Functional Responses of Coyotes and Lynx to the Snowshoe Hare Cycle

Ecology, 79(4), 1998, pp. 1193-1208 ? 1998 by the Ecological Society of America

FUNCTIONAL RESPONSES OF COYOTES AND LYNX TO THE SNOWSHOE HARE CYCLE

MARK O'DONOGHUE,"5 STAN BOUTIN,2 CHARLES J. KREBS,' GUSTAVO ZULETA,3 DENNIS L. MURRAY,26 AND ELIZABETH J. HOFER4 'Ecology Group, Department of Zoology, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4 Canada 2Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9 Canada 3INEUCI Institute (CONICET), Department of Biology, University of Buenos Aires, Ciudad Universitaria, Pab. 2, Piso 4, 1428, Buenos Aires, Argentina 4Mile 1055 Alaska Highway, Silver Creek, Yukon YJA 3V4 Canada

Abstract. Coyotes and lynx are the two most important mammalian predators of snowshoe hares throughout much of the boreal forest. Populations of hares cycle in abundance, with peaks in density occurring every 8-11 yr, and experimental results suggest that predation is a necessary factor causing these cycles. We measured the functional responses of coyotes and lynx during a cyclic fluctuation of hare populations in the southwest Yukon, to determine their effect on the cyclic dynamics. We used snow-tracking and radio telemetry to examine changes in the foraging behavior of the predators. Coyotes and lynx both fed mostly on hares during all winters except during cyclic lows, when the main alternative prey of coyotes was voles, and lynx switched to hunting red squirrels. Both predators showed clear functional responses to changes in the densities of hares. Kill rates of hares by coyotes varied from 0.3 to 2.3 hares/d, with the most hares killed one year before the cyclic peak, while those of lynx varied from 0.3 to 1.2 hares/d, with the highest one year after the peak. Maximum kill rates by both predators were greater than their energetic needs. The functional response of coyotes was equally well described by linear and type-2 curves, and that of lynx was well described by a type-2 curve. Kill rates by coyotes were higher during the increase in density of hares than during the cyclic decline, while the reverse was true for lynx. Coyotes killed more hares early in the winter, and cached many of these for later retrieval. Lower densities of hares were associated with longer reactive distances of both predators to hares, but with little apparent change in time spent searching or handling prey. In summary, our data show that the two similarly sized predators differed in their foraging behavior and relative abilities at capturing alternative prey, leading to different patterns in their functional responses to fluctuations in the density of their preferred prey. Key words: Canis latrans; coyote; functional response, components of; Lepus americanus; lynx; Lynx canadensis; predation; population cycle; snowshoe hare.

INTRODUCTION sole cause of cycles in the abundance of small mam- Populations of snowshoe hares (Lepus anericanus) mals but that it likely did: (1) hasten the decline of undergo regular cycles in abundance throughout the herbivore populations already declining for other rea- northern boreal forest in North America, with ampli- sons (e.g., food shortage); (2) increase the amplitude tudes over two orders of magnitude, and 8-11 yr be- of cycles by driving prey populations to very low num- tween cyclic peaks (Elton and Nicholson 1942, Keith bers; (3) increase the period of cycles, due to a lag 1990). These cycles have major effects on predators of effect of predators persisting into periods of low prey hares and other herbivores in the relatively simple bo- numbers (delayed density dependence); and (4) pos- real ecosystem (Finerty 1980). sibly synchronize cycles over large geographic areas The role of predation in generating cyclic fluctua- due to the high mobility of many predators. This agrees tions in abundance of prey has been much studied and with the hypothesis put forward by Lloyd Keith and debated. In a review, Finerty (1980) summarized the colleagues, based on studies spanning two complete prevailing view that predation was unlikely to be the cycles of hares in Alberta (Keith and Windberg 1978, Keith et al. 1984, Keith 1990). The Keith Hypothesis Manuscript received 12 November 1996; revised 20 May proposed that the cycle in hare numbers was generated 1997; accepted 22 May 1997; final version received 13 June by an interaction between the hares and their winter 1997. food supply, with predation playing a key role only 5Present address: Box 251, Mayo, Yukon Territory, YOB the of et al. IMO Canada. during decline phase the cycle (Keith 1977). 