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Factors limiting population growth of non-cyclic collared lemmings at low densities Reid, Donald Grant 1995

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FACTORS LIMITING POPULATION GROWTH OF NON-CYCLIC COLLARED LEMMINGS AT LOW DENSITIES  by DONALD GRANT REID B.Sc.(Hons), The University of Guelph, 1977 M.Sc., The University of Calgary, 1984 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE STUDIES DEPARTMENT OF ZOOLOGY We accept this thesis as conforming to the required standard  THE UNIVERSITY OF BRITISH COLUMBIA September 1995 © Donald Grant Reid, 1995  __________________________  In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the head of my department  or  by  his  or  her  representatives.  It  is  understood  that  copying  or  publication of this thesis for financial gain shall not be allowed without my written permission.  (Signature)  Department of  LO  The University of British Columbia Vancouver, Canada  Date  DE-6 (2/88)  1 3  SM’3 199S  11  ABSTRACT  I examined factors limiting population growth of collared lemmings  (Dicrostonyx kilangmiutak) at low densities (<3 adults/ha), at Pearce Point, Northwest Territories, Canada. Populations were followed by mark-recapture, and radiotelemetry. They fluctuated annually, typically with summer declines, and winter increases. I tested the hypothesis that predation mortality limits population growth in summer, by comparing a population in an 11 ha predator exclosure (PE) with three control populations (18-25 ha). Predation, principally by red fox (Vulpes vulpes) and rough-legged hawks (Buteo lagopus), was the proximate cause of most adult and neo natal mortality. No other mortality factor compensated for decreased predation mortality in PE. Adult survival and recruitment increased significantly in PE. Controls declined in 1990 and 1991. PE declined less quickly. It did not grow, because weanlings dispersed long distances (53 mId), and frequently left PP. I conclude that predation mortality is sufficient and necessary to limit summer population growth. Three other factors potentially limiting population growth in PP were investigated. Social interactions did not inhibit reproduction because neither the proportion of lemmings reproductively active, nor litter sizes, differed between PE and controls. Food availability did not limit growth because principal foods were not depleted in PP. net primary production was similar to that in regions where lemmings irrupt, and enhanced production with fertilization was not consumed by lemmings. Behavioural sensitivity to predation risk appeared limiting because growth rates of neonates were higher in PE than on controls.  111  Lemmings bred in all winters (1987-92). Variance in rates of winter population growth was significantly explained by a combination of mean daily temperature in autumn, when lemmings change morphology, and an index of cold stress in winter. Summer predation mortality was destabilizing. Specialist and semi-generalist predators drove lemmings to densities too low for persistence of these predators. Generalist predators continued to limit lemmings in the absence of specialists and semi-generalists. The summer predator community at Pearce Point, consisting mostly of generalists or semi-generalists, contrasts with a predominantly specialist predator community at arctic sites where lemmings irrupt. A relatively diverse prey base, especially including arctic ground squirrels (Sperniophilus parryii), seemed critical for the maintenance of predators that limit lemmings in summer.  iv TABLE OF CONTENTS ABSTRACT  .  TABLE OF CONTENTS  ii iv  LIST OF TABLES  vii  LIST OF FIGURES ACKNOWLEDGEMENT  xii  INTRODUCTION  1  CHAPTER 1: LIMITATION OF COLLARED LEMMING POPULATION GROWTH AT LOW DENSITIES BY PREDATION MORTALITY INTRODUCTION METHODS Study area Population density Mortality and litter fates Predator exciosure Predator populations Statistics RESULTS Characteristics of study grids Predator community Predation mortality adults Predation mortality subadults Predator exclusion density Effect of radiocollars Predator exclusion survival Predator exclosure recruitment and population grvth Juvenile dispersal Tundra voles DISCUSSION Predation limitation Dispersal Tundra voles Relevance to population cycles  11 12 13 14 14 14 14 16 19 22 29 32 32 37 40 43 43 46 47 48  CHAPTER 2: DO PREDATORS REGULATE LEMMINGS AT LOW DENSITIES IN SUMMER ? INTRODUCTION  50 50  -  -  -  -  -  6 6  V  METHODS. Study Area Prey populations Prey Mortality Prey Reproductive Status and Productivity Prey Growth Food Limitation RESULTS Density Dependent Predation Mortality Social Inhibition of Reproduction Behavioural Sensitivity to Predation Risk Food Limitation DISCUSSION Density Dependence in Predation Mortality Inhibition of Reproduction Food Limitation Behavioural Sensitivity to Predation Risk. Other Limiting Factors Community Dynamics Predator Regulation CHAPTER 3: POSSIBLE FACTORS LIMITING WINTER POPULATION GROWTH IN COLLARED LEMMINGS INTRODUCTION METHODS Study Area Climate Data Population Estimation Winter Snow Distribution Microtine Winter Nests RESULTS Extent of winter breeding Ermine predation Nest Distribution Snow and Temperature Regimes DISCUSSION Ermine Predation Snow Distribution Winter Temperature Regimes Other Factors Affecting Winter Population Growth  52 52 53 53 55 56 56 59 59 65 70 77 88 88 91 93 95 96 97 98  •  .  101  ioi  •  .  •  .  •  .  105 105 105 107 108 108 109 109 111 111 114 125 125 126 127 128  vi CHAPTER 4: PATTERNS OF PREDATION ON NON-CYCLIC LEMMINGS: THE GENERALIST PREDATOR HYPOTHESIS. INTRODUCTION METHODS Study Area Microtine Populations Habitats Predator Numerical Responses Predator Diets Predator Functional Responses RESULTS Microtine Demography Numerical Responses of Predators Predicting Lemming Body Weight Fox diet Grizzly Bear Diet Rough-legged Hawk Feeding Experiment Rough-legged Hawk Diet Diets of Other Raptors DISCUSSION Generalist Predator Hypothesis Procedures Impact on the Lemming Population The Specialist-Generalist Continuum What Allows Generalist Predators to Persist?  131 131 133 133 135 136 136 137 144 144 144 148 152 152 173 173 173 179 185 185 190 191 193 196  CHAPTER 5: WHY DON’T ALL LEMMING POPULATIONS IRRUPT? INTRODUCTION CHARACTERISTICS OF POPULATION IRRUPTIONS GEOGRAPHIC PATTERNS IN LEMMING IRRUPTIONS FACTORS LIMITING POPULATION GROWTH AT LOW DENSITIES HOW DO REGIONS OF IRRUPTIVE AND NON-IRRUPTIVE 7 DYNAMICS Summer Predators Snow Depth Food Availability HYPOTHESES  212 212 224 227 227  CONCLUSION  229  LITERATURE CITED  232  197 197 198 200 207  vii LIST OF TABLES  Table 1.1. Characteristics of the predator exciosure (PE) and three control (Cl, C2 & C3) study grids  10  Table 1.2. Numbers and breeding success of the principal lemming predators  .  .  .  15  Table 1.3. Fates of resident adult lemmings on control grids (C) with predator access, and in the predator exclosure (PE)  17  Table 1.4. Fates of lemming litters initiated on control areas (C) and predator exciosure (FE)  20  Table 1.5. Tests of the null hypothesis that the Dicrostonyx density in the predator exclosure was not larger than the mean of sample estimates from controls.  25  Table 1.6. Instantaneous weekly rates of population change (r) for microtines  .  .  .  .  28  Table 1.7. Jolly-Seber estimates of average probability of survival  30  Table 1.8. Proportion of adult lemmings retrapped after one and two weeks  31  Table 1.9. Total adult recruits divided by total first and second litter pregnancies  38  Table 1.10. Intensity of recruitment (number of recruits per hectare)  39  Table 2.1. Proportion of lemming-weeks in which individual adult-sized lemmings were reproductively active  68  Table 2.2. Litter sizes of primiparous (spring-born), multiparous (overwintering) and first summer litter females  69  Table 2.3. Mean ± S.E. post-partum weights of adult female lemmings  78  Table 2.4. Mean ± S.E. percent cover (± 0.5%) of principal lemming foods  79  Table 2.5. Mean above-ground mass (g/0.125 m ) of vascular plants and 2 lichens, and net above-ground primary production  80  Table 2.6. Comparison of estimates of net above-ground primary production in plant communities at Pearce Point, N.W.T., with estimates for similar communities at Canadian arctic sites where lemmings are known to undergo substantial fluctuations in density  84  vu’ Table 2.7. Mean changes in standing crop (% cover) from August 1990 to August 1991 for three collared lemming foods under four different fertilization treatments  85  Table 2.8. Two-way analysis of variance investigating the effects of herbivore exclosure and fertilization treatments on variance in mean change in standing crop (% cover) of live Drvas integrifolia from August 1990 to August 1991  86  Table 2.9. Mean changes in percent cover of two collared lemming food groups on paired one hectare control and fertilized plots in two heath communities  87  Table 2.10. Absolute abundance of Dryas integrifolia (% cover) at three radii from maternal burrows of three females at parturition  89  Table 3.1. Numbers of females on study grids in late summer (end of August) and in early summer (early June)  110  Table 3.2. Instantaneous weekly rates of change of microtines, microtine nest densities, and nest occupancy by ermine  112  Table 3.3. The association of microtine winter nests with remnant winter snow.  .  .  115  Table 3.4. Mean ( S.F.) instantaneous weekly rates of population change (r) from late August to early June for Dicrostonyx, combined with three indices of thermal stress which might effect r  122  Table 4.1. Numbers of confirmed predation mortalities of radio-collared adult collared lemmings attributable to individual predator species  147  Table 4.2. Numbers of raptor pairs establishing breeding territories, numbers of nests successful and young fledged, and numbers of adult and weaned juvenile mammalian predators, in relation to mean adult Dicrostonyx density (#/ha) and combined mean adult Dicrostonyx and Microtus densities (#/ha) in spring (early June) and summer (early July) on three study grids  149  Table 4.3. The linear regressions of live body weight (g) of Dicrostonyx (dependent variable) on lengths (cm) of mandible, ulna, and upper and lower molar tooth rows, and from weight (g) of hair  153  Table 4.4. Percent frequency of occurrence of all prey remains in red fox scats. Table 4.5. Mean ± S.E. biomass (g) per scat for red fox, and percent of total biomass of principal prey groups in summers 1990 and 1992  .  .  156 159  ix Table 4.6. Mean (± S.E.) biomass (g) per scat for red fox and percent of total biomass of principal prey groups in summer 1991  161  Table 4.7. Adult and juvenile red fox defecation rates (scats/d) and biomass consumption rates (g/d) converted to per capita consumption rate of adult and subadult Dicrostonyx, and total numbers of Dicrostonyx killed per summer (a) 1990 and 1992, and (b) 1991  165  Table 4.8. Summary of conditions and results of the captive feeding experiment with a rough-legged hawk, including proportion of lemmings recovered in pellets, and pellet casting rate  174  Table 4.9. Percent frequency of occurrence of remains in rough-legged hawk pellets  175  Table 4.10. Conversion of Dicrostonyx remains in rough-legged hawk pellets to consumption rates of individual lemmings and lemming biomass (g/d) by adult hawks  176  Table 4.11. Percent frequency of occurrence of all items in peregrine falcon pellets  182  Table 4.12. Percent frequency of occurrence of all items in pellets of gyrfalcons, gulls and golden eagles Table 4.13. Mean (S.D.) number of individual lemming remains per pellet, for avian predators other than rough-legged hawks  186  Table 5.1. Summary of data collected by the Canadian Arctic Wild Life Enquiry, concerning relative stability in lemming abundance, for 1935 to 1949, in eleven regions of the Canadian arctic  201  Table 5.2. Summary of factors which are sufficient to limit lemming population growth at low densities, and those that are necessary to curtail irruptive population growth  208  Table 5.3. Presence (Y) or absence (N) of lemming predators as summer breeders at sites where lemmings have been intensively studied  213  x LIST OF FIGURES Fig. 1.1. Jolly-Seber estimates of collared lemming densities in the predator exclosure (PE) and three control grids (Cl, C2 and C3)  23  Fig. 1.2. Jolly-Seber estimates of collared lemming density, and the 95% confidence intervals around these estimates, on the predator exclosure (PE) and three control grids (Cl, C2 and C3)  26  Fig. 1.3. Kaplan-Meier survivorship functions for collared lemmings in the predator exclosure (PB) and on two control grids (Cl and C2) during summer 1990  33  Fig. 1.4. Kaplan-Meier survivorship functions for collared lemmings in the predator exclosure (PE) and on two control grids (Cl and C2) during summer 1991  35  Fig. 1.5. Jolly-Seber estimates of tundra vole densities  41  Fig. 2.1. The relationship between percent of adult lemmings killed during the summer and adult lemming density in spring for two populations: Cl (triangles) and C2 (stars) from 1988 to 1992  60  Fig. 2.2. The relationship between percent of resident adult lemmings killed within a two-week period and lemming density  63  Fig. 2.3. The relationship between litter size and female weight post partum as observed in a predator exciosure (squares) and on control grids (stars). Fig. 2.4. The relationship between total growth rate of litters and female weights post partum as observed in a predator exclosure (squares), a predator exclosure with fertilization (triangles) and control grids (stars).  .  .  .  .  .  66  71  Fig. 2.5. The relationship between mean per capita neonatal growth rate on a litter by litter basis and female weight postpartum as observed in a predator exclosure (squares), a predator exdosure with fertilization (triangles) and control grids (stars)  73  Fig. 2.6. The relationship between growth rate of juvenile lemmings and their body weights  75  Fig. 3.1. Map of the distribution of winter nests (dark points) with respect to distribution of remnant snow in late May (hachured line) on PB grid, spring 1991  116  xi Fig. 3.2. Profiles of mean weekly snow depth (cm) over the nine month periods for winters 1987 through 1990. Data were collected at Clinton Point, approximately 65 km east of the study area  118  Fig. 3.3. Profiles of mean weekly snow depth (cm) over the nine month period for winters 1990 through 1992. Data were collected at Clinton Point  120  Fig. 3.4. Relationship between instantaneous weekly rate of population change overwinter and the average of mean daily temperatures (°C) during the autumn (September and October) when Dicrostonyx are changing from summer to winter morphology  123  Fig. 4.1. Mean densities (numbers/ha) of resident collared lemmings (solid line) and tundra voles (broken line) on the three study grids  145  Fig. 4.2. Frequency distributions (percent) of maximum diameters of red fox scats collected at (a) the natal den from 29 May to 6 July 1991 (n=83), (b) the natal den from 7-20 July 1991 (n=47), (c) the natal den in August 1991 (n=58), and (d) away from the natal den in June and early July 1991 (n=23)  154  Fig. 4.3. Functional response of adult foxes to adult lemming density  171  Fig. 4.4. Functional response of adult rough-legged hawks to adult lemming density  180  Fig. 5.1. Map illustrating jurisdictions with arctic tundra (a, Alaska; Y, Yukon; N, Northwest Territories; Q, Quebec; L, Labrador), the eleven regions (numbers) summarized by the Arctic Wild Life Enquiry (Chitty 1950), and, in northern Alaska, the division (dotted line) between the coastal plain and the foothills (after Hartman and Johnson 1984)  202  Fig. 5.2. Ranges of (a) red fox (Vulpes vulpes), and (b) arctic fox (Alopex lagopus), in northern North America (from Banfield (1974) and Hall (1981))  217  Fig. 5.3, Ranges in arctic North America of two lemming species complexes, (a) Lemmus , and (b) Dicrostonyx , and ranges of four rodent species potentially sympatric with lemmings, and acting as potential alternate food for red fox: (c) arctic ground squirrel, (d) tundra red-backed vole, (e) tundra vole, and (I) singing vole Fig. 5.4. Map of isohyets (dotted lines) of mean total annual snowfall (cm) in arctic North America  221  225  xii ACKNOWLEDGEMENT  It is very inaccurate to call this thesis mine alone. Without the intellectual, emotional and logistic support of many others, it would not exist. The lemming study at Pearce Point was started by Charley Krebs, Rudy Boonstra and Alice Kenney. I owe a great deal to their willingness to accept me, inexperienced in small mammal biology, into the team. Without their encouragement and groundwork, in developing study techniques and relevant ideas, this research would not have been possible. Charley and Alice also gathered a great deal of the data in all three field seasons, and Alice analysed the remote sensing data. Able and dedicated field assistance was also provided by Carita Bergman, Maria Leung, Xavier Lambin, Beth Scott, Nicholas Williams, Jason Ruben, Chris Ruben, Marcus Ruben and Joe Ruben. Nicholas Williams ably tackled population estimation of ground squirrels. Thanks to Michele Cherry, Shannon Beglaw, Sand Russell and Anna Reid for patient and exacting assistance in the laboratory. Members of my supervisory committee, Tony Sinclair, Jamie Smith, Dolph Schiuter and Fred Bunnell, frequently challenged my thinking, and helped focus my efforts. Many other colleagues were equally stimulating and encouraging; special thanks to Christoph Rohner, David Hik, Dennis Chitty, Erkki Korpimaki, Nic Larter, Fritz Mueller, Per-Olof Palm and Erik Lindstrom. The Hunters and Trappers Committee of Paulatuk gave me permission to study lemmings on Inuvialuit land. Thanks to the Committee members, particularly Peter Green, Noel Green and Tony Green, for their interest in the research. The research would not have been possible without the logistic support of: Irene Wingate and Dick Cannings of the Zoology Department at U.B.C.; Gary White and Les Kutny of the Inuvik Research Laboratory, Science Institute of the Northwest Territories; Bruce McLean, Chris Shank, Derek Melton and Paul Fraser of the Wildlife Management Division, Renewable Resources, Government of the Northwest Territories; and the Tuktoyaktuk staff of the Polar Continental Shelf Project, Energy Mines and Resources Canada. Thanks to Bev Day and coworkers at the Orphaned Wildlife Rehabilitation facility (OWL) in Delta, B.C., for their enthusiastic cooperation in the rough-legged hawk feeding experiment. Thanks to Dr. Nic Larter, Renewable Resources, Government of the N.W.T., Inuvik, for providing lemming carcasses used in some analyses. Funding was provided by National Science and Engineering Research Council (NSERC) of Canada operating grants to C.J.Krebs, Canadian Wildlife Service University Research Support Fund grants, and Department of Indian and Northern Affairs Northern Scientific Training Grants. I was supported by University of British Columbia Graduate Fellowships, the Anne Valleé Memorial Scholarship U991), and the Arctic Institute of North America Jennifer Robinson Scholarship (1992). My wife, Maria Leung, provided perpetual love and encouragement throughout this undertaking. Likewise my parents, Ian and Barbara Reid, and my sister, Anna Reid, gave fully of their love and support. Thanks. I remain grateful to the lemmings themselves, and the other creatures on the arctic tundra at Pearce Point, all of whom offered me wonderful insights into their lives.  1 INTRODUCTION  Ecologists have expended a great deal of effort in attempts to document and explain the population dynamics of microtine rodents. The central focus of this effort has been the periodic irruptions or tt t in the abundance of many vole and cycles’ lemming species (Elton 1942, Krebs and Myers 1974, Taitt and Krebs 1985, Stenseth and Ims 1993). Cycles are multiannual patterns of change in abundance or density characterized by four phases: a low density phase lasting at least one and often two or three years, an increase phase of rapid population growth generally within one year, a peak phase with high densities at least ten times the low and generally lasting less than a year, and a decrease phase of variable duration leading back to a low (Krebs and Myers 1974, Taitt and Krebs 1985). Cycles are not ubiquitous. These rodents exhibit a variety of dynamics within and between species, ranging from multiannual patterns of varying period and amplitude, to relatively constant densities with annual fluctuations of small magnitude (Taitt and Krebs 1985, Hansson and Henttonen 1985). Two themes are evident in the history of this scientific investigation of microtine population dynamics. First, there has been a persistent debate between those searching for a single ecological factor both sufficient and necessary to explain the entire cyclic dynamic, and those who hold that multiple factors must be invoked, perhaps individually or in combination, at various stages of the population fluctuation (Taitt and Krebs 1985, Lidicker 1988). Second, there has been a recurring difference in orientation between those who investigate extrinsic factors (e.g., predation, food, weather), and those who investigate intrinsic factors (e.g., social  2 behaviour, physiological stress, age-structure) (Chitty 1960, Caughley and Krebs 1973, Stenseth and Ims 1993). Collared lemmings (Dicrostonyx spp.) are microtine rodents, considered to be a holarctic species complex. Various populations apparently survived the Pleistocene glaciations in different refugia, and subsequently colonized most arctic tundra regions (Macpherson 1965, Jarrell and Fredga 1993). Collared and brown lemmings (Lemmus spp.) were subjects of one of the first scientific investigations of cyclic patterns in rodent dynamics (Elton 1942). Because of their dramatic density fluctuations they captured the attention of other research efforts (Krebs 1964, Fuller et a!. 1975a,b, Batzli et a!. 1980). However, even early investigations suggested that lemmings did not undergo multiannual density fluctuations in all regions (Chitty and Nicholson 1942, Chitty 1950). At Pearce Point, Northwest Territories, Canada, within one of the regions of more constant dynamics, collared lemming densities fluctuate annually within a small range which is typical of low densities in cyclic situations (Krebs et a!. 1995). This thesis is a more detailed, and partly experimental, investigation of factors limiting collared lemmings to low densities at Pearce Point. I do not directly address the two debates mentioned above. However, I implicitly follow a multiple, extrinsic factor approach, if not in experimental design, at least in the focus of investigation. I believe this is desirable for a number of reasons. First, population regulation is best demonstrated by investigating all potential limiting factors to discover which one(s) are necessary to curtail population growth (Krebs 1995). Second, different patterns of population fluctuation exhibited by collared lemmings in different portions of their  3 range, suggest that different limiting factors operate either geographically, or temporally within populations (cf. Hansson 1987). Third, lemmings live in a seasonal environment with major changes in predator community and food availability between seasons. Different limiting factors are therefore likely to operate seasonally. Fourth, theory (e.g., McNamara and Houston 1987), and field experiments (Taitt and Krebs 1983, Desy and Batzli 1989), indicate that two key factors, predation mortality and food availability, can have interactive effects on population dynamics. Fifth, a true cycle, though sufficiently described in theory by one driving variable with time lag (May 1976), does not adequately describe empirical patterns of population change. Instead, these patterns seem better described as having two relatively quick changes in dynamics: the initiation of increase from a low, and the initiation of decrease from a peak. I interpret this as an escape from one set of limiting factor(s) in the low, and the exposure to a potentially different set of limiting factor(s) at the peak. This is a study of factors limiting collared lemming population growth at low densities. Peak populations irrupt from such low densities, and a preliminary assessment of a non-cyclic situation indicates fairly constant low densities (Krebs et a!. 1995). This implies that irruptive situations consistently differ from non-irruptive situations in the changing action through time of one or a few ecological factors limiting population growth at low densities. This is largely a study of the limiting effect of predation on population growth. The role of predation in both cyclic and non-cyclic situations deserves attention. Field studies on cyclic lemmings demonstrate a strong limiting effect of predation mortality, at least at the beginning of a low phase (Pitelka et al. 1955, Maher 1970,  4 MacLean et al. 1974). Lemmings in the low phase of a cycle continue to breed, and therefore have high potential rates of population increase, but this increase is not immediately realized (Krebs 1964). This is the case at Pearce Point, where lemmings also suffer high rates of summer predation mortality (Krebs et a!. 1995). Therefore, predation is strongly implicated as the principal limiting factor at low densities. This thesis contains the following five chapters:  1. Limitation of collared lemming population growth by predation mortality. This is an experimental test of the hypothesis that predation mortality is sufficient and necessary to limit collared lemmings at low density at Pearce Point.  2. Do predators regulate lemmings at low densities in summer? This chapter addresses predation mortality within two paradigms of population regulation, the density-dependent and mechanistic paradigms (Sinclair 1989, Krebs 1995). It includes an experimental and comparative investigation of the potential operation of alternate limiting factors (food availability, reproductive inhibition and predation risk) on lemming population growth at low density in summer.  3. Possible factors limiting winter population growth in collared lemmings. This chapter uses correlation and regression analyses to evaluate the role of ermine predation, autumn temperatures, and winter and spring snow depths, as factors explaining variance in overwinter rates of population change.  4. Patterns of predation on non-cyclic lemmings: the generalist predator hypothesis. This chapter uses the generalist predator model, which attempts to explain relative stability in prey densities, as a hypothesis to investigate patterns of summer predation by the predator community at Pearce Point. It includes assessment of the  5 predators’ numerical and functional responses, and changes in their diets with changing lemming density.  5. Why don’t all lemming populations irrupt ? This chapter develops alternative hypotheses suggesting why some North American lemming populations irrupt and others do not. It includes summaries of geographical patterns in irruptions, our knowledge of factors necessary to curtail lemming population growth, and our knowledge of the distribution of predator and prey species in arctic tundra.  6 CHAPTER 1 LIMITATION OF COLLARED LEMMING POPULATION GROWTH AT LOW DENSITIES BY PREDATION MORTALITY INTRODUCTION  In many regions of arctic North America collared lemmings of the genus  Dicrostonyx exhibit substantial, and often cyclic, multi-annual population fluctuations. These have been reported for D. hudsonius in Ungava (Elton 1942), D. richardsoni in northern Manitoba (Shelford 1943; Scott 1993) and Eskimo Point (Mallory et a!. 1981), and D. groenlandicus near Baker Lake (Krebs 1964), near Igloolik (Rodgers and Lewis 1986), on Devon Island (Fuller et al. 1975b), and on the Alaskan north slope (Batzli et a!. 1980).  Ecological factors causing cyclic population changes have not been experimentally investigated for Dicrostonyx, but hypotheses cover the full spectrum of explanations for microtine cycles (Taitt and Krebs 1985; Stenseth and Ims 1993). High densities of Dicrostonyx, often in synchrony with brown lemmings (Lemmus trimucronatus), are generally followed by strong numerical responses of arctic (Alopex lagopus) and red fox (Vulpes vulpes) (Elton 1942; Macpherson 1969), ermine (Mustela erminea) (Krebs 1964: MacLean et a!. 1974) and a number of avian predators (Pitelka et a!. 1955; Watson 1957; Maher 1970). Predation by nomadic avian and mammalian predators may synchronize lemming declines over broad geographical regions (Ydenberg 1987; Ims and Steen 1990). Enhanced breeding success by these predators, when lemmings are numerous, increases their numerical response (Watson 1957; Macpherson 1969), and is hypothesized to intensify the depth of the decline in  7 lemming densities and prolong the phase of low density (one or two years) through strong limitation on population growth (Pitelka et a!. 1955; Maher 1967, 1970; MacLean et a!. 1974). Similar explanations for the population dynamics of other microtine rodents during the decline and low phase of periodic irruptions have been provided by other studies in North America (Pearson, 1966, 1971; Fitzgerald 1977), and Europe (Hansson 1984a; Henttonen 1985; Henttonen et a!. 1987; Korpimaki et a!. 1991). Limitation by predation mortality is assumed to wane, as predators decline with increasingly scarce prey densities, and eventually be insufficient to limit exponential prey population growth. The first detailed study of D. kilangmiutak, at Pearce Point, on the mainland of the western Northwest Territories, Canada, revealed persistent low densities (less than three per hectare) over three consecutive years, and frequent declines in summer populations (Krebs et a!. 1995). Populations often recovered with winter breeding, as previously observed by Krebs (1964) and Fuller et al. (1975a). Predation was the proximate cause of at least 66% of summer mortalities in 1988, and 79% in 1989, leading Krebs et a!. (1995) to hypothesize that predation mortality was the most likely factor limiting summer population growth. This chapter reports an experimental investigation of the hypothesis that predation mortality is sufficient and necessary to limit collared lemmings (D. kilangmiutak) to low densities at Pearce Point. I tested four predictions of the predation mortality hypothesis: (i) predation is the proximate cause of the great majority of mortalities, (ii) predator removal decreases mortality (predation is not replaced by another source of mortality in a compensatory fashion) and therefore  8 increases survival, (iii) predator removal enhances rates of population change, (iv) predator removal enhances recruitment. I also report demographic data on the tundra vole (Microtus oeconornus), the only other common microtine rodent in the area, to look for possible patterns shared with lemmings. METHOD S  Study area The study area (40 km ) was the vicinity of Pearce Point (69°48’N, 122°40’W), 2 on the south shore of Amundsen Gulf, western mainland Northwest Territories, Canada. The bedrock of dolomites and limestones, interrupted by dikes of basalt, is frequently exposed in cuffed hills rising to 130 m a.s.l.. Surficial geology has been influenced by Pleistocene glacial scouring and deposition, and by movement of wind blown sands in the delta of a local river, draining the Melville Hills to the south.  Population density Four areas of tundra, each 18 to 25 ha and each including a range of available microtine habitats, were chosen for study grids. Each was fairly discrete, being bordered in part by rocky outcrops or water courses, but partly linked to other areas by continuous similar habitats. Vegetation communities were primarily upland heath  (Dryas integrifolia / Carex rupestris / Salix arctica) and mesic hummock (Carex membranacea / Dryas integrifolia / mosses), and also included some ribbon-like wet meadow (Carex aquatilis) bordering water bodies (Table 1J). Collared lemmings occupied drier habitats, and tundra voles occupied the wetter communities on this spectrum (Bergman and Krebs 1993). On each area a grid of reference stakes was surveyed, and all microtine  9 burrows were marked. I quantified the population densities of microtines by livetrapping every one or two weeks from early June (end of snow-melt) to late August (first snow-fall) of 1990, 1991 and 1992, using Longworth live traps, and markrecapture with ear tags. I used the Jolly-Seber open model for population estimation. In early spring, open traps (c. 60/grid) and nest boxes (c. 12/grid) left over winter were the best places to find microtines, as most burrows were flooded. For an initial trapping session, and alternate ones thereafter, microscope slides covered in talcum powder were placed in all burrow mouths, and examined 18-24 h later for presence of microtine tracks indicating active burrows (Boonstra et at. 1992). The trapping session then involved immediately setting traps at these active burrows in the morning, and checking them in the afternoon and again in the evening, when they were locked open. At alternate sessions, I used trap locations chosen by tracks on slides the previous session. To assess how representative study grids were of regional population patterns, I counted active microtine burrows in one-hectare quadrats located randomly through the study area, both on study grids and elsewhere, in early August 1990. Juveniles were rarely caught more than once. Consequently, density estimates are based on residents alone, defined as adults plus those few juveniles caught at least twice on the same grid. For each capture, location, weight and reproductive condition (males scrotal or abdominal; females  -  -  testes  vagina perforate or non-perforate, lactating or non  lactating, pubic symphysis closed, partly open or open) were recorded.  10 Table 1.1. Characteristics of the predator exciosure (PB) and three control (Cl, C2 & C3) study grids.  PE  Cl  C2  C3  Dryas heath  55.2  65.6  67.1  83.7  Carex-Dryas hummock  39.6  16.1  22.2  9.0  Carex marsh  1.0  0  1.4  0.4  Unvegetated  4.3  18.3  9.3  6.9  8  3  3  Surface cover (%)  Elevation range (m)  25  Distance (m) to Natal fox den Rough-legged hawk nest  4000  3200  2800  1400  200  50  600  2400  11  Mortality and litter fates Adult Dicrostonyx were fitted with radiotransmitters (Biotrack Inc., model SS-1) mounted to cable ties as neck collars. Radio and harness weighed approximately 3 g. Individuals were relocated every two or three days on grids, or by extensive searching throughout the study area. This allowed estimation of the date of death to within two or three days. Radios frequently led to microtine carcasses, remains, or merely the radios in dens or nests of predators. Cause of death was classified by autopsy on carcasses, or by assessment of lemming remains and disturbance at burrows. The Jolly-Seber model was used to estimate survival rates. I also used the Kaplan-Meier procedure for survivorship estimation of radiocollared lemmings, with staggered entry of individuals during the course of the summer, and progressive censoring due to radio failure or survival to the end of the study period (Pollock et al. 1989). To test the possibility that radio packages compromised survival, I followed densities on one of the four grids in 1991 (Control #3) without using any radiocollars. The numbers of litters born, and their fates, were assessed indirectly, by monitoring female reproductive condition at least weekly to estimate date of parturition, along with records of her movements and burrow use. Lactating female  Dicrostonyx typically use one maternal burrow (Brooks 1993; unpubi. data this study), and juveniles are weaned at 15 to 20 d (Brooks and Banks 1973). Termination of lactation, and extensive movements away from a natal burrow prior to the expected weaning date, were taken as a failure to wean the litter. To assess potential causes of litter mortality, I monitored natal burrows at each radiotelemetry check for evidence  12 of flooding or excavation by predators. In 1992 data on juvenile survival and movements immediately after weaning were gathered using miniature radios (weight 1 g; AVM Inc., model SM-i) glued to a small patch of shaved skin on the animal’s back. Radio life was 10-14 days, but radios stayed on those lemmings which were not killed, only for an average 7.3 d (S.E. 0.83, n  =  7).  