. Adaptive foraging by predators as a cause of predator-prey cycles. Evolutionary Ecology 6, 56-72.Abrams, P.A. 1 992b. Why don’t predators have positive effects on preypopulations? Evolutionary Ecology 6, 449-457.Abrams, P.A. 1 992c. Predators that benefit prey and prey that harm predators:unusual effects of interacting foraging adaptations. American Naturalist 140,573-600.Abrams, P.A. 1993. Why predation rate should not be proportional to predatordensity. Ecology 74, 726-733.Adams, P.A. and Matsuda, H. 1993. Effects of adaptive predatory and anti-predator behaviour in a two-prey-one-predator system. Evolutionary Ecology7, 312-326.Adams, L. 1959. An analysis of a population of snowshoe hares innorthwestern Montana. Ecological Monographs 29, 141-1 70.Akçakaya, H.R. 1992. Population cycles of mammals: evidence for a ratiodependent predation hypothesis. Ecological Monographs 62, 119-142.Albon, S.D., Clutton-Brock, T.H., and Guinness, F.E. 1987. Early developmentand population dynamics in red deer. II. Density-independent effects andcohort variation. Journal of Animal Ecology 56, 69-81.Anderson, P.K. 1986. Foraging range in mice and voles: the role of risk.Canadian Journal of Zoology 64, 2645-2653.125Batzli, G.O. 1992. Dynamics of small mammal populations: a review. InWildlife 2001: Populations. (D.R. McCullough and R.E. Barrett, eds.). pp.831-850. Elsevier, London.Bider, J.R. 1961. An ecological study of the hare Lepus americanus. CanadianJournal of Zoology 39, 81-1 03.Boonstra, R. 1994. Population cycles in microtines: the senescencehypothesis. Evolutionary Ecology 8, in press.Boonstra, R. and Boag, P.T. 1987. A test of the Chilly hypothesis: Inheritanceof life-history traits in meadow voles Microtus pennsylvanicus. Evolution 41,929-947.Boonstra, R. and Boag, P.T. 1992. Spring declines in Microtus pennsylvanicusand the role of steroid hormones. Journal of Animal Ecology 61, 339-352.Boonstra, R. and Singleton, G.R. 1993. Population declines in the snowshoehare and the role of stress. General and Comparative End rocrinology 91,126-143.Boulanger, J. 1993. Evaluation of capture-recapture estimators using a cyclicsnowshoe hare population. Unpublished M.Sc. Thesis, University of BritishColumbia.Boulanger, J. and White, G. 1990. A comparison of home-range estimatorsusing Monte Carlo simulations. Journal of Wildlife Management 54, 310-315.Bouskila, A. and Blumstein, D.T. 1992. Rules of thumb for predation hazardassessment: predictions from a dynamic model. American Naturalist 139,161-176.Boutin, S. 1980. Effect of spring removal experiments on the spacing behaviourof female snowshoe hares. Canadian Journal of Zoology 58, 2167-2174.Boutin, S. 1 984a. The effect of conspecifics on juvenile survival andrecruitment of snowshoe hares. Journal of Animal Ecology 53, 623-637.Boutin, 5. 1 984b. Effect of late winter food addition on numbers andmovements of snowshoe hares. Qecologia 62, 393-400.Boutin, S. 1984c. Home range size and methods of estimating snowshoe haredensities. Acta Zoologica Fennica 171, 275-278.126Boutin, S. 1990. Food supplementation experiments with terrestrial vertebrates:patterns, problems, and the future. Canadian Journal of Zoology 68, 203-220.Boutin , S. 1994. Testing predator-prey theory by studying fluctuatingpopulations of small mammals. Wildlife Research, in press.Boutin, S.A., Gilbert, B.S., Krebs, C.J., Sinclair, A.R.E., and Smith, J.N.M. 1985.The role of dispersal in the population dynamics of snowshoe hares.Canadian Journal of Zoology 64, 106- 6115.Boutin, S.A., Krebs, C.J., Sinclair, A.R.E., and Smith, J.N.M. 1986. Proximatecauses of losses in a snowshoe hare population. Canadian Journal ofZoology 64, 606- 610.Bradley, A.J., McDonald, l.R., and Lee, A.K. 1980. Stress and mortality in asmall marsupial (Antechinus stuartli, Macleay). General and ComparativeEndrocrinology 40, 188-200.Bronson, F.H. 1984. The adaptability of the house mouse. Scientific