6 Present address: Department of Fish and Wildlife Re- Recent empirical and theoretical studies suggest that sources, University of Idaho, Moscow, Idaho 83844 USA. predation may be a necessary factor in causing cyclic 1193 1194 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4 dynamics of prey. In the southwest Yukon, neither ex- sity (Holling 1959b), (2) predators switching among perimental food addition nor exclusion of mammalian prey types, habitats, or foraging tactics (Royama 1970, predators alone changed the timing or magnitude of Murdoch and Oaten 1975, Akre and Johnson 1979), cyclic declines in numbers of snowshoe hares (Krebs (3) adaptive variation in foraging rates (Holling 1966, et al. 1995). Only when hares were both provided with Hassell et al. 1977, Dunbrack and Giguere 1987), and supplemental food and protected from predators did the (4) changes in the behavior or vulnerability of prey, or dynamics of the cycle change, suggesting that a three- prey having a refuge below a fixed density (Holling trophic level explanation must be invoked (Krebs et al. 1965, Murdoch and Oaten 1975, Taylor 1984). Only 1995). Mathematical models support the proposal that type-3 responses describe density-dependent predation predation is a necessary factor in the hare cycle (Ak- (although, in combination with positive numerical re- qakaya 1992, Royama 1992, Stenseth 1995). sponses, all types of functional responses may lead to Likewise, Scandinavian researchers have presented density-dependent predation), and there is evidence theoretical (Hanski et al. 1991, 1993, Hanski and Kor- from field (e.g., Pech et al. 1992) and theoretical (e.g., pimaki 1995) and empirical (Henttonen et al. 1987, Hassell and Comins 1978, Nunney 1980) studies that Korpimaki and Norrdahl 1991, Korpimaki 1993) evi- sigmoidal functional responses may stabilize predator- dence that predation is an essential factor in generating prey interactions. 3-4 yr cycles of microtine rodents in northern Fen- The main predators of snowshoe hares are the same noscandia. Strong functional responses by a large suite throughout much of their range: lynx (Lynx canaden- of generalist predators may regulate vole numbers in sis), coyotes (Canis latrans), Great Horned Owls (Bubo southern regions (Erlinge et al. 1983, 1984, 1988), virginianus), and Goshawks (Accipiter gentiles). Keith while delayed numerical responses of specialist pred- and colleagues (Keith et al. 1977) estimated the pop- ators, mostly weasels, cause a lag and cyclic dynamics ulation sizes and kill rates of these predators during a in the north (Korpimaki et al. 1991). complete hare cycle in order to analyze the effects of The effects of any predators on populations of their predation on hare dynamics. They found that both coy- prey are determined by their numerical (changes in otes and lynx responded to the increase in hare numbers reproduction, survival, or aggregation) and functional with increasing kill rates. Coyotes killed virtually no responses (changes in kill rates) to prey density (So- hares at cyclic lows, while they killed an estimated lomon 1949). In order for predation to have a regula- 0.66/d per coyote when numbers of hares were high. tory effect, the proportion of a prey population killed The kill rate by lynx increased about threefold over the must both increase with prey density (i.e., density de- same time period. The functional responses of coyotes pendent), and be greater than the net production of prey and lynx were judged to be type 3 and type 2, respec- at prey densities exceeding an equilibrium (Sinclair and tively (Keith et al. 1977). Pech 1996). Depensatory predation, in which the per- Lynx are usually considered prototypical specialists centage of prey killed increases with declining prey on snowshoe hares, and virtually all studies of their abundance, can result from time lags in the responses food habits have shown hares to be their predominant of predators to fluctuations in prey abundance. The prey (Saunders 1963, Brand and Keith 1979, Parker et shapes and timing of the numerical and functional real. 1983, Ward and Krebs 1985). They are morpholog- sponses of predators to prey are thus critical to deter- ically well adapted to hunting in the deep snows of the mining the effects of predation on prey populations. north (Murray and Boutin 1991), and their geographic However, there have been very few direct measure- range overlaps almost exactly with that of hares (Ban- ments of both these responses in wild populations of field 1974). animals (Boutin 1995). Coyotes, in contrast, are often considered prototyp- Holling (1959b) described three basic forms of func- ical generalists. Over their large and expanding range tional responses of predators to changes in density of in North America, they are adapted to a wide variety prey. Type- I responses describe linearly increasing kill of habitats, climates, and foods (see papers in Bekoff rates with prey density up to a threshold, above which 1978). Morphologically, coyotes are not well suited for the rate is constant. Type-2 responses describe kill rates hunting in deep, soft snow because they have a high increasing at a monotonically decreasing rate with prey foot-load relative to other northern mammals (Murray density (i.e., a convex curve approaching an asymp- and Boutin 