Predator exciosure One of the four populations (grids) was chosen for a predator exclosure treatment (referred to as PE) to test some of the predictions experimentally. This treatment covered 11.4 ha of an 18-ha grid. Border fence posts were erected in autumn 1989. In June 1990 a covering, approximately 2 m above ground, was erected to exclude avian predators. This consisted of a lattice of 0.6-cm diameter nylon rope, suspended from iron poles 20 m apart. This lattice supported parallel lines, 0.7 m apart, of monofilament nylon fishing line (14 kg test strength) tightly strung between the lines of rope. In late June 1990, a fence of 2.5-cm mesh chicken wire fencing was erected around the periphery of the exciosure. This fence stood 1.5 m above ground,  with a ground-level apron of 0.3 m either dug into the ground or covered with mud and rocks. The construction successfully lasted three summers and the two intervening winters, with minor repairs. Mesh size was large enough for microtines to pass through, and they frequently did so. I live-trapped daily for arctic ground squirrels (Spermophilus parryii) and ermine, which were taken one to eight kilometres away and released. Sign in  13 spring indicated that fox and ermine entered the exciosure in winter.  Predator populations Notes were made of raptors prospecting for nest sites in spring, along with their degree of territorial defence. A thorough search of all cliffs within the 40 km 2 area in June gave a complete enumeration of breeding pairs initiating incubation, and their clutch sizes. However, I could not reach nests of glaucous gulls (Larus hyperboreus), Thayer’s gulls (Larus thayeri), and common ravens (Corvus corax) on inaccessible cliffs. Breeding success was quantified by visiting nests in early July to enumerate numbers of young chicks, and in mid-August to count young just before or at fledging. I visited known fox dens biweekly to collect scats, and note pelage and size of all foxes observed. This allowed identification of individual foxes based on colour patterns, a count of juveniles, and an estimate of whether or not young were weaned. Estimates of ermine activity were based on casual observations, incidental livetrapping and characteristically eaten microtine carcasses, but an ermine population estimate was not attempted. In 1991 and 1992 numbers of arctic ground squirrels were indexed by placing microscope slides covered in talcum powder in a fixed sample of burrow mouths and counting the proportion marked within 24 hours. In 1992 all ground squirrels were counted on three, adjacent, one-square-kilometre areas using live-trapping (Tomahawk traps) at all burrows, coloured ear-tagging, radiocollaring, and periodic observations of the areas. Grizzly bear (lJrsus arctos) activity was based on tracks and casual observations.  14  Statistics The predator exciosure treatment was not replicated in any one year. To test for significant deviation of the population parameters in the exciosure from those of the three concurrent control populations, I used the modification of the Student-t test comparing a single observation with the mean of a sample (Sokal and Rohif 1981:231). RESULTS  Characteristics of study grids Hummock vegetation was most abundant on PE, and least abundant on C3, but Dryas heath showed the reverse pattern (Table 1.1). The hummock gave more protective cover but had a lower density of Dryas food than the heath, so the consequences of this gradient are unclear. C3 was considerably farther than other grids from a rough-legged hawk nest, but was the closest to the natal fox den (Table 1.1). CI probably received more intensive raptor surveillance with its proximity to a rough-legged hawk nest.  Predator community The predator community varied little between 1990 and 1991, but changed markedly in 1992 when rough-legged hawks did not breed, and red fox breeding failed, followed by disappearance of two of three known adults (Table 1.2). In spring 1992, the carcasses of three other red foxes were found. They had died during the 1991-92 winter, probably from starvation judging by the poor quality of their bone marrow.  15 Table 1.2. Numbers and breeding success of the principal lemming predators in the study area.  Number of territorial pairs  Avian predator  1990  1991  1992  Rough-legged hawk  4  6  Peregrine falcon  5  Golden eagle Gyrfalcon  Number of nests successful (fledglings)  1990  1991  0  2 (3)  3 (5)  0  5  6  5(10)  2 (2)  4(10)  1  1  1  1 (1)  1. (1)  1 (2)  0  0  1  0  0  1 (2)  Number of  Number of young  adults  Mammalian predator  1992  weaned  1990  1991  1992  1990  1.991  1992  Redfox  2  3  3tol  3  2  0  Ermine  ?  ?  ?  >1  >3  >2  Grizzly bear  1  1  2  0  0  0  16 Eleven resident ground squirrels occupied 3 2 km prior to the emergence of young in 1992. The proportion of slides marked in squirrel burrows in four sample areas within 24 h in late July declined by 55% from 0.38 (S.E. 0.12) in 1991 to 0.17 (S.E. 0.06) in 1992.  Predation mortality adults -  Predation was the dominant proximate cause of death of radiocollared adult lemmings in summer, accounting for between 33 and 73% of mortalities on control grids (Table 1.3). These are probably underestimates as the fate of 4 to 24% of lemmings and voles remained unknown (Table 1.3). Rough-legged hawks and red foxes were the dominant predators in 1990 and 1991 (Table 1.3). Predation pressure was much reduced in 1992 because rough-legged hawks were absent and foxes scarce. Grizzly bears were occasional visitors in all years, but excavated lemmings on study grids only in 1991. Ground squirrels were persistent but infrequent predators. Ermine were not observed on the study grids except in late 1992, when juvenile ermine killed juvenile lemmings in PE (Table 1.4). Ermine depredated a mean of 7.6% (S.E. 0.96) of microtine winter nests on the four study grids in winter 1990-91, and 5.3% (S.E. 2.99) in winter 1991-92. The predator exciosure did not exclude all predation (Table 1.3). Rough-legged hawks killed lemmings when the nylon was in poor repair or depressed by snow. Ground squirrels dug under the fence, and a grizzly bear got in over the fence. Foxes were excluded. In 1990, 16 of 23 (70%) predation deaths inside the exclosure occurred before it had been completely constructed, and the proportion of lemmings lost to predators did not differ between controls (0.58) and PE (0.58)  39 (58) 13 (19) 7 0 6 21(31) 21  All raptors  Rough-legged Hawk  Peregrine Falcon  Unidentified raptor  All mammals  RedFox  44 (66)  67  All predators  Total dying  Total radioed  C  1990  8  10 (25)  4  1  8  13 (33)  23 (58)  24 (60)  40  PE*  5  9 (17)  7  1  17  25 (48)  38 (73)  40 (77)  52  C  1991  0  6 (24)  1  0  4  5 (20)  11(44)  12 (48)  25  PE  0  0 (0)  1  0  0  1 (17)  2 (33)  2 (33)  6  C  1992  0  0 (0)  0  0  0  0 (0)  0 (0)  1 (9)  11  PB  Table 1.3. Fates of resident adult lemmings on control grids (C) with predator access, and in the predator exciosure (PB), during summers of 1990, 1991 and 1992, based on telemetry. Percentages in parentheses.  6  Survived  ( 0) 12 (48)  0  ( 0)  ( 0)  ( 0) 3 (50)  0  1 (17)  0  0  ( 9)  ( 9)  7 (64)  2 (18)  1  1.  0  0  0  0  0  PE  Survived is the number of individuals still alive at the end of the summer.  5 (10)  ( 0)  ( 4)  ( 4)  ( 0)  1 (17)  0  0  0  C  **  11(28)  0  1  1  0  0  2  0  4  PE  1992  Raptors killed 11, and mammals 5, lemmings before PE completed. Seven (18%) predation deaths were in PE.  ( 9)  0  7 (14)  1 ( 2)  1 (2)  4 (8)  2  0  2  C  1991  *  **  1  ( 0)  1 ( 3)  ( 2)  ( 2)  0  ( 6)  5 (13)  0  2  0  0  PE*  ( 7)  1990  16 (24)  Dispersed  Unknown fate  1  5  Unknown pred.  Accidental death  0  Ground Squirrel  4  0  Ermine  Natural death  0  C  Grizzly Bear  Table 1.3. (continued)  Co  19 (Chi-square  =  0.005, df  =  1, P  =  0.943) (Table 1.3). However, by the end of the  summer, the proportion of lemmings still alive was significantly higher in PE (0.28) than on controls (0.09) (Chi-square  =  6.446, df  =  1, P  =  0.011).  In 1991, the proportion of lemmings killed was significantly lower in PE (0.44) than on controls (0.73) (CM-square  =  6.168, df  =  1, P  =  0.013), and a significantly  higher proportion was alive at the end of the summer in PE (0.48) than on controls (0.10) (Chi-square  =  14.459, df  =  1, P  <  0.001) (Table 1.3).  In 1992, lemming densities were lower than in 1990 and 1991 (Figure 1.1), and predator densities declined (Table 1.2). The proportion of lemmings killed on controls, and in the exciosure, decreased compared with previous years, but sample sizes were too small for statistical tests (Table 1.3).  Predation mortality subadu its -  Predation was the predominant proximate cause of death of lemming litters on all grids; I lacked data on fates of vole litters (Table 1.4). Predators killed litters directly, by entering or excavating burrows, or indirectly, by killing the lactating female. Direct and indirect predation on controls accounted for the loss of 37% of litters in 1990, 52% in 1991 and 14% in 1992. The proportion of litters lost to predators in PE was substantially less than that on controls in all three years (Table 1.4). The proportion of litters successfully weaned in PE in 1990 was higher than on controls, but not significantly so (Chi-square  =  2.368, df  =  1, P  df  =  0.013). The effect of the exciosure appeared weaker in 1992 with a higher  =  1, P  =  0.124). The difference was significant in 1991 (Chi-square  =  6.139,  0  Infanticide  1 (3)  8 (23)  1. (3)  cause  Unknown  Predation  Storm  -  Mother died  -  14 (40)  Weaned  Lost  35  C  Initiated  Number of litters  1990  0  0  0  1 (7)  9 (64)  14  PE  1 (4)  0  1 (4)  8 (35)  7 (30)  23  C  1991  2 (5)  3 (8)  0  0  24 (63)  38  PE  0  0  0  0  4 (57)  7  C  1992  0  0  0  0  6 (75)  8  PE  Table 1.4. Fates of lemming litters initiated on control areas (C) and predator exclosure (PE) in each summer study period. Percentages in parentheses.  t%Z C  0 0  Ground squirrel  Ermine 6 (17)  0  Bear  5 (14) 5 (14)  Total  C  Fox  -  Unknown fate  -  -  -  -  Predation  Number of litters  Table 1.4. (continued) 1990  3 (21)  0  0  0  1. (7)  1. (7)  PE  2 (9)  0  0  1 (4)  3 (13)  4 (17)  C  1991  4 (11)  0  1 (3)  4 (11)  0  5 (13)  PE  2 (29)  0  1 (14)  0  0  1 (14)  C  1992  0  2 (25)  0  0  0  2 (25)  PE  FL  22 proportion of control litters successfully weaned, but sample sizes were too small for statistical testing. Other known causes of litter mortality included rain storms flooding burrows, thereby forcing mothers to bring neo-nates above ground, and infanticide as evidenced by incisor wounds and partial consumption of the body, starting with the cranium. I have few data on fate of lemmings from weaning to sexually active adult size. In 1992, when predator densities were relatively low, seven of fifteen weanlings radioed in the exclosure were killed by predators before their radios fell off. Six of the seven, representing three different litters, were killed by ermine at or close to the natal burrows. The seventh was killed by a raptor well outside the exclosure.  Predator exclusion  -  density  The density of Dicrostonyx in PE remained relatively high during summers 1990 and 1991, and diverged from the rapidly declining densities on controls (Fig. 1.1). The null hypothesis that lemming density in PE was not larger than the mean of control densities holds for estimates at the beginning of summers 1990 and 1991, but can be rejected for estimates at the end of the two summers (Table 1.5). By late summer PE densities were significantly higher than the mean of control densities (Fig. 1.2). The instantaneous weekly rate of population change over the summer period was higher in FE compared with the mean of controls in both 1990 and 1991, but not significantly so (1990: t 0.10 <P  <  0.20) (Table 1.6).  =  1.46, df  =  2, 0.10  <  P  <  0.20; 1991: t  =  1.69, df  =  2,  23  Fig. Li. Jolly-Seber estimates of collared lemming densities in the predator exclosure (PE) and three control grids (Ci, C2 and C3) over the three summer study periods. Densities in winter (shaded bars) are interpolated and exact temporal patterns are unknown. Vertical arrows indicate weeks when density comparisons in Table 1.5 were made.  0  >  UD  ci)  ci)  cm  ci)  (ID C  >  C,  june july aug  july  aug  Time (weeks)  june  june  july  aug  25 Table 1.5. Tests of the null hypothesis that the Dicrostonyx density in the predator exclosure was not larger than the mean of sample estimates from control grids (d.f. = 2 in all cases; one-tailed test)  1990  Beginning  *  t  of summer  End  *  of summer  *  Weeks  0.85  =  0.40  <  P  t  =  4.39  P  for  1991  <  which  <  t 0.50  0.05  0.05  comparisons  1992  1.97  =  <  P  =  8.86  t P  <  <  t  0.10  were  P  t  0.02  0.02  <  =  P  made  9.15  =  7.68  <  are  0.02  indicated  on  Fig.  1.1.  26  Fig. 1.2. Jolly-Seber estimates of collared lemming density, and the 95% confidence intervals around these estimates, on the predator exclosure (PE) and three control grids (Cl, C2 and C3), in mid-August 1990, and early August 1991.  27  2.2 PE 2.0 1.8 PE 1.6 vu c-  a,  1.4 1.2  -  >_10 I— (/)  zO.8 C30.6-  T  C2 C21.  0.4 02  cii. 1990  C3  clii  I 1991  28 Table 1.6. Instantaneous weekly rates of population change (r) for microtine species on the predator exclosure (PE) and three control grids (Cl, C2, and C3). N is the period in weeks over which the estimates were made. In blank cells the species was absent or at densities too low for estimation.  Dicrostonyx  Microtus  1990  1991  1992  1990  1991  1992  N=  9  10  11  9  10  11  PE  -0.03  -0.03  0.04  -  -  Cl  -0.18  -0.20  C2  -0.07  -0.11  0.10  C3  -0.19  -0.29  0.06  -  -  -0.12 -  0.12  -0.14 -  -0.05  0.13 -  0.14  29  In 1992 the situation was different. Few lemmings survived the previous winter, and two control grids had no lemmings in spring. The density in PP was significantly higher than the mean of controls both at the beginning and end of the summer (Table 1.5). In 1992 instantaneous weekly rates of population change were positive in PE and on all controls; populations were able to grow in the relative absence of predators (Table 1.6; Fig. 1.1). The mean density of active microtine burrows on control grids in August 1990 (1.0 / ha; n  =  6 quadrats) was not significantly different from the mean density on  quadrats located randomly through the study area (0.6 / ha; n Whitney U  =  =  11 quadrats) (Mann-  41.5, F> 0.10), indicating that control grids adequately represented  microtine densities in the study area.  Effect of radiocollars The Jolly estimates of average probability of survival over four weeks for resident lemmings on C3, without collars in 1991, was higher than survival of radioed residents on other controls in 1990 and 1991, but fell within or close to the 95% confidence intervals for other estimates (Table 1.7). This difference was not significant in 1991 (t  =  2.33, df  =  1, 0.20 <P  <  0.40, one-tailed test). The proportion of adults on  C3 (without collars), retrapped one and two weeks after initial capture, was slightly higher than proportions on Cl and C2 (with collars), but differences were not significant (Table 1.8). The trends in the data indicate that radiocollars slightly compromise lemming survival in the first week after receiving the collar. However, densities on C3 declined in a similar fashion to those on other control grids over the  30 Table 1.7. Jolly estimates of average probability of survival over a standard four week period for resident microtines (both sexes combined) on the predator exclosure (PE) and three control grids (Cl, C2 and C3). Extreme values of 95% confidence intervals are in brackets. N is the period in weeks over which the data were available. In blank cells the species was absent or at densities too low for estimation.  Dicrostonyx  Microtus  1990  1991  1992  1990  1991  N=  8  7  12  8  7  FE  0.62  0.66  0.79  -  -  (.47-.76)  (.51-.81)  0.33  0.25  (.19-.47)  (.05-.46)  0.35  0.34  (.19-.52)  (.17-.51)  0.25  0.47  (.00-.50)  (.30-.65)  Cl  C2  C3  (.50 -1.00) -  -  -  0.33  0.45  (.09-.57)  (.05-.96)  -  -  0.63  0.44  (.00-1.00)  (.26-.63)  31 Table 1.8. Proportion of adult lemmings retrapped after one and after two weeks following initial capture, on Cl and C2 (with radiocollars), and C3 (without radiocollars) in 1991. N is the number of individuals. Test statistic (Chi-square) tests the null hypothesis that C3 does not differ from Cl, and C3 does not differ from C2.  Proportion retrapped after  Cl (N=16)  One week  C2  C3  (N=29)  (N=28)  0.52  0.56 2 (X  =  0.084,  2 (X  =  0.468,  P  =  0.77)  P  =  0.49)  Two weeks  0.41  0.38 2 (X  =  0.121,  2 (X  =  0.013,  P  =  0.73)  P  =  0.91)  0.61  0.43  32 full course of the 1991 summer (Fig. 1.1; Table 1.6). I conclude that any negative influence of radio packages on lemming movements and survival is short-lived, and does not significantly affect summer population processes.  Predator exclusion  -  survival  The Jolly estimator of the average probability of survival over four weeks indicates that resident lemmings survived longer under the predator exclosure than on the three control grids (Table 1.7). This pattern was significant in 1990 (t = 4.803, df  =  2, P  <  0.05), but not in 1991 (t  =  2.118, df  =  2, 0.05 <P  <  0.10).  The Kaplan-Meier estimates showed no significant differences in lemming survivorship curves between PE and Cl (log-rank test statistic PE and C2 (log-rank test statistic  =  -1.499, P  =  =  -0.220, P  =  0.8), or  0.13) in 1990 (Fig. 1.3). However  survivorship in PE stabilized mid-way through July, when construction was completed, indicating that the exclosure had a strong effect when it operated (Fig. 1.3). In 1991 the Kaplan-Meier lemming survivorship curves for PE and Cl differed significantly (log-rank test statistic (log-rank test statistic  =  -3.205, P  <  =  -3.432, P  <  0.01), as did those for PE and C2  0.01)(Fig. 1.4). The exciosure enhanced  survivorship of adult resident lemmings, and survival in PE was significantly higher than either in Cl (z  =  3.09, P  <  0.01), or C2 (z  =  2.83, P <0.01), by the end of the  summer (Fig. 1.4).  Predator exclosure recruitment and population growth -  Only juveniles from the first and second summer litters would have grown large enough to be recruited as adults during the study periods. Recruits to the adult  33  Fig. 1.3. Kaplan-Meier survivorship functions for collared lemmings in the predator exclosure (PE) and on two control grids (Cl. and C2) during summer 1990.  34  w-c,’J aOO  U) L) c:1)  .QH  •  C’*J iLO CD 0 000000000  PA!AJfl J0  0  35  Fig. 1.4. Kaplan-Meier survivorship functions for collared lemmings in the predator exclosure (PB) and on two control grids (Cl and C2) during summer 1991.  CD  .  7cC C!)  Probability of Survival 000000000 I  I  I  I  I  I  ,x  ___-  _,——  -I —  /  /  / .  ..—.....  I,  I’  1’  /3.1 ( / /  t3iE  )  CX  000  9  37 populations were uncommon on all grids (Table 1.9), suggesting substantial mortality during dispersal. More juveniles recruited per pregnancy where pregnancies were few (i.e. where densities were particularly low) (Table 1.9). Perhaps open space encouraged settlement, or predation pressure diminished at very low densities. Even in these circumstances, numbers of recruits per litter were still low, and there must have been substantial mortality, or emigration of juveniles, prior to recruitment. Recruitment of lemmings to the adult population, after the weaning of the first summer litter, was significantly higher on a unit area basis in PE compared to controls in all years (Table 1.10). The origin was uncertain for 21 of 25 (84%) recruits on control grids, and 10 of 15 (67%) of recruits to PE. Two recruits to PE were known to come from Cl. Only three of 15 (20%) recruits to FE, and four of 25 (16%) recruits to controls, were caught as subadults on the same grid. These data again suggest that juveniles often disperse beyond the population scale chosen for this study. Despite improved recruitment to PE, this protected population did not grow in 1990 or 1991.  Juvenile dispersal Ten radioed juvenile lemmings were followed for a mean of 5 d after weaning (S.E. 1.13) until their radios fell off (n=6) or they were killed by a predator (n=4). All ten left the natal burrow within two days of weaning. Rates of travel were highly variable, and appeared slow in the first few days after weaning, and sped up for some individuals thereafter. Since they were followed for varying periods, data on distances travelled may be somewhat biased. However, the straight-line distances from natal burrow to last location with a radio gave a mean daily distance travelled of 53.1 (S.E. 17.6, n  =  10) m/d. Four of nine weanlings radioed inside the exclosure  38 Table 1.9. The ratio of toW adult recruits divided by total first and second litter pregnancies (raw data in parentheses) on the predator exclosure WE) and two control grids (Cl and C2).  Grid  1990  1991  PB  0.38 (5/13)  0.17 (5/29)  Cl  0.07 (1/15)  0.50 (3/6)  C2  0.29 (4/14)  0.33 (4/12)  1992  1.00 (5/5) -  a3.00 (3/0)  39 Table 1.10. Intensity of recruitment (number of recruits per hectare) on predator exclosure (PE) and three control grids (Cl, C2 and C3). Sample sizes of recruits in parentheses. Statistics are for the t-test of the null hypothesis that recruitment on PE does not exceed mean recruitment on control grids (one-tailed, d.f.= 2).  Grid  —  1990  1991  1992  PE  0.44 (5)  0.44 (5)  0.44 (5)  Cl  0.05 (1)  0.16 (3)  0  C2  0.22 (4)  0.22 (4)  0.16 (2)  C3  0.08 (2)  0.24 (6)  0.08 (2)  t  3.076  4.755  3.896  P  <0.05  <0.05  <0.05  40 had left it before their radios fell off, and all four were followed for at least five days. We gathered daily movement data for four weanlings over periods of five days or more. The mean distances between daily radiolocations for three males were 6, 51, and 126 m, and for one female, 174 m. These juveniles travelled in remarkably straight lines; the sum of daily distances travelled divided by straight-line distance from natal burrow to last location gave values of 1.39, 1.45, 1.38 and 1.20 respectively. The longest daily distance travelled was 600 m. Tundra voles Tundra voles existed in appreciable numbers on only two grids (Cl and C3), and were occasional residents on the two other grids (C2 and PB). Vole densities declined on one grid in 1990, and both grids in 1991 (Fig. 1.5), following a similar pattern to lemmings. However, they exhibited slower rates of decline than lemmings (Table 1.6), and the vole population on C3 actually increased in 1990. In 1992, both vole populations increased as did lemmings (Fig. 1.5; Table 1.6). The 1992 increase on Cl, from zero in spring, resulted from immigration of maturing adults born in the first summer litter. Winter density changes in voles were similar to those in lemmings, with population increases in 1990-91, and declines in 1991-92 (Fig. 1.5). Adult voles were radiocollared only in 1990. Seven of nine radioed adults were killed by predators (rough-legged hawk, red fox and golden eagle), and two had unknown fates. The Jolly estimator of vole survival on control grids was slightly higher than that for lemmings on the same grids (Table 1.7). However, vole survival exceeded the highest observed lemming survival only on C3 in 1990 (Table 1.7). Average  41  Fig. 1.5. Jolly-Seber estimates of tundra vole densities on two grids (Cl and C3) over the three summer study periods. Densities in winter (shaded bars) are interpolated, and exact temporal patterns are unknown.  JoHy-Seber Density (# / ha pppppppp I  ro  w  -  I  I  c,n  cn  I  C.  D CD  0*  /  UJ  —  -  Hc CD Co  rm  -L  (D< 7V tD  t  I C  CD  Co  0  C  43 probabilities of survival for adult voles without collars in 1991, were intermediate to, and not significantly different (t  =  0.22, F> 0.50) than values in 1990, with collars  (Table 1.7). DISCUSSION  Predation limitation There are various approaches for investigating whether predation mortality is a sufficient condition to limit prey population growth. Protecting a population by experimentally excluding predators, and comparing the demographic responses of protected prey with unprotected prey, is the most insightful approach (Krebs 1988), and the one followed here. With experimental reduction of the resident predators’ access to lemmings, there were significant reductions in predation mortality, and total mortality, for adult and neo-natal lemmings. Also with decreased predator access, there was a significant increase in adult lemming survival, and significantly enhanced recruitment of maturing juveniles into the adult population. Consequently, the protected population diverged significantly from control populations in its density trajectory in 1990 and 1991. Overall I confirmed three of four predictions of the hypothesis that predation mortality is sufficient to limit collared lemmings to low densities. The only prediction not satisfied was growth in the protected population. The results also indicate that predation mortality is a necessary condition for limitation of collared lemmings at low densities during summer. First, no other mortality factor compensated for the reduction of predation mortality in the protected population. Second, the virtual absence of the principal lemming predators, rough legged hawks and red foxes, in summer 1992, was, in effect, a partial regional  44 predator exclusion, and coincided with growth in all populations, in contrast to declines in other years. Remaining predators continued to keep this growth low. I do not know how much growth might occur before another limiting factor would operate, making predation mortality an unnecessary condition. The lack of population growth in PE in 1990 and 1991 requires explanation. If predation mortality is sufficient to limit lemmings to low densities, experimental removal of such limitation should result in strong population growth. Such growth would be contingent on the following conditions: (i) the experimental setup protects all population processes from predation and thereby adequately mimics regional declines or extinctions of predators; (ii) there is no other limiting factor sufficient to curtail growth at low densities; (iii) sufficient time has elapsed for theoretically expected time lags (May 1976) to pass. I doubt that each of these conditions was satisfied, and so discuss each one in detail. First, the exclosure did not keep out all predators, and was too small to encompass dispersal distances of many weanlings. Consequently potential population growth was curtailed by continued mortality of resident adults, by predation on weanlings leaving the protected area, and by predation on subadults outside the protected area which might have immigrated and been recruited to the protected population. I believe that these conditions explain the lack of growth in the exclosure. In summer 1992, with a regional decline in resident predators, two controls and PE showed limited population growth. This resulted from immigration of maturing juveniles born in early summer litters. These immigrants in turn reproduced. This suggests that a predator removal experiment of sufficiently large scale would lead to  45 population growth. Second, this is only a study of summer population processes. In winter, limiting factors other than predation mortality might operate. The higher lemming densities in PE compared with controls in spring of 1991 and 1992, indicated that PE was at least partly effective in reducing predation mortality during the preceding winters. However, overwinter rates of population change on all grids were positive in 1990-91 and negative in 1991-92, despite the fact that ermine and red fox bred in both 1990 and 1991, and the proportion of microtine nests depredated by ermine did not differ significantly between these winters (Chap. 3). Obviously predation continued in winter but was insufficient to curtail population growth in both winters. Overwinter population growth results from breeding, which occurred in each year of this study, and is common in Dicrostonyx (Krebs 1964; Fuller et at. 1975a). Perhaps other factors, such as an effect of habitat availability or thermal cover on survival and reproductive success, operate in winter, Whatever the case, winter breeding is necessary for recovery from heavy summer declines, and is likely essential for long-term population persistence, as has been indicated by Fuller et a!. (1975a). Third, a time lag of approximately nine months in a first-order driving variable generates stable limit cycles of three or four year periodicity (May 1976). A likely place for such a time lag to operate is in the low density period. Such a lag has been identified in some Scandinavian microtine species, but without clear evidence of the contributing factor(s) (Hornfeldt 1994). A possible cause is prey behaviour. Under heavy predation risk, theory suggests that individual prey must trade-off food  46 acquisition with survival (McNamara and Houston 1987). If such behavioural decision-making is not flexible, there may be a time lag as successive generations of prey learn that the world is safer. This may be significant in a predator exclosure experiment for a prey species where risk sensitivity, expressed in depressed rates of growth, maturation or reproduction, has population consequences. For example, with avian predators flying over an exclosure, prey likely still receive stimuli inducing risk avoidance. I have insufficient data to address this possibility. However, observations of Ci) juveniles maturing and breeding during the summer of birth, (ii) litter sizes at Pearce Point comparable to those reported elsewhere (Chapter 2, Krebs 1964), and (iii) population growth in PE in 1992, all suggest that risk sensitivity does not strongly affect potential population growth. Dispersal The distances travelled by juveniles within 10 days of weaning are noteworthy, as natal dispersal distances are generally thought to be less than one or two hundred metres in microtine rodents (Madison 1985; McShea and Madison 1992). The dispersal distances in this study at low density, traversed many home-range sized areas of unoccupied habitat (unpubl. data). Open habitat is therefore not the only condition necessary for settlement. Perhaps other necessary conditions are the presence of a conspecific of the opposite sex, and the absence of a competitively dominant conspecific of the same sex. The factors inducing natal dispersal in lemmings are not fully understood. The short time between departure of mothers and departure of weanlings from natal  47  burrows, and the distances weanlings of both sexes travelled, suggest inherent avoidance of local settlement. They have perhaps evolved to avoid inbreeding, or to avoid immediate competition with an adult conspecific of the same sex, especially in males, whose adult home ranges and frequencies of movement are substantially greater than those of females at low densities (Brooks 1993). They may also reduce risk of attack by predators (which acquire knowledge of lemming movements and residence by sight and smell), as has been suggested by Brooks (1993) for adult females. Tundra voles  Similar patterns of population change in voles and lemmings suggest that similar factors limit their populations. Limited data indicate that predation on tundra voles in summer is severe enough to curtail their population growth. However this limitation is less severe than that on lemmings. Tundra voles are more agile, and live in wetter habitats with more vegetative cover than habitats typically occupied by lemmings. The increase in winter 1990-91 might reflect unmeasured late summer and autumn reproduction in 1990, rather than winter breeding. Vole breeding appeared to last longer in autumn than lemming breeding. No juvenile-sized voles were caught in spring, but the population in spring did include adult-sized females which had not bred. Reported vole densities were substantially less than lemming densities. This was an artefact of measuring density over all available habitats. Within the wetter vegetation communities used by voles, their densities were similar to or higher than regional lemming densities.  48  Relevance to population cycles The preliminary study by Krebs et a!. (1995), and data presented here, indicate that lemmings at Pearce Pt. have persisted at densities of less than three per hectare for six years. I conclude that these populations do not exhibit multiannual cyclicity because density fluctuations are annual, with highest densities (one to three per hectare) frequently recurring in successive years. The highest densities were approximately an order of magnitude less than peak densities following an irruption in other studies: 40/ha (Shelford 1943), 15-25 (Brooks and Banks 1971), and 27 (Batzli  et al. 1980). The data support the hypothesis of Pitelka et a!. (1955), Maher (1970) and MacLean et al. (1974), that predation mortality can prolong the period of low density in lemmings, at least for a year or two. However, lemmings at Pearce Pt. are apparently unable to escape this persistent limitation, a fact which needs explanation. First, winter breeding may be insufficient to make up for summer declines and ongoing winter losses. Consequently, spring densities might never excede levels that migratory, hibernating and resident active predators can limit during the subsequent summer. Autumn densities are so low that winter density increases likely result from multiple litters during the winter. These issues are addressed in Chapter 3. Second, Dicrostonyx habitats at Pearce Pt. are comprised entirely of prostrate species, and lack the the bushy willow (Salix spp.) and birch (Betula spp.) growth of other regions. This reduced cover increases vulnerability to predation. Third, the summer predator community at Pearce Point includes many generalist predators (grizzly bear, arctic ground squirrel, golden eagle, peregrine  49 falcon, gyrfalcon, common raven and glaucous gull) which rarely occur together in other tundra regions. Densities of these generalist predators changed little when lemmings were rare in spring 1992. I presume that they broadened their prey base to include such species as arctic ground squirrel, or merely concentrated more on their other foods, such as plants and birds. Only the rough-legged hawk appeared to be a specialist lemming predator, failing to settle and breed in 1992. Some red fox and ermine, though generally thought of as microtine specialists, persisted when microtines were scarce, probably by broadening their prey base. These issues are addressed in Chapter 4.  