American250, 116-125.Bryant, J.P., Wieland, G.D., Clausen, T., and Kuropat, P. 1985. Interactions ofsnowshoe hares and feitleaf willow in Alaska. Ecology 66, 1564-1573.Bryant, J.P., Kuropat, P.J., Reichart, P.B., and Clausen, T.P. 1991a. Controlsover the allocation of resources by woody plants to chemical antiherbivoredefense. In Plant Defenses Against Mammalian Herbivory (Eds. R.T. Paloand C.T. Robbins) pp. 84-102. CRC Press, Boca Raton.Bryant, J.P., Reichart, P.B., Clausen, T.P., Provenza, F.D., and Kuropat, P.J.1991b. Woody plant-mammal interactions. In Herbivores: Their Interactionwith Plant Metabolites. Vol. 2 (Ed. G.A. Rosenthal and M.R. Berenbaum). pp.344-370. Academic Press, New York.Buehler, D.A. and Keith, L.B. 1982. Snowshoe hare distribution and habitat usein Wisconsin. Canadian Field-Naturalist 96, 19-29.Calhoun, J.B. 1949. A method for self-control of population growth amongmammals living in the wild. Science 109, 333-335.Carreker, R.G. 1985. Habitat suitability index models: snowshoe hare. U.S.Fish and Wildlife Service Biological Report 82(10.101). 21 pp.Cary, J.R. and Keith, L.B. 1979. Reproductive change in the 10-year cycle ofsnowshoe hares. Canadian Journal of Zoology 57, 375-390.127Cassini, M.H. and Galante, M.L. 1992. Foraging under predation risk in the wildguinea pig: the effect of vegetation height on habitat utilization. AnnalesZoologi Fennici 29, 285-290.Caughley, G. and Krebs, C.J. 1983. Are big mammals simply little mammalswrit large? Qecologia 59, 7-17.Charnov, E., Orians, G.H. and Hyatt, K. 1976. Ecological implications ofresource depression. American Naturalist 110, 247-259.Cheeke, P.R. 1983. The significance of fibre in rabbit nutrition. Journal ofApplied Rabbit Research 6, 103-1 06.Chitty, D. 1952. Mortality among voles (Microtus agrestis) at Lake Vyrnwy,Montgomeryshire in 1936-9. Philosophical Transactions of the Royal SocietyLondon, Series B, 236, 505-552.Chitty, D. 1958. Self-regulation of numbers though changes in viability. ColdSpring Harbour Symposium on Quantitative Biology 22, 277-280.Chitty, D. 1959. A note on shock disease. Ecology 40, 728-731.Chitty, D. 1967. The natural selection of self-regulatory behaviour in animalpopulations. Proceedings of the Ecological Society of Australia 2, 51-78.Chitty, D. 1987. Social and local environments of the vole Microtus townsend!!.Canadian Journal of Zoology 65, 2555-2566.Chilly, D. 1993. Do Lemmings Commit Suicide? Beautiful Hypotheses and UglyFacts. Unpublished Manuscript.Chitty, D., and Phipps, E. 1966. Seasonal changes in survival in mixedpopulations of two species of vole. Journal of Animal Ecology 35, 313-331.Christian, J.J. 1950. The adreno-pituitary system and population cycles inmammals. Journal of Mammalogy 31, 247-259.Christian, J.J. 1980. Endocrine factors in population regulation. In Biosocialmechanisms of population regulation (Eds. M.N. Cohen, R.S. Malpass andH.G. Klein) pp. 55-115. Yale University Press, New Haven.Clark, C.W. 1993. Dynamic models of behaviour: an extenstion of life historytheory. Trends in Ecology and Evolution 8, 205-209.Clark, C.W. 1994. Anti-predator behaviour and the asset protection principle.Behavioural Ecology, in press.128Connell, J.H. 1980. Diversity and the coevolution of competitors, or the ghost ofcompetition past. Qikos 35, 131 -1 38.Curio, E. 1993. Proximate and developmental aspects of antipredatorbehaviour. Advances in the Study of Behaviour 22, 135-238.Cushing, B.S. 1985. Estrous mice and vulnerability to weasel predation.Ecology 66, 1976-1 978.de Poorter, M. 1984. An experimental test of predictions from differenthypotheses of self-regulation in the snowshoe hare (Lepus americanusErxleben, 1777). Unpublished Ph.D. Thesis, Vrije Universiteit Brussel.Desy, E.A. and Batzli, G.O. 1989. Effects of food and predation on behaviour ofprairie voles: a field experiment. Ecology 70, 411-421.Desy, E.A., Batzli, G.O., and Jike, L. 1989. Comparison of vole movementsassessed by live trapping and radiotracking. Journal of Mammalogy 70, 652-656.Dickman, C.R. 1992. Predation and habitat shifts in the house mouse, Musdomesticus. Ecology 73, 313-322.Dixon, K. and Chapman, K. 1980. Harmonic mean measure of animal activityareas. Ecology 61, 1040-1044.Doyle, F.l. and J. N. M. Smith. 