1991). Coyotes are fairly recent immigrants tote), and type-3 responses are sigmoidal in shape. into the far north, appearing in the Yukon between 1910 Type-2 responses may be typical of specialist preda- and 1920 (G. Lotenberg, unpublished report). tors, predators with few alternative prey, or they may Theoretical (Murdoch and Oaten 1975, Hassell and arise due to adaptive adjustment of search rates and May 1986, Crawley 1992) and empirical (e.g., Erlinge time to the benefits and costs of foraging (Abrams et al. 1983, Henttonen et al. 1987, Korpimaki 1993) 1990, 1992). Type-3 responses are more typical of gen- evidence predicts that the effects of generalist and spe- eralist predators, and they may result from a number cialist predators on prey populations are likely to be of mechanisms: (1) predators learning to recognize, very different. Rapid functional responses of generalist capture, or handle prey better with increasing prey den- predators may increase the stability of predator-prey June 1998 PREDATION BY COYOTES AND LYNX 1195 interactions, while the delay in the numerical responses responses to hares of both predators are determined by of specialists may introduce lags and dynamic insta- their respective daily metabolic requirements (esti- bility. mated at -0.9 hares per day for coyotes [Litvaitis and While there is ample evidence that the hare cycle Mautz 1980], and 0.4 hares per day for lynx [Nellis et has persisted since long before coyotes immigrated into al. 1972], from trials with captive animals). Alterna- the north (Elton and Nicholson 1942), there is little tively, one or both species may exhibit surplus killing quantitative evidence of their effect on hare popula- or wastage (Kruuk 1972), and kill more animals than tions, populations of alternative prey, and other pred- expected at high densities of hares. ators. Very few studies have been conducted of coyotes STUDY AREA in contiguous boreal forest (Theberge and Wedeles 1989, Murray and Boutin 1991, Murray et al. 1994, This study was conducted in the southwest Yukon 1995); Keith's study area was approximately one-third Territory, Canada (60?57' N, 138?12' W), in a broad agricultural land, which was used by coyotes exten- glacial valley of -350 km2. The study area was bound- sively during periods of low hare numbers (Todd et al. ed to the north and south by alpine tundra, to the west 1981). The functional responses in Keith's study area by Kluane Lake, and to the east by Kloo Lake and the were calculated using an unverified energetic model Jarvis River. Elevation ranges from -830 to 1170 m. for coyotes (i.e., assuming no surplus killing or wast- The dominant vegetation of the area is white spruce age), and an assumption that lynx rested only once per forest (Picea glauca) with scattered aspen stands (Pop- day (Keith et al. 1977). There is therefore a need for ulus tremuloides), and a dense but patchy understory direct measurement of the functional responses of coy- of willow (mostly Salix glauca and S. alaxensis), bog otes and lynx in the boreal forest to better understand birch (Betula glandulosa), and soapberry (Shepherdia their effects on the snowshoe hare cycle. canadensis) (Douglas 1974). The climate is cold con- tinental, with mean January temperatures of -18'C, OBJECTIVES, HYPOTHESES, AND PREDICTIONS and -65 cm average snow accumulation. Snow cover The goals of this paper are to present and contrast is usually continuous from October through May. the functional responses of coyotes and lynx to the METHODS snowshoe hare cycle, and to examine the associated This study was conducted as a part of the Kluane changes in the "components" of these responses (Holl- Boreal Forest Ecosystem Project, an experimental ing 1959b, 1966): rate of successful search, foraging study of the vertebrate food web in the northern forests time, and handling time. This research is aimed at meet- (Krebs et al. 1995). Field work was started in 1986, ing part of a larger objective of evaluating the total and continued through the winter of 1994-1995. With impact of mammalian predators on the dynamics of the exception of some scat collection, live-trapping, snowshoe hares. Both predators are approximately the and radio telemetry, field work was conducted during same size (9-12 kg adult body size in the southwest the winter months, from October to April. Yukon), and they are therefore reliant on essentially the same prey base. Estimation of hare and predator densities Specifically, we present the average kill rates of coy- We estimated densities of snowshoe hares by live- otes and lynx each winter during a cycle in abundance trapping on 1-3 60-ha grids each March and October- of hares in the southwest Yukon. We then examine the November, from 1986 through 1995 (Boutin et al. predators' travel rates, reactive distances, capture suc- 1995). Population estimates were made using the jack- cess, foraging time, and handling time to determine knife estimator in program CAPTURE (White et al. mechanisms contributing to the functional responses. 