50 CHAPTER TWO DO PREDATORS REGULATE LEMMINGS AT LOW DENSITIES IN SUMMER?  INTRODUCTION  Collared lemmings (Dicrostonyx spp.) and brown lemmings (Lemmus trimucronatus) exhibit wide fluctuations in population density across arctic North America (Elton 1942, Shelford 1943, Krebs 1964, Fuller et a!. 1975b, Batzli et a!. 1980). As densities fall from peak numbers, predation mortality may speed the rate of decline, and may push densities to lower levels, increasing the amplitude of the fluctuation (Pitelka et a!. 1955; Maher 1967,1970; MacLean et a!. 1974). The strong numerical response of predators to high lemming densities, and the lagged response by some predators, may prolong the low density phase in the population fluctuation (Pitelka et a!. 1955; Maher 1967,1970; MacLean et a!. 1974). Collared lemmings (Dicrostonyx ki!angmiutak) at Pearce Point in the western mainland Canadian arctic persisted at densities of less than three per hectare, for at least six years. Density frequently declined in summer and increased in winter (Krebs et a!. 1995, Chapter 1). Predation mortality was deemed both sufficient and necessary to curtail summer population growth and cause summer population declines (Chapter 1). Adult and neo-natal survival were significantly enhanced in a predator exclosure, and no other mortality factor compensated for the reduction in predation mortality (Chapter 1). However, the lack of growth in the protected population indicated that other limiting factors might be operating at low densities. Lemming population growth could be limited by numerous factors other than  51 predation mortality (Stenseth and Ims 1993). Reproduction may be decreased or inhibited by spacing behaviour (Chitty 1960, 1967), infanticide (Mallory and Brooks 1978), stress (Christian 1950, 1978, Boonstra 1994), or risk of predation (Ylonen 1994). Food quantity (Batzli 1983, 1985), and quality in terms of chemical defences (Jung and Batzli 1981), may affect maturation rate, litter size or social interactions. Habitat heterogeneity may limit dispersal success (Stenseth 1986; Ostfeld 1992). Risk of predation while feeding may limit individual growth and maturation (Desy and Batzli 1989). To determine whether or not predators regulate lemmings, I must address two paradigms of population regulation. The density-dependent paradigm involves a systematic search for relationships between demographic parameters and population density (Sinclair 1989, Murdoch 1994). In this chapter I investigate the possibility of density-dependent regulation through predation, by assessing per capita mortality from predation as a function of lemming density (cf. Sinclair 1989). The mechanistic paradigm of population regulation holds that regulation can only be inferred when all plausible alternative limiting factors have been investigated (Krebs 1995). In this chapter I investigate possible limitation of population growth, both in the predator exclosure and in unprotected areas, through three alternative factors: social interactions inhibiting reproduction, predation risk, and food availability. I infer that social factors were not inhibiting reproduction in the predator exclosure if: (i) the proportion of adults reproductively active was not lower on PE than on controls, (ii) litter sizes were not lower on PE than controls, and (iii) there was no significant relationship between lemming productivity and density (a measure  52 of social crowding). I infer that behavioural sensitivity to varying degrees of predation risk was not limiting population growth in the exciosure if: (i) litter sizes in PE were not larger than those in areas exposed to predation; (ii) growth rates in PE were not higher than those in areas exposed to predation. I infer that food quantity was not limiting if the following conditions hold: (i) lemmings in PB did not deplete the standing crop of their principal foods, Dryas integrifolia, Salix spp. and Carex spp. (Bergman and Krebs 1993), more than lemmings outside the exclosure, (ii) there was no difference between net above-ground primary production at Pearce Point compared with other similar habitats where Dicrostonyx fluctuates markedly in density, (iii) enhanced primary production by fertilization, significantly increased the standing crop of foods compared with untreated tundra, (iv) changes in food abundance following enhancement of primary production were not significantly greater in a herbivore exclosure compared with changes outside the exclosure, and (v) pregnant females did not choose maternal burrows with higher surrounding food availability than that at their previous maternal burrow.  METHOD S  Study Area The study was conducted at Pearce Point (69°48’N, 122°40’W), on the south shore of Amundsen Gulf, western mainland Northwest Territories, Canada. The dominant vegetation communities are: (i) an upland heath of Dryas integrifolia with varying amounts of Carex rupestris, Kobresia sp., Salix arctica, and Draba spp.; (ii) a  53  mesic hummock community dominated by D. integrifoha, C. membranacea, C. atrofusca, C. misandra, S. reticulata, and S. arctica; (iii) a wet marsh dominated by C. aquatilis, and Eriophorum angustifolium.  Prey populations Four areas of tundra, each 18 to 25 ha, were chosen for detailed study of lemming demography. Each area (termed a grid) had reference stakes at 30 m intervals, allowing accurate location of traps and lemmings. An 11.4 ha predator exclosure (referred to as FE) was built on one grid in 1990. This was largely successful in reducing mammalian and avian predators in summers 1990-1992 (Chapter 1). Three grids were kept as control populations (Cl, C2 and C3). Densities of collared lemmings were estimated by mark-recapture using the Jolly-Seber open population model. Grids were live-trapped with Longworth traps every one or two weeks from early June to late August, each year from 1988 to 1992 (Krebs et al. 1995, Chapter 1). Because subadults were relatively difficult to trap and dispersed rapidly (Chapter 1), densities were calculated only for residents, defined as adult lemmings and subadults caught at least twice.  Prey Mortality Adult lemmings (>35g) were fitted with a miniature radio (Biotrack Inc., model SS-1) mounted on a cable-tie collar (package weight 3.0  -  3.5 g). Lemmings were  relocated every two or three days. Causes of death were determined from: radio location at predator nests, dens or burrows; predator sign such as tracks and excavations at the lemming’s burrow; lemming remains such as parts of skeleton, pelt or abdominal organs near the recovered radio; predator teeth marks on the radio  54 package; and whitewash or droppings near the radio package. The fate of 18% of lemmings on control grids remained unknown, as the radio was permanently lost (Chapter 1). For analyses presented here, I used only verified predation mortalities. Mortality data from two study grids (Cl and C2) were used for all investigations of density dependence. C3 was excluded because adults were not radio-collared in 1991. I investigated density dependence in predation mortality in two ways. For comparisons between summers, I calculated percent adult lemmings killed on a grid during the entire summer as a function of the lemming density on the grid at the beginning of the summer (early June of 1988 through 1992). This addressed the cumulative effect of predators over the summer, but data were biased towards the higher densities most common in early June (Chapter 1). For comparisons within summers, and at lower densities, I tallied the percent of resident adults falling prey on Cl and C2 in successive two-week periods through the summers as a function of density in the first of the two weeks. Numbers of two-week periods varied between years: 1988 (4), 1989 (4), 1990 (5), and 1991 (6). In 1992 lemmings were absent from Cl and C2 for most of the summer. Data points on a grid within a summer were not independent. To obtain independence I randomly sampled one two-week period per grid (two grids) per summer (four summers), giving eight data points for each analysis. Ten analyses were performed to estimate means and variances of regression coefficients describing the linear relationship between percentage killed and density. Geometric mean regressions were also calculated (Ricker 1984), because dependent as well as  55 independent variables were subject to measurement error, whereas least squares regression assumes no error in measurement of the dependent variable (Krebs 1989).  Prey Reproductive Status and Productivity At each capture, and at many radiolocations between captures, lemmings were handled and weighed, and their reproductive status was assessed. Males were classed as reproductively active (testes scrotal) or inactive (testes abdominal). Females were classed as reproductively active if at least one of the following conditions held: vagina perforate (oestrous), pregnant (based on palpation, weight gain, or back calculation from birth date), or lactating (nipples large and white). Birth history was classified based on the pubic symphysis: closed (non-parous), slightly open (parous), or open (birth imminent or very recent). Pelage characteristics allowed me to differentiate subadults from adults. In early June the population consisted of lemmings with either adult or subadult pelage. The latter were classed as spring-born individuals, having been born under the snow in April or May (Krebs 1964). Lemming productivity was measured as the litter size within four days of birth, as judged by the reproductive status and history of the female. Natal burrows were not excavated. The sample comprised litters born in traps, in plywood nest boxes which were permanently installed on all study grids (c. 0.5  -  1.0 / ha), or in  tussocks above ground. The hypothesis that lemming productivity is a function of lemming density was tested by correlating each observed litter size with the estimated Jolly-Seber lemming density on the grid in the weeks of birth and conception, which occurs 20 to 22 days before birth (Hasler and Banks 1975).  56 The proportion of the adult population reproductively active was taken as the sum of lemming-weeks in which marked adults were reproductively active, divided by the total number of lemming-weeks for which data were gathered, over a 13-week period from the beginning of June to end of August in summers 1990-92. These data are biased towards early summer because lemmings were more abundant in June and populations declined during the summers. Prey Growth Litter growth was the total weight gain per day, for all neo-nates combined, determined over at least six days starting on or after day five post-partum, and ending close to weaning (days 15 to 17 post-partum). The sample includes two litters born and raised in nest boxes in small predator exclosures (1,250 2 m each) on fertilized tundra. Data are limited because females rarely kept litters above ground. Juvenile growth was calculated as the mean weight gain per day for reproductively inactive, weaned lemmings less than 35 g over periods ranging from 3 to 21 days. Adult male growth was taken as the mean change in weight per day over less than 21 d, not including the first week after receiving a radiocollar. Only one data point per male was used in the analysis. Adult female weights vary greatly with pregnancy. I used weights taken within six days after parturition. Food Limitation The investigation of food limitation follows the five conditions outlined in the Introduction. Food depletion: Changes in abundance of principal lemming foods were  57  calculated by comparing visually-estimated percent cover (± 5%, 2.5% for cover <5%) of these foods in randomly located 0.5m x 0.5m plots between mid-August 1990 and mid-August 1992. Sampling areas were inside PE, on Dryas heath communities on Cl and C2, and on Dryas heath immediately adjacent to but outside PB. Net above-ground primary production: Changes in above-ground standing crop of all vascular plants and lichens in the upland Dryas/Carex heath and in the mesic Dryas/Carex hummock communities were measured using clip-plots (Wein and Rencz 1976; Svoboda 1977). Within one small homogeneous portion of each community a 6.25 m by 10.0 m grid was established for random location of 20, 0.25 x 0.50 m plots, the optimal size for this sampling (Wein and Rencz 1976). In the first week of June I clipped 10 plots of all above-ground vegetation, and sorted these by species, and by dead and live components. In the first week of August, at peak growth, I clipped and sorted an additional 10 plots from each community. No two plots shared a side. Clipped samples were dried at 60°C until stable in mass, and weighed. The difference in mean dry weights of each component between August and June represented the net above-ground primary production of that component, less any consumption and senescence. Differentiating dead and live components in June was straight-forward, except for Dryas on which some leaves remain alive but reddish-brown in winter, and on which dead leaves remain attached for a number of years (Svoboda 1977). In June, only leaves with red petioles were classed as alive. This rule was tested by following leaf green-up, and the fate of marked, red-petioled leaves (total  ,  =  277), on three  Dryas plants in each of two herbivore exclosures (one in each vegetation community).  58 All red-petioled leaves became green by late June, though 10.5% showed partial necrosis and may have died during the growing season. No leaves without red petioles became green. In August I was unable to readily differentiate live and dead standing crop of Dryas stems, so I estimated the dry weight increment of stem during the growing  season as 21% of the net green leaf and shoot production (see Svoboda 1977). Enhancement of primary production: The interaction of enhanced production and grazing was investigated in (1) a small-scale (less than a lemming home range) factorial experiment combining enhanced productivity, by fertilization, with decreased grazing, by herbivore exciosure, and (ii) a large-scale (larger than a lemming home range) enhancement of production by fertilization. For the small-scale experiment I built three 6 m x 21 m herbivore exclosures, each with a perimeter fence of 1.0 cm mesh chicken wire. Two were in Dryas heath close to grids C2 and C3, and one was in a mesic hummock community near PE. I established four pairs of 4 m x 4 m plots, such that one plot of each pair fell within the exclosure, and one immediately outside. Pairs of plots were systematically assigned one of following fertilization treatments in the following sequence: control (unfertilized); 50 kg/ha; 125 kg/ha; and 250 kg/ha (19:19:19 N:P:K fertilizer). Plots in a fertilization sequence were separated by 1 m, and were fertilized in early June 1990 and 1991. Changes in standing crop in each 4 m x 4 m plot were assessed by visual estimation of percent cover (± 5%, and 2.5% for cover <5%) of key lemming foods  (Dryas, Salix arctica and S. reticulata) within four randomly located 0.5 m x 0.5 m plots. Data were gathered at peak growth in early August 1990 and 1991.  59 For the large-scale enhancement experiment I fertilized two, one-hectare portions of Dryas heath, one on C2 and one on C3. I applied 19:19:19 N:P:K fertilizer at 125 kg/ha in early June of 1990, 1991 and 1992. Adjacent to each fertilized hectare I monitored one hectare of tundra with similar vegetation, as a control area. In each fertilized and control hectare I randomly located eight, 0.5m x 0.5m plots for visual estimation of percent cover (± 5%, and 2.5% for cover <5%) of key lemming foods at peak of summer growth in early August. The large-scale treatment effect was measured as the mean change in standing crop from 1990 to 1992 on the two fertilized hectares compared to changes on the two control hectares. The small-scale treatment effect was similarly measured as the mean of changes in standing crop from 1990 to 1991 on each of the four fertilizer treatments inside the three exciosures, compared to changes immediately outside the exclosures. Female burrow choice: I measured percent cover (± 5%, and 2.5% for cover  <  5%) of live Dryas leaves in 10, 25cm x 25cm plots at each of 1 m, 3 m, and 5 m radii from the natal burrows of radiocollared females on PE in 1992, at the end of lactation and beginning of the subsequent lactation. Plot positions at each radius were chosen randomly from 20 potential compass bearings from the natal burrow mouth, and plot corners were permanently marked with metal pins. RESULTS Density Dependent Predation Mortality The relationship between percent adult lemmings killed during summer and lemming density in spring is positively density dependent, but with wide scatter in the data (y  =  0.102  +  0.369 x, R 2  =  0.47, F  =  7.014, P  =  0.029) (Fig. 2.1). The geometric  60  Fig. 2.1. The relationship between percent of adult lemmings killed during the summer and adult lemming density in spring for two populations: Cl (triangles) and C2 (stars) from 1988 to 1992. The trends in the data are summarized by the geometric mean regression lines (Ricker 1984) for all data (solid line), and all years except 1992 (broken line).  (0  E 0  o 4-’  0) 1  V  aV  0  ‘5 C  o 2 o  0  100 90 80 n. ‘U  60 50 40 30 20 10  —io-— 7 0  7  z  7  A  7  I  7  I  0.6  7  I  0.4  7  0.2  7  7  7  7  1  /  1.4  I  A  I  A  1.2  Spring density (resident adults I ha)  7  A  1.6  V  z  1.8  2  62 mean regression still indicates positive density dependence when the 1992 data are removed. The scatter partly reflects variable foraging effort by predators between study grids, varying numerical responses of migratory predators (e.g., rough-legged hawks) at nest establishment, and varying breeding success of resident predators (e.g., red foxes). For example, the high percentage killed on Cl at a spring density of 0.65/ha (Fig. 2.1) occurred in 1991 when rough-legged hawks initiated six nests, two more than in any other season (Chapter 1), and occupied a nest adjacent to this grid. There is also considerable sampling error in assessing predation mortality on study plots which are much smaller than the foraging ranges of predators. Predation mortality tended to be positively density-dependent when assessed over two-week intervals, but in least squares regression analyses the relationship was significant (P <0.05) in only four of the ten tests (those with R 2 . 0.59) (Fig. 2.2). The slope of the geometric mean regression lines was always positive, describing a mean increase in proportion killed of 32.9% (S.E.  =  4.32) for each additional lemming per  hectare. The density at which no lemmings were killed was on average 0.29 individuals/ha. Some of the scatter can be explained by temporary changes in the predator community. For example, red foxes did not reach study grids (with relatively high densities) until early July in 1990, perhaps because they were unable to cross a stream in flood. Also, sporadic grizzly bear predation in mid-summer 1991 (at moderate to low lemming densities) increased the percent killed substantially. However, much of the scatter is still unexplained. Although per capita predation mortality did decline with declining lemming density during the summer, the relationship was not very  63  Fig. 2.2. The relationship between percent of resident adult lemmings killed within a two-week period, and lemming density at the beginning of the two-week period, for two populations: Cl (triangles) and C2 (stars). Each graph represents a random choice of one, two-week data point from each population in each of four summers (1988-1991). Solid lines are geometric mean regression lines (Ricker 1984), and R 2 values are Pearson coefficients of determination.  64  ¶  15  -5  77 0:2  0:4  0:8  02  4  ‘.2  / .: z ‘5  0  2  0 46  i:4  N  -  -5/  /02  0:4  0:o  02  1  12  1:  1  ‘-  0  ‘5  a)  10  C  0  -5  (f)  0.80  2 R 02  0:4  o:e  02  4  1.2  1:0  1:4  1  /7  5 2 R 02 .4_i  ;7  5  01  0.5  00  1  18  =  II  0.29 1.5  .5  J.  2  Lz** 02  .5 .15  0.88  ,..-.-  0:4  02  02  4  i2  1:  0.4  05  05  1  1.5  1.4  02  4  ‘.2  1:4  i:6  ‘.2  1:,  ‘.2  2 R  /___ 02  =  1.5  10  15  15  15  WE  MN  -5  =  -5  0.00  -  2 R 02  0:4  0:0  oat  //  40  ‘5 15 S  : Density  (resident  N  0:2  0:4  02  0:0  4  adults / haj  65 predictable.  Social Inhibition of Reproduction Adult-sized lemmings were reproductively active in 86-100% of individual lemming-weeks in June, July and August, and the proportion of lemming-weeks for which lemmings were reproductively active was not systematically lower or higher on PE than on controls in any year (Table 21.). Limited data indicate a slightly higher rate of reproductive activity in 1992, when predators and lemmings were scarce. The small sample of weeks when individual lemmings were inactive was comprised of spring-born females still maturing in early June, and some adults ending breeding in mid to late August. Litter size increased significantly with female weight post partum (Fig. 2.3). Reproductive history explained a considerable part of the residual variation: for primiparous females litters were less than expected from female weight (mean residual -0.53, S.E. 0.299); for multiparous females first litters were larger than expected (mean residual +1.01, S.E. 0.306), second litters larger than expected (mean residual +0.45, S.E. 0.556), and third litters less than expected (mean residual -0.99, S.E. 0.246). Sample sizes were too small to compare PE to controls within each category. However, litters born in PE showed no systematic tendency to larger size than those from controls (Fig. 2.3). With control and PE litters lumped together, litter sizes at Pearce Pt. tended to be lower, especially in early summer, than embryo counts reported by Krebs (1964) at Baker Lake in 1962 (a year of low but increasing densities) (Table 2.2). However, Baker Lake counts were only significantly larger for the first summer litter of  66  Fig. 2.3. The relationship between litter size and female weight post partum as observed in a predator exciosure (squares) and on control grids (stars).  67  8  2  r 2_047  1• 030  P —0.03 40  50  60  70  Female mass post partum (g)  80  68 Table 2.1. Proportion of lemming-weeks in which individual adult-sized lemmings were reproductively active. Numbers of lemming-weeks for which data were available are in parentheses. Sampling period covers 13 weeks in each year, from beginning of June to end of August.  PP  1990  1991  Over-  0.96  0.96  winter  (24)  (79)  Spring-  0.86  0.93  born  (37)  All males  Cl  1992  1990  1991  0.91  0.95  (45)  (19)  1.00  0.98  0.88  (100)  (32)  (42)  ( 8)  0.95  0.90  0.97  0.88  0.90  (38)  (31)  (35)  (66)  (21)  -  C2  1992  -  1990  1991  0.98  0.97  (41)  (30)  0.91  1.00  1.00  (43)  (22)  (32)  0.96  0.86  (46)  (59)  1992  -  females  -  females  -  -  69 Table 2.2. Litter sizes of primiparous (spring-born), multiparous (overwintering) and first summer litter females at Pearce Point, N.W.T., and embryo counts of equivalent litters at Baker Lake, N.W.T. in 1962 (data from Krebs 1964, Table 16). Litter periods refer to the chronological sequence of successive litters during the summer.  Litter sizes  Pearce Pt.  Baker Lake  Litter Age class  period  mean S.E.  n  mean S.E.  Primiparous  I  4.40  0.24  5  5.35  0.32  17  Multiparous  I  5.44  0.50  9  7.17  0.54  6  II  5.75  0.56  8  5.50  0.42  14  III  4.00  0  3  4.67  0.88  3  III  3.50  0.50  2  4.00  0  1  First summer litter  n  70 multiparous females (t  =  2.28, 13 d.f., P <0.05).  There was no relationship between litter size and the lemming density on the study grid where the females gave birth, either at time of conception (r P  =  0.84), or at birth (r  =  0.17, n  =  27, P  =  =  0.05, n  =  18,  0.40).  Behavioural Sensitivity to Predation Risk  Total daily growth of neonates increased significantly with female weight post partum (Fig. 2.4). Limited data suggest that this daily growth was higher in FE (mean residual +0.41, S.E. 0.23) than controls (mean residual -0.55, S.E. 0.10) at any given female weight. Per capita daily growth of neo-nates showed no clear relationship to female weight post-partum (Fig. 2,5), but rates in FE were higher than those on controls at any given female weight. Daily growth rates of juveniles decreased significantly with body weight (Fig. 2.6), but this relationship was quite variable probably because of the differing lengths of time over which data were gathered. Rates in FE were not higher than controls (Fig. 2.6). Daily growth rates of scrotal males were not significantly related to body weight (r  0.20, P  =  0.24, n  on control grids (t  =  -0.57, 36 d.f., F> 0.30). Weights in FE (mean 46.5, S.E. 2.8, n  =  =  38), and growth rates in FE were not higher than those  10) were higher than those on controls (mean 39.9, S.E. 2.2, n was not significant (t  =  1.64, 36 d.f., 0.1  >  =  =  28), but the difference  F> 0.05).  In a two-way analysis of variance there was no effect of the PE on post-partum  71  Fig. 2.4. The relationship between total growth rate of litters and female weights post partum as observed in a predator exciosure (squares), a predator exclosure with fertilization (triangles) and control grids (stars).  72  5-  I  030  4b  50  Female weight post partum (g)  73  Fig. 2.5. The relationship between mean per capita neonatal growth rate on a litter by litter basis and female weight postpartum as observed in a predator exciosure (squares), a predator exclosure with fertilization (triangles) and control grids (stars).  74  1.3 1.2 1.1  C  C  !  0.8 0.7 06 0.5 0.4 0.3 O.2 01 00  o  c  40  50  60  Female weight post partum (g)  70  80  75  Pig. 2.6. The relationship between growth rate of Juvenile lemmings and their body weights. IndMduals living In the predator exiclosure are indicated by squares, and control individuals by stars.  76  14-  r —0.66  1.3 1.2 1.1 1 o.g 0.8 07  P <0001  C  * *  C C  C  * C  2  u.6 0.5 0.4 0,3 0.2 0.1 0  *  C C  * C C C * C  *  ib  i  i  1  ië  20  22  Weight (g)  2  26  28  30  32  34  77  female weights (F  =  0.10, P  =  0.75, for first and second litter periods; Table 2.3).  However, post-partum weights varied significantly between successive litters (F 5.32, P  =  =  0.003), increasing from first (June) to second litters (July), and decreasing for  third litters (August). There was no interaction effect (F  =  1.32, P  =  0.28).  Food Limitation Food depletion: Changes in percent cover of the three principal collared lemming foods were not substantial in either PE or on three control areas (Table 2.4), and differences between PP and the mean of controls were not significant for any food (Dryas: t 0.10 <P  <  =  0, 2 d.f., P> 0.9; Salix: t  =  0.98, 2 d.f., P> 0.9; Carex: t 5  =  2.25, 2 d.f.,  0.20).  Net primary production: The net above-ground primary production of vascular plants in 1992 was 40.0 g/m 2 in the drier heath community, and 53.6 g/m 2 in the wetter hummock community (Table 2.5). Net primary production of Dryas was slightly higher in the heath, especially for leaves and flowers. The production of sedges, willows and forbs was higher in the hummock community. These values may be underestimates, especially for forb and willow production, since sample areas could have been grazed, most likely by arctic ground squirrels (Spermophilus parryii) and caribou (Ran gifer tarandus). Assuming that all the primary production of three principal food groups (Dryas leaves and flowers, Salix leaves, and Carex) is available to lemmings, then as  much as 88% of the net primary production in both the heath and hummock communities is potential lemming food. These estimates of net above-ground production are similar to values obtained  78 Table 2.3. Mean ± S.E. post-partum weights of adult female collared lemmings comparing predator exclosure and control grids for three litter periods during the summer. “n’ records sample size.  Predator  Control  exclosure  grids  Age  Litter  class  period  n  mean ± S.E.  Spring-  I  6  43.3 ± 2.4  11  45.3 ± 1.8  born  II  5  53.6 ± 1.5  4  47.0 ± 1.7  III  3  51.7±6.1  0  Winter  I  7  48.5 ± 2.4  9  50.8 ± 1.8  adults  II  6  52.4 ± 3.7  8  52.6 ± 1.6  III  5  50.6±4.2  1  51.0±0  III  1  58.0 ± 0  1  36.0 ± 0  Summer born  n  mean ± S.E.  79 Table 2.4. Mean ± S.E. percent cover (± 0.5%) of three principal collared lemming foods measured in 0.5m x 0.5m plots in PE and three control areas (C2, C3, and immediately outside PE) in early August 1990 and 1992. Tt records number of plots. n tt  Lemming food  Dryas  Salix spp.  Carex spp.  Site  Year  integrifolia  PE  1990  14 ± 2.8  3 ± 0.5  17 ± 2.6  (n=25)  1992  16 ± 2.7  5 ± 0.9  15 ± 2.0  C2  1990  14±1.6  2±0.3  7±1.7  (n=8)  1992  18± 1.9  2±0.3  7± 1.5  C3  1990  11±2.0  0±0  3± 0.4  (n=8)  1992  16 ± 3.4  0±0  3 ± 0.5  Outside  1990  17 ± 6.2  7 ± 1.3  12 ± 3.0  PB  1992  14 ± 4.2  9 ± 2.6  14 ± 3.0  (n=7)  Salix spp.  -  Carex spp.  live *  live and dead  stem  -  live and dead  -  -  Dryas integrifolia  and component  Plant species, class  **  0.8  (0.88)  (1.12)  (1.61)  (1.33) 0.8  2.7  (0.41)  (1.13)  4.3  0.9  3.7  August June  Heath  0  1.6  0.6  2.8  NPP  Hummock  (0.76)  1.1  (4.48)  14.6  (1.76)  3.0  (0.35)  0.5  (3.18)  11.3  (0.47)  1.0  August June  “-“  0.6  3.3  0.4  2.0  NPP  Table 2.5. Mean above-ground mass (g/0.125 m ) of vascular plants and lichens, and net above-ground 2 primary production (NPP; growth from June to August 1992) of these plants, in two collared lemming habitats (heath and hummock) at Pearce Point, N,W.T., based on clip sampling of ten, 0.125 m 2 plots in each community in early June, after snow melt, and in early August, at peak growth. Values in parentheses are standard deviations. means the species is absent; “n.m. means production cannot be measured. Plant identifications from Porsild and Cody (1980) and Cody (1992).  C  species,  class  (1.34)  (1.61)  40.0  (0.13)  (0.35)  0  Total (g/m ) 2  0.2  0.2  0  0  5.0  *****  3.1  3.1  -  (0.23)  (0.10)  -  0.2  NPP  —-------  0.2  August June  —  Heath  Total (g/0.125 m ) 2  Lichens  Eguisetum arvense  Saxifraga oppositifolia  Forbs  and component  Plant  Table 2.5 (continued)  —  n.m.  (0.08)  (0.12) n.m.  0.1  n.m.  (0)  0  53.6  6.7  n.m.  0.1  n.m.  0.3  NPP  —---  0.2  n.m.  (0.28)  0.3  August June  —  Hummock  Co  .  rupestris, , petricosa 1 , nardina, C.  arctica; in the hummock  scirpoidea.  arctica and  .  reticulata.  Unidentified.  in the hummock Polygonum viviparum, Oxyria digvna and Armeria maritima.  In the heath Chrysanthemum integrifolium, Draba corymbosa and Stellaria longipes;  In the heath only  membranacea, C atrofusca, , misandra, and  scirpoidea and Kobresia myosuroides; in the hummock it includes primarily  In the heath this includes primarily  following Svoboda (1977).  Live includes only leaves and inflorescences; stem is calculated as 21% of live,  *****  **  *  Table 2.5 (continued)  00  83 from other Canadian arctic tundra communities where collared lemmings are known to undergo substantial increases in population density in some years (Chitty 1950; Fuller et at. 1975b) (Table 2.6). Enhancement of primary production:  In the small-scale fertilizer and  herbivore exclusion experiment the percent cover of Dryas increased progressively with heavier fertilization, both inside and outside the exclosures, but willows showed little or no response (Table 2.7). In a two-way analysis of variance, fertilization and exclosure treatments both explained significant amounts of the variance in Dryas percent cover, but there was no significant interaction effect (Table 2.8). Dryas outside the exclosures responded less strongly to fertilization at sites C2  and C4, where I noted that lemmings had fed in and nested under the snow beside the fertilized plots adjacent to the exclosure during the 1990-91 winter. Some of the potential increases in Dryas standing crop following fertilization were apparently consumed on these small plots outside the exciosures. However, the effect of fertilization on live Dryas outside the exciosures was still significant (F  5.81, P  =  0.02), indicating that not all the enhanced production was being consumed. In the large-scale experiment, percent cover of fertilized live Dryas increased significantly after one year (t  =  3.5, df  =  2, P  <  0.05, one-tailed; Table 2.9), and to an  extent similar to Dryas inside the small-scale exciosures (Table 2.7). This increase was more pronounced and strongly significant compared to controls after two years (t 11.3, df  =  =  2, P <0.005, one-tailed; Table 2.9). Fertilization increased ground cover of  Dryas by an average 54% after one year, and 99% after two years. Dryas is a perennial  cushion plant on which previous growth remains attached for years after it has died.  84 Table 2.6. Comparison of estimates of net above-ground primary production ) in Dryas integrifolia / Carex rupestrisheath and 2 (g/m .p integrifolia / membranacea hummock communities at Pearce Point, N.W.T., with estimates for similar communities at Canadian arctic sites where lemmings are known to undergo substantial fluctuations in density. .  Net primary Plant community  .  Site  production (g/m ) 2  integrifolia /  Pearce Pt.(70°N)  40.0  rupestris  Banks I., Big R.(73°N)  15.2  Victoria I. (71°N)  41.4  Devon I., Truelove  26.0  heath  1  2  lowland (75°N) integrifolia / C. membranacea hummock  Pearce Pt. (70°N)  53.6  Banks I., Thomsen R.,  54.8  (73°N) Devon I., Truelove  54.3  lowland (75°N)  Data sources: 1 Svoboda 1977, Table 12. 2 Svoboda 1977, Table 11. Beach ridge community similar to heath community at Pearce Pt. (Svoboda 1977, Table 8). Muc 1977, Table 4. Frost-boil meadows have species composition closest to hummock areas at Pearce Pt. (Muc 1977, Table 1).  85 Table 2.7. Mean changes in standing crop (% cover) from August 1990 to August 1991 for three collared lemming foods (Dryas integrifolia (D.i), Salix arctica (S.), and S. reticulata ()) under four different fertilization treatments, in paired 4m x 4m plots either inside or outside three herbivore exciosures. Blank cells indicate the species was not present.  Inside  Outside  exciosure  exclosure  Fertilizer treatment  D.i.  S.a.  Unfertilized  1  0  control  1  50kg/ha  S.r.  2  -1  4  0  1  3  1  9  0  0  -1  -1  1  0  0  0  1  0  3  0  0  8  6  0  8  0  1  11 9  -1  S.r.  5  9  250kg/ha  S.a.  1  7  125kg/ha  D.i.  3  1  8  0  2  6 0  0  5  0  2  86 Table 2.8. Two-way analysis of variance investigating the effects of herbivore exclosure and fertilization treatments on variance in mean change in standing crop (% cover) of live Dryas integrifolia from August 1.990 to August 1991. Raw data are in Table 2.7.  Source of  Sum of  variance  squares  Exclosure  40.042  1  40.042  11.720  0.003  Fertilizer  188.792  3  62.931  18.419  0.000  2.458  3  0.819  0.240  0.867  54.667  16  3.417  Exclosure fertilizer Error  d.f.  