1994. Population responses of northerngoshawks to the 10-year cycle in numbers of snowshoe hares. Condor,submitted.Elton, C.S. 1924. Periodic fluctuations in the numbers of animals: their causesand effects. Journal of Experimental Biology 2, 119-163.Elton, C. and Nicholson, M. 1942. The ten-year cycle of numbers of lynx inCanada. Journal of Animal Ecology 11, 215-244.Erlinge, S., Gäransson, G., Hogstedt, 3., Jansson, G., Liberg, 0., Loman,J.,Nilsson, l.N., von Schantz, T., and Sylven, M. 1984. Can vertebratepredators regulate their prey? American Naturalist 123, 125-133.Feinsinger, P., Spears, E.E., and Poole, R.W. 1981. A simple measure of nichebreadth. Ecology 62, 27-32.Feist, D.D. 1980. Corticosteroid release by adrenal tissue of Alaska snowshoehares in a year of population decline. Journal of Mammalogy 61, 134-136.129Ferron, J. 1993. How do density and food supply influence social behaviour inthe snowshoe hare (Lepus americanus)? Canadian Journal of Zoology 71,1084-1089.Finerty, J.P. 1980. The population ecology of cycles in small mammals. YaleUniversity Press, New Haven.FitzGibbon, C.D. and Lazarus, J. 1994. Anti-predator behaviour of Serengetiungulates: individual differences and population consequences. In SerengetiIl: Research, Management and Conservation of an Ecosystem (Eds. A.R.E.Sinclair and P. Arcese), University of Chicago Press, Chicago. in press.Ford, R.G. and Pitelka, F.A. 1984. Resource limitation in populations of theCalifornia vole. Ecology 65, 122-136.Gilbert, B.S. 1990. Use of winter feeding craters by snowshoe hares.Canadian Journal of Zoology 68, 1600-1602.Gilbert, B.S. and Boutin, S. 1991. Effect of moonlight on winter activity ofsnowshoe hares. Arctic and Alpine Research 23, 61-65.Gilliam, J.F. and Fraser, D.F. 1987. Habitat selection under predation hazard:test of a model with foraging minnows. Ecology 68, 1856-1862.Graf, R.P. 1985. Social organization of snowshoe hares. Canadian Journal ofZoology 63, 468-474.Graf, R.P. and Sinclair, A.R.E. 1987. Parental care and adult aggressiontowards juvenile snowshoe hares. Arctic 40, 175-178.Grange, W.B. 1932. The pelage and colour changes of the snowshoe hare,Lepus americanus phaenotus Allen. Journal of Mammalogy 13, 99-116.Green, R.G. and Larson, C.L. 1938. A description of shock disease in thesnowshoe hare. American Journal of Hygiene 28, 190-212.Green, R.G. and Evans, C.A. 1940. Studies on a population cycle of snowshoehares on the Lake Alexander area. II. Mortality according to age groups andseasons. Journal of Wildlife Management 4, 267-278.Gross, J.E., Hobbs, N.T., and Wunder, B.A. 1993. Independent variables forpredicting intake rate of mammalian herbivores: biomass density, plantdensity, or bite size? Qikos 68, 75-81.130Hanski, I., Hansson, L. and Henttonen, H. 1991. Specialist predators,generalist predators, and the microtine rodent cycle. Journal of AnimalEcology 60, 353-367.Hart, J.S. and Pohi, J. 1965. Seasonal acclimatization in varying hares.Canadian Journal of Zoology 43, 731-744.Hassell, M.P. and R.M. May. 1985. From individual behaviour to populationdynamics. In Behavioural Ecology: Ecological Consequences of AdaptiveBehaviour (Eds. R.M. Sibly and R.H. Smith) pp. 3-32. Blackwells, Oxford.Hestbeck, J.B. 1987. Multiple regulation states in populations of smallmammals: a state-transition model. American Naturalist 129, 520-532.Holmes, W.G. 1984. Predation risk and foraging behavior of the hoary marmotin Alaska. Behavioural Ecology and Sociobiology 15, 293-301.Houston, A.l., McNamara, J.M., and Hutchinson, J.M.C. 1993. General resultsconcerning