1982). A sample of hares was radio-collared during Changes in these components with prey density can this period (n = 803 hares from 1987-1988 through result in either type-2 or type-3 functional responses, 1994-1995, not including those on fenced and food and it is valuable to look at the separate components addition experimental grids; radio collars from Lotek, to understand the predators' reactions to changing den- Newmarket, Ontario), and they were monitored each sity of hares (Abrams 1990). 1-2 d for estimation of survival rates (Krebs et al. We postulate two null hypotheses: (1) The shapes of 1995). the functional responses of coyotes and lynx are de- We estimated the numbers of coyotes and lynx in termined only by the relative abundances of hares and our study area by monitoring the movements of radio- alternative prey. If this were true, then the functional collared animals, and "filling in" the locations and responses and dietary composition of both species numbers of uncollared predators using evidence from should be similar as hare numbers fluctuate. Alterna- their tracks and, in the case of coyotes, their howling tively, lynx may respond very quickly to increasing (details in O'Donoghue et al. 1997). hare density and have type-2 functional responses, while coyotes may switch to and from alternative prey Snow-tracking of coyotes and lynx as the relative abundances of prey change, resulting in We followed the tracks of coyotes and lynx each type-3 responses. (2) The asymptotes of the functional winter from 1987-1988 through 1994-1995, beginning 1196 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4 as soon as there was enough snow, usually in mid- to tory attempt as independent. Proportions of diet by late October, and finishing at the end of March. Nine- biomass were calculated by multiplying numbers of teen different observers snow-tracked predators during prey killed by 1500 g for hares, 250 g for red squirrels the eight winters of study. This was the main method (Tamiasciurus hudsonicus), and 20 g for small mam- that we used for determining species and frequencies mals. of kills and attempted kills, hunting success rates, lengths of chases, proportions of prey eaten, frequen- Scat analysis cies of scavenging and caching, and frequencies of We analyzed scats of coyotes and lynx collected in beds. We also collected scats along these tracks for all winters to supplement our estimates of the preda- later analysis. tors' diets obtained from the tracking data. Scats were Fresh tracks were selected along snowmobile trails frozen and stored until ready for analysis, at which time and roads in our study area on any days that weather they were autoclaved for 20-30 min. We divided our and snow conditions permitted. We were usually unable scat samples into separate months for each year and to distinguish among individual predators based on predator, and selected subsamples for analysis to max- their tracks, and so we chose tracks to follow that imize the spatial distribution over the study area and spread our tracking effort as evenly as possible over avoid selecting multiple scats from the same trails. the study area, between coyotes and lynx, and among Scats were analyzed by several different observers and different group sizes of predators. Once a track was in three laboratories, each using slightly different tech- selected, it was usually followed backwards (relative niques for handling scats and quantifying the undi- to the animal's direction of travel) until it was lost due gested remains of prey species. In all protocols, scats to poor snow conditions or confusion with the tracks were manually broken apart, 10-30 random samples of of other animals. We then tried to follow it forwards hairs were selected, and hairs from these subsamples as far as possible, to have continuous segments of max- were identified based on color-banding, and patterns of imum length; this sometimes required several days of cuticular scales and medullary pigments (e.g., Moore following the same tracks. et al. 1974). We counted the distance tracked on hand-held tally We report the results of scat analyses here only as counters (numbers of paces were later converted to the relative frequency of occurrence of different prey meters, using observer-specific conversion factors), items in scats, since this measure does not depend on and recorded events along the tracks on microcassette the protocol used for quantifying the contents of scats. recorders. At each site of a kill, we recorded the prey Although smaller sized prey are frequently overrepre- species, number of bounds by the predator, proportion sented in scat samples (Floyd et al. 1978, O'Gara of the carcass consumed (estimated subjectively), 1986), Johnson and Hansen (1979) reported that rela- which parts were left uneaten, whether or not any of tive frequency of occurrence of prey in scats