Mean  F-ratio  P  squares  *  87 Table 2.9. Mean changes in percent cover of two collared lemming food groups (live Dryas integrifolia, and live Carex/Kobresia), and the exposed surface of dead Dryas, on paired one hectare control (unfertilized) and fertilized plots in two heath communities (C2 and C3), measured from August 1990 to August 1991 (one-year) and to August 1992 (two-years). Blank cells indicate data not available.  Change in percent cover  Live Dryas Fertilization  Time  treatment  period  Unfertilized  Dead Dryas  C2  C3  C2  C3  One-year  1  3  -1  -1  control  Two-years  4  5  0  0  Fertilized  One-year  8  6  -7  -6  (125 kg/ha)  Two-years  12  13  -7  -7  Live Carex  C2  C3  -1  0  8  9  88 This dead material covers much of the ground surface in Dryas heath communities, and live growth covers only part of the top of this cushion. Increases in live Dryas standing crop resulted in significant declines in exposed cover of dead Dryas in the first year (t  -11.0, df  =  2, P  <  0.005, one-tailed). However, the exposed cover of  dead Dryas did not decline further in the second year (Table 2.9). The additional increase in cover of live Dryas in the second year was comprised primarily of new lateral branches beyond the edges of the established cushion. Increments in standing crop of another set of potential lemming foods, Carex and Kobresia species, were also significant over two years (t  =  12.7, df  =  2, P  <  0.05,  one-tailed; Table 2.9), representing an average 90% increase in ground cover. Willows were too infrequent or small to assess changes. Burrow choice: A limited sample of three pregnant females, each changing maternal burrows between litters in late July, did not consistently choose new burrows with increased Dryas abundance compared to the Dryas abundance they left behind at the end of their previous lactation (Table 2.10). DISCUSSION Density Dependence in Predation Mortality  The data indicated positive density dependence between cumulative summer predation mortality and spring lemming density, and between predation mortality, assessed over two-week periods within summers, and lemming density. However, there was a great deal of scatter in the results, and the relationships had little predictive power. The lack of clear relationships may reflect the diversity of summer predators,  89 Table 2.10. Absolute abundance of Dryas integrifolia (% cover) at three radii from maternal burrows of three females at parturition, expressed as a proportion of j integrifolia abundance at the previous maternal burrows at the end of their previous lactations.  Female  Radius (m)  (i)  (ii)  (iii)  Change in Dryas abundance  1  +  3  +1.94  5  +0.56  1  +  3  -0.37  5  -0.49  1  -  0.79  1.66  0.30  3  -0.35  5  +0.33  90 their varying responses to lemming density, and the small scale of the study grids compared to predator home ranges. Specialist lemming predators, such as the roughlegged hawk (Potanov 1986, Smith 1987), likely continue to kill many lemmings even at low densities, perhaps in an inverse density dependent fashion. The red fox, normally thought of as a generalist (Voigt 1987), is expected to change its diet to include alternative prey when lemmings are scarce, thereby acting in a positively density dependent fashion. Some generalist predators, such as peregrine falcon and arctic ground squirrel, continued to kill lemmings at very low densities in 1992 (Chapter 1). A mix of predators with differing degrees of specialization likely causes increased scatter in relationships between per capita mortality and density. Study grids (18-25 ha) were much smaller than the hunting ranges of foxes (probably greater than 40 km . Chapter 4), and hawks (probably greater than 15 2 2 km Chapter , 4). Therefore, predation rates on grids could easily differ from rates throughout the study area, increasing the scatter in the data. Positive density dependence in predation mortality has rarely been demonstrated with small rodent prey, and does not necessarily result in a stable prey population. Erlinge et a!. (1983, 1984, 1988) and Erlinge (1987) provided evidence for positive density dependence in winter predation mortality on non-cyclic voles, with total annual predation approximating the annual production of voles. The system appeared to be stable, but was fairly unusual in that the generalist vole predators primarily ate other species, notably rabbits (Oryctolagus cuniculus), so voles were preyed on heavily only when relatively common or vulnerable (Erlinge 1987). In western Finland predation on voles by breeding raptors is positively density  9:1  dependent with very little time lag (Korpimaki and Norrdahl 1989, 991a,b; Korpimaki 1993), and least weasel predation on voles in winter is delayed density dependent with a time lag of approximately nine months (Korpimaki 1993). Vole densities still varied cyclically in this system. Peak densities were probably dampened and declines initiated by the raptor predation, which often exceeded production (Korpimaki and Norrdahl 1991b). Declines may have been exacerbated by the least weasel predation (Korpimaki 1993). The system was not stable, and was distinctly seasonal. Sinclair et al. (1990) provided evidence for positive density dependence in predation on low to medium densities of house mice (Mus musculus) in Australia, but inverse density dependence when mice reached high densities. It was unclear whether predation exceeded production at low densities, but the principal avian predators were migratory, allowing mice to escape predator limitation, and, in some winters with excellent food conditions, reach outbreak densities. Fitzgerald (1977) demonstrated destabilizing inverse density dependence in weasel predation on cyclic voles in alpine California, as did Pearson (1966) studying feral cats and cyclic voles in coastal California. Positive density dependence does not necessarily result in a stable prey population, often because the predation still exceeds production and operates only in some seasons.  Inhibition of Reproduction I found no evidence that reproduction was inhibited or decreased in the predator exciosure. The proportion of adults reproductively active was the same in PB as on control grids, and was high in all summers. Litter size was not lower in PE than on controls. Production of young was not significantly affected by density. I  92 conclude that there was no substantial social inhibition of reproduction in the exciosure. Social inhibition of reproduction in lemmings has been inferred to occur at high densities, and has been demonstrated in some laboratory studies. Birth rates decline during and soon after periods of high density in fluctuating populations of Dicrostonyx as a result of slower maturation, shorter reproductive periods and smaller body sizes (Krebs 1964; Fuller et a!. 1975b; Mallory et al. 1981). Rates at which litters are weaned in the lab may be depressed because of infanticide by strange adult males and females within a few days post-partum (Mallory and Brooks 1978, 1980). In this study lemmings were always at low densities so social interactions were would have been relatively few. I could not assess maturation rates because very few individuals were followed from birth to adult status. However, juveniles grew as quickly in PE as they did on control grids. I found no shortening of the reproductive period in FE, where densities were higher. Adult female weights were not higher in PE than on controls. Adult males were larger in FE, perhaps because of better survival and continuing growth as adults. Lemmings were occasionally infanticidal, which certainly limits population growth to some extent. A minimum of 4% of litters on control grids and 5% in PE were killed by infanticide in 1991, judging by sign on carcasses and termination of lactation by the female (Chapter 1). Radiocollared adult males were often located in the same, or adjacent, burrow as lactating females at or shortly after parturition, which is to be expected in a species with post-partum oestrous. Adult females, however, were generally widely spaced and seldom more than 20 m from their natal  93 burrow. The low adult survival (Chapter 1) led to frequent turnover in territorial males during the summer. Consequently surviving females likely encountered strange males every few weeks. Infanticide in these circumstances is best explained by the sexual selection hypothesis (Hrdy 1979), where males kill young they did not sire, so as to increase their future reproductive potential. I cannot rule out the use of young as a nutritional resource by the killer, but think that alternative hypotheses such as competition for resources, social pathology or parental manipulation of sex ratio (Hausfater and Hrdy 1984) are unlikely. Mallory and Brooks (1978) postulated that females encounter strange males infrequently at low densities. However, heavy predation mortality changes the adult composition of the population frequently at these densities, so potentially enhances the rate of infanticide. PE did not protect against this in 1991 because some territorial males were killed inside, or when they moved outside. Infanticide did occur, but appeared to be insufficiently common to explain the lack of population growth in PE, and was likely an indirect result of predation mortality. Food Limitation  The results satisfied four of the five predictions of the hypothesis that food was not limiting. First, lemmings in PE did not deplete the standing crop of their principal foods more than did lemmings on control grids. Second, net above-ground primary production at Pearce Point was close to or higher than that in similar vegetation communities in other Canadian arctic situations where Dicrostonyx reach considerably higher densities. Since the majority of the primary production was in lemming foods, food quantity appeared sufficient for population growth. Third,  94 radiocollared lemmings occupied the fertilized one-hectare patches of heath, and could have consumed the additional production. However, the increases in standing crop of Dryas on the fertilized patches were similar to the increases in the herbivore exciosures in the same habitats, indicating that lemmings did not consume an appreciable amount of the enhanced production. Fourth, adult females did not always choose new maternal burrows with higher food availability than that near their previous burrow. Taken together, these results provide strong evidence that food abundance was not limiting population growth in summer. The fifth prediction, that the herbivore exclosure would not significantly enhance the effect of fertilizer treatments compared with fertilized areas without protection from grazing, was not satisfied. At two of the three exclosures, increases in standing crop were greater inside than outside. This reflects a problem of scale in the design. The very small treatment areas (4 m x 4 m) provided local hotspots of food which were grazed by lemmings in winter. None of the tests of the hypothesis of no food limitation was completely adequate. They were conducted at spatial scales smaller than the space occupied by a population. However, because of their similar results, I am confident that population growth in PE was not limited proximally by summer food quantity. Food limitation of Dicrostonyx has not been assessed at low population densities. Most hypotheses regarding food limitation have addressed high density populations, especially of the brown lemming (Lemmus trimucronatus), which sometimes consumes the majority of its standing crop of foods in winter (Thompson 1955; Schultz 1964; Batzli and Jung 1980).  95 Behavioural Sensitivity to Predation Risk. Ideally food and predation should be studied together because of the potential population consequences of the behavioural tradeoffs individuals must make between acquiring food and avoiding predation (McNamara and Houston 1.987). Such decisions concern when, where and how to feed and reproduce (Lima and Dill 1.990). The results indicate no effect of the predator exciosure treatment (reduced risk) on reproductive rate. Lemmings in PE were not reproductively active for longer periods, and did not produce larger litters, than did control lemmings. Collared lemming litter sizes have not varied significantly between years in other studies despite substantial annual variation in the abundance of predators (Krebs 1964; Fuller et a!. 1975a). However, changes in both litter size and female post partum weight through successive litters, follow changes in food availability, with rapid leaf proliferation in June and July, and senescence in August. This could reflect sensitivity to predation risk; females might acquire more food within a safe distance of cover as leaf growth procedes, and less food as leaves senesce. Limited data also indicate that total daily growth of litters, and per capita daily growth of neonates, were higher in FE than controls. Higher encounter rates with predators and their sign may force lactating females to remain stationary or return to a burrow more often, or induce them to stay in a burrow longer or travel shorter distances to feed. Lactating females in FE might have foraged longer and more often than control females. Whether improved litter growth rates can enhance population growth will  96 depend on whether weanling females reach maturity faster, and at larger body size, thereby producing relatively large litters earlier in life. However, juveniles in PE did not grow faster, probably because many of those weaned in PE subsequently emigrated, and many of those found in FE were likely immigrants (Chapter 1). Immigrants would have been weaned in high risk areas, and may have been unable to respond quickly to the safer conditions. Adult males did not grow faster in FE, though differences would be harder to detect at the low rates (0.2  -  0.3 g/d)  observed. However, males tended to be larger in FE, probably because they survived longer. Adult females did not differ in weight between FE and controls. The predator exciosure successfully kept out foxes and to a lesser extent other mammalian predators, but avian predators could still fly over. Lemmings in PE probably continued to perceive some predation risk, so this treatment was an incomplete test of potential behavioural sensitivity to risk. I tentatively conclude that risk sensitivity limits population growth, but with effects too small to explain the lack of population growth in FE or controls.  Other Limiting Factors I now consider some factors which might limit population growth, but which I did not directly assess. Induced or constitutive defence chemicals might inhibit reproduction and become limiting following heavy grazing (Haukioja 1980, Bryant et at. 1991; Seldal et al. 1994). Secondary plant compounds in graminoids may stimulate reproduction (Berger et a!. 1981). Since I did not observe reduced reproductive effort, in PE or comparing Pearce Ft to Baker Lake, I consider it unlikely that these factors limited summer population growth at Pearce Point.  97 Habitat heterogeneity might affect population growth by influencing dispersal success through habitats of differing patchiness and quality (Stenseth and Ims 1993). Densities of microtines on study grids were similar to densities in other parts of the study area (40 km ) (Chapter 1), so I do not consider study grids to be inferior 2 habitats. Juveniles dispersed an average 53 m/d in the first 10 days after weaning, and many born in PE emigrated. They also suffered substantial predation mortality even when predators were relatively uncommon in 1992. Low rates of juvenile immigration to PE, because of predation mortality, were probably responsible for lack of population growth (Chapter 1). Habitat barriers such as cliffs and a river delta may have frustrated some potential immigrants.  Community Dynamics At a community level, the summer results are consistent with the general model of Hairston et al. (1960); predators strongly limit herbivore populations which are then unable to limit vegetative growth. Other resident herbivores at Pearce Pt. are tundra voles, which are also strongly limited by predation mortality in summer (Chapter 1), and arctic ground squirrels. Oksanen et al. (1981) predict that at primary productivities of 50-150 g/m 2 herbivores should be non-cyclic because they are food limited, and as productivity increases their densities should periodically support carnivores which induce irruptive dynamics. The results are contrary to these predictions. The predator community at Pearce Point was relatively persistent from year to year (Chapter 1). Lemmings can show both multi-annual irruptions (Banks I.) and persistent low densities, within this same range of productivities. Lemmings appear not to be food  98 limited at low and relatively stable densities. Evidently the three-level trophic exploitation system can persist at quite low productivities. Adding seasonality to previous models, Oksanen (1990) predicted that for a rapidly reproducing herbivore with short generation time, seasonality is a destabilizing force and should result in chaotic populations limited proximally by food. The results do not fit this model either. Seasonality at Pearce Pt. seems to be stabilizing; strong summer predation limitation is relaxed in winter, allowing population growth and annual density fluctuations of limited amplitude.  Predator Regulation Models of predation regulation in the density dependent paradigm posit a prey density below which prey productivity exceeds predation mortality, and therefore prey population growth is possible (Sinclair 1989, Hanski et a!. 1991). Resulting prey dynamics could be stable, or fluctuate around an equilibrium. I could not measure productivity adequately because I lacked data on fates of juveniles. However, recruitment of adult lemmings was very low in summer (Chapter 1), and the analyses of predator diets indicated that most subadults weaned in summer were killed by predators (Chapter 4). Therefore, predation of adults exceeded recruitment of adults throughout the summer. The result is a destabilizing effect of predation on lemmings in summer. The density dependent predation mortality at Pearce Point is not stabilizing for the following reason. Predation mortality depresses lemming populations at Pearce Pt. until they reach 0.1 to 0.4 adults per hectare (Fig. 2.2, Chapter 1). At such densities, rough-legged hawks do not nest in spring, and experience poor breeding  99 success in late summer, and red fox breeding fails. Consequently, these two principal predators fall out of the system, as in 1992. When these two predators are rare or absent, lemming populations grow, but when they are both present, lemmings continually decline through the summer (Chapter 1). The heavy predation mortality in summer is therefore destabilizing. The persistence of lemmings between years results from winter breeding in the absence of most predators. Rosenzweig and MacArthur (1963) conclude that a stable equilibrium in such exploitative interactions depends on predators’ access to alternative prey, low prey capture efficiency of predators, and interference or territorial behaviour among predators constraining their access to prey. These conditions are not satisfied at Pearce Point. Rough-legged hawks are unable to fully compensate for declining lemming availability with alternative prey (Chapter 4). Prey-capture efficiency is likely high because of the lack of cover with low vegetation (see Janes 1985), shallow lemming burrows, and lack of darkness in summer. Mammalian and avian predators appear unable to constrain each other’s use of the same space. Lemming persistence at Pearce Point therefore depends, not on stability through density dependent predation, which is unstable in summer, but instead on the changing predator community between seasons, which allows population growth in most winters (Krebs  et a!. 1995, Chapter 1). I could identify no factor, other than predation mortality, strongly limiting population growth in summer. The small limiting effects of infanticide and predation risk are most likely side-effects of predation mortality. Habitat heterogeneity remains to be fully investigated. From the mechanistic point of view, predation mortality  100  remains the most likely regulatory factor at low densities in summer. Such regulation is contingent on winter population growth, which, during this study, did not produce spring densities in excess of those which summer predators could depress. Factors limiting winter growth are addressed in Chapter Three.  101 CHAPTER THREE POSSIBLE FACTORS LIMITING WINTER POPULATION GROWTH IN COLLARED LEMMINGS  INTRODUCTION  Winter field studies of collared lemmings (Dicrostonyx spp.) have been limited in scope. Yet lemmings experience winter conditions for at least eight months of the year, so winter population processes, including breeding under the snow, are crucial for their year-round persistence (Fuller et a!. 1975a). Some information is available from laboratory studies and from the field sign these arvicolid rodents leave of their winter activity. Collared lemmings exist as summer and winter morphs. Changes from one morph to the other can be induced in the lab by shifts in photoperiod from summer to winter regimes (Hasler et a!. 1976, Malcolm and Brooks 1985, Mallory et a!. 1986). Individuals raised under winter photoperiods grow faster and reach heavier asymptotic body weights than those under summer photoperiods (Hasler et a!, 1976, Mallory et a!. 1981,1986, Malcolm and Brooks 1985, Reynolds and Lavigne 1989). Winter morphs also assume a more rounded body shape (Malcolm and Brooks 1993). Collared lemmings are the only microtine to moult from a dark summer pelage to a white winter coat, and they develop bifid claws on the third and fourth digits of the forefeet (Hansen 1957). These changes are adaptive. Summer morphs have to increase their resting  \%  102 metabolic rates significantly faster than winter morphs (198% increase at 0°C compared to 16-30% for winter morphs) at temperatures below thermoneutrality (15°C to 20°C) (Chappell 1980, Reynolds and Lavigne 1988). Much of the energetic advantage for winter morphs derives from the thick winter coat and piloerection (Scholander 1950, Chappell 1980), and these winter morphs have significantly reduced minimal thermal conductances (Reynolds and Lavigne 1988). The change in body shape results in a decreased surface area, which also reduces rate of heat loss in winter (Malcolm and Brooks 1993). Increased absolute energy requirements resulting from increased body mass were apparently met in the lab, not by increased food intake, but by increased length of the gastro-intestinal tract in winter morphs (Reynolds and Lavigne 1989). White coat colour seems unlikely to improve energy balance, but is likely an adaptation to avoid detection by predators (Chappell 1980). The bifid claws are assumed to enhance digging in snow (Hansen 1957). Winter morphs can breed in subnivean temperatures of -20°C, and survive temperatures as low as -35°C (MacLean et a!. 1974; Fuller et a!. 1975a). The insulation provided by the nests of dead vegetation they build (MacLean et a!. 1974) is probably critical for such survival and reproduction (Casey 1981). Chappell (1980) maintained the internal temperature of heated copper casts of lemmings, placed in nests at -20°C, with energy inputs equivalent to metabolic rates at thermoneutrality. In a simulation model of brown lemming (Lemmus trimucronatus) energetics, Collier et a!. (1975) found that larger females had improved survival and reproductive capability in winter, but that the energy costs of lactation, combined with consequent additional costs while foraging and rewarming the nest, could often exceed the capabilities of most females.  1.03 Subnivean temperatures appear critical to an understanding of winter population processes. Judged by distribution of nests in spring, lemmings choose areas of deepest snow as winter habitat (MacLean et al. 1974, Fuller et al. 1975a). Snow moderates cold ambient temperatures, keeping temperature at or near the ground substantially warmer at least through early and mid-winter (MacLean et a!. 1.974; Fuller et a!. 1975a; Chappell 1980). Temperature at the ground gradually declines through the winter to a low in March (e.g., -25°C, Fuller et a!. 1975b), and the temperature gradient is reversed for a period in spring (April, May or June) because snow insulates a colder ground from warming air temperatures (Fuller et a!. 1975a; Chappell 1.980). Collared lemmings bred in April or May of every year of population cycles at both Baker Lake, Northwest Territories (N.W.T.) (n Truelove Lowland, Devon I., N.W.T. (n  =  4 yr) (Krebs 1964), and  4) (Fuller et a!. 1975b). Breeding from  November through March was less common at Baker Lake (Krebs 1964), and probably did not occur in all winters on Devon I. (Fuller et a!. 1975b). Weather and snow conditions may limit winter breeding. Shelford (1943) found that winters with breeding leading to a peak density at Churchill, Manitoba, were relatively warm with heavy snow, especially in early winter. At the same locality, Scott (1993) found peak abundances to be correlated with years which combined relatively cold autumn temperatures, minimizing the freeze-thaw cycles in October, and warmer than average temperatures and heavier than average snowfall in November and December. Similarly at Baker Lake, Krebs (1964) found that a winter population increase occurred when autumn was dry, without surface freezing of rain, and was followed  104 by relatively heavy snow. At Barrow, Alaska, MacLean et al. (1974) found that winter breeding leading to a peak was associated with warmer than average spring temperatures. They surmised that deep snow in spring (April to June) keeps the ground cold for longer, thereby making spring breeding more costly (see also Fuller et a!. 1975a). Lemming populations do not increase in all winters with apparently suitable snow and temperature conditions (Krebs 1964, MacLean et a!. 1974). Predation, especially by ermine (Mustela erminea) and least weasels (M. nivalis), may be sufficient to cause overwinter population declines even when lemmings are breeding under the snow (Maher 1967, MacLean et a!. 1974). At Pearce Point, N.W.T., collared lemmings have bred in spring (April or May) under the snow, and perhaps earlier in the winter, in six consecutive winters (Krebs et a!. 1995; Chapter 1). Breeding under the snow was necessary for populations to recover from frequent summer declines driven principally by predation mortality, but in some winters populations declined (Krebs et a!. 1995; Chapter 1). In this chapter I first estimate the extent of reproduction required to achieve observed rates of winter population change at Pearce Point. Second, I test the hypothesis that ermine predation explains differences in population growth between winters. Third, I assess whether wintering microtines use habitats with the deepest snow. Fourth, I assess how much of the variance in rates of winter population change can be explained by a combination of: (i) cold during autumn moult (September and October) limiting potential body growth and accumulation of energy reserves; (ii) thermal conditions under the snow (a combined function of ambient air temperature  105 and snow depth) limiting the proportion of females reproducing and their individual reproductive output during winter (November through March); and (iii) snow depth in spring (April and May) limiting the proportion of females breeding and their reproductive success. METHODS Study Area The study took place at Pearce Point (69°48’N, 122°40’W), on the south shore of Amundsen Gulf, western mainland N.W.T., Canada. The coastal tundra is comprised of dry Dryas/Carex heath, mesic Carex/Salix/Dryas hummock (frost-boil), and wet Carex meadow vegetation communities, all within 20 m a.s.1.. The following climate data are from maps in Maxwell (1980), based on years 1941-72. Pearce Point lies close to the 100 cm isohyet for annual mean total snowfall. The mean date of snow cover formation is October 1, but snow cover can be delayed until November 1. Monthly snowfall is highest in September (17 cm), October (22 cm) and April (12 cm). However, mean snow depth at the end of October is only 5  -  10  cm, because of autumn melting. Mean snow depth reaches 20 cm by the end of November, and 25 cm by the end of January, but stays at that depth until rapid melt in May. The mean daily temperature is approximately 2°C in September, -27.5°C in January, and -5°C in May. Climate Data Mean daily temperature and daily snow-depth were measured at the Department of National Defence radar base at Clinton Point (69°35’N, 120°48’W), approximately 65 km east of Pearce Point, at 101. m a.s.l., but also close to the coast.  106 Data were made available by the Atmospheric Environment Service of Environment Canada. I use these data to represent winter conditions at Pearce Point, since I lack winter data from the study area itself. Long-term climate data (Maxwell 1980) indicate that conditions at Clinton Point are very similar to those at Pearce Point. To estimate the effect of temperature and snow depth on lemming population growth, I derived three indices of thermal stress, corresponding to three time periods with differing degrees of reproduction (Krebs 1964). Autumn cold stress: I used the mean of all mean daily temperatures for September and October as an index of the cold stress a lemming encounters while changing from summer to winter morph. These morphological and physiological changes can be induced at thermoneutral temperatures, by decreasing photoperiod to light available less than 25% of the time (Hasler et al. 1976, Malcolm and Brooks 1985, Reynolds and Lavigne 1988). The role of colder temperatures in the field is unknown. Between August and November the time the sun is above the horizon at Point Barrow, Alaska (71°N) decreases from 65 to 20%, reaching a mean of 9% for November (Chappell 1980). September and October are therefore the critical months for photoperiod-induced changes in morphology. Winter cold stress: During winter (November through March) I calculated an index of cold stress as the sum of all daily snow depths over the period, divided by the sum of mean daily temperatures over the period. Since all mean temperatures were below freezing, this gave the ratio of centimetre-days of snow to degree-days of frost. Higher values of the index actually reflect lower stress under the insulative blanket of snow. Spring cold stress: During spring (April and May) I estimated the insulative power of the snow as the mean daily snow depth  107 over the period. Population Estimation Population densities of collared lemmings and tundra voles (Microtus oeconomus) were estimated using mark-recapture and the open Jolly-Seber population model. Animals were caught alive in Longworth traps and individually identified with numbered ear tags. Densities were estimated on four grids, each 18 to 25 ha, from early June to late August in each of six summers (1988 through 1992). A large portion (11.4 ha) of one grid (PE) was maintained as a predator exclosure, and three other grids were controls (Cl, C2 and C3). However the exciosure was not successful at excluding mammalian predators in winter because drifting snow allowed red foxes (Vulpes vulpes) to enter over the fence, and ermine could get through the fence. Also, most winter nests on PE were outside the exclosure. So I consider PE an untreated population for the winter. Details of trapping and population estimation are in Chapter 1. I did not measure birth and death rates during the winter. Instead I use instantaneous rates of population change, calculated from densities in late summer and early the following summer, as a composite measure of demographic processes. To estimate how many winter litters were necessary to explain the population changes observed between summers, I used a simple difference equation model with three time periods corresponding to the stress indices: autumn, winter and spring. I considered only females of two age-classes, adult (, 35 g) and subadult. I lacked data on number of subadult females in early autumn, but assume these were at least as frequent as adults. I assumed that each nest occupied by ermine represented the  108 death of a female lemming. I assumed a winter litter size of three (Krebs 1964), and a 50:50 sex ratio of neonates. Winter Snow Distribution In late May I mapped the distribution of remaining snow patches on study grids (1991 on PE, Cl and C2; 1992 on PB and C2). I assume that this remnant snow coincides with areas of deepest snow during the winter. This is reasonable because most remnant patches were in the lee of hills or banks where snow drifts form. Drifted snow is relatively dense because wind-blown crystals break and then pack tightly in drifts (Kind 1981). Deep, dense snow melts relatively slowly because upper snow layers insulate lower layers from melting air temperatures, and compact, fine grained snow reflects a high proportion of incoming radiation (Male and Gray 1981). Microtine Winter Nests The density of microtine winter nests was estimated by systematically searching grids, and plotting nest locations, in early summer after snow-melt (PB, Cl, C2 and C3 in 1991; FE and C2 in 1992). In 1992 I did not search Cl and C3 systematically, so cannot estimate nest density. However, I did collect other information on these nests in 1992. I was unable to differentiate lemming nests from those of voles. Weasels line nests they occupy with microtine fur, and leave scats and prey remains nearby (Maher 1967, MacLean et a!. 1974). The only Mustela species in the study area was the ermine. Each nest was examined for sign of occupancy by ermine, and the vicinity was searched for scats and remains (typically stomachs, feet and tails). All nests with ermine sign were removed to search them for prey remains and  109 ear tags. All other nests were destroyed to insure they were not recounted the subsequent year. The association of winter nests with deep snow was tested by comparing the actual distribution of nests, either under snow or in the open in late May, to a random distribution. The random distribution assumes numbers in proportion to the percent of ground either covered or clear of snow in late May. RESULTS  Extent of winter breeding I use data from 1990-91, a winter of population growth, and 1991-92, a winter of decline, to estimate the extent of winter breeding. The number of overwinter adult females in spring 1991 was higher than the number of adults late the previous summer on three of four grids (Table 3.1). However, only one ear-tagged adult female from summer 1990 was found on all grids in spring 1991. Evidently nearly all late summer adults failed to survive the winter, and therefore nearly all overwinter  adults in spring had been born late the previous summer, or had been born in winter. To assess how many litters may have been born in winter, I contrast low and high survival scenarios, with data from grid C2 in 1990-91, the grid with the highest rate of increase, and only lemmings present (Table 3.1). In a low survival scenario I  assume only one subadult female for each adult in late summer, and monthly survival rates of 0.6, 0.7 and 0.8 for autumn, winter and spring periods respectively. The adults surviving to winter would have to produce at least three litters to reach observed early summer 1991 numbers. In a high survival scenario, with two  :iio Table 3.1. Numbers of females on study grids in late summer (end of August) and in early summer (early June), after the intervening winter, and minimum number of females killed by ermine during winter.  