the trade-off between gaining energy and avoiding predation.Philosophical Transactions of the Royal Society London, Series B, 341, 375-397.Huggard, D.J. 1993. The effect of snow depth on predation and scavenging bywolves. Journal of Wildlife Managment 57, 382-388.Hughes, J.J. and Ward, D. 1993. Predation risk and distance to cover affectforaging behaviour in Namib Desert gerbils. Animal Behaviour, in press.Hughes, J.J., Ward, D. and Perrin, M.R. 1993. The effects of predation risk andcompetition on habitat selection and activity of gerbils in the Namib Desert.Ecology, in press.lves, A.R. and Dobson, A.P. 1987. Antipredator behaviour and the populationdynamics of simple predator-prey systems. American Naturalist 130, 431-447.Jedrzejewski, W., Rychlik, L., and Jedrzejewski, B. 1993. Responses of bankvoles in odours of seven species of predators: experimental data and theirrelevance to natural predator-vole relationships. Oikos 68, 251-257.Keith, L.B. 1963. Wildlife’s ten-year cycle. University of Wisconsin Press,Madison.Keith, L.B. 1966. Habitat vacancy during a snowshoe hare decline. Journal ofWildlife Management 30, 828-832.131Keith, L.B. 1974. Some features of population dynamics in mammals.Proceedings International Congress of Game Biologists 11, 17-58.Keith, L.B. 1983. Role of food in hare population cycles. Qikos 40, 385-395.Keith, L.B. 1990. Dynamics of snowshoe hare populations. In CurrentMammalogy (Ed. H.H. Genoways). pp. 119-195. Plenum Press, New York.Keith, L.B., Todd, A.W., Brand, C.J., Adamcik, R.S. and Rusch, D.H. 1977. Ananalysis of predation during a cyclic fluctuation of snowshoe hares.Proceedings of the International Congress of Game Biologists 13, 151-175.Keith, L.B. and Windberg, L.A. 1978. A demographic analysis of the snowshoehare cycle. Wildlife Monographs 58, 1-70.Keith, L.B., Cary, J.R., Rongstad, O.J., and Brittingham, M.C. 1984.Demography and ecology of a declining snowshoe hare population. WildlifeMonographs 90, 1-43.Keith, L.B., Bloomer, S.E.M., and Willebrand, T. 1993. Dynamics of asnowshoe hare population in fragmented habitat. Canadian Journal ofZoology 71, 1385-1392.Kenward, R. 1990. Ranges IV. Institute of Terrestrial Ecology, Furzebrook, UK.Kidd, N.A.C. and Lewis, G.B. 1987. Can vertebrate predators regulate theirprey? A reply. American Naturalist 130, 448-453.Kotler, B.P. 1984. Risk of predation and the structure of desert rodentcommunities. Ecology 65, 689-701.Kolter, B.P. 1985. Microhabitat utilization in desert rodents: a comparison oftwo methods of measurement. Journal of Mammalogy 66, 374-378.Kotler, B.P. 1992. Behavioural resource depression and decaying perceivedrisk of predation in two species of coexisting gerbils. Behavioural Ecologyand Sociobiology 30, 239-244.Kotler, B.P., Blaustein, L., and Brown, J.S. 1992. Predation facilitation: thecombined effects of snakes and owls on the foraging behavior of gerbils.Annales Zoologici Fennici 29, 199-206.Korpimaki, E. 1993. Regulation of multiannual vole cycles by densitydependent avian and mammalian predation? Oikos 66,359-363.132Korpimaki, E., Norrdahl, K., and Valkama, J. 1994. Reproductive investmentunder fluctuating predation risk: microtine rodents and small mustelids.Evolutionary Ecology, in press.Krebs, C.J. 1978. A review of the Chitty Hypothesis of population regulation.Canadian Journal of Zoology 56, 2463-2480.Krebs, C.J. 1985. Do changes in spacing behaviour drive population cycles insmall mammals. In Behavioural Ecology (Eds. R.M. Sibley and R.H. Smith).pp. 295-312. Blackwell Scientific Publications, London.Krebs, CJ. 1986. Are lagomorphs similar to other small mammals in theirpopulation ecology? Mammal Review 16, 187-194.Krebs, C.J. 1989. Ecological Methodology. Harper and Row, New York.Krebs, C.J. 1993. Are lemmings large Microtus or small reindeer? A review oflemming cycles after 25 years and recommendations for future work. InBiology of Lemmings (Eds. N.C. Stenseth