of coyotes the carcass was cached, and a detailed description of was closely related to the percentage intake by biomass. any signs left. We recorded the prey species and number of bounds for all unsuccessful attempts. At sites where Monitoring of radio-collared predators predators scavenged old kills or retrieved caches, we We live-trapped coyotes and lynx, mostly during the estimated the amount of food eaten when possible (e.g., fall and winter months, using padded foot-hold traps impressions from cached prey were sometimes clear (No. 3 Soft-catch traps, Woodstream Corporation, Li- enough to see what parts of the prey were cached), and titz, Pennsylvania), cable snares (Fremont leg snares, noted any evidence of the initial cause of death of the Fremont Humane Traps, Candle Lake, Saskatchewan), prey. All beds were classified as crouches (or hunting and box traps (techniques similar to Mowat et al. 1994). beds), "short" beds (where the predator had lain down We checked traps at least once per day, and locked but did not stay long enough to melt the snow), or traps open when the temperature was <-20'C. During resting beds. the first 4 yr of the study, we immobilized captured We analyzed tracking data using the MGLH (Mul- animals using a 7:1 mixture of ketamine hydrochloride tivariate General Linear Hypothesis) procedure in SYS- and xylazine hydrochloride, but we switched to using TAT (Wilkinson 1990), and considered P < 0.05 the a mixture of tiletamine hydrochloride and zolazepam criterion for rejecting null hypotheses. We considered hydrochloride (Telazol, A. H. Robbins Company, Rich- each instance of a chase or kill by a predator, rather mond, Virginia) since then (Poole et al. 1993). than each individual predator (which we were unable We fitted animals with radio collars weighing 250- to distinguish), as an independent data point in our 350 g (Telonics, Incorporated, Mesa, Arizona); most statistical analyses. The outcomes of encounters be- of these had internal mercury switches sensitive to tween predators and their prey depend on many factors movement, which allowed us to monitor the activity of (including the behaviors and conditions of both ani- collared animals. The pulse rate of the radio signal mals, habitat, snow conditions, and weather), and while switched between 60 and 90 beeps/min, depending on it would have been valuable to control for individual the inclination of the mercury switch. predators, we felt justified in considering each preda- We monitored the radio-collared animals to gather June 1998 PREDATION BY COYOTES AND LYNX 1197 information on their travel rates and activity patterns, taken as the overall percentage time active per animal in order to interpret the snow-tracking data. From 1989 per year, and then the means of all coyotes and all lynx through 1995, we opportunistically measured normal within each year were calculated to give us estimates travel rates of coyotes and lynx when they were in of the average percentage time that coyotes and lynx accessible locations. To do this, we first walked in on were active each winter. Confidence limits were cal- a collared animal until we gained a very accurate fix culated using arcsine-transformed data. We carried out on its location (either by actually seeing the animal or a further check on the accuracy of this method in 1991- waiting until it left a bed, which we subsequently lo- 1992, by listening to the signals of three coyotes for cated). We then monitored the animal's activity until 122 h and of nine lynx for 295 h, and subjectively it either settled down into a bed or was in a location classifying them as active or inactive each 5 min based that we could once again pinpoint. On occasions that on variations in signal strength and pulse rate. We cal- we successfully determined two exact locations without culated the overall percentage time active of these an- disturbing the animal, we then followed the animal's imals in the same manner as with data from the au- tracks between the two sites and measured its exact tomatic receiver. travel distance, from which we calculated a travel rate. We also monitored the signals of radio-collared coy- Calculation offunctional responses otes and lynx during continuous blocks of time from We used travel rates and activity patterns estimated 1990 through 1995, to determine their activity patterns. from radio-collared animals to transform kills per ki- We set up monitoring stations at several high-altitude lometer trail from our snow-tracking data to kills per locations in the study area, where we could regularly day. Kill rates were adjusted for group size (including receive the signals of collared animals wherever they coyote pups and lynx kittens) for all tracks where more moved in their home ranges. We used a Lotek SRX- than one animal was followed. We calculated the 400 programmable receiver with a data logger (Lotek, amount of "active predator time" represented by our Newmarket, Ontario) to