Late  Early summer  summer  of next year  Minimum # females by ermine  Adult  Over-winter  Spring-born  (i.e. nests occupied)  Winter  Grid  females  females  males  1990-91  PE  8  6  6  5  Cl  4  6  2  4  C2  3  7  5  3  C3  2  3  4  3  Total  17  22  17  15  PE  11  0  3  0  Cl  1  0  0  3  C2  2  0  0  1  0  1  2  0  4  6  1991-92  C3  Total  15  111 subadults for every adult in autumn, and monthly survival rates of 0.8, 0.9 and 0.9 for autumn, winter and spring respectively, early summer numbers could be explained with only one winter litter per female. These latter survival rates are quite high for microtine rodents, so it seems likely that the strongest population growth from summer to summer is the result of multiple litters in winter, as well as spring reproduction. During the 1991-92 declines, there may have been little or no winter reproduction, but some lemmings survived to breed in spring. I found only springborn lemmings in early summer 1992, indicating that the few adults surviving winter died during the spring. The severe decline on PE may be attributed to red fox predation (in the absence of any sign of ermine predation, Table 3.2), emigration, or very stressful weather conditions. Ermine predation There was no significant difference between 1990-91 and 1991-92 in proportion of nests occupied by ermine (Mann-Whitney U  =  11.5 <U ), 1 . 0 0 although all microtine  populations grew in winter 1990-91 but declined in winter 1991-92 (Table 3.2). The instantaneous weekly rate of population change was not significantly correlated with the percentage of nests occupied by ermine (r  =  0.21, F  =  0.28, P  0.62) over both years (Table 3.2). For winter 1990-91 there was an insignificant trend to lower rates of population change on grids with higher percentage of nests occupied (r  =  -0.75, F  =  2.55, P  =  0.25).  Nest Distribution Winter nests were positively associated with areas of deepest snow  0.0008 0.0008  both microtines  Dicrostonyx only  3.11 4.3  Nest density (#/ha)  Nests per capita  5 (8.9)  Number (%) occupied  by ermine  autumn population  56  Total found  Microtine nests:  -  -  rate of change:  Instantaneous weekly  PE  (9.5)  4  5.3  2.50  42  0.0165  0.0165  Cl  C2  (5.6)  3  7.2  3.23  54  0.0277  0.0277  1990-91  (6.3)  3  (0)  0  4.7  3.39  1.92 9.6  61  -0.0184  -0.0116  PE  48  0.0520  0.0433  C3  1 (2.1)  (13.6)  7.4  2.87  48  -0.0446  -0.0446  C2  3  -  -  22  0.0000  -0.0165  Cl  1991-92  (5.6)  2  -  36  -0.0679  -0.0613  C3  Table 3.2. Instantaneous weekly rates of change of microtines, microtine nest densities, and nest occupancy by ermine on the four study grids over two winters of intensive study (1990-91 and 1991-92). Surveys of Cl and C3 were incomplete in 1992 so nest densities cannot be calculated.  autumn population  a proportion of the  Minimum # killed as  by ermine  Minimum # killed  Microtine remains:  Table 3.2. (continued)  0.38  5  PE  0.75  6  Cl  1990-91  0.93  7  C2  0.80  4  C3  0  0  PB  5  Cl  1991-92  0.15  1  C2  4  C3  I-k  114 accumulation on four of five cases assessed (Table 3.3; Fig. 3.1). The insignificant association on C2 in 1992 may have resulted from a late snow-melt, and my mapping of snow cover before many areas of thin snow cover had melted. Snow and Temperature Regimes Snow depth profiles for the five winters studied (Fig. 3.2 and 3.3) followed generally the same pattern as found in long-term climate data (Maxwell 1980). Most snowfalls in September melted, but snow accumulated rapidly in late October and early November, after which it was relatively stable for the rest of the winter. However, snow depths towards the end of January were all below the 25 cm longterm mean (Maxwell 1980). Only in 1990-91 did snow depths exceed this level in late winter. Dicrostonyx populations grew in three of five winters, and declined in two, and the indices of thermal stress varied substantially between years (Table 3.4). The autumn stress index explained the highest proportion of variance in rate of change (r 2 =  0.67, F  =  6.124, P  =  0.09)(Fig. 3.4). Combining the index of thermal stress in winter  with the autumn index, the explained proportion of variance in rate of population change increased substantially (r 2  =  0.98, F  =  41.09, P  =  0.02). The addition of the  spring index of thermal stress, mean daily snow depth, increased the explanatory power of the model only marginally (r 2  =  0.99, F  =  21.72, P  =  0.16).  The intensity of cold experienced by lemmings when moulting and changing body shape in autumn had lasting effects on population growth in some winters. Autumn 1991 was the coldest of five, and was followed by the steepest population decline (Fig. 3.4). Autumns 1987 and 1988 were the mildest, and subsequent winters  115 Table 3.3. The association of microtine winter nests with remnant winter snow. Snow cover was mapped in late May, and nest distribution, though mapped after snow melt, is related to snow distribution in late May.  Spring 1991  Spring 1992  PE  Cl  C2  PE  C2  Percent under snow  69.8  40.6  27.5  39.6  55.6  Percent in open  30.2  59.4  72.5  60.4  44.4  Percent snow-covered  14.4  8.5  7.2  15.7  48.6  Percent snow-free  85.6  91.5  92.8  84.3  51.4  Sample size of nests  53  32  51  53  45  G test statistic  83.71  24.41  19.05  17.44  0.89  P  <0.001  <0.001  <0.001  <0.001  >0.10  Distribution of winter nests in late May:  Distribution of snow:  116  Fig. 3.1. Map of the distribution of winter nests (dark points) with respect to distribution of remnant snow in late May (hachured line) on PB grid, spring 1991.  0 I  2 I  50,  118  Fig. 3.2. Profiles of mean weekly snow depth (cm) over the nine month periods for winters 1987 through 1990. Data were collected at Clinton Point, approximately 65 km east of the study area.  119  45—  40  • 198849  35 .  1987-88  —•—•-  1989-90  30 25  >,  20  I  I  I  Sept Oct  Nov Dec  Jan Feb Mar Apr  Winter months  May June  120  Fig. 3.3. Profiles of mean weekly snow depth (cm) over the nine month period for winters 1990 through 1992. Data were collected at Clinton Point.  121  45‘—b’  1  40  1990-91  —  1991-92  —•  30 25  >  /  /  20  /  15 I  105. il 0  i I  ‘1  iiiiiiiiiiii  Sep Oct  Nov Dec  1111111111111  ‘‘111111  Jan Feb Mar Apr  Winter months  May June  122 Table 3.4. Mean ( S.E.) instantaneous weekly rates of population change (r) from late August to early June for Dicrostonyx alone on four study grids, combined with three indices of thermal stress which might affect r. These are: Autumn the average of the mean daily temperatures for September and October (°C); Winter the cumulative cm-days of snow cover divided by the cumulative degree-days of frost for November through March; Spring the mean daily snow depth. -  -  -  Indices of thermal stress  Winter  1987-88  r  0.0326  Autumn  Winter  *  -0.66  0.627  6.4  *  -1.41  0.521  8.6  *  -2.38  0.579  5.0  -2.82  0.926  15.0  -4.45  0.720  20.8  Spring  (0.0131) 1988-89  0.0151 (0.0075)  1989-90  -0.0092 (0.0073)  1990-91  0.0243 (0.0108)  1991-92  -0.0327 (0.0149)  *  data from Krebs et a!. (1995)  123  Fig. 3.4. Relationship between instantaneous weekly rate of population change overwinter and the average of mean daily temperatures (°C) during the autumn (September and October) when Dicrostonyx are changing from summer to winter morphology.  124  a  0.OB2  r —0.67  0.05 0.04 0  a  0.03  90-91  0.02 88-89 0.01  0 ‘-  -0.01•  69-90  0  0  O.0 -0.03 91-92  -0,04 -0.05  I  -  -4  -  -  Mean daily autumn temperature (C)  -1  u  125 had high rates of population growth. However, cold autumns could be ameliorated or exacerbated by thermal conditions during winter. For example, average population growth in 1989-90 was less than expected based on autumn temperatures (Fig. 3.4), because there was little snow in winter (Table 3.4, Fig. 3.2). By contrast, growth in 1990-91 was substantially higher than expected based on autumn temperatures (Fig. 3.4), because of thick snow (Table 3.4, Fig. 3.3). DISCUSSION  Ermine Predation The intensity of ermine predation explained little of the variance in winter population growth of microtines in the two years studied. Only within a winter of relatively good thermal conditions (1990-91) did the expected inverse correlation of population growth and intensity of ermine predation hold. Perhaps in this winter, with a high ratio of snow depth to cold temperatures, thermal conditions under the snow were not strongly limiting, and the limiting effect of ermine predation could be expressed. In the colder 1991-92, effects of ermine predation may have been masked by the stronger proximal limitation of cold. In such a winter ermine predation may have been compensatory, or just of low intensity, perhaps because cold puts severe energetic costs on ermine with their elongate body shape (Brown and Lasiewski 1972). The data on ermine predation cover only two winters, so the conclusion that ermine predation explains little of the variance in population growth remains tentative. Theoretical models (Hanski et al. 1993, Hanski and Korpimaki in press) and field data from Fennoscandia (Korpimaki et al. 1991, Korpimaki 1993) and North  126 America (Fitzgerald 1977), suggest that delayed numerical responses of least weasels and ermine to peak microtine populations can cause declines and prolong periods of low density. North American data from some lemming declines support this hypothesis; highest proportions of nests occupied by Mustela spp. coincided with declines on Banks I. (20%, Maher 1967), Devon I. (11-16%, Fuller et a!. 1975a) and at Point Barrow (34%, MacLean et a!. 1974). The proportion of nests occupied at Pearce Pt. was lower, indicating a smaller limiting effect of this predation. The role of ermine predation during low lemming densities varied in other studies. MacLean et a!. (1974) observed no weasel predation, but relatively low snow cover, in the first winter following a decline. There was no substantial lemming population growth until the subsequent winter, when snow cover was much deeper but weasels occupied 5.6% of nests. Fuller et a!. (1975a,b) observed substantial lemming population growth in a summer following a winter with 11 % of nests occupied. Evidently factors other than ermine predation can limit winter population growth at low densities, prolonging the low density phase. Also, factors operating in summer sometimes curtail growth and prolong the low phase. At Pearce Point, ermine predation does not explain differences in population growth between winters, though it is a persistent limiting factor.  Snow Distribution Distribution of lemmings among habitats in winter was strongly influenced by distribution of snow, as previously observed (Maher 1967, MacLean et a!. 1974, Fuller  et a!. 1975a). Wind redistributes snow in drifts, and may keep upland tundra bare or thinly covered. Areas with little or no snow cover are poor winter habitat because of  127 high energy costs and predation risk for lemmings foraging in the open. Snow distribution, if it varies little between winters, probably cannot explain much of the variance in rate of population growth within a study area. However, it may explain differences between regions with differing annual snowfalls. Within the range of Dicrostonyx, annual mean total snowfall varies from less than 50 cm to greater than 200 cm, and mean snow depths in late October from 5 to 50 cm (Maxwell 1980). Pearce Point has relatively little snow on average (ca 100 cm/yr, and 5-10 cm at the end of October, Maxwell 1980), so the limiting effects of snow distribution and depth may be more pronounced here than in eastern regions, where snow is deeper (Maxwell 1980). Winter Temperature Regimes The critical factors limiting winter population growth at Pearce Point appear to be intensity of autumn cold, and depth of snow cover per degree-day of frost in winter. The association of strong population growth with relatively deep snow, especially in November and December, has been noted before (Krebs 1964, MacLean et a!. 1974, Scott 1993). However, combining snow depth with ambient air temperature is a useful index of thermal stress because it relates directly to the energetic costs faced by lemmings under the snow. This supports earlier suggestions (Shelford 1943, Krebs 1964) that relatively deep snow is a necessary condition for the winter breeding which fuels a population irruption. The discovery that autumn cold may curtail winter population growth is new, but expected given the increased metabolic costs faced by summer morphs exposed to freezing temperatures (Chappell 1980, Reynolds and Lavigne 1988). Autumn cold  128 might affect population growth in a number of ways. First, higher metabolic costs  induced by cold should force summer morphs to spend more time foraging, making them more vulnerable to autumn predation. Second, higher metabolic costs may diminish energy for body growth after maintenance requirements have been met, especially for late summer young shifting to winter morphology. This is critical since growth to a larger body mass and more rounded body shape are adaptive for energy conservation (Malcolm and Brooks 1993) and for reproduction in low temperatures (Collier et al. 1975). Third, in severe cold, maintenance energy requirements may not be met, and lemmings may die of exposure. I have no data to address these three mechanisms, but suspect that the third is rare, and the second most likely. Duration of snow cover in spring explained little of the variance in population growth, probably because spring breeding is the last in a sequence of demographic processes starting in autumn. The number of females breeding in spring and their individual reproductive efforts depend primarily on their individual histories in autumn and winter. The winters studied did not include any with benign autumn and winter conditions followed by a spring of long-lasting snow. In such a case, the impact of poor spring conditions on population growth may be stronger, as suggested by MacLean et al. (1974).  Other Factors Affecting Winter Population Growth The frequency and dispersion of foods could influence population growth because distance travelled and time spent away from the nest in feeding affect winter energy balance and reproductive success (Collier et a!. 1975). I lack data on standing crops of foods before each winter. However, these crops appeared to change little  129 between years, so seemed unlikely to strongly influence rates of population change between years within this study. Food availability increases as more tundra is covered in snow. However, I do not know how differing depths of snowfall relate to snow distribution. I can only say that food availabilky, especially as it is influenced by snow distribution, may have been a limiting factor at Pearce Pt. in any of the winters studied. I recommend quantifying standing crops of lemming foods, and snow distribution, in any attempts to explain regional variation in rates of winter population growth. Mallory et a!. (1986) proposed that age structure may influence winter reproductive potential; lemmings born in spring and surviving the summer may not acclimate to winter as well as summer-born young, so an autumn population with a high proportion of older individuals may have relatively lower rates of survival and reproduction. I cannot address this idea adequately because I lack data on recruitment of late summer young as autumn adults. However interannual differences in autumn age structure were probably small because populations suffered heavy mortality in all summers, and there was little recruitment of animals from early summer litters (Chapter 1). A younger age structure, following a summer of population growth, may enhance winter population growth (Mallory et a!. 1986), but only if autumn cold does not impede growth to optimal body size for winter reproduction. Hansson and Henttonen (1985) found a correlation between both snow depth and period of snow cover, and the amplitude of microtine population irruptions in northern Europe. They hypothesized that deeper snow precludes successful foraging  130 by generalist predators such as foxes, thereby enhancing winter survival of  Clethrionomys and Microtus species. Lindstrom and Hornfeldt (1994) found less of these small rodents in fox diets as snow depth increased. Collared lemmings are uniquely adapted to winter with frequent reproduction under the snow (Fuller et a!. 1975a, Malcolm and Brooks 1985, Mallory et a!. 1986, Reynolds and Lavigne 1988). Consequently deep snow that protects them from fox predation should have dramatic effects on population growth, as long as mustelid predators are not abundant. At Pearce Point, snow may get drifted and packed by wind such that it protects lemmings from fox predation, but I lack data on the intensity of this predation. In conclusion, relatively deep snow may enhance winter population growth by providing protection from some predators, as well as by providing thermal cover, and access to food over a relatively wide area.  131 CHAPTER FOUR PATIERNS OF PREDATION ON NON-CYCLIC LEMMINGS: THE GENERALIST PREDATOR HYPOTHESIS  INTRODUCTION  Some microtine rodent populations do not exhibit multiannual cyclicity with high amplitude density fluctuations, but show slower rates of change in density often with an annual pattern (Taitt and Krebs 1985). Andersson and Erlinge (1977) proposed that these more constant prey densities over time might result from limitation to population growth in two ways: (i) generalist predators, with type-Ill functional responses, operating in a community with a relatively diverse prey base (generalist predator hypothesis), or (ii) nomadic avian or mammalian predators  responding rapidly in local abundance and breeding success to growing rodent populations (nomadic predator hypothesis). Hanski et a!. (1991) demonstrated through mathematical modelling that increasing the number of generalist predators, in a predator prey model with multiannual fluctuations, tends to reduce the amplitude and period of fluctuations, eventually to a stable equilibrium point. Rosenzweig and MacArthur (1963) also undertook a theoretical investigation of exploitative predator-prey systems. They concluded that stability in such systems depended on the following conditions: (a) sufficient alternative food to sustain the generalist predators when preferred prey are scarce, (b) relatively inefficient prey capture by these generalist predators, principally because prey have a secure refuge, and (c) predator population growth limited by some factor other than food, and most  132 likely by territorial behaviour. Some of the same species exhibiting constant densities, also exhibit high amplitude, multiannual density fluctuations in other portions of their range (Hansson and Henttonen 1985). The specialist predator hypothesis proposes that an irruption occurs when a population escapes limitation by specialist predators, which have few or no alternative prey when rodents become scarce (Andersson and Erlinge 1977, Hanski et al. 1993). In some other ecological communities rodent irruptions occur despite the existence of predators with a diverse prey base. As an explanation for these dynamics, the alternative prey hypothesis proposes that the alternative prey only partially compensates for declining rodent numbers. Consequently the predators decline, allowing a rodent irruption (Angelstam et a!. 1984, Lindstrom et a!. 1987). The generalist-specialist distinction is not always clear. A true generalist keeps numbers of a prey type within a narrow range by rapidly compensating for any declines in one prey by using other prey. A true specialist can never fully compensate for declines in its prey, so drives prey to lower levels, ultimately too low to maintain itself. Between these extremes, some predators may compensate for declining primary prey to varying degrees depending on annual circumstances, or the local diversity of the prey base. These I will call hlsemi_generalistsu. At Pearce Point, Northwest Territories, Canada, on the western arctic mainland coast, collared lemmings (Dicrostonyx ki!angmiutak) and tundra voles (Microtus oeconomus) remained at low densities over six years, in conjunction with a fairly constant and diverse predator community (Krebs et a!. 1995, Chapter 1). Densities of resident adult microtines rarely exceeded two per hectare, and generally showed  133 annual fluctuations with summer declines, and winter increases driven by breeding under the snow. Predation mortality, principally by red fox and rough-legged hawk (Buteo lagopus), was sufficient and necessary to explain summer population declines of adult microtines, but the fates of subadults remained unclear (Chapter 1). The constancy in microtine numbers makes this system a suitable candidate for testing the generalist predator hypothesis. In this chapter, I test the generalist predator hypothesis by assessing how well each of the principal lemming predators adheres to the following predictions: (i) the dominant predators do not show strong numerical responses to variations in lemming density, (ii) the proportion of lemming biomass in predator diets declines with decreasing lemming abundance, and is compensated for by increased consumption of alternative prey, (iii) predators show weak functional responses at low lemming densities, and stronger functional responses at higher lemming densities (type-Ill response), (iv) at very low lemming densities predators consume virtually no  lemmings due to low capture efficiency. I also test an earlier prediction (Chapter 1) that the majority of subadult lemmings born in summer are killed by predators. METHODS Study Area Intensive research was conducted in a 40 km 2 area immediately inland from Pearce Point, Northwest Territories, Canada (69°49’N, 122°43’W), on the north coast of the western Canadian mainland, from late May to early September of 1990, 1991 and 1992. Gently rolling, glacially scoured hills are frequently broken by dolomite and basalt cliffs, both along the coast and inland. Collared lemmings used three upland  134  habitats: Dryas integrifolia heath, D. integrifolia / Carex rupestris heath, and D. integrifolia / Carex membranacea hummock communities (Krebs et a!. 1995). Tundra voles were restricted to ribbon-like wet Carex aquatilis meadows and wetter hummock communities along stream and lake shores (Bergman and Krebs 1993; Krebs et a!. 1995). Brown lemmings (Lemmus trimucronatus) were extremely rare, and found only in one area of extensive Eriophorum / Carex tussock meadow. A fourth resident vertebrate herbivore, the arctic ground squirrel (Spermophilus parryii) was widespread through the drier upland communities, where well-drained soils provided excellent denning opportunities. Substantial numbers of caribou (Rangifer tarandus) passed through the area in mid to late summer. The numerous cliffs provided excellent nesting habitat for several avian predators: rough-legged hawk, golden eagle (Aquila chrysaetos), peregrine falcon (Falco  peregrinus), gyrfalcon (Falco rusticolus), raven (Corvus corax), Thayer’s gull (Larus thayeri) and glaucous gull (L. hyperboreus). The following alternative prey species were regular non-colonial nesters or summer residents within a 10 km inland radius  of Pearce Pt: tundra swan (Cygnus columbianus), Canada goose (Branta canadensis), common eider (Somateria mollissima), semipalmated plover (Charadrius semipalniatus), golden plover (Pluvialis dorninica), Baird’s sandpiper (Calidris bairdii), pectoral  sandpiper (Calidris melanotos), horned lark (Eremophilia alpestris), American pipit (An thus rubescens), Lapland longspur (Cal carius lapponicus) and snow bunting (Plectrophenax nivalis). The following species were numerous on migration: snow goose (Chen caerulescens), northern pintail (Anas acuta), oldsquaw (Clangula hyernalis), red-breasted merganser (Mergus serrator), sanderling (Calidris alba).  135 Microtine Populations Population densities of lemmings and voles were estimated with the Jolly Seber open population model using data gathered in weekly or biweekly livetrapping (Longworth traps), marking with ear tags, and repeated recapture, on three areas (grids), each 18 to 25 ha, and each including a range of vegetation communities. Juveniles of summer cohorts were caught infrequently, so densities are of resident microtines only (i.e. adults and subadults caught at least twice on the same grid). A predator exciosure was built on a fourth grid, but data reported here refer only to the three control grids. For further details on procedures see Chapters 1 and 2. Lemmings over 35 g (adults) were fitted with a radio-transmitter (Biotrack Inc., model SS-1) mounted to a cable tie as neck collar (total weight c. 3 g) in all three years. Voles over 35 g (larger adults) received radiocollars only in 1990. Relocations of radiocollared individuals every two or three days gave data on cause and timing of death. At each capture individual weight, using a spring-loaded Pesola scale, and reproductive condition were recorded. Date of parturition was estimated using changes in weight, degree of closure of the pubic symphysis, and teat size. Lactating female Dicrostonyx typically use one maternal burrow (Brooks 1993; unpubi. data this study), and juveniles are weaned at 15 to 20 days (Brooks and Banks 1973). I assumed that a litter was not successfully weaned if either lactation ended, or the female was located at least twice in a burrow >30 m from the natal burrow, prior to the expected weaning date (see Brooks 1993). A small sample of litters born above ground in traps, nest boxes or sedge tussocks gave an estimate of mean litter size  136 within four days of birth. By combining these data, I estimated the numbers of juveniles weaned per unit area (Chapter 1).  Habitats Habitats as classified by Krebs et at. (1995) were mapped to quantify the regional availability of collared lemming habitats. For study grids, mapping was done on foot. For a regional assessment, digital Landsat data were used in a supervised classification of habitats. The area of each habitat type available to lemmings was assessed in two zones, with obvious differences in representation of the habitats. A coastal zone (21.82 2 km ) , in which exposed sand and rock was more common, included all study grids. An inland zone (832.96 km ) had relatively even vegetative 2 cover, with little sand or rock.  Predator Numerical Responses Numerical responses of predators include both the numbers of adults establishing breeding territories in spring, and the numbers of young successfully weaned or fledged in summer. I lack data on predator numbers in winter. In late May and early June all cliffs within the 40 km 2 study area, including areas up to 6 km inland from Pearce Pt. harbour, were searched for raptors establishing nests or showing territorial behaviour. I recorded clutch size, hatching success, and fledging success with subsequent visits to all cliffs in mid-June, early July, and early to mid August. One red fox natal den was located in the 40 km 2 study area. I observed the den from a distance periodically, and visited it regularly to collect scats (see below). From these observations, and frequent sightings of foxes, numbers of adults and juveniles  137 were counted. Individual foxes were readily recognized by their unique coat colouration and pattern as adults, and after mid-July as juveniles. I captured one nonlactating female in a Novak leg-snare in June 1991, and gave her a coloured ear tag. Ravens, and both species of gulls, nested on inaccessible mainland and island sea-cliffs, and I was unable to accurately count active nests and breeding success. I did not accurately estimate populations of arctic ground squirrels, another lemming predator (Boonstra et al. 1990), in all years. However, I obtained an index of squirrel abundance in early July of 1991 and 1992 by placing microscope slides covered in talcum powder (see Boonstra et a!. 1992) in all burrow mouths in three areas separated by at least two kilometres, and counting the proportion of slides tracked by squirrels within 24 hours. Also in 1992, live-trapping (Tomahawk traps) and coloured ear-tagging of squirrels at all burrows on three, one-square-kilometre study blocks, were combined with periodic observations of the blocks, to get an absolute count of adult squirrels prior to weaning of juveniles. Ermine (Mustela erminea) were summer and winter residents, and bred in the study area each summer judged by casual observations, but I did not make an accurate population estimate. I estimated grizzly bear (Ursus arctos) numbers based on occasional sightings and track sizes. Predator Diets Collections: I collected pellets of all resident raptorial birds, except the raven, and scats of two mammalian predators, the red fox and grizzly bear. Regurgitated pellets of raptors and gulls were collected systematically at egg-laying in late May and early June (pre-incubation sample), at hatching in late June and early July (incubation sample) and at fledging in mid to late August (nestling sample) (cf. Poole  138 and Bromley 1988), at a series of obvious raptor perches (cliff tops, glacial erratics, rock outcrops) throughout the study area. The 1990 collections did not include perches used by gulls or golden eagles, and the collection area was expanded in 1991 and 1992 to sample these species. Because eagle eggs hatch in early June at this latitude (Poole and Bromley 1988) all eagle pellets were lumped together as a nestling collection. Nearly all gull pellets were probably from glaucous gulls judged by observations of perch use by gulls. To minimize disturbance, I did not collect pellets and prey remains at or below nests during the reproductive period. At each collection every pellet was removed, its length and maximum diameter were recorded, and it was individually bagged and labelled I collected fox scats systematically from the same sites as the raptor pellets, systematically from the natal den and two other intermittently-used dens, and opportunistically whenever fresh scats were found. In 1990 systematic collections were monthly, and in 1991 and 1992 biweekly. At each collection, every scat was removed, its maximum diameter recorded, and it was individually bagged and labelled. Most scats were collected at the natal den. This sample likely consisted of scats from adults and juveniles, which might have had different diets. I used the frequency distribution of maximum diameters of scats to differentiate juvenile from adult scats. I collected all grizzly bear scats encountered. Analyses: Fox scats were autoclaved, and soaked in water for 24 to 72 hours to loosen material. To remove soluble material, I washed scats through a series of seives, with paper towel on top of the lowest seive to catch small undigested  139 remains. Remains were air dried. All bones (as small as microtine molar teeth), large feathers, eggshell, insect parts and large pieces of vegetation were separated by hand, leaving a set of remains consisting mostly of mammalian hair sometimes mixed with small feathers, small pieces of vegetation and inorganic debris (mostly sand). The percentage by weight of each component of this latter set of remains was estimated by eye, taking account of the higher density of inorganic debris. All sets of remains were weighed (± O.05g). Remains were identified to species (mammals), or order (birds, insects), using reference material collected in the field and from museum collections, and using molar teeth descriptions in Banfield (1974), hair keys in Kennedy and Carbyn (1981) and Adorjan and Kolenosky (1969), and feather keys in Day (1966). Since molar teeth are the most recognizable microtine remains in fox scats (Lockie 1959), and each of the 12 molar teeth of each of the three microtines in our study area is unique, I recorded the frequency of each molar tooth in each scat. When remains included two microtines, I calculated the relative proportions of hair and bone weights based on the relative proportions of molar teeth (Lockie 1959). When microtine skeletal material was lacking, I differentiated voles from lemmings by hair colour. Raptor pellets and bear scats were separated by hand into the same sets of remains as fox scats, and components were identified using the same reference material and keys. Conversions to biomass: For fox scats I used information in Lockie (1959), Goszczynski (1974) and Reynolds and Aebischer (1991) to provide the following  140 multiplicative factors to convert total weight of undigested remains by species (mammals) or order (birds) to biomass of prey killed: voles (23), ground squirrels (45), large mammals such as caribou (Rangifer tarandus) and grizzly bear (100), passeriform and charadriiform (“smalli birds (45), anseriform and galliform (“large’ ) t birds (61), eggshell (9.1). For lemmings I used a factor of 28, because adult lemmings are substantially larger, with shorter appendages, and a more globular body form with lower surface to volume ratio, compared to the vole species studied by Lockie (1959) and Goszczynski (1974). Insects were ignored in biomass estimations, as they were mostly in trace quantities in the scat. I assumed that foxes ate a similar proportion of ground squirrel carcasses as they would lagomorphs, because of the similar body sizes of these prey. I used a factor of 100 for large mammals, a figure intermediate to those provided by Lockie (1959) and Goszczynski (1974). An alternative approach to biomass estimation suggested for foxes by P.