and R.A. lms). pp. 247-260.Linnean Society Symposium Series 15. Academic Press, London.Krebs, C.J. and Myers, J.H. 1974. Population cycles in small mammals.Advances in Ecological Research 8, 267-399.Krebs, C.J., Gilbert, B.S., Boutin, S., Sinclair, A.R.E. and Smith, J.N.M. 1986a.Population biology of snowshoe hares. I. Demography of food-supplementedpopulations in the southern Yukon, 1976-1984. Journal of Animal Ecology 55,963-982.Krebs, C.J., Boutin, S., and Gilbert, B.S. 1986b. A natural feeding experimenton a declining snowshoe hare population. Qecologia 70, 194-1 97.Krebs, C. J., Boonstra, R., Boutin, S., Dale, M. R. T., Hannon, S., Martin, K.,Sinclair, A. R. E., Smith, J. N. M. and Turkington, R. 1992. What drives thesnowshoe hare cycle in Canada’s Yukon? In Wildlife 2001: Populations.(D.R. McCullough and R.E. Barrett, eds.). pp. 886-896. Elsevier, London.Krebs, J.R. and Kacelnik, A. 1991. Decision-making. In Behavioural EcologyThird Edition (Eds. J.R. Krebs and N.B. Davies) pp. 105-136. Blackwells,London.Lambin, X. and Krebs, C.J. 1991 a. Spatial organization and mating system ofMicrotus townsendii. Behavioural Ecology and Sociobiology 28 353-363.Lambin, X. and Krebs, C.J. 1991b. Can changes in female relatednessinfluence microtine population dynamics. Oikos 61, 126-132.133Lazarus, J. 1990. Looking for trouble. New Scientist 27, 62-65.Lenth, R.V. 1981. On finding the source of a signal. Technometrics 23, 149-154.Lidicker, W. Z., Jr. 1988. Solving the enigma of microtine “cycles”. Journal ofMammalogy 69, 225-235.Lima, S.L. 1992. Life in a multi-predator environment; some considerations foranti-predator vigilance. Annales Zoologici Fennici 29, 217-226.Lima, S.L. and Dill, L.M. 1990. Behavioural decisions made under the risk ofpredation; a review and prospectus. Canadian Journal of Zoology 68, 619-640.Litvaitis, J.A. 1990. Differential habitat use by sexes of snowshoe hares (Lepusamericanus). Journal of Mammalogy 71, 520-523.Litvaitis, J.A. 1991. Habitat use by snowshoe hares, Lepus americanus, inrelation to pelage color. Canadian Field Naturalist 105, 275-277.Litvaitis, J.A., Sherburne, J.A. and Bissonette, J.A. 1 985a. A comparison ofmethods used to examine snowshoe hare habitat use. Journal of WildlifeManagement 49, 693-695.Litvaitis, J.A., Sherburne, J.A. and Bissonette, J.A. 1 985b. Influence ofunderstory characteristics on snowshoe hare habitat use and density.Journal of Wildlife Management 49, 866-873.Longland, W.S. and Price, M.V. 1991. Direct observations of owls andheteromyid rodents: can predation risk explain microhabitat use? Ecology 72,2261-2273.Ludwig, D. and Rowe, L. 1990. Life-history strategies for energy gain andpredator avoidance under time constraints. American Naturalist 135, 686-707.Lundberg, P. 1988. Functional responses of a small mammalian herbivore: thedisc equation revisited. Journal of Animal Ecology 57, 999-1006.MacLulich, D.A. 1937. Fluctuations in the Numbers of the Varying Hare (Lepusamericanus). University of Toronto Studies, Biology Series 43.Magnhagen, C. 1991. Predation risk as a cost of reproduction. Trends inEcology and Evolution 6, 183-186.134Manville, C.J., Barnum, S.A. and Tester, J.A. 1992. Influence of bait onarboreal behavior of Peromyscus leucopus. Journal of Mammalogy 73, 335-336.Mangel, M. and Clark, C.W. 1988. Dynamic Modelling in Behavioural Ecology.Academic Press, Princeton, N.J.Matsuda, H. and Abrams, P.A. 1993. Timid consumers: self-extinction due toadaptive change in foraging and anti-predator effort. Theoretical PopulationBiology, in press.May, R.M. 1974. Stability and Complexity in Model Ecosystems. PrincetonUniversity Press, Princeton, N.J.May, R.M. 1976. Models for single populations. In Theoretical Ecology:Principles and Applications (Ed. R.M. May). pp. 4-25. Saunders,Philadelphia, PA.McNamara, J.M. 1990. The starvation predation tradeoff and some behaviouraland ecological consequences. In