-O. Palm (unpubl. data), and for ermine by Gamberg and Atkinson (1988) assumes that mammalian hair is not digested at all. This is a valid assumption judged by the microscopic appearance of hair in fox scats. To determine the relationship between hair and body weights, I removed hair from pelts of 14 Dicrostonyx collected by N. Larter on Banks I., N.W.T., by soaking pelts in water for a few days, and gradually scraping away the hair (Gamberg and Atkinson 1988). A conversion factor was derived from the weight of hair as a proportion of body weight. For raptors, conversion factors relating remains in pellets to biomass ingested were unavailable. Mandible length is a good predictor of body weight (Hamilton 1980), but mandibles were partially digested in most pellets. However, the molar  141 tooth rows on dentary and maxillary bones were frequently intact, along with numerous separate molar teeth. I can use these to assess lemming biomass ingested if I assume that: (i) all lemming heads are ingested, (ii) all lemmings ingested are represented by at least one tooth, and (iii) the length of the molar tooth rows are significant predictors of body weight. To test the first two assumptions for roughlegged hawks, volunteers fed freshly thawed lemmings, originally from a laboratory colony, to a captive hawk in a 5 x 5 x 3 m outdoor aviary (Orphaned Wildlife Rehabilitation Centre, OWL, Delta, British Columbia), at approximately midday in April, and at two rates: 2 lemmings/d for seven days, followed by four lemmings/d for thirteen days. Pellets were collected daily, and the hawk was weighed at the beginning and end of each period. Light regimes differed from the 24 h daylight of an arctic summer, but temperature regimes were not much warmer at the southern latitude of the experiment. To test the third assumption, I measured tooth row lengths of 17 collared lemmings collected on Banks I., N.W.T., in summer 1993. Conversion to number of individuals killed: For foxes, estimates of daily consumption rates (g/d) in each time period are derived from lemming biomass (g) per scat by multiplying by an assumed defecation rate (scats/d) (see below). This consumption rate (g/d) is converted to numbers of individual adult and subadult lemmings consumed each day, based on the proportions of adults and subadults in the diet for that time period (see below), and the mean live weights of these age classes (g) in the population, based on live trapping during the same time period. For foxes, daily defecation rate varies from one to six scats for a poorly fed fox (ingesting 200 g/d) to eight to twelve scats for a well fed fox (600-800 g/d), giving a  142 reasonable mean of seven for an intermediate diet of 300-500 g/d (P-O. Palm, unpubi. data). To differentiate adult (>35g) from subadult (<35g) lemmings in scats, I used the bony parts most frequently found intact (ulna, and upper and lower molar tooth rows), and for which a linear dimension varied with body size. I used a sample of 17 collared lemmings from Banks I., to determine the regression relationships between body weight and the lengths of these bony parts. For each collection period I assumed that the ratio of subadults to adults in scats represented the relative proportions of those age classes ingested. I also assumed that subadult remains represented only weaned individuals, since bones of suckling juveniles are brittle and unlikely to pass intact through fox digestive tracts. For rough-legged hawks I used the captive feeding experiment (see above) to determine what proportion of lemmings ingested were represented by unique molar teeth in pellets, and therefore calculate a conversion factor relating number of individuals in pellets (maximum number of unique molar tooth) to number of individuals ingested. I used this experiment to test the assumption that the ratio of adult to subadult lemmings in pellets, as determined by molar tooth row lengths, represented the relative proportions of these age classes ingested. Calculating daily consumption rates depends on casting rate of pellets, which I also calculated from the captive feeding experiment. For foxes and hawks, the sex ratio of lemmings ingested was estimated from the incidence of undigested male and female pelvic bones, differentiated on the length of the ischium and the width of the pubis (Dunmire 1955).  143 Total impact of predation: For fox predation, daily consumption rates of adult and subadult lemmings were converted to total impact for the time period by multiplying by the number of foxes (adult or juvenile) present during the time period, and the length of the period (d). The results from each time period were summed to give total impact over the summer. An estimate of the area foxes used in summer to kill all adult lemmings in scats was based on numbers of adult radio-collared lemmings killed on study grids over a summer, and the area of collared lemming habitat on study grids and in the two regional zones of differing habitat availability. Collared lemmings were located 97% of the time in three habitat types (Dryas heath, Dryas/Carex heath, and Carex/Dryas hummock) (Krebs et a!. 1995), which I consider collectively as lemming  habitat. Lemming habitat comprised 36.6 ha of the study grids on which mortality data were collected, allowing a calculation of numbers killed/ha of lemming habitat. Foxes hunted throughout the coastal zone, so the number of lemmings they killed in this zone was the number killed/ha of lemming habitat multiplied by the number of hectares of lemming habitat in this zone. The remainder of their kill was from the inland zone. The area of inland zone they used was based on the numbers killed/ha of lemming habitat on study grids, and the proportion of lemming habitat in the inland zone. The total estimated area traversed by foxes was the entire coastal zone plus the area of the inland zone required for the remaining kill. To calculate the impact of fox predation on subadult lemmings I assume that subadults were weaned in lemming habitat, and killed within the area traversed by foxes hunting adults. Numbers of subadults available were based on mean litter size,  144 number of litters weaned/ha of lemming habitat on study grids, and the total area of lemming habitat in the area traversed by hunting foxes. The total impact of adult rough-legged hawk predation was calculated in the same manner as red fox predation. I lacked data on diets of nestlings. Predator Functional Responses I have good estimates for adult lemming densities only. Predator functional responses are therefore considered only for predation on adult lemmings. For foxes and rough-legged hawks, daily consumption rates of adult lemmings were taken from the scat and pellet analyses (see above) and plotted against the regional adult lemming density for the same time period, estimated as the mean of densities on three control grids.  RESULTS  Microtine Demography Mean densities of resident Dicrostonyx declined sharply during summers 1990 and 1991, while Microtus on the same study grids maintained relatively stable or slightly declining densities (Fig. 4.1). Both species virtually disappeared from grids in winter 1991-92, remaining absent or at extremely low densities through summer 1992 until August. Red foxes and rough-legged hawks, together, were the cause of between 57% (1991) and 72% (1990) of all confirmed predation mortalities of adult lemmings (Table 4.1). A number of the mortalities attributed to an unspecified raptor could have been rough-legged hawk kills, but may also have been peregrine falcon or gull kills.  145  Fig. 4.1. Mean densities (numbers/ha) of resident collared lemmings (solid line) and tundra voles (broken line) on the three study grids. Solid bars represent winter, during which densities are interpolated.  146  1,2-  1.1 ‘  * Cl,  1990  1991  1992  09 0.8  0.7 Cl)  ‘5  a  06 0.5 A 1”  04  “-7  0.3  ‘  0.2 ‘%_.“,__  ‘ 0.1  0  I  I  I  I  Junejulyaug  I  I  I  I  I  I  I  June  I  I  I  I  I  I  I  I  Julyaug  Time (weeks)  I  “  june  July  aug  147 Table 4.1. Numbers of confirmed predation mortalities of radio-collared adult collared lemmings attributable to individual predator species. The sex ratio (male:female) of adults killed by the two principal predators is indicated in parentheses.  Predator species  1990  Red fox  21 (7:14)  1991  1992  4 (2:2)  0  Suspected fox  5  4  0  Arctic ground squirrel  0  2  0  Grizzly bear  0  2  0  Ermine  0  0  0  Rough-legged hawk  7 (4:3)  Peregrine falcon  0  1  1  Unknown raptor  6  7  0  39  37  1  Total  17 (11:6)  0  148 Ermine did not kill lemmings on study grids in summer, though they did in winter (Chapters 1 and 3). Ermine appeared to avoid tundra beyond 50 m of rocky cover in summer. For lemmings, mean litter size across all cohorts and all years was 5.0 (S.E. 0.27, n  =  27). In 1990 lemmings weaned 14 litters on study grids exposed to predation  (36.6 ha lemming habitat), and in 1991 seven litters. Numerical Responses of Predators Microtine densities differed little between years 1990 and 1991, but both microtine species were extremely rare in 1992 (Table 4.2, Fig. 4.1). Red fox and roughlegged hawks, the principal lemming predators, showed obvious numerical responses to low microtine densities in 1992 (Table 4.2; Fig. 4.1). Three red foxes died during the 1991-92 winter. The female ear-tagged in 1991 was seen at the den with one pup on 14 June 1992, but not again. The den was virtually unused after 21 June, and only one of three adults from June was seen later in the summer. At least two roughlegged hawk pairs were seen in late May 1992, but none nested. By contrast, three other raptors, and the other mammalian predators, showed little or no numerical response to the very low microtine densities in 1992 (Table 4.2). Numbers of nesting gulls of both species were noticeably lower in 1992, perhaps in response to low lemming densities, but I lack quantitative data. Steep summer declines in lemming abundance in 1990 and 1991 appeared to affect red fox and rough-legged hawk breeding success. I do not know how many fox pups were born, but in 1991 only two of five pups were weaned. In 1990, rough legged hawks abandoned two nests (eight eggs) in early July, just prior to hatch, and  149 Table 4.2. Numbers of raptor pairs establishing breeding territories, numbers of nests successful and young fledged, and numbers of adult and weaned juvenile mammalian predators, in relation to mean adult Dicrostonyx density (#/ha) and combined mean adult Dicrostonyx and Microtus densities (#/ha) in spring (early June) and summer (early July) on three study grids. 1990  1991  1992  Dicrostonyx  1.03  0.84  0.01  Both microtines  1.15  1.09  0.03  Dicrostonyx  0.73  0.62  0  Both microtines  0.88  0.88  0.01.  Spring densities:  Summer densities:  Raptor territorial pairs: Rough-legged hawk  4  6  0  Peregrine falcon  5  5  6  Golden eagle  1  1  1  Gyrfalcon  0  0  1  Rough-legged hawk  2 (3)  3 (5)  0  Peregrine falcon  5(10)  2 (2)  4(10)  Golden eagle  1 (1)  1 (1)  1 (2)  Gyrfalcon  0  0  1 (2)  Successful nests (# fledglings)  150 Table 4.2. (continued) 1990  1991  1992  Red fox  2 (3)  3 (2)  3 to 1 (0)  Ermine  ? (.2)  ? (3)  ? (2)  Grizzly bear  1 (0)  1 (0)  2 (0)  Mammal adults (# weaned young)  151 three young fledged from the remaining eight eggs. In 1991, three pairs abandoned nests (11 eggs) in late June, close to hatch, and five young fledged from 11 other eggs. Chicks were food stressed judged by aggressive actions of larger chicks aimed at smaller ones, and discovery of chick remains below two nests. By contrast peregrine falcons fledged 10 young from 14 eggs in 1990, and also in 1992 when lemmings were scarce. Their low success in 1991 (two fledged from 16 eggs) resulted from predation on one nest, and two intense storms, one of which washed a nest off a cliff, the other hitting when young were downy but quite large. In 1992, gyrfalcons and golden eagles fledged all young hatched. At least one gyrfalcon used the area in 1990, but I found no evidence of nesting. The mean proportion of microscope slides with ground squirrel tracks on four sample areas was 0.38 (S.E. 0.12) in 1991, and 0.17 (S.E. 0.06) in 1992, indicating a decline between years. In 1992, 11 resident squirrels occupied three km 2 prior to the emergence of young. The density of double burrows (cf. Carl 1971) was 9.3/km 2 (S.E. 1.4, n  =  2 blocks). 4, one km  Grizzly bears occasionally visited the study area, each individual spending only from two to ten days in a summer, though one denned in the area in winter 1990-91. In 1990 and 1991 one pair of rough-legged hawks (RLH) nested seven km west on the coast, and in all years a pair of peregrine falcons (PF) nested seven km inland, but we lack complete data on these nests outside the intensive study area. Beyond these the nearest raptor nests (RLH and PF) were 12.5 km inland. One pair of RLH nested at this site in 1992, suggesting that microtine densities inland may have been  152 higher than at the coast. In summary, and as far as numerical responses are concerned, rough-legged hawks, red foxes and perhaps glaucous gulls, acted as specialists, whereas grizzly bears, golden eagles, peregrine falcons and gyrfalcons acted as generalists.  Predicting Lemming Body Weight Ulna length, mandible length (cf. Hamilton 1980), and upper and lower molar tooth row lengths were all significant predictors of live body weight for Dicrostonyx (Table 4.3). Hair weight was also a significant predictor of body weight (Table 4.3). Hair comprised a mean 2.8% ±0.14% S.E. of body weight, giving a conversion factor of hair weight in scats to body weight ingested of 36.  Fox diet Differentiating adult and juvenile scats: There was a shift in the percent frequency of maximum diameters of fox scats at the natal den in 1991 from June to mid-July, and again from mid-July to August (Fig. 4.2). The frequency distribution of diameters of scats collected away from the den in June and July 1991, presumably all adult scats, was most similar to the August distribution at the den (Fig. 4.2). I assume that juveniles contributed the great majority of scats <1.5 cm in diameter in June and July, and use this diameter to differentiate juvenile from adult scats at the natal den. Composition: Few fox scats were collected in both June 1990, when collections were not made at the natal den, and July and August 1992, when only one fox was observed and regular collections found very few scats (Table 4.4). Fox diets were similar in 1990 and 1991 on a percent frequency of occurrence  153 Table 4.3. The linear regressions of live body weight (g) of Dicrostonyx (dependent variable) on lengths (cm) of mandible, ulna, and upper and lower molar tooth rows, and from weight (g) of hair.  Independent  Regression equation  variable  n  2 r  F  P  Mandible length  log y  =  0.855  +  4.367 log x  16  0.73  37.1  <0.001  Ulna length  log y  =  1.012  +  2.684 log x  17  0.91  146.8  <0.001  Upper tooth row  log y  =  -2.626  +  4.954 log x  17  0.85  84.6  <0.001  Lower tooth row  log y  =  -1.783  +  4.011 log x  17  0.80  60.9  <0.001  Hair weight  y  14  0.99  836.6  <0.001  =  34.45 x  154  Fig. 4.2. Frequency distributions (percent) of maximum diameters of red fox scats collected at (a) the natal den from 29 May to 6 July 1991 (n=83), (b) the natal den from 7-20 July 1991 (n=47), (c) the natal den in August 1991 (n=58), and (d) away from the natal den in June and early July 1991 (n=23).  ________  155  25 20 15  10 5 °1.1  1.2 1.3 1.4 1.5 1.8 1., 1.9 19  2  21 2:2 2:3 2!4  25  >\  U C cD D  b  20  j5 11  1. 1.3 1. 1.5 1. 1. 1.8 1.12.2 24  25  20 15  C  10  cI_) U L_  I1I  1.5 I.E 1.7  .H 1 2  2.1 2.2 2.4  a)  25 a d  20 15  nu  10  5 011  1. 1.4 1. 1.8 1.7 1.8 1.9  Maximum  2L  23 2:4  diameter (cm)  8 0 8 8 0 0 8  Lemmus  Spermophilus  Rangifer  ljrsus  Vulpes  Unidentified  100  Microtus  Dicrostonyx  Mammalia:  Prey type  June  0  2  0  8  20  0  20  80  July  1990  0  0  3  11  53  0  13  82  Aug  2  4  4  0  24  0  14  92  2-22  June  0  0  0  2  54  0  21  77  -July 6  2  2  0  0  45  0  29  75  7-20  June 23 July  1991  0  0  0  19  62  0  32  70  -Aug 3  July 21  Table 4.4. Percent frequency of occurrence of all prey remains in red fox scats.  0  0  0  14  50  5  50  64  4-17  Aug  0  0  0  20  74  0  52  83  18-31  Aug  0  3  0  37  34  0  37  63  June  0  0  0  30  60  0  40  50  & Aug  July  1992  01  -  3  7 0  —  -------  35  46  22 —------  37 55 52 50 38  61  13  Sample Size:  0  0 0 0  0 0 0 0  2  0  Crustacea:  0  17 24 15 0 4  11  3  Coleoptera / Hymenoptera 0  23  0  15 4  4  5  8  15  Eggshell  Insecta:  ---  14  20 14 19 29  12  8  11  8  8  Unidentified  10  0  20  40  20  0  11 2 14 5  7  6  5  Charadriiform Passeriform  5  15  10 6  0  2  0  4  0  0  7  0  0  0  0  —---  & Aug  July  4  6  June  1992  0  —--  18-31  4-17  -Aug 3  7-20  2-22  -July 6  Aug  Aug  July 21  June 23 July  June  1991  8  0  2  0  Galliform  /  24  Aug  18  July  15  June  1990  Anseriform  Ayes:  Prey type  Table 4.4. (continued)  -  ci  158 and a biomass per scat basis (Tables 4.4, 4.5 and 4.6). Dicrostonyx was by far the most common food item, but was found in fewer scats and contributed less in biomass later in the summer, as lemming densities declined. The frequency and biomass of Microtus and Spermophilus generally increased as the summer progressed; voles bred steadily through this period, and ground squirrels became more common with the emergence and dispersal of juveniles after mid-July. Caribou was a common prey item only in late summer 1991, Some caribou calves became separated from their mothers in the study area on migration in July and August, and foxes may have been able to kill a weak calf or scavenge from a carcass. There was one adult caribou carcass and one grizzly bear carcass in the intensive study area in 1990, providing scavenging opportunities for foxes. One adult male ermine was found, with its skull crushed by fox, at the natal den in June 1991. Birds were taken in all months, but were most frequent and contributed most in biomass in July and August (Tables 4.4, 4.5 and 4.6) coincident with vulnerable young leaving the nest (especially in sandpipers and plovers) and with adult moult (especially in ducks and geese). Unidentified bird remains (bones and feather shafts) could most often be assigned to “large (anseriform and galliform) or “small” (charadriiform and passeriform) bird classes for biomass estimation, even if they could not be classified to order. Remains of red-breasted merganser, oldsquaw, snow goose, and snow bunting were found at the natal den. Gallinaceous bird remains were likely rock ptarmigan (Lagopus mutus), which were very rarely seen in the study area, but may have been more common inland. Most insect remains were bumblebees (Bombus sp.), and an unidentified crab species comprised the crustacean remains.  0.6 ± 0.5 ( 1)  84.8 ± 11.5  Egg  Total  ( 0)  <0.1  Small bird  81.8 ± 6.9  0.3 ± 0.2 ( 0)  0.1 ± 0.1 ( 0)  89.1 ± 9.3  0.9 ± 0,7 ( 1)  2.7 ± 2.2 ( 3)  10.2 ± 3.5 (12)  25.4 ± 8.9 (29)  7.0 ± 6.0 ( 8)  Large bird  1.3 ( 3)  3.2 ± 1.7 ( 4)  4.6 ± 3.3 ( 5)  Large mammal  +  30.1 ± 6.4 (37)  2.8  34.3 ± 5.9 (42)  34.0 ± 6.0 (42)  38  August  3.8 ± 1.8 ( 4)  9.8 ± 4.0 (11)  1.4 ± 1.4 ( 2)  36.2 ± 5.4 (41)  Spermophilus  67.6 ± 10.0 (80)  35.3 ± 5.1 (40)  11.1 ± 3.4 (12)  b)  Dicrostonyx  66.2 ± 10.8 (78)  3.2 ± 3.2 ( 4)  a)  Dicrostonyx  44  13  Microtus  n:  Adult scats  July  June  1990  -  22  13 June  ( 0)  142.3 ± 11.2  0  1.8 ± 0.9 ( 1)  7.1 ± 3.1 ( 5)  27.7 ± 10.6 (19)  31.5 ± 10.3 (22)  33.4 ± 12.5 (23)  40.9 ± 10.6 (29)  45.3 ± 11.2 (32)  1  28 June  13  -  90.8 ± 20.1  0.1 ± 0.1 ( 0)  2.4 ± 1.8 ( 3)  3.3 ± 3.3 ( 4)  9.0 ± 8.4 (10)  24.6 ± 16.9 (27)  16.1 ± 6.9 (18)  35.3 ± 9.8 (39)  38.5 ± 11.7 (42)  14  1992  ( 0)  87.3 ± 17.7  1.6 ± 1.0 ( 2)  0  12.2 ± 9.7 (14)  3.0 ± 2.0 ( 3)  23.4 ± 8.9 (27)  19.3 ± 9.0 (22)  27.7 ± 11.6 (32)  28.4 ± 12.2 (33)  10  July & August  Table 4.5. Mean ± S.E. biomass (g) per scat for red fox, and percent of total biomass (parentheses) of principal prey groups in summers 1990 and 1992. Juvenile and adult scats are recorded separately where sample size permits. All biomass estimations are based on conversion of all prey remains, except for Dicrostonyx a) which is based on hair alone. “n” is sample size of scats.  0 3.9 ± 3.6 ( 8) 3.7 ± 3.7 ( 7) 0  51.5± 6.8  Large mammal  Large bird  Small bird  Egg  Total  (0)  (0)  6.6 ± 4.3 (13)  Spermophilus  34.9 ± 5.5 (68)  33.5 ± 5.0 (65)  17  July  2.3± 2.3(4)  b)  Dicrostanyx  June  1990  Microtus  a)  Dicrostonyx  Juvenile scats n:  Table 4.5. (continued)  August 1 -  13 June  14 -  28 June  1992  July & August  C  0.3± 0.2(0)  0.8 ± 0.6 ( 2) 0.6± 0.4(1)  0.7 ± 0.5 ( 1) 0.9± 0.5(2) 0  59.4 ± 6.6  7.5 ± 4.7 (11) 3.2± 0.9(5) 0.5 ± 0.2 ( 1)  70.2 ± 9.2  5.4 ± 44 ( 7) 4.8± 2.1(6) <0.1  75.1 ± 6.2  10.9 ± 6.8 ( 9)  3.3± 2.5(3)  0.1 ± 0.1 ( 0)  118.9 ± 15.0  Large bird  Smallbird  Egg  Total  41.9 ± 5.5  ( 0)  2.8 ± 1.3 ( 4)  0.6 ± 0.5 ( 1)  1.5 ± 0.7 ( 3)  0.9 ± 0.9 ( 1)  0.2 ± 0.2 ( 0)  1.7 ± 1.4 ( 1)  Large mammal  0  30.3 ± 6.2 (42) 17.4 ± 5.7 (42)  23.6 ± 4.5 (40)  13.2 ± 3.6 (19)  29.3 ± 6.7 (39)  17.7 ± 7.1 (15)  Spermophilus  ( 0)  11.0 ± 2.3 (15) 8.6 ± 2.7 (21)  6.0 ± 1.8 (10)  9.9 ± 3.1 (14)  6.6 ± 2.7 ( 9)  5.2 ± 2.8 ( 4)  Microtus  ( 0)  26.6 ± 3.3 (37) 13.5 ± 3.4 (32)  26.7 ± 5.5 (45)  35.0 ± 5.9 (50)  29.0 ± 6.2 (39)  80.0 ± 12.0 (67)  b)  Dicrostonyx  26.4 ± 3.5 (36)  12.8 ± 3.3 (31)  28.1 ± 6.1 (47)  35.7 ± 6.9 (51)  26.9 ± 6.1 (36)  80.2 ± 13.0 (67)  a)  Dicrostonyx  72.8 ± 6.0  0.1 ± 0.1 ( 0)  1.7 ± 0.7 ( 2)  46  22  37  33  27  n:  Adult scats:  29  Augl8-31  July21 -Aug3  July7-20  June2-22  June23 -July6  Aug4-17  1991. Juvenile and adult scats are recorded separately for periods in which they could be differentiated. Other details as in Table 4.5.  Table 4.6. Mean (j S.E.) biomass (g) per scat for red fox and percent of total biomass (parentheses) of principal prey groups in summer  a)  0  0.6 ± 0.4 ( 2)  0  <0,1  37.2 ± 3.8  Large mammal  Large bird  Smalibird  Egg  Total  (0)  (0)  (0)  5.6 ± 2.8 (15)  Spermophilus  27.5 ± 2.6 (74)  (0)  (0)  (0)  43.1 ± 3.2  0  3.1± 2.2(7)  0  0  11.9 ± 3.7 (28)  2.2 ± 1.2 (5)  26.0 ± 3.4 (60)  24.5 ± 3.3 (57)  25.5 ± 2.6 (69)  3.5 ± 1.9 ( 9)  b)  Dicrostonyx  25  June23 -July6  21  June2-22  Microtus  a)  Dicrostonyx  Juvenile scats: n:  Table 4.6. (continued)  (0)  (0)  39.5 ± 3.5  0  1.4± 1.1(4)  1.9 ± 1.0 (5)  0  10.2 ± 3.1 (26)  6.1 ± 2.6 (15)  19.9 ± 4.4 (50)  18.8 ± 4.3 (46)  22  July7-20 July21 -Aug3  Aug4-17  Augl8-31  163 In June 1992 fox diet was similar to that in late summer 1990 and 1991 (Tables 4.4 and 4.5), with a relatively high incidence and biomass of birds, and mammals other than lemmings. This pattern appears directly related to the extremely low lemming densities. Foxes still managed to find lemmings to eat, perhaps by travelling inland or by finding pockets of higher density than those on study grids. For adult scats, estimates of lemming biomass derived from combined weights of bone and hair (conversion factor 28) were very similar to those derived from hair weight alone in 1990 and 1991, but conversion from hair gave slightly higher estimates in 1992 perhaps because of more complete digestion of bone by foodstressed foxes (Tables 4.5 and 4.6). For juvenile scats, estimates derived from hair were consistently lower, possibly because of poorer digestive efficiency of juvenile foxes (Lockie 1959). Juvenile diets were less diverse than adult diets for the same time period (Tables 4.5 and 4.6). They had higher proportions of lemmings, completely lacked large mammals, and virtually lacked eggs. These patterns are to be expected given that nearly all juvenile foods in these periods would be provisioned by adults. However, adult foxes apparently consumed more ground squirrel and large bird prey than they provided to juveniles. Daily consumption: Since the numerical responses of foxes indicated some food stress in mid-summer 1991 (pup mortality), and severe stress in 1992 (no pups weaned; disappearance of adults), it is likely that defecation rates were lower in these periods. Biomass per scat remained high in 1990, but declined in 1991, another indication of food stress. I assumed no food stress in 1990 or June 1991 (defecation  164  rate of seven scats/day), and some stress in July and August 1991. (six scats/day). In 1992 I assumed a rate of four scats/day (Table 4.7). Total daily consumption was highest in early June and comprised mostly of lemmings at a time when lemmings were particularly vulnerable, with snow melting and flooding burrows (Table 4.7). Daily consumption of lemmings dropped strongly by July and tended to fall through the rest of the summer. In 1990 foxes compensated for declines in lemming consumption by increased consumption in July and August of voles, large birds, and particularly ground squirrels. Total daily consumption did not decline strongly as summer progressed. In 1991, however, declines in lemming consumption were not well compensated for by increased consumption of alternative prey, until late August, when ground squirrel consumption increased substantially. Foxes already made quite heavy use of voles and ground squirrels in June and July, and appeared unable to increase this use to make up for the decline in lemming consumption. Consequently adult consumption fell well below 1990 levels by early August, and juvenile consumption was less than in 1990. In early June 1992, total daily consumption was remarkably high despite low lemming consumption. However, foxes appeared unable to sustain their relatively high use of alternative prey by mid-June and July, and consumption of all species declined. Impact on the lemming population: The three habitats used by lemmings comprised 56.05% of the coastal zone, and 90.94% of the inland zone. In 1990 foxes  29.4  50.0  Mean live Dicrostonyx weights (g) Adults  Subadults  3/1  260.4  192.5  Ratio adult/subadult lemmings in scats  Total  Juvenile fox consumption rate (g/d) Dicrostonyx  593.6  473.2  Adult fox consumption rate (g/d) Dicrostonyx  Total  7  7  Assumed defecation rate (scats/d)  19.5  47.9  3/5  360.5  244.3  623.7  253.4  July  1990  June  (a)  19.6  43.1  3/10  572.6  240.1  7  August  29.4  50.0  2/3  569.2  163.6  4  1-13 June  22.2  46.5  3/3  363.2  141.2  4  14-28 June  1992  19.5  47.9  0/2  349.2  110.8  4  July & Aug  Table 4.7. Adult and juvenile red fox defecation rates (scats/d) and biomass consumption rates (g/d) converted to per capita consumption rate of adult and subadult Dicrostonyx, and total numbers of Dicrostonyx killed per summer (a) 1990 and 1992, and (b) 1991. Note that in June, per capita daily consumption by juvenile foxes was cut in half for calculating total consumption by the fox population, because juvenile foxes are not fully weaned until late June.  cJ’  Subadults  Total Dicrostonyx killed per summer Adults  Subadults  Total Dicrostonyx killed per day Adults  Number of juvenile foxes  Subadults  Adults  Number of Dicrostonyx killed per day per juvenile fox  Number of adult foxes  Subadults  Number of Dicrostonyx killed per day per adult fox Adults  (a) (continued)  Table 4.7. (continued)  2189  565  171  5.7 6.3 7.8 36.5  25.9  8.5  1430  0 6.3 5.1 11.0  3  3 15.2  5.1  1.1  20.6  3.0  3  3  5  2  2  3.2  5.7  2.1  2.6  7.3  5.3  2.6  1  0  July & August  2.1  14-28 June  1.7  1-13 June  2.2  August  3.1  July  1992  7.9  June  1990  c5)  29.1  50.3  Mean live Dicrostonyx weights (g) Adults  Subadults  8/6  260,4  192.5  Ratio adult/subadult lemmings in scats  Total  Juvenile fox consumption rate (g/d) Dicrostonyx  832.3  560.0  Adult fox consumption rate (g/d) Dicrostonyx  Total  7  June 2-22  Assumed defecation rate (scats/d)  (b)  Table 4.7. (continued)  22.2  46.5  4/4  301.7  182.0  525.7  203.0  6  June 23 July 6 -  22.2  46.7  3/7  237.0  119.4  421.2  210.0  6  July 7-20  1991  22.2  44.1  3/8  356.4  160.2  6  July 21 Aug 3 -  22.2  44.3  1/5  251.4  81.0  6  Aug 4-17  22.2  41.0  4/17  436.8  159.6  6  Aug 18-31  Subadults  Total Dicrostonyx killed per summer Adults 1852  1239  22.4  30.2  Total Dicrostonyx killed per day Adults  Subadults  5  Number of juvenile foxes  2.0  2.7  Number of Dicrostonyx killed per day per juvenile fox Adults  Subadults  3  5.8  7.8  June 2-22  Number of adult foxes  Subadults  Number of Dicrostonyx killed per day per adult fox Adults  (b) (continued)  Table 4.7.(continued)  16.8  16.8  3  2.6  2.6  3  3.0  3.0  June 23 July 6 -  23.4  9.9  3  2.8  1.2  3  5.0  2.1  July 7-20  1991  21.0  8.0  5  4.2  1.6  July 21 Aug 3 -  12.5  2.5  5  2.5  0.5  Aug 4-17  25.0  6.0  5  5.0  1.2  Aug 18-31  Co  169 consumed approximately 1430 adult lemmings (Table 4.7). Twenty-one adult lemmings (31% of the adult population) were killed by foxes on the 36.6 ha of lemming habitat on study grids (Table 4.1). This converts to 702 adults killed in the coastal zone (21.82 2 km ) , with the remainder being killed in 12.68 km 2 of lemming km total area, in the inland zone. In 1990 the fox population habitat, or 13.94 2 required a minimum area of 35.76 km . 2 In 1991, foxes killed a minimum of four adult lemmings (8% of all adults) on study grids. This converts to 134 adults in the coastal zone, the remainder (1,105) being killed on 101.38 km 2 of good habitat, or 111.48 km 2 of total habitat, inland. In 1991, total area hunted by foxes was 133.30 km . Actual predation impacts and areas 2 used by foxes are probably intermediate between these quite different annual estimates. In 1990 the estimated fox hunting range included 2,491 ha of lemming habitat. Lemmings weaned 0.38 litters/ha of lemming habitat, with a mean litter size of five. This converts to 4,733 weaned subadults. Of these, an estimated 2,189 (46.2%) were killed by foxes (Table 4.7a). In 1991, hunting range included 11,361 ha of lemming habitat, and lemmings weaned 0.19 litters/ha lemming habitat, or 10,793 weanlings. Of these, 1,852 (17.2%) were killed by foxes. The percentage killed in either year was likely intermediate between these estimates. Foxes tended to take more females than males during the summer, based on deaths of radiocollared adults (Table 4.1), and the ratio of male to female ratio of pelvic bones in scats: 1990 (0:4), 1991 (12:14). Functional response: The relationship between number of adult lemmings  170 killed! fox! day and the adult lemming density (Fig. 4.3) is adequately described by a linear model (y  7.486 x, r 2  0.87, F=72.556, P  <  variance is explained by an exponential model (y  =  =  =  0.001). However, more of the 10.995 x ,r 2 2  =  0.91). I conclude  that the functional response of foxes to adult lemming density approximates a type III curve, but without any data at high enough lemming densities to indicate saturation of fox kill rates (Fig. 4.3). Up to an adult lemming density of 0.65/ha, foxes showed a slow increase in number of adult lemmings killed!d. These data were from time periods when the diet was comprised largely of prey other than lemmings (e.g., July and August), perhaps indicating prey switching. The 1992 data are plotted at densities on study grids, which may have somewhat underestimated regional densities. Nevertheless, even when lemmings were extremely rare, foxes continued to consume one or two each day, and the lemmings lacked a low density refuge from this predation. At lemming densities  >  0.65/ha, foxes increased their kill rate markedly. These data  were from June. I cannot estimate the functional response to the entire lemming population, because I lack accurate estimates of subadult densities. I suspect that the response would be closer to linear, with a weaker rate of increase with density, because foxes consumed more subadults/day as these became available later in the summer. In summary, foxes can be classed as semi-generalists as far as their diet is concerned. They fully or partially compensate for declining lemming abundance, and exhibit features of a type- III response.  171  Fig. 4.3. Functional response of adult foxes to adult lemming density. Data plotted are the number of adult lemmings ingested per day by each adult fox to feed itself for each of the time periods in Table 4.4.  172  1o.  8  1990  a  z1991  7  E1992  6  E E —  4 3 2  E 0 :  0:2  0:4  06  08  Adult lemming density (# I ha)  12  173 Grizzly Bear Diet Of 16 bear scats collected over three summers, 10 (63%) contained arctic ground squirrel remains, and three (19%) contained collared lemming remains. Rough-legged Hawk Feeding Experiment When fed two lemmings per day the captive hawk lost a little weight, digested lemmings somewhat more thoroughly, and cast pellets at a slightly slower rate than when fed four a day, when it gained weight (Table 4.8). It discarded no lemming heads when dismembering prey, and generally swallowed lemmings whole, up to four at a time. It removed the gastrointestinal tract more frequently when fed at the higher rate. It consumed all food offered, except for one day at the higher rate, when two lemmings were not consumed within 24 h. I derived the following correction factors, based on the proportion of lemmings fed which were recovered in pellets (Table 4.8), to convert number of individual lemmings in pellets to number ingested: when slightly food-stressed (74 g/d) 1.27; and when well-fed (137 g/d), 1.02. Over the entire experiment, the ratio of adult to subadult lemmings offered was 26/28, but the ratio recovered in pellets, based on intact molar tooth rows in dentary and maxillary bones, was 9/4. Of adults fed, 34.6% were recovered with at least one tooth row intact, whereas only 14.3% of subadults were recovered. I use these proportions to correct observed ratios in pellets collected in the field. Rough-legged Hawk Diet Composition: In percent frequency of occurrence, lemmings dominated the rough-legged hawk diet throughout the summer (Table 4.9). Lemming biomass ingested dropped substantially in late summer (Table 4.10), and hawks consumed an  174 Table 4.8. Summary of conditions and results of the captive feeding experiment with a rough-legged hawk, including proportion of lemmings recovered in pellets, and pellet casting rate.  Feeding rate: lemmings/d g/d (± S.E.) Hawk weight (kg)  start  First  Second  period  period  2  4  74.0 (± 2.0)  136.5  ( 6.23)  1.340  1.325  1.325  1.505  Duration (d)  7  12  Number of pellets cast  6  13  -  -  end  Number (%) lemmings recovered  11 of 14 (79%) 39 of 40 (98%)  Mean lemmings/pellet (S.E.)  1.83 (± 0.31)  Casting rate (pellets/d)  0.9  3.00 (± 0.42) 1.1  0  0 0  Vegetation  Sand/pebbles  0  Eggshell  Insecta: Coleoptera/ Lepidoptera  0  7  Ayes: Anseriform  Unidentified  0  Spermophilus  0  0  Microtus  Charadriiform/ Passeriform  100  13  22  0  1  1  8  2  1  13  98  68  40  2  0  2  18  5  26  13  82  (n=62)  (n=92)  (n=13)  Mammalia: Dicrostonyx  (to 25 Aug)  (to 7 July)  (to 9 June)  Nestling  Incubation  Before incubation  1990  39  64  2  0  2  2  0  0  10  95  (n=42)  (to 1 June)  Before incubation  38  88  4  0  0  13  0  0  17  96  (n=24)  (to 5 July)  Incubation  1991  Table 4.9. Percent frequency of occurrence of all remains in rough-legged hawk pellets.  45  74  3  3  6  32  0  13  23  100  (n=31)  (to 15 Aug)  Nestling  100  13  0  0  0  0  0  0  13  100  (n=8)  (to 3 June)  Before incubation  1992  100  14  0  0  0  0  0  14  29  86  (n=7)  Rest of summer  cii  1.1 2.41  11/8  Casting rate (pellets /d)  Mean # individuals ingested/d  Conversion to adult and subadult lemming consumption rates: Ratio adult to subadult remains  0.88 1.53  Number of subadults ingested/d  2  Number of adults ingested/d  Corrected ratio 32/56  2.19  Mean # individuals ingested/pellet  Correction factor  1.46  0.79  168/308  58/44  2.25  0.9  2.50  1.27  (1.16)  (0.90) 1.02  1.97  2.15  (to 7 July)  (to 9 June)  1  Conversion to individuals ingested/d: Mean (S.D.) individual remains/pellet  Incubation  Before incubation  1990  1.12  0.36  52/161  18/23  1.48  0.9  1.64  1.36  0.68  66/133  23/19  2.04  1.1  1,85  1.02  (1.15)  (1.32) 1.27  1.81  (to 1 June)  Before incubation  1.29  (to 25 Aug)  Nestling  1.23  1.25  43/42  15/6  2.48  0.9  2.76  1.27  (1.27)  2.17  (to 5 July)  Incubation  1991  1.47  0.64  43/98  15/14  2.11  0.9  2.34  1.27  (1.29)  1.84  (to 15 Aug)  Nestling  1.11  0.47  9/21  3/3  1.58  0.9  1.75  1.27  (0.74)  1.38  Before 9 June  1992  Table 4.10. Conversion of Dicrostonyx remains in rough-legged hawk pellets to consumption rates of individual lemmings and lemming biomass (g/d) by adult hawks during the principal time periods of the study.  