Behavioural Mechanisms of FoodSelection. (Ed. R.N. Hughes). pp. 39-59. Springer Verlag, Berlin.McNamara, J.M. and Houston, A.l. 1987. Starvation and predation as factorslimiting population size. Ecology 68, 1515-1519.McNamara, J.M. and Houston, A.l. 1990. Starvation and predation in a patchyenvironment. In Living in a Patchy Environment. (Eds. B. Shorrocks and I.Swingland). pp. 23-43. Oxford University Press, Oxford.McNamara, J.M. and Houston, A.l. 1990. State-dependent ideal freedistributions. Evolutionary Ecology 4, 298-311.Mech, L.D., Nelson, M.E. and McRoberts, R.E. 1991. Effects of maternal andgrandmaternal nutrition on deer mass and vulnerability to wolf predation.Journal of Mammalogy 72, 146-151.Mihok, S. and Boonstra, R. 1992. Breeding performance in captivity of meadowvoles (Microtus pennsylvanicas) from decline and increase-phasepopulations. Canadian Journal of Zoology 70, 1561-1566.Morris, D.W. 1988. Habitat-dependent population regulation and communitystructure. Evolutionary Ecology 2, 253-269.135Munck, A., Guyre, P., and Holbrook, N. 1984. Physiological functions ofglucocorticoids during stress and their relation to pharmacological actions.Endocrinology Review 5, 25-44.Murray, D. 1990. Aspects of winter foraging in lynx and coyotes fromsouthwestern Yukon during an increase in snowshoe hare abundance. M.Sc.Thesis, University of Alberta, Canada.Murray, D.L. and Boutin, S. 1991. The influence of snow on lynx and coyotemovements in southwestern Yukon: Does morphology affect behaviour?Qecologia 88, 463-469.Nams, M. 1993. Bar coding bees and other wild ways to watch wildlife. RangerRick 27, 14-16.Nams, V.0. 1990. Locate II. Pacer, Truro, N.S., Canada.O’Donoghue, M. 1983. Seasonal habitat selection by snowshoe hare in easternMaine. Transactions Northeast Fish and Wildlife Conference 40, 100-107.O’Donoghue, M. and Krebs, C. J. 1992. Effects of supplemental food onsnowshoe hare reproduction and juvenile growth at a cyclic population peak.J. Animal. Ecology 61, 631-641.Oksanen, T, Oksanen, L., and Gyllenberg, M. 1992. Exploitation ecosystems inheterogenous habitat complexes II: impact of small-scale heterogeneity onpredator-prey dynamics. Evolutionary Ecology 6, 383-398.Orr, C.D. and Dodds, D.G. 1982. Snowshoe hare habitat preferences in NovaScotia spruce-fir forests. Wildlife Society Bulletin 10,147-150.Ostfeld, R.S. 1992. Small-mammal herbivores in a patchy environment:individual strategies and population responses. In Effects of ResourceDistribution on Animal-Plant Interactions (Eds. M.D. Hunter, T. Ohgushi andP.W. Price). pp. 43-74. Academic Press, San Diego.Otis, D.L., Burnham, K.P., White, G.C., and Anderson, D.R. 1978. Statisticalinference from capture data on closed animal populations. WildlifeMonographs 62, 1-135.Partridge, L. and Harvey, RH. 1985. Costs of reproduction. Nature 316, 20.Pease, J.L., Vowles, R.H. and Keith, LB. 1979. Interaction of snowshoe haresand woody vegetation. Journal of Wildlife Management 43, 43-60.136Pech, R.P., Sinclair, A.R.E., and Newsome, A.E. 1994. Predation models forprimary and secondary prey species. Wildlife Research, in press.Peckarsky, B.L., Cowan, C.A., Penton, M.A., and Anderson, C. 1993. Sublethalconsequences of stream-dwelling predatory stoneflies on mayfly growth andfecundity. Ecology 74, 1836-1846.Persson, L. 1993. Predator-mediated competition in prey refuges: theimportance of habitat dependent prey resources. Oikos 68, 12-22.Pettersson, L.B. and Brönmark, C. 1993. Trading off safety against food: statedependent habitat choice and foraging in crucian carp. Qecologia 95, 353-357.Pietz, P.J. and Tester, J.R. 1983. Habitat selection by snowshoe hares in northcentral Minnesota. Journal of Wildlife Management 47, 686-696.Pollock, K.H., Winterstein, S.R., Bunick, C.M., and Curtis, P.D. 1989a. Survivalanalysis in telemetry studies: the staggered entry design. Journal of WildlifeManagement 53, 7-15.Pollock, K.H., Winterstein, S.R., and