a)  2  44.0 45.0 89.0  Adult biomass ingested (g/d)  Subadult biomass ingested (g/d)  Total biomass ingested (g/d)  82.4  42.9  39.5  29.4  50.0  28  38.5  21.6  16.9  19.3  47.0  49  4  73.8  39.6  34.2  29.1  50.3  1207 (864)  838 (667)  21 (0)  12  (to 1 June)  Before incubation  93.1  31.2  61.9  25.4  49.5  34  12  (to 5 July)  Incubation  1991  63.2  34.8  28.4  23.7  44.4  41  6  (to 15 Aug)  Nestling  To correct for proportion of ingested individuals recognizable in pellets (1.02 when well-fed; 1.27 when food-stressed) To correct for differential digestion of adult and subadult jaws (34.6% adult jaws recovered; 14.3% subadult jaws recovered) Pre-incubation period is approximate and based on data in Poole and Bromley (1988). Figures in parentheses refer to numbers of days in June used to calculate the summer (June, July and August) consumption.  29.4  Mean subadult weight (g)  50.0  804 (657)  Subadult lemmings  Conversion to biomass ingested/d: Mean adult weight (g)  396 (311)  21 (9)  8  (to 25 Aug)  (to 7 July)  (to 9 June)  8  Nestling  Incubation  1990  Before incubation  Adult lemmings  Total (summer) consumption by adults:  Period (d)  Conversion to total consumption: Number of adult hawks  Table 4.10. (continued)  55.9  32.3  23.6  29.1  50.3  Before 9 June  1992  178  increasing proportion of voles, ground squirrels and birds (Table 4.9). I lack data to convert all alternative prey remains to biomass ingested. However, if I assume the same correction factors and casting rates for pellets containing voles as those of lemmings, and use mean vole weights from live-trapping (both age classes combined), then the voles provided between 3.9 and 9.2 g/d, which does little to compensate for the declining rate of lemming consumption. Given the high rate of nest abandonment close to hatching, it appears that many rough-legged hawk pairs were unable to compensate for the declining rate of lemming consumption. A few pairs were successful each year, and therefore were able to kill sufficient alternative prey to feed themselves and a few young. Prey remains after fledging of two young from one nest in 1990 included one ground squirrel, two  Calidris sandpipers, one duck, and small passerine feathers. Impact on lemming population: On study grids in 1990, hawks killed at least seven adult lemmings (10% of all adults), and, in 1991, seventeen adult lemmings (33%). Extrapolating from the 36.6 ha of lemming habitat on grids, hawks removed 234 adults from the coastal zone in 1990, and 568 in 1991. The remainder of their estimated summer kill (77 in 1990, 99 in 1991) was from inland, giving a total hunting 2 in 1991. area of 26.25 km 2 in 1990, and 24.17 km In 1990 this hunting range included 1,626 ha of good habitat, and lemmings weaned 0.38 litters/ha lemming habitat. With litter size of 5, this converts to 3,089 weanlings available, of which hawks consumed an estimated 657 (21.3%) (Table 4.10). In 1991, hawk hunting range encompassed 1,437 ha of good habitat, and lemmings weaned 0.19 litters/ha lemming habitat. This converts to 1,365 weanlings available, of  179 which hawks consumed an estimated 864 (63.3%). There was a tendency for hawks to take more males than females based on deaths of radiocollared adults (Table 4.1). Sex ratio (male:female) data from pellets were limited and showed no clear trend: 1990 (1:2), 1991 (3:1). Functional response: The rate at which adult hawks ingest adult lemmings generally increases with increasing adult lemming density (Table 4.10, Fig. 4.4). A linear model explains a significant proportion of the variance (y F  =  34.095, P  =  =  2 1.031 x, r  =  0.85,  0.001), although there is a lot of scatter. No other meaningful  relationship clearly fits the data (Fig. 4.4). I conclude that the functional response is type-IT, without any evidence of saturation of kill rates at higher densities. The wide scatter may in part result from inaccurate data. I lack accurate estimates of lemming density in the pre-incubation period (May), but use the highest density in early June to represent this period (two data points with the highest densities in Fig. 4.4). The 1992 pre-incubation data point is plotted at the mean density on study grids, which may have underestimated regional densities. Across the range of lemming densities observed, the rough-legged hawks did not increase their kill rates as fast as foxes (Fig. 4.3), indicating that hawks are less flexible in their responses to lemming abundance. In summary, rough-legged hawks were specialists, being unable to compensate for declining lemming abundance, and having a type-IT functional response.  Diets of Other Raptors Lemmings comprised a substantial proportion, on a frequency of occurrence basis, of the diet of all other raptors and gulls at Pearce Pt. (Tables 4.11 and 4.12),  180  Fig. 4.4. Functional response of adult rough-legged hawks to adult lemming density. Data plotted are for pre-incubation periods in each year, and incubation and nestling periods in two years (Table 4.10), and represent adult lemmings ingested by an adult hawk to feed itself.  181  1,41.2 199o ‘1991  )E1992 0.8  E E  0.6 •1.’  -  0.4  -  0.2  E Z  U  u  02  0:4  06  08  Adult lemming density (# I ha)  1.2  0  Ayes: Anseriform  0 0  Vegetation  Sand/pebbles  —-------  0  0  Insecta: Coleoptera  Unidentified  -  0  Unidentified  -  0  Spermophilus  100  0  Microtus  Charadriiform/ Passeriform  67  Mammalia: Dicrostonyx  —  n=3  —  43  25  0  11  —-------  46  21  4  0  7  43  n=28  65  15  0  0  78  13  0  10  13  25  -  n=40  -  Before Incubation Nestling incubation (to 9 June) (to 7 July) (to 25 Aug)  1990  —  60  60  0  10  50  20  0  0  0  80  n=1O  —  -  61  61  4  0  71  32  0  0  0  14  n=28  -  --------  44  50  0  6  78  6  0  17  0  33  nz18  Before Incubation Nestling incubation (to 1 June) (to 5 July) (to 15 Aug)  1991  Table 4.11. Percent frequency of occurrence of all items in peregrine falcon pellets.  -  —  100  8  0  0  92  15  0  0  0  23  n=13  -  100  12  2  0  84  26  0  4  4  16  n=50  —--------------  100  41  0  5  77  18  0  0  5  14  n=22  -  Incubation Nestling Before incubation (to 3 June) (to 15 July) (to 30 Aug)  1992  --00 to  5  0 5  Charadriiform/ Passeriform  Eggshell  Unidentified  0  Vu! pes  41  0  Rangifer  Galliform  23  Spermophilus  9  0  Microtus  Ayes: Anseriform  55  14  0  0  0  14  14  100  0  0  0  0  25  0  4  I  14  29  0  0  0  0  43  7  22  Mammalia: Dicrostonyx  III  II  1990  7  0  7  13  27  0  0  53  0  7  15  II  1992  Gyrfalcon  -  -  14  0  36  7  7  0  0  71  0  0  14  III  15  0  0  0  23  0  23  23  0  69  13  I  -  10  15  10  5  30  0  0  30  5  70  20  II  1991  11  11  22  0  22  0  11  11  0  11  9  III  Gull  9  18  18  27  9  0  0  18  9  36  11  I  29  71  0  0  14  0  0  0  0  43  7  II & III  1992  Table 4.12. Percent frequency of occurrence of all items in pellets of gyrfalcons, gulls and golden eagles during three collection periods (I before laying; II incubation; III nestling) (Dates as indicated in Table 4.11).  16  0  11  0  16  5  0  95  0  32  19  All  1991  0  0  0  0  14  14  0  86  0  0  7  All  1992  Golden eagle  Co  0 0 0 0 32 32  Echinodermata  Mollusca  Crustacea  Vegetation  Sand/pebbles  II  Insecta (Coleoptera)  Table 4.12 (continued)  1990  71  43  0  0  0  0  III  100  75  0  0  0  0  I  93  53  0  0  0  0  II  1992  Gyrfalcon  100  64  0  0  0  0  III  69  77  0  8  0  0  I  55  55  10  0  15  5  II  1991  33  56  11  0  33  0  III  Gull  100  0  9  0  0  0  I  100  57  14  0  0  0  II&III  1992  63  89  0  0  0  21  All  1991  100  71  0  0  0  43  All  1992  Golden eagle  185 though they were not the dominant prey of these predators, except perhaps for gulls. The incidence of lemmings in pellets generally declined with declining lemming densities through the summers. However, even in summer 1992, when lemmings were rare, they were still remarkably common in gull and peregrine falcon diets (see also Table 4.1). Although many of the species in gull diets may have been scavenged, I think that lemmings were primary gull prey as no other predator left lemming parts available to be scavenged. I lack data on casting rates, and frequency of ingestion of lemming heads for all these predators, so cannot accurately estimate total impact. However, the incidence of individual lemmings in pellets of these predators (Table 4.13) indicates relatively high mortality rates by gulls and peregrine falcons, and continued predation by these species in 1992 when lemmings were scarce. Casting rate for peregrines, as with other falcons (Balgooyen 1971, Duke et al. 1976), is likely close to one pellet per day. If we assume that peregrine falcons ingested all lemming heads, the number of lemmings per pellet (Table 4.13) is particularly high in early summer, reaching 77% of the incidence in rough-legged hawk pellets in pre-laying period 1991 (Table 4.10), and is considerably lower in late summer. Each adult peregrine continued to eat one lemming every one or two weeks in 1992. DISCUSSION  Generalist Predator Hypothesis The generalist predator hypothesis predicts that lemming numbers remain relatively constant because (i) dominant predators do not respond numerically to lemming density, (ii) declining lemming biomass in the diet is compensated for by  Gull  Golden eagle  Gyrfalcon  Peregrine falcon 0.54  II  0.20  III  -  -  -  0.57  -  -  (0.65) (0.79)  0.32  (0.58) (0.79) (0.52)  0.67  I  1990  0.07  II  0.22  III  1.25  0.11  (1.12)  0.47  -  (0.95) (1.29) (0.33)  1.08  -  (1.43) (0.26) (0.55)  1.40  I  1991  0.14  II  0.06  III  0.43  (0.26)  0.07  (0.67) (0.53)  0.36  0  0  0  (0.38) (0.47) (0.24)  0.15  I  1992  Table 4.13. Mean (S.D.) number of individual lemming remains per pellet, based on molar teeth, for avian predators other than rough-legged hawks during pre-incubation (I), incubation (II), and nestling (III) periods. Sample sizes as in Tables 4.11 & 4.12. Blank cells indicate no pellets collected, except all periods lumped for eagles, and periods II & III lumped for gulls in 1992.  187 increased consumption of alternative prey, (iii) predator functional responses are type III, and (iv) predators consume very few lemmings at low lemming densities. The data from Pearce Point do not provide consistent support for the generalist predator hypothesis as an explanation for the constancy of lemming densities. Some predictions were satisfied for some predators, but all predictions were never satisfied for any one predator. The rough-legged hawk acts as a lemming specialist, with a strong numerical response to changing lemming numbers, an inability to compensate for declining lemming consumption with alternative prey, and a type-IT functional response. Other studies also show that small rodents are the dominant prey of rough-legged hawks on arctic tundra, with various birds (principally passerines) and arctic ground squirrels comprising a minor component of the diet (White and Cade 1971, Springer 1975, Smith 1987, Popanov 1988). Rough-legged hawks also show rapid numerical responses in nesting densities to fluctuating microtine densities (White and Cade 1971, Poole and Bromley 1988), so could be considered nomadic specialists (Galushin 1974). The red fox is a semi-generalist. In some summers it is able to compensate for declining lemming consumption with alternative prey, and exhibits some features of a type-ITT functional response. However, foxes still rely primarily on lemmings, especially in spring, and fail to breed successfully when lemming densities are very low in spring. I know of no comparable study of red fox on arctic tundra. The other raptors,- peregrine falcons, gyrfalcons and golden eagles,- react to changing lemming densities as generalists. Lemmings are not their principal prey, so  188 they show little or no numerical response to lemming density, and are able to compensate for declining lemming availability by increased use of their principal prey. I do not know how they responded functionally to changing lemming abundance. Previous studies of tundra raptors have shown little or no use of microtine rodents by gyrfalcons (White and Cade 1971, Poole and Boag 1988), by peregrine falcons (White and Cade 1971, Hunter et at. 1988), or by golden eagles (Poole and Bromley 1988). The results from Pearce Point are unusual, especially for peregrine falcons. Diet estimation at Pearce Point was based on pellets, but White and Cade (1971) and Hunter et a!. (1988) estimated diet from prey remains at nests. The latter method tends to underestimate the contribution of small mammals to raptor diets, because the entire small mammal is often ingested, or small bones are lost in the nest structure (Marti 1987, Simmons et a!. 1991). This might partly explain the paucity of lemming remains in previous reports of peregrine falcon diets. The heavy use of ground squirrels by gyrfalcons probably reflects a regional scarcity of ptarmigan in summer. Glaucous gulls may be lemming specialists in this system, but the data are inconclusive. Ermine are often thought of as microtine specialists, yet they can breed at very low lemming densities at Pearce Pt., and likely survive by broadening their prey base to include various birds. Grizzly bears and arctic ground squirrels probably function as generalists since they are largely herbivorous, and, in the case of bears, consume substantial numbers of ground squirrels (Pearson 1975). None of the predators at Pearce Pt., except gyrfalcons and golden eagle, satisfied the prediction (Rosenzweig and MacArthur 1963) that predation on  189 lemmings be rare at very low lemming densities, because of low capture efficiency. Lemmings lack secure hiding places, especially from mammalian predators which dig to reach adults and juveniles in burrows. When above ground, lemmings have little cover. Perhaps more than any other factor, this lack of secure refuge allows principal predators to drive lemmings to such low densities, and allows such a diverse assemblage of predators to persistently prey on lemmings even at low densities. Rosenzweig and MacArthur (1963) also predicted that in a system with stable prey, predator populations should be limited by factors other than food, and likely by territoriality. However, at Pearce Point, rough-legged hawks and red foxes appeared food-limited, and there was little evidence of territoriality. Nest abandonment by hawks, and fox pup mortality coincided with the rapid decline of lemmings in late June and July. The total daily consumption fell below maintenance levels for adult hawks in late summer, and for foxes in summer 1991. Rough-legged hawks are apparently food-limited in central arctic Canada, with numbers of successful nests, and mean brood sizes correlated with microtine prey abundance (Poole and Boag 1988, Poole and Bromley 1988). In north boreal Sweden, where foxes feed primarily on cyclic microtine prey, Englund (1970) found a positive correlation between indices of reproduction and vole abundance; foxes appeared food limited. Rough-legged hawks and peregrine falcons acted aggressively towards one another when establishing nests in spring, but their hunting ranges appeared to overlap considerably. No raptors nested within 1.55 km of the golden eagles, an avoidance noted by Poole and Bromley (1988). Red fox regularly hunted throughout hunting ranges of all raptors, and ground squirrels were distributed throughout the study  190 area. Consequently, it seems likely that there was substantial exploitative competition between predators for the declining prey base of lemmings. In summary, the generalist predator hypothesis is not a sufficient explanation for the relative constancy of lemming numbers at Pearce Point. Although some of the predators acted as generalists, the dominant predators were specialists or semigeneralists. When these species were present in summer, lemmings declined to densities which could no longer sustain breeding by hawks in the current summer, and which would not allow settlement and successful breeding by hawks and foxes the subsequent spring. The system was unstable in summer because of the insufficiency of alternative prey for all predators, the lack of territoriality among predators, and the lack of secure refuges for lemmings at low densities. Procedures  Determination of predator diets and impact depends on numerous assumptions which might bias results. Here I discuss the most important assumptions. First, I used 28 as the factor to convert undigested remains in fox scats to an estimate of biomass consumed. This choice was validated by the very similar estimates of biomass derived from another method, conversion of weight of lemming hair in scats. Second, I assumed that the conversion factor does not change with fox age or degree of satiation. Juvenile foxes, and well-fed foxes, digest food less thoroughly (Lockie 1959, Reynolds and Aebischer 1991). Consequently, consumption rates for juvenile foxes, and for foxes in early June, may have been overestimated. I have no way of correcting this. In most time periods the estimated total daily consumption fell within or close to the range of estimated daily requirements: 320-380  191 g/d for captive foxes (Lockie 1959, Sargeant 1978) and 450-550 g/d for more active, free-ranging foxes (Scott 1941., Ryszkowski et at. 1973). Estimated daily consumption was particularly high in early June, perhaps in part because of the above bias. However, lemmings were more vulnerable at this time, as snow melt removed cover  and most burrows were flooded. This was the only time foxes cached lemmings, indicating they were satiated. Foxes may eat more in early summer as they recover body condition after the winter. Third, I assumed that the proportion of adult to subadult remains in fox scats represented the proportions ingested. I think this is the most problematic assumption. Foxes digest bone. Thinner, weaker subadult lemming bones are likely better digested, as observed when feeding lemmings to a captive hawk. Consequently I probably overestimated the consumption of adult lemmings by foxes, and underestimated subadult consumption, but to an unknown degree. Fourth, estimates of total impact on the regional lemming population were derived by extrapolating observed mortality rates from study grids, which were small compared with foraging ranges of predators. Grids were from one to four kilometres from the fox den, and experienced a wide range of rates of fox predation. This gives confidence that regional fox predation rates were within the observed range. However, one grid was within 500 m of a hawk nest in 1990, and immediately adjacent to a nest in 1991. Hawk predation rates from grids may have overestimated regional rates, and so I may have underestimated the area used by hunting hawks. Impact on the Lemming Population I lack data on the hunting ranges of the principal predators, but estimated the  192 areas required by foxes, to consume all the adult lemmings indicated by analysis of their scats, as 35.8 km 2 in 1990 and 133.3 km 2 in 1991. The largest home range record for red fox in North America, in an alpine tundra habitat in northern British Columbia, is 34  2  (Jones and Theberge 1982, Voigt 1987). The foxes were  frequently observed travelling throughout the 40 km 2 intensive study area. The natal den was only one km from the border of this area, so foxes undoubtedly used an even larger area for hunting. Despite the fact that estimates of hunting ranges may have been too large, because of potential biases in scat analyses (above), they are close to reported values and to my direct observations of area used by foxes, so are reasonable. All hawks together needed at least 24-27 km 2 to satisfy observed kill rates. These estimates seem reasonable given that one pair of rough-legged hawks, in the northern taiga of Finland, used a 10 km 2 foraging range to feed nestlings in partially forested bog habitats (Pasanen and Sulkava 1971). Recruitment of summer-born lemmings as adults, on grids accessible to predators, was very low (0.12  -  0.21 individuals! ha! summer), and did not reach  high levels in the predator exclosure (0.44 individuals! ha! summer) (Chapter 1). The study grids, including the exclosure, fell within the foraging ranges of hawks and foxes, and therefore subadults on these grids probably were killed at near the rates estimated: in 1990 a combined 68% for the two predators, and in 1991 a combined 81%. The various other predators could also have consumed substantial numbers of subadults. These results confirm my contention that most subadult lemmings were killed by predators before maturing, and that the lemming population in the predator  193 exciosure did not grow because most potential immigrating recruits were killed (Chapter 1). Individual foxes have a substantially higher limiting effect on lemming population growth than individual rough-legged hawks, because of their higher daily food requirements, and their tendency to take more females than males. The latter pattern has also been observed by Brooks (1993) and Krebs et a!. (1995). Predation on females removes not only current adults, but also the litters currently suckling and in  utero. The Specialist-Generalist Continuum. There is evidence for the generalist predator hypothesis from European studies. Microtine populations tend to be non-cyclic in southern latitudes (south of 60°N). In these areas the rodents belong to a diverse community of herbivores supporting a number of generalist predators, principally the red fox (Vulpes uulpes) and the common buzzard (Buteo buteo), and winter snow is not deep enough to prevent successful hunting by these predators (Hansson and Henttonen 1985, 1988). In one such community in southern Sweden, Erlinge et a!. (1983, 1984), and Erlinge (1987), demonstrated that predation is the principal factor limiting small rodent population growth. In this system, generalist predators showed strong functional responses to rodent densities by switching from their principal prey, the rabbit  (Oryctolagus cuniculus), to rodents, with short time delay, when rodents were particularly vulnerable and abundant. The numbers of generalist predators were limited by territoriality. Erlinge (1987) concluded that the conditions proposed by Rosenzweig and MacArthur (1963) were met in his system.  194 Korpimaki and Norrdahl (1989, 1991a,b) tested the nomadic predator hypothesis with cyclic microtine rodents in western Finland. They demonstrated that some raptors, whose principal foods are microtine rodents, show rapid numerical responses to microtine densities through immigration and enhanced breeding success in areas with irruptive rodent populations. These raptors showed strong type-TI functional responses to rodent density (Korpimaki and Norrdahl 1989, 1991a). They may have influenced the amplitude of the cycle, by curtailing irruptive population growth, but rodent densities still fluctuated cyclically. The raptors alone were insufficient to stabilize prey densities. Rosenzweig and MacArthur’s (1963) conditions were not assessed for all predators, but probably did not hold for these raptors, which were weakly territorial (Korpimaki and Norrdahl 1991a). Specialist mustelid predators, most notably the least weasel (Mustela nivalis spp.), are the dominant small rodent predators in a number of communities where rodents fluctuate cydically. Their strong, but delayed numerical responses to high rodent numbers, their total reliance on rodent prey in winter, and their adaptations for hunting rodents in their burrows, act together to drive the rodents to densities too low for continued support of the predators (Fitzgerald 1977, Korpimaki et a!. 1991, Korpimaki 1993). The Pearce Point community lies somewhere intermediate on this specialist generalist spectrum. In contrast to the northern European systems, from which the specialist-generalist model is derived, collared lemmings at Pearce Point (i) are faced every summer by a generalist predator population, and (ii) are able to breed most winters, and thereby recover from very low densities in autumn.  195 The migratory and resident generalist predators at Pearce Point stabilize lemming numbers in summer, because they limit lemming population growth, even when one or other of the principal, more specialist, predators has disappeared. The more specialist predators (hawks and foxes) destabilize lemming numbers because they drive summer lemming declines with no temporal or spatial refuge. Winter and spring breeding under the snow is stabilizing at Pearce Point because it allows lemmings to return to early summer densities high enough to support the full complement of summer predators. Winter breeding in northern Fennoscandian Microtus, Clethriononiys and Lemmus spp. is generally associated with the increase phase of a population irruption (Hansson 1984b, Kaikusalo and Tast 1984). The lack of breeding by these rodents in most winters is likely destabilizing, because they cannot compensate for continuing winter predation, and may decline to densities which cannot support specialist or semi-generalist predators the subsequent summer. This pattern occurred in winter 1991-92 at Pearce Point (Chapter 3). Diets and numerical responses of red fox and rough-legged hawks at Pearce Point are similar to patterns observed in some boreal systems. In these regions some generalist predators, notably red fox, preferentially prey on small rodents, but take an increasing proportion of alternative hare and grouse prey when rodents are scarce. However, the predators cannot fully compensate for declining vole consumption when voles are scarce, and therefore decline in abundance themselves; they are semi generalists (Angelstam et a!. 1984, Lindstrom et a!. 1987). The alternative prey hypothesis has been proposed to explain the resulting cyclic variations in all prey species (Keith 1974, Angelstam et a!. 1985). However, lemmings at Pearce Point do  196 not show multiannual cycles. Pearce Point differed from these boreal systems in that microtine prey dynamics were stabilized by winter breeding (Chapter 3), and most or all of the generalist predators were absent in winter. Peregrine falcons, eagles, bears and ground squirrels were not active residents in winter, but I lack information on the winter ecology of red fox. Foxes showed high site fidelity between summers, judged by the presence of recognizable adults. They may have been resident for part of the winter, though what sustained them, given the low autumn lemming densities and the hibernation or emigration of key alternative prey, remains a crucial unanswered question.  TA/hat Allows Generalist Predators to Persist ? Arctic ground squirrels appear to be a key species in understanding how the diversity of semi-generalist and generalist predators persist at Pearce Point. For red foxes, they are the main alternative prey to lemmings in terms of biomass, and foxes probably could not persist without them. They are also a principal prey for generalist predators such as the golden eagle, gyrfalcon, and grizzly bear. They provide a substantial source of food in late summer for the specialist rough-legged hawks, and the generalist peregrine falcons. They are also lemming predators themselves (Boonstra et al. 1990, Chapter 1). I therefore hypothesize that, without ground squirrels, the system would likely lose the three generalist lemming predators and the red fox, leaving a relatively underutilized lemming prey base ready for exploitation by more specialist lemming predators, such as the rough-legged hawk, arctic fox  (Alopex lagopus), and jaegers (Stercorarius spp.).  197 CHAPTER FIVE WHY DON’T ALL LEMMING POPULATIONS IRRUPT?  INTRODUCTION  Microtine rodents, including North American lemmings (Lemmus spp., Dicrostonyx spp.), are well known for their density fluctuations (Elton 1942, Krebs and Myers 1974). Virtually all populations of Lemmus studied to date fluctuate widely in density (Stenseth and Ims 1993). Most populations of collared lemmings (Dicrostonyx spp.) studied in North America also irrupt in some years, exhibiting greater than ten fold changes in density (Elton 1942, Shelford 1943, Krebs 1964, Fuller et a!. 1975b, Mallory et a!. 1981, Rodgers and Lewis 1986, Pitelka and Batzli 1993). However, not all collared lemming populations show such wide density fluctuations. In this study, densities of Dicrostonyx kilangmiutak did not follow a multiannual pattern, with a clear irruptive increase to a peak, followed by a decline. Instead they stayed at consistently less than three individuals per hectare for six years, with annual fluctuations (Krebs et a!, 1995, Chapter 1 ). Accurate density estimates have not been made in all previous studies of collared lemmings, especially when they are rare (e.g., low phase of cycles) (Krebs et a!. 1995). However, estimates of numbers per hectare at the relatively short-lived peak of an irruption include 40 (Shelford 1943), greater than 40 (Watson 1956), 15-25 (Brooks and Banks 1971), and 27 (Batzli et a!. 1980). Non-irruptive populations of Dicrostonyx also exist in the northern foothills of the Brooks Range of Alaska (Batzli and Jung 1980, Pitelka and Batzli 1993).  198 In this chapter I investigate potential reasons why some lemming populations irrupt while others do not irrupt. I ask the following questions: (i) what are the characteristics of a population irruption from low densities in lemmings ? (ii) what are the geographic patterns of irruptions in North American lemmings ? (iii) what are the factors necessary to limit lemming populations to low densities ? and (iv) how do these differ between regions where lemmings irrupt and regions where lemming populations are relatively stable (e.g., Pearce Point) ? I end with a set of alternative hypotheses suggesting why some lemming populations are relatively stable. CHARACTERISTICS OF POPULATION IRRUPTIONS I define a lemming irruption as sustained population growth exceeding a ten fold increase in density, and reaching a high density (>10 lemmings/ha) which is not repeated annually. This is essentially Taitt and Krebs’ (1985) definition of a cyclic population fluctuation in microtine rodents, where the irruption is the increase phase. Because of the short duration of many lemming studies, I do not assume cyclicity with attendant increase phases, but speak of irruptions. Ten-fold increases in density can occur in a non-irruptive situation, where densities are consistently less than 3/ha, where highest densities are reached almost every year, and where lemmings never reach the abundance of cyclic peaks (see above)(Chapter 1; Krebs et al. 1995). Therefore a peak density of more than ten individuals per hectare is a necessary criterion to differentiate irruptive and non-irruptive situations. This represents the lower limit of an order of magnitude difference between maximum densities at a non-irruptive situation (Pearce Point) and at irruptive situations.  199 The period of low density is frequently the longest of all phases in microtine population cycles (Krebs and Myers 1974, Stenseth and Ims 1993), and this holds for most populations of lemmings studied over many years in North America (Shelford 1943, Batzli et at. 1980, Rodgers and Lewis 1986). If the population has declined from much higher densities, the length of the breeding periods may be shorter, and the rate of maturation slower, at the beginning of the low period compared with subsequent year(s) (Krebs 1964, Fuller et at. 1975b). However, reproduction continues, and litter sizes at low densities do not differ substantially from those at higher densities (Krebs 1964, Batzli et at. 1980). Low density populations frequently decline somewhat in summer, despite reproduction, and often recoup these losses by winter breeding (Krebs 1964, Fuller et at. 1975b). The scale and speed of population growth in an irruption is obviously the result of successful reproduction, and repeated recruitment of successive cohorts to the breeding population (Krebs 1964, Batzli et at. 1980). An irruption often starts with an increasing summer population (Shelford 1943, Fuller et a!. 1975b, Batzli et at. 1980). The shift from low to irruptive densities is always accompanied by winter breeding (Krebs 1964, Fuller et at. 1975b, Batzli et at. 1980). Small increases in survival of adult females and their offspring can have dramatic impacts on density, because female survival ensures weaning of the current litter, and with post-partum oestrus, juveniles and subadults rapidly comprise the majority of the population (Batzli et at. 1980). There is no indication that immigration plays a key role in initiating irruptions, because low densities generally occur synchronously over quite large regions (Elton 1942, Krebs 1964).  200 Any attempt to discriminate between non-irruptive and irruptive populations  must address the factors limiting reproduction and recruitment in both summer and winter, specifically: survival of adults, reproductive output of adults, survival of neonates to weaning, survival of weanlings through dispersal, and maturation rate of juveniles. GEOGRAPHIC PATTERNS IN LEMMING IRRUPTIONS  The most comprehensive attempt to document regional trends in arctic small mammal abundance was the Canadian Arctic Wild Life Enquiry undertaken from 1935 to 1949 by Charles Elton, and Dennis and Helen Chitty of the Bureau of Animal Population at Oxford University. The researchers asked resident observers (mostly Hudson’s Bay Company employees), by questionnaire, to record whether small rodent, arctic fox and snowy owl abundance had increased, decreased or remained the same since the previous year. Records of change in small rodent numbers were based on observations by the respondent and other local trappers and traders. Data were summarised annually within 11 regions (Fig. 5.1). Here I summarize the results across all 14 years for the 11 regions, giving the proportion of observers reporting substantial change in the small rodent population (i.e. increase or decrease in abundance), and the proportion indicating no change in abundance. In regions 1,2,5,6,7 and 8 (Fig. 5.1) observers infrequently (<20% of reports) classified small rodent populations as “no-change”, indicating that the rodents fluctuated frequently (Table 5.1). Reports of increase exceeded reports of decrease, often by a substantial margin, suggesting that declines in abundance were often precipitous. Fluctuations of lemmings were remarkably regular, with peak abundance  1  49 40 11.  Lemming abundance  Increase  Decrease  No change 3  35  63  2  55  18  27  3  24  42  34  4  19  22  59  5  Regions  4  37  59  6  12  39  49  7  12  40  47  8  27  37  37  9  46  19  35  10  Table 5.1. Summary of data collected by the Canadian Arctic Wild Life Enquiry, concerning relative stability in lemming abundance, for 1935 to 1949, in eleven regions of the Canadian arctic. Numbers are the percentages of all observer reports, summed over the fourteen years, indicating annual increase, decrease, or no change in the lemming abundance. For region locations see Fig. 5.1. Data are taken from data summaries in Chitty and Elton (1937), Chitty (1938), Chitty (1939), Chitty (1940), Chitty and Chitty (1941), Chitty and Nicholson (1942), Chitty (1943), Chitty and Chitty (1945) and Chitty (1950).  