Conroy, M.J. 1989b. Estimation andanalysis of survival distributions for radio-tagged animals. Biometrics 45, 99-109.Pollard, I. 1986. Prenatal stress effects over two generations in rats. Journalof Endocrinology 109, 239-244.Pullianinen, E. 1983. The refuge theory and habitat selection in the mountainhare on a subarctic fell in Finnish Forest Lapland. Finnish Game Research41, 39-44.Radvanyi, A. 1987. Snowshoe hares and forest plantations: a literature reviewand problem analysis. Canadian Forestry Service, Northern Forestry Centre,Edmonton, AB, Information Report NOR-X-290.Reid, D.G., Krebs, C.J., and Kenney, A. 1993. Predation and collared lemmingpopulation dynamics. Abstracts of Sixth International Theriological Congress,Sydney (Ed. M.L. Augee). p. 255.Reznick, D. and Yang, A.P. 1993. The influence of fluctuating resources on lifehistory: patterns of allocation and plasticity in female guppies. Ecology 74,2011-2019.137Rodgers, A. R. and Sinclair, A. R. E. 1994. Diet choice and nutrition ofsnowshoe hares: interactions of energy, protein and plant secondarycompounds. Canadian Journal of Zoology, submitted.Rogowitz, G.L. 1988. Forage quality and use of reforested habitats bysnowshoe hares. Canadian Journal of Zoology 66, 2080-2083.Rohner, Ch. and Krebs, C.J. 1994. Snowshoe hares and great horned owlpredation: which individuals are at greatest risk? Manuscript in preparation.Rosenzweig, M.L. and Abramsky, Z. 1980. Microtine cycles: the role of habitatheterogeneity. Qikos 34, 141 -146.Rossiter, M.C. 1991. Environmentally-based maternal effects: a hidden force ininsect population dynamics? Qecologia 87, 288-294.Rowe, L. and Ludwig, D. 1991. Size and timing of metamorphosis in complexlife cycles: time constraints and variation. Ecology 72, 41 3-427.Royama, T. 1992. Analytical Population Dynamics. Chapman and Hall,London.Ryan, M.J. 1985. The Tungara frog: a study in sexual selection andcommunication. University of Chicago Press, Chicago.Saarikko, J. 1992. Risk of predation and foraging activity in shrews. AnnalesZoologici Fennici 29, 291-299.Schmitz, O.J., Hik, D.S., and Sinclair, A.R.E. 1992. Plant chemical defence andtwig selection by snowshoe hares: an optimal foraging perspective. Qikos 65:295-300.Schmutz, J.A. and White, G.C. 1990. Error in telemetry studies: effects ofanimal movement on triangulation. Journal of Wildlife Management 54, 506-510.Scott, D.P. and Yahner, R.H. 1989. Winter habitat and browse use bysnowshoe hares, Lepus americanus, in a marginal habitat in Pennsylvania(USA). Canadian Field Naturalist 103:560-563.Shipley, L.A. and Spalinger, D.E. 1992. Mechanics of browsing in dense foodpatches: effects of plant and animal morphology on intake rate. CanadianJournal of Zoology 70, 1743-1752.Sibly, R.M. and Calow, P. 1986. Physiological Ecology of Animals. BlackwellScientific Publications, London.138Sievert, P.R. and Keith, L.B. 1985. Survival of snowshoe hares at a geographicrange boundary. Journal of Wildlife Management 49, 854-866.Sih, A. 1987. Prey refuges and predator-prey stability. Theoretical PopulationBiology 31, 1-12.Sih, A., Krupa, J., and Travers, S. 1990. An experimental study on the effectsof predation risk and feeding regime on the mating behaviour of the waterstrider. American Naturalist 135, 284-290.Sinclair, A.R.E. 1986. Testing multifactor causes of population limitation: anillustration using snowshoe hares. Qikos 47, 360-364.Sinclair, A.R.E. 1989. Population regulation in animals. In Ecological Concepts(Ed. J.M. Cherrett). pp. 197-241. Symposium of the British EcologicalSociety 29. Blackwell Scientific Publications, London.Sinclair, A.R.E. and Smith, J.N.M. 1984. Do plant secondary compoundsdetermine feeding preferences of snowshoe hares? Qecologia 61, 403-410.Sinclair, A.R.E., Krebs, C.J., Smith, J.N.M., and Boutin, S. 1988a. Populationbiology of snowshoe hares. III. Nutrition, plant secondary compounds andfood limitation. Journal of Animal Ecology 57, 787-806.Sinclair, A. R. E., M. K. Jogia, and R. J. Andersen. 