38  31  31  11  C  202  Fig. 5.1. Map illustrating jurisdictions with arctic tundra (A, Alaska; Y, Yukon; N, Northwest Territories;  Q, Quebec; L, Labrador), the eleven regions (numbers)  summarized by the Arctic Wild Life Enquiry (Chitty 1950), and, in northern Alaska, the division (dotted line) between the coastal plain and the foothills (after Hartman and Johnson 1984). Study sites mentioned in the text are indicated with a dot and label (CS, Cape Sabine; A, Atkasook; W, Wainwright; PB, Point Barrow; P, Pitt Point; U, Umiat; BI, Banks Island; PP, Pearce Point; BL, Baker Lake; TL, Truelove Lowland; I, Igloolik; EP, Eskimo Point; C, Churchill; CP, Cumberland Peninsula).  C  204 every three or four years (Elton 1942, Chitty 1950). In regions 3, 10 and 11, reports of no-change were frequent (Table 5.1), suggesting more constancy in rodent numbers. On the western Canadian arctic mainland (region 11), many observers did not report substantial fluctuations in abundance (Chitty and Nicholson 1942). Regions 3 and 10 fall largely south of the tree-line, where the small rodent community probably did not indude Lemmus or Dicrostonyx (Hall 1981). Region 11, however, is comprised mostly of tundra habitats, well within the range of lemmings (Hall 1981) (Fig. 5.3). Two other regions, 4 and 9, were intermediate between the other groupings in reports of no-change, and reports of increases did not exceed declines (Table 5.1). A number of field studies confirm a contrast between regions of relative constancy and inconstancy. First I consider regions of relative inconstancy. Elton (1942) summarised information from many observers in northern Quebec and Labrador (regions 1 and 2) to show that lemmings and their principal predators, arctic fox (Alopex lagopus) and red fox (Vulpes vulpes), follow definite cycles in abundance with a predominantly four-year period. On the Cumberland Peninsula of southern Baffin Island (region 6), Watson (1956) reported a concurrent irruption of Lemmus and Dicrostonyx, and a snap-trapping success as high as that at the peak densities of irruptions reported by Krebs (1964) and Mallory et a!. (1981). Fuller et al. (1975b), recorded a greater than ten-fold variation in abundance of Dicrostonyx, over a six-year period, at Truelove Lowland on northern Devon Island (region 7). Manniche (1910, reported in Elton 1942) recorded substantial density changes, though not accurately quantified, in Dicrostonyx in northeastern Greenland, indicative of an  205 irruption and precipitous decline. On Banks Island, Dicrostonyx and Lemmus occasionally irrupt to short-lived high densities (Manning and Macpherson 1958, Larter, unpubi. data). The only exception to this pattern is the relatively constant population of between zero and three lemmings per hectare over five summers at Igloolik (Rodgers and Lewis 1986). Although Igloolik is on an island in region 7 (Fig. 5.1), this island is close to the mainland, and may be ecologically more similar to region 9. Of the regions with intermediate levels of stability, region 4 is the best studied. Shelford (1943) and Brooks and Banks (1971) working at Churchill, Krebs (1964) at Baker Lake, and Mallory et a!. (1981) at Eskimo Point (Arviat), all report dramatic density fluctuations greater than ten-fold in amplitude. Shelford (1943) reported a period of three or four years between cyclic peaks of Dicrostonyx at Churchill in the 1930s. Scott (1993) reports a continued periodicity of four years at Churchill in the 1950s, and from 1967 to the present. The period of fluctuations at Baker Lake and Eskimo Point were not known. In an ongoing study of lemming demography at Walker Bay, Kent Peninsula, in region 9, both lemming species declined precipitously from a peak in 1993 to very low densities in 1994 (Krebs and Wilson, unpubl. data), Region 11 was anomalous in the Arctic Wild Life Enquiry data, and is also anomalous in field studies. At Pearce Point, on the Northwest Territories (N.W.T.) mainland, Dicrostonyx kilanginiutak have persisted at low densities over six years with no evidence of cyclic irruptions, and densities rarely exceeding two animals per hectare (i.e. similar to low densities reported by Shelford (1943) and Krebs (1964)) (Krebs et a!. 1995, Chapter 1). There have been no detailed field studies of lemmings  206 in northern Yukon (part of region 11), but there are no substantial changes between years in the proportion of fox dens used to rear pups (i.e. natal dens)(Smits and Slough 1993). Because the proportion of natal dens occupied is much higher in summers of lemming irruptions (Macpherson 1969, Eberhardt et a!. 1983), Smits and Slough (1993) speculate that lemmings on the Yukon coastal plain do not irrupt regularly, if at all At Point Barrow, Alaska, the northernmost tip of the coastal plain (Fig. 5.1), Lemmus sibiricus undergoes periodic irruptions, with amplitude of at least three  orders of magnitude, and periodicity of three to six years. Dicrostonyx torquatus is rarer at this site, but when present, irrupts in synchrony with Lemmus. (Pitelka 1973, Batzli et a!. 1980). At three other sites on the coastal plain, Wainwright, Pitt Point and Inaru River (between Barrow and Atkasook) (Fig. 5.1), Pitelka and Batzli (1993) report irruptive populations of both lemming species. At Atkasook, on the inland coastal tundra (Fig. 5.1), Batzli and Jung (1980) report a microtine community with consistently low densities over four years (197578); average numbers per hectare over all habitats range from 0.3 to 1.6 for Lemmus, 0.4 to 0.7 for Dicrostonyx, and 0.03 to 0.9 for Microtus. Densities frequently declined during the summer, with low adult survival, and density changes within seasons were generally greater than those between years (Batzli and Jung 1980). One interpretation of these data is a lack of irruptive dynamics. Pitelka and Batzli (1993) applied an index of cyclicity (s) (Henttonen et a!. 1985) to another data set from Atkasook (1955-59), and found both lemmings to be cyclic. However, their capture rates were low, even in the year of highest abundance, and peak densities were  207 substantially less than those found on the north coast (Pitelka and Batzli 1993). It seems that irruptions at Atkasook are irregular and of low amplitude. At two sites in the foothills, Cape Sabine and Umiat, lemming densities varied within less than an order of magnitude, and were mostly non-cyclic, according to the  index of cyclicity applied over only four years (Pitelka and Batzli 1993). In summary, patterns of population fluctuation describe two regions within arctic North America. Lemmings undergo large, and often regular, irruptions on the tundra of the Ungava-Labrador peninsula, on the islands of the arctic archipelago, on the Alaskan coastal plain, and on the mainland tundra of the Northwest Territories, Canada, east of approximately the Coppermine River. In the latter area, fluctuations at some sites may be absent or less regular and extreme. When sympatric, both species irrupt synchronously, and Leminus generally reach higher peak densities than Dicrostonyx (Watson 1956, Krebs 1964, Batzli et at. 1980; but see Rodgers and Lewis  1986). The second region includes the tundra of the Canadian mainland west of the Coppermine River, through northern Yukon, and includes the foothills of the Brooks Range of Alaska. In this region Dicrostonyx is generally more common than Lemmus, and populations rarely, if ever, irrupt to the high densities typical in the first region (Krebs et at. 1995, Pitelka and Batzli 1993). FACTORS LIMITING POPULATION GROWTH AT LOW DENSITIES  Numerous ecological factors, extrinsic and intrinsic, are sufficient to limit population growth in lemmings at low densities (Table 5.2), but factor effects differ in magnitude and vary in time and space. The impact of summer predation by a diverse  Food defences  Food nutrient quality  Food availability  (Batzli et al. 1980) (Chap 2)  Summer  Yes? (Batzli 1983)  No? (Batzli et al. 1980)  Summer Winter & Summer  Yes? (Batzli and Jung 1980)  Winter  No  Yes? (Collier et al. 1975)  Yes (Chap 2)  Summer Winter  ?  Summer  Winter  Yes (Pitelka et al. 1955) (Maher 1970) (Chap 1)  Winter  Predation mortality  Predation risk  Yes (MacLean et al. 1974) (Maher 1967)  Season  Factor  Sufficient to limit growth?  (Batzli et al. 1980) (Chap 2)  No?  No?  No?  No  No? (Batzli et al. 1980) (Krebs 1964)  No (Chap 2)  ?  Yes (Chap 1,2 & 4) (Batzli et al. 1980)  (Chap 1)  No (MacLean et al. 1974) (Batzli et al. 1980)  Necessary to curtail irruption?  Table 5.2. Summary of factors which are sufficient to limit lemming population growth at low densities, and those that are necessary to curtail irruptive population growth.  Season Autumn  Winter  Summer  Autumn  Winter & Summer Winter & Summer Summer  Winter & Summer  Factor  Cold temperature  Thin snow depth  Flooding (rain)  Ice coating vegetation  Age structure & senescence  Reproductive inhibition  Infanticide  Aggressive spacing behaviour  Table 5.2 (continued)  No (Krebs et al. 1995) (Chap 2) (Brooks 1993)  Yes (Brooks 1993) (Chap 2)  No (Chap 2)  Yes? (Boonstra 1994)  Yes (Fuller 1967) (Batzli et al. 1980)  Yes (Batzli et al. 1980) (Chap 1)  Yes (Shelford 1943) (MacLean et al. 1974) (Fuller et al. 1975b) (Chap 3)  Yes? (Fuller et al. 1975b) (Reynolds & Lavigne 1988) (Chap 3)  Sufficient to limit growth?  No (Krebs et al. 1995) (Chap 2)  No (Chap 2)  No (Chap 2)  No? (Boonstra 1994)  No  No (Chap 1)  No? (Shelford 1943) (Krebs 1964) (MacLean et al. 1974) (Chap 3)  No? (Chap 3)  Necessary to curtail irruption?  C  210 community of migratory and resident predators can be large, affecting adult, subadult and juvenile survival, adult reproductive output, and perhaps maturation rate of juveniles (Chapters 1,2 & 4). The impact of predation risk appears smaller, potentially affecting maturation of juveniles and adult reproductive output, and being an ancillary condition to predation mortality (Chapter 2). Many factors operate only for short and irregular periods of time (e.g., flooding and icing). Although their limiting effects might be strong, affecting survival of all age-classes, they are negligible in many years. Some factors are likely the legacy of a population irruption and subsequent decline (e.g., winter predation by specialist predators; adult skew in age structure), so are of marginal interest in understanding a persistent low. Some factors such as food quality and availability or winter snow depth, are best thought of as enabling factors; both an abundance of high quality food, and thick widespread snow providing access to food, are likely to facilitate population growth. Only one factor, summer predation mortality, is clearly necessary to curtail a population irruption (Table 5.2). At Pearce Point, where lemmings do not irrupt, survival of adults and neo-nates, reproductive output of adults, and recruitment of adults all increase with removal of predators in summer (Chapter 1). Predators consume the great majority of dispersing subadults (Chapter 4). Without this predatory impact on all age-classes, population growth would proceed. At sites with irruptions, diverse predators are abundant at the beginning of the low density phase, but have declined dramatically by the pre-irruptive summer, allowing leniming population growth this summer (Shelford 1943, Batzli et al. 1980). Some resident specialists, such as the least weasel (Mustela nivalis), may disappear  211 locally (Thompson 1955. MacLean et at. 1974). Most migratory avian predators do not breed, or even stay in the region (Pitelka et at. 1955). Semi-specialists, such as the arctic fox, are also rare and not breeding (Macpherson 1969). Consequently, limitation by predation mortality is minimal prior to an irruption. However, minimal predation mortality is not the only condition necessary for irruptive population growth. An irruption depends on winter population growth, which requires (i) continued good survival of reproductive adults and their offspring, and (ii) sufficient energy and nutrients for survival and repeated reproduction. The first condition is satisfied by the disappearance of most resident predators the previous summer. The only exception may be least weasels, which can locate the expanding population in winter, and respond numerically by breeding under the snow (MacLean et at. 1974, Batzli et at. 1980). The irruption has already occurred by this time (late winter), though the peak may be truncated (Batzli et a!. 1980, Pitelka and Batzli 1993). The second condition stems from the fact that mere survival in winter is energetically very costly (Reynolds and Lavigne 1988), and depends on the insulative value of a nest, and of snow cover (MacLean et at. 1974, Fuller et a!. 1975a, Chappell 1980, Casey 1981). The energetic costs of pregnancy and lactation are high, especially given the additional costs of rewarming the nest and sucklings following a foraging bout, and the cost of foraging in cold temperatures (Collier et at. 1975, Batzli et at. 1980). Therefore survival and reproduction are likely enhanced where absolute quantity of foods is higher, and where snow is deeper (Collier et at. 1975). Deeper snow provides more insulation from ambient temperatures, and, after drifting by  212 wind, covers larger areas of tundra, providing access to food over a larger area. Irruptive growth is delayed during winters of unusually low snow accumulation (Shelford 1943, Krebs 1964). Deep snow may also protect lemmings from fox predation (cf. Lindstrom and Hornfeldt 1994). Therefore, substantial accumulation of snow is necessary for winter population growth. In summary, three conditions appear necessary for irruptive population growth: minimal predation mortality (especially in summer), adequate food availability, and adequate snow depth. Batzli et a!. (1980) came to the same conclusion regarding irruptive growth in Alaska. In some areas the latter two conditions could conceivably be satisfied in all years, but in other areas they may only be satisfied sporadically, resulting in less regular and slower population growth in the absence of predation mortality. HOW DO REGIONS OF IRRUPTIVE AND NON-IRRUPTIVE DYNAMICS DIFFER?  Summer Predators In regions where lemmings irrupt, the summer predator community is remarkably consistent, and dominated by small rodent specialists (Table 5.3). These include jaegers (Stercorarius spp.), snowy owl (Nyctea scandiaca), short-eared owl (Asio flammeus), rough-legged hawk (Buteo lago pus), and least weasel. Depending on availability of alternative prey, the arctic fox may rely to varying extent on lemmings in summer. Only in coastal areas can they come close to compensating for low lemming abundance with alternative foods, but do so by becoming more mobile (Macpherson 1969, Chesemore 1975, Riewe 1977, Batzli et a!. 1980). Ermine (Mustela  a  N ? N N N Y  N  Predator  BIRDS Pomarine Jaeger  Parasitic Jaeger  Long-tailed Jaeger  Glaucous Gull  Golden Eagle  Rough-legged Hawk  Peregrine Falcon  N  ?  N  N  N  ?  N  b  4  N  *  N  N  Y  Y  N  c  *  *  N  N  N  N  N  d  6  Y  N  N  Y  Y  Y  N  e  7  Region  Y  Y  Y  Y  *  *  N  f  11  N  N  N  Y  *  *  Y  g  Alaska coast  *  *  *  N  Y  *  N  h  Alaska foothills  Table 5.3. Presence (Y) or absence (N) of lemming predators as summer breeders at sites where lemmings have been intensively studied. Sites are organized by Arctic Wild Life Enquiry regions (Chitty 1950), and coded as follows: (a) Churchill (Shelford 1943), (b) Churchill (Brooks 1993), (c) Baker Lake (Krebs 1964), (d) Baffin I. (Watson 1956), (e) Truelove Lowland (Pattie 1977, Riewe 1977), (f) Pearce Point (Chapters 1 & 4), (g) Barrow (Batzli et a!. 1980), (h) Atkasook (Batzli and Sobaski 1980, Bee and Hall 1956, White and Cade 1971). An asterisk (*) means species is transient, and a question mark (?) means data are lacking.  N N  *  Y  N  Y? N  Wolverine  Arctic ground squirrel  N  N  N  N  N  Least weasel  Y  Y  N  Y  Ermine  Y  *  Y  Y  Arctic fox  N  *  N?  ?  Redfox  N  *  N  Wolf  N  Y  N  N  MAMMALS Grizzly bear N  ?  ?  ?  Common Raven  Y  *  N  Y  Snowy Owl  Y  Y N N  N N Y  N N  N  Y  N  Y  Y  N  Y Y  Y  N  *  *  N  Y  N  N  N  *  Y  Y  *  Y  Y  N  Y  y  y  *  N  N  Y  h  g  Alaska Alaska coast foothills  f  11  N  N  N  N  Y  *  N  N  *  Y  Y  N  *  N  7  e  6  Region  d  c  Short-eared Owl  N  b  N  a  4  Gyrfalcon  Table 5.3. (cont.)  215 erminea) may partly compensate for low lemming abundance in summer by feeding on birds, but are lemming specialists in winter (Riewe 1977, Batzli et at. 1980). All these predators show dramatic numerical responses to lemming abundance, with varying degrees of delay. Most importantly, these responses result in all predators being very scarce or non-existent after lemmings have been at low densities (<2/ha) for a year or more (Elton 1942, Shelford 1943, Pitelka et a!. 1955, Watson 1957, Macpherson 1969, Maher 1970, MacLean et at. 1974, Riewe 1977). Where lemmings do not irrupt, the predator community is dominated by generalist predators (Table 5.3). At Pearce Point, the arctic fox is replaced by the red fox, which eats primarily lemmings but is able in some years to compensate for a scarcity of lemmings by feeding on other species (Chapter 4). The other generalist predators include peregrine falcon (Falco peregrinus), gyrfalcon (Falco rusticolus), golden eagle (Aquila chrysaetos), glaucous gull (Larus hyperboreus), grizzly bear (lirsus arctos) and arctic ground squirrel (Spermophitus parryii) (Table 5.3). The system also includes some specialist or semi-specialist species, the rough-legged hawk and ermine, in common with irruptive regions. All these species continue to breed at spring lemming densities of 1-2/ha (Chapters 1 and 4). Pitelka and Batzli (1993) did not clearly list the predator community at sites with non-irruptive lemmings in the foothills of the Brooks Range. However, this region includes the breeding ranges of all the generalist predators at Pearce Point, except glaucous gulls (Bee and Hall 1956, White and Cade 1971, Batzli and Sobaski 1980). The different composition and temporal persistence of predator communities at sites without irruptions requires explanation. One critical species shift is from arctic  216 to red fox. Competition with red fox may define the southern limit of arctic fox breeding range, at least in western North America (Chesemore 1975). Ranges of red and arctic fox overlap extensively in the southern tundra and northern taiga zones (Fig. 5.2), but much of this overlap reflects movements beyond the breeding ranges, especially by arctic foxes (Wrigley and Hatch 1976, Garrott and Eberhardt 1987). The two foxes breed within 10 km of each other on the northern coastal plain of Yukon (Smits and Slough 1993). This may be exceptional because red fox are dominant over arctic fox in agonistic encounters and in competition for food (Rudzinski et al. 1982, Schamel and Tracy 1986), and may prey on arctic fox (Frafjord et a!. 1989). The distributions of the two species may be in long term flux, and quite variable in time and space. Red fox expanded their range onto the tundra west of Hudson Bay in the 1930s (Marsh 1938). They colonized southern Baffin Island in the early 1900s, and gradually expanded their range northward, eventually reaching Cornwallis and Devon Islands in the 1960s (Macpherson 1964). In arctic Russia, a similar northward range expansion of red fox occurred this century, with displacement of arctic fox from some breeding sites. This expansion was attributed to a warming climate (Skrobov 1960, Chirkova 1968). The factors limiting the northern range, and the local distribution, of red fox are not clear. Hersteinsson and MacDonald (1982) suggest that red fox are limited by  217  Fig. 5.2. Ranges of (a) red fox (Vulpes vulpes), and (b) arctic fox (Alopex lagopus), in northern North America (from Banfield (1974) and Hall (1981)).  00  [‘.3  219 their need for a more diverse prey base than that supporting arctic fox. Red fox, being larger, have higher daily food needs (320-470 g/d; Lockie 1959, Ryszkowski et al. 1973, Sargeant 1978) compared with arctic fox (c. 205 g/d; Riewe 1977). Consequently, they will depress rodent populations faster than arctic fox, and are more likely to need alternative foods in order to survive without becoming nomadic. Red fox could utilize breeding birds (including seabirds, waterfowl, ptarmigan (Lagopus spp.), shorebirds and passerines), medium-sized mammals such as arctic  ground squirrels and arctic hare (Lepus arcticus), and carrion (e.g., caribou (Rangifer tarandus) carcasses) to supplement a summer diet of small rodents. Not all of these are available year-round, unless foxes cache food for winter. In northern Yukon, red and arctic fox both rely on microtine rodents in summer, but breeding adult and juvenile red fox consumed a higher proportion of birds, principally waterfowl (Smits  et a!. 1989). At Pearce Point, the red fox can fully or at least partially compensate for declining summer lemming abundance principally by feeding on arctic ground squirrels, but also on tundra voles and birds (Chapter 4). Red fox in alpine tundra of Alaska and Yukon rely heavily on arctic ground squirrels in summer (Jones and Theberge 1983). A red fox female in northwest Alaska killed at least four squirrels a day in mid-summer to feed a family (Carl 1971). Ground squirrels and birds appear sufficient to sustain red fox breeding when microtine rodents do not suffice, but how red fox sustain themselves in winter is unclear (Chapter 4). Arctic ground squirrels are confined to mainland tundra, excluding Ungava, having radiated from Beringia following the Wisconsin glaciation, and not being able to establish themselves as breeding populations on islands because of their need to  220 hibernate (Macpherson 1965). Consequently they are not found in two large regions where lemmings irrupt: Ungava, and the arctic islands (Fig. 5.3). Red foxes in these regions may have other alternative prey such as birds, arctic hare, ptarmigan or caribou, to supplement a diet of lemmings. For example, red foxes raising young by a seabird colony on Digges Island, off the Ungava coast, raised young on a mixed diet of collared lemmings and thick-billed murres (Uria lomvia) (Gaston et a!. 1985). To survive winter in these regions, foxes likely rely more on cached food, or a nomadic scavenging existence (Andriashek et a!. 1985). However, unless red foxes return to breed at the same sites in consecutive years, their distribution on the eastern arctic islands is unlikely to affect the frequency of lemming irruptions. The diversity of microtine rodent species also tends to be higher in communities with red foxes and non-irruptive lemmings. Irruptive populations of lemmings occur in regions with one or both lemming species, but rarely any other small rodent (Fig. 5.3)(Krebs 1964, Fuller et a!. 1975b, Batzli et a!. 1980). In non irruptive situations, Lemmus becomes relatively uncommon, apparently because of habitat limitations, and other microtines, such as the tundra vole (Microtus oeconomus), the tundra red-backed vole (C!ethrionomys rutilus) and the singing vole (Microtus miurus), appear in the system (Batzli and Jung 1980, Pitelka and Batzli 1993, Krebs et a!. 1995). If foxes select lemmings (in particular Dicrostonyx) first, reducing their abundance, then other microtines may act as alternative prey, as do ground squirrels and tundra voles at Pearce Point (Chapter 4). Arctic foxes appear adapted to situations with less diverse and less predictable food resources. In summer, the inland pairs supplement a diet of small rodents with  221  Fig. 5.3. Ranges in arctic North America of two lemming species complexes, (a) Lemmus, and (b) Dicrostonyx , and ranges of four rodent species potentially  sympatric with lemmings, and acting as potential alternate food for red fox: (c) arctic ground squirrel, (d) tundra red-backed vole, (e) tundra vole, and (f) singing vole.  223 eggs, birds, insects, carrion and berries (Garrott and Eberhardt 1987). Their breeding success is high when small rodents are abundant (Garrott and Eberhardt 1987), but they are unable to compensate for a scarcity of small rodents with these other foods (Macpherson 1969). They may try to compensate by feeding more on waterfowl eggs, nestlings and perhaps adults (Anthony et al. 1991, Underhill et a!. 1993), but these food sources are short-lived. Consequently arctic foxes become nomadic scavengers and hunters in some summers and most winters (Chesemore 1975, Garrott and Eberhardt 1987). Arctic ground squirrels are absent, or rare items in arctic fox diets (Chesemore 1968, Macpherson 1969, Garrott and Eberhardt 1987), probably because the squirrels are scarce in most breeding areas. However, arctic fox at Prudhoe Bay, Alaska (where squirrels are present), do eat more squirrels when lemmings are scarce (Garrott et a!. 1983). This might partly explain the less extreme lemming fluctuations at Prudhoe Bay compared with Barrow, where squirrels are rare (Batzli et a!. 1980). The second major distinction between predator communities (Table 5.3) was the greater diversity of generalist predators where lemmings do not irrupt. Once again the arctic ground squirrel was a critical prey item. Of the generalists at Pearce Point, the golden eagles fed primarily on ground squirrels, the gyrfalcons replaced their primary prey, ptarmigan, with ground squirrels (see also Poole and Boag 1988), and the ground squirrels were found in 63% of grizzly bear scats (Chapter 4). The primary protein source for tundra bears in Yukon is ground squirrels (Pearson 1975), and grizzly bears exerted significant late summer predation pressure on arctic ground squirrels in northwest Alaska (Carl 1971). Peregrine falcons were an exception, taking few ground squirrels. However, ground squirrels themselves were also one of the  224 generalist lemming predators (Boonstra et a!. 1990, Chapter 1). At this one wellstudied site with non-irruptive lemmings, arctic ground squirrels appear to be the crucial extra prey item allowing persistence in summer of red fox and a suite of generalist lemming predators. Ground squirrel range overlaps regions where lemmings irrupt, but they are absent or sparsely distributed at mainland lemming study sites with irruptions, including Baker Lake and Walker Bay (Table 5.3). Ground squirrel distribution is limited primarily to well-drained soils providing an adequate substrate for denning and digging hibernacula (Carl 1971). Their distribution in mainland regions is therefore limited by surficial geology, and confined to areas of relatively sandy alluvium, till or eskers (Carl 1971, Batzli and Sobaski 1980). The dispersion of squirrels, and consequently their availability to a predator, varies substantially from area to area. Snow Depth Annual mean total snowfall is not lower in regions without irruptions compared with regions with irruptions (Fig. 5.4). Therefore the lower snowfalls experienced by the central Canadian mainland coast, western islands, and Alaskan coastal plain, can be sufficient in some winters to allow irruptive growth. However, inadequate snow may preclude irruptive winter breeding, even when predators are scarce and food abundant (Shelford 1943, Krebs 1964, MacLean et a!. 1974). The result is a longer period between consecutive irruptions, and potentially less regularity in the period and amplitude of irruptions. Long-term lemming data are lacking from a region of heavy snowfall, but the regularity of peaks (mean period 4 ± 0.2 (S.E.)  225  Fig. 5.4. Map of isohyets (dotted lines) of mean total annual snowfall (cm) in arctic North America. Data are taken from Maxwell (1980) and Hartman and Johnson (1984).  226  227 years) in fox pelts from Ungava reported by Elton (1942) suggests a regular cycle in that region of higher snowfall.  Food Availability Both lemming species occupy a range of vegetation communities. Comparisons of winter food availability between regions are suspect unless vegetation communities are very similar, and unless one can quantify live tissue in standing crops of lemming foods. This has not been done frequently enough to make any suitable comparisons between regions of differing constancy in lemming numbers. HYPOTHESES I propose a number of alternative hypotheses, each of which might be sufficient to explain the paucity or absence of lemming irruptions on the tundra of the western Canadian mainland and the north slope of the Brooks Range in Alaska. Each one stems from the strong limiting effect of generalist predators with sufficient alternative prey. Erlinge et al. (1991) also concluded that heavy predation by generalist predators best explained the lack of cyclic irruptions in some Fennoscandian populations of the field vole (Microtus agrestis). I hypothesize that a lemming population cannot irrupt when: (a) it exists within the hunting range of a breeding population of red foxes, which uses this range in consecutive summers. (b) it exists within the overlapping hunting ranges of the following generalist lemming predators: grizzly bear, arctic ground squirrel and peregrine falcon. (c) it coexists with a persistent arctic ground squirrel population. These are not mutually exclusive hypotheses. Based on current knowledge,  228 each one might be sufficient, or some combination of them might be sufficient, to explain a lack of irruptions. An arctic ground squirrel population may be the sole sufficient condition, because the other two conditions are frequently met when ground squirrels are present, and therefore prey for the generalist predators. However, there is probably some threshold density below which ground squirrels do not exist in sufficient numbers or proximity to lemmings to provide sufficient prey to sustain generalist predators, nor kill a substantial proportion of the lemmings themselves. This threshold is likely determined by habitat quality, in particular den site availability and dispersion (Carl 1971). For example, arctic ground squirrels exist in the Baker Lake region (Table 5.3), but at low densities because habitats are widely dispersed and associated with eskers. They therefore are likely to have little direct or indirect impact on lemmings in this area. Differentiating among hypotheses will require annual estimation of numbers and breeding status of all summer predators in areas where lemming population numbers are monitored. Simulation modelling of community dynamics, using parameters in this thesis, may help determine threshold densities at which ground squirrels can support red foxes and other generalist predators during summer. The most insightful field data regarding the hypotheses are likely to come from areas where red and arctic fox distributions overlap, but where ground squirrels are absent. Sites could include Herschel Island in northern Yukon, Baffin Island, or a number of moderate sized islands in Hudson Strait between Baffin Island and Ungava.  229 CONCLUSION  The population dynamics of collared lemmings (Dicrostonyx kilangmiutak) at Pearce Point, N.W.T., are clearly different in summer and winter. In most snow-free periods, lemming populations decline, or remain fairly stable, despite production of at least two, and more often three, litters by each female. In periods of snow cover, populations recover with breeding under the snow in mid-winter and spring. The principal pattern is one of annual fluctuations with highest densities most frequently occurring in spring, but never exceeding three adults per hectare. The snow-free summers expose lemmings to heavy predation mortality which strongly limits their population growth. Predators drive summer declines or limit growth to modest gains. A diverse assemblage of predators preys heavily on all lifestages: adults, subadults and neonates. When predation mortality is experimentally reduced, survival of all life stages increases, and no other limiting factor compensates for reduced predation mortality. Consequently, predation mortality is sufficient and necessary to limit growth and maintain lemmings at low densities in summer. A search for alternative factors operating at low densities in summer, reveals that neither food availability nor social inhibition of reproduction appear to limit summer population growth. Heavy predation mortality however, appears to predispose the population to additional, though weak, limiting factors. These are infanticide of neonates, probably by strange males, and suppressed individual growth rates of neonates, because of the lactating female’s sensitivity to predation risk. When summer predation mortality is intense, it is destabilizing; predators drive lemmings  230 to low densities at which the predators can no longer sustain themselves. Winter population growth requires the production of successive litters under the snow. Suitable winter habitat coincides with the distribution of deepest snow, probably because of the thermal and predation cover provided by snow. Variance in rates of population change among seasons of snow cover is well explained in a multiple regression analysis by a combination of the extent of cold stress in autumn (September and October), when lemmings are changing from summer to winter morphology, and the cold stress in winter, as indexed by the degree of thermal cover provided by each cm-day of snow per degree-day of frost. Ermine predation explains little of the interannual variation in winter population growth. Lemmings may be food limited in winter. Despite winter population growth, densities by spring have not been high enough, in six years of study, to exceed those which predators can maintain at low densities in summer. The summer predator community includes specialist (rough-legged hawk, and perhaps glaucous gull), semi-generalist (red fox, ermine), and generalist (grizzly bear, golden eagle, peregrine falcon, gyrfalcon, arctic ground squirrel) predators. Roughlegged hawks and red foxes are the principal lemming predators. At lemming densities greater than one per hectare in early summer, hawks settle and breed, and red foxes breed successfully. At very low lemming densities in early summer, only generalist predators continue to breed successfully. However, these generalists continue to exert substantial mortality on lemmings even at low densities, and thereby continue to limit population growth when both specialists and some semi generalists are absent. The persistence in this community of generalists and semi-  231 generalists appears directly tied to arctic ground squirrels, which are fairly abundant and evenly distributed. The ground squirrels are the primary prey for golden eagles, gyrfalcons and grizzly bears. They are the primary alternative prey for foxes when lemmings are scarce. They are also lemming predators themselves. Pearce Point is situated in a region of arctic North America where populations of microtine rodents, in particular collared lemmings, rarely if ever irrupt to densities greater than ten per hectare. This region includes the Canadian mainland, west of approximately the Coppermine River, and the northern foothills of the Brooks Range of Alaska. It contrasts with other North American tundra regions where populations of microtine rodents, notably collared and brown lemmings, irrupt periodically and often cyclically. Ecological communities in these regions differ substantially in the composition of their predator conmnmities. Where lemmings irrupt, most predators are lemming specialists and frequently disappear from the community in the pre irruptive summer. Where lemmings do not irrupt, most predators are generalists or semi-generalists. 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