1988b. Camphor fromjuvenile white spruce as an antifeedant for snowshoe hares. Journal ofChemical Ecology 14, 1505-1 51 4.Sinclair, A.R.E, Gosline, J.M., Holdsworth, G., Krebs, C.J., Boutin, S., Smith,J.N.M., Boonstra, R., and Dale, M. 1993. Can the solar cycle and climatesynchronize the snowshoe hare cycle in Canada? Evidence from tree ringsand ice cores. American Naturalist 141, 173-1 98.Sinclair, A.R.E. and Arcese, P. 1994. Population consequences of predationsensitive foraging: the Serengeti wildebeest. Ecology, submitted.Smith, C.H. 1983. Spatial trends in the Canadian snowshoe hare, Lepusamericanus, population cycles. Canadian Field-Naturalist 97, 151-1 60.Smith, J.N.M., Krebs, C.J., Sinclair, A.R.E., and Boonstra, R. 1988. Populationbiology of snowshoe hares. II. Interactions with winter food plants. Journalof Animal Ecology 57, 269-286. -139Stuart-Smith, K. 1992. Do lemming, vole, and snowshoe hare cycles affectother small birds and mammals in northern ecosystems? Musk-Ox 39, 181-188.Suhonen, J. 1993. Predation risk influences the use of foraging sites by Tits.Ecology 74, 1197-1203.Sullivan, T.P. and Crump, D.R. 1984. Influence of mustelid scent-glandcompounds on suppression of feeding by snowshoe hares (Lepusamericanus). Journal of Chemical Ecology 10, 1809-1821.Sullivan, T.P. and Crump, D.R. 1986. Feeding responses of snowshoe hares(Lepus americanus) to volatile constituents of red fox ( Vulpes vulpes) urine.Journal of Chemical Ecology 12, 729-739.Sullivan, T.P. and Moses, R.A. 1986. Demographic and feeding responses of asnowshoe population to habitat alteration. Journal of Applied Ecology 23, 53-63.Sullivan, T.P. Nordstrom, L.O. and Sullivan, D.S. 1985. Use of predator odorsas repellents to reduce feeding damage by herbivores. 1. Snowshoe hares(Lepus americanus). Journal of Chemical Ecology 11, 903-919.Swikhart, R. and Slade, H. 1985. Testing for independance of observations inanimal movements. Journal of Wildlife Management 49, 1019-1025.Taitt, M.J. and Krebs, C.J. 1985. Population dynamics and cycles. In Biologyof New World Microtus (Ed. R.H. Tamarin). American Society ofMammalogists Special Publication 8, 567-620.Trostel, K., Sinclair, A.R.E., Walters, C.J. and Krebs, C.J. 1987. Can predationcause the 10-year hare cycle? Oecologia 74, 185-192.Underwood, R. 1982. Vigilence behaviour in grazing African antelopes.Behaviour 79, 81 -1 08.Vaughan, M.R. and Keith, L.B. 1981. Demographic response of experimentalsnowshoe hare populations to overwinter food shortage. Journal of WildlifeManagement 45, 354-380.Whittaker, M.E. and Thomas, V.G. 1983. Seasonal levels of fat and proteinreserves of snowshoe hares in Ontario. Canadian Journal of Zoology 61,1339-1345.Wilkinson, L. 1988. Systat. Evanston, IL.140Williamson, C.E. 1993. Linking predation risk models with behaviouralmechanisms: identifying population bottlenecks. Ecology 74, 320-331.Wolfe, M.L., Debyle, N.V., Winchell, C.S. and McCabe, T.R. 1982. Snowshoehare cover relationships in northern Utah. Journal of Wildlife Management46, 662-670.Wolff, J.O. 1978. Food habits of snowshoe hares in interior Alaska. Journal ofWildlife Management 42, 148-1 53.Wolff, J.O. 1980. The role of habitat patchiness in the population dynamics ofsnowshoe hares. Ecological Monographs 50, 111-130.Wolff, J.O. 1981. Refugia, dispersal and geographic variation in snowshoehare cycles. In Proceedings World Lagomorph Conference 1979 (Eds. K.Myers and C.D. Mclnnes) pp. 441-449. University of Guelph, Ontario.Ylönen, H., Jedrzejewska, B., Jedrzejewki, W., and Heikkilã, J. 1992.Antipredatory behaviour of Clethrionomys voles: ‘David and Goliath’ armsrace. Annales Zoologici Fennici 29, 207-216.

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
https://iiif.library.ubc.ca/presentation/dsp.831.1-0088088/manifest

Comment

Related Items