monitor the activity of pred- tracks in each winter, by predator species, by dividing ators. We set this to record the pulse rate and signal the total track distances by measured travel rates, and strength of a target animal's collar each 30 s, based on adding standard times for observations of kills and three signal pulses each reading. At these settings, we scavenging (0.75 h for each kill of a hare, based on could record -18 h of continuous activity before the observations of a captive lynx, 0.25 h for each kill of memory of the data logger was full. a squirrel, 0.08 h for each kill of a small mammal, 0.50 We conducted a series of trials with activity moni- h for each digging up and feeding on a cache, and 0.25 toring to develop a statistical technique to interpret h for each instance of scavenging). We then divided these data. We simultaneously monitored the signals of the active times for coyotes and lynx by the percentage target animals using the automatic receiver and an ob- times they were active each year to estimate the total server listening constantly to the signal. Observers re- amount of coyote and lynx time (including resting pe- corded continuous records of the activity of one coyote riods) represented by our snow-tracking each winter. for 20 h (in four different sessions), and five lynx for Kill rates of hares per day were calculated by predator 45.75 h (in 15 different sessions). We used the activity each winter, by dividing our measured numbers of kills recorded by the observers as the standards for inter- by the numbers of "coyote days" and "lynx days" that preting the data records from the automatic receiver. we had followed. We used discriminant function analysis to analyze We calculated the functional responses of coyotes the activity data. We first calculated separate discrim- and lynx by plotting kill rates against the fall and spring inant functions for coyotes and lynx based on our trial densities of hares, and the means of these two, based data. We calculated the mean, median, variance, and on live-trapping. For descriptive purposes, we fitted range of the pulse rate and signal strength in a 5-min Rolling's disc equation (1959a) to these data, using the sliding window from the data record of the automatic NONLIN least-squares curve-fitting procedure in SYS- receiver. These were standardized within each collar to TAT (Wilkinson 1990). It would have been desirable a mean - 0 and standard deviation = 1, and each period to statistically test whether the data were best described was classified as "active" or "inactive" based on our by type-i, type-2, or type-3 curves. However, given trial monitoring. The discriminant functions calculated that we only had eight data points (from eight winters) with these variables correctly predicted active periods per predator, and no replication at each density of hares, for coyotes 92% of the time and for lynx 79% of the this would have been little more than an exercise in time, and inactive periods for coyotes 77% of the time, curve-fitting, with little power to distinguish among the and for lynx 78% of the time. We used these discrim- true shapes of the curves (Trexler et al. 1988). inant functions to classify all of the activity records caches from the automatic receiver. Monitoring of We calculated the overall percentage time active each We observed caching of prey and use of caches by winter for each animal monitored, in six 4-h blocks, both coyotes and lynx during the first years of this beginning with 2400-0359. The mean of these was study. We had no way of knowing, however, how often 1198 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4

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L 0 0 0- 1986- 1988- 1990- 1992- 1994- 1987 1989 1991 1993 1995 0-_ (I Winter n 27 32 52 67 44 75 135 70 .-Other FIG. 1. Estimated densities of snowshoe hares (means of autumn and late winter estimates from live-trapping on 1-3 100 IM7 4 60-ha grids), coyotes, and lynx (estimates based on locations of radio-collared animals and snow-tracking; O'Donoghue et 80 al. 1997), from 1986 through 1995 in the southwest Yukon. The mean coefficients of variation were 34 and 44% for au- 60 - I IX tumn and late winter estimates of hares, respectively (Boutin et al. 1995). 40 20- and when caches were returned to, or whether the caches that we located while snow-tracking had been killed 0 by the same species that ate it later in the winter, killed 1987- 1989- 1991- 1993- by a different species, or had originally died of causes 1988 1990 1992 1994 besides predation. Distinguishing among these alternatives is important in understanding the kill rates and Winter foraging tactics of the predators. FIG. 2. Percentage of kills by prey species located along Beginning in the winter of 1992-1993, we began tracks of coyotes and lynx during winter, 1987-1988 through monitoring caches made by coyotes and lynx, which 1994-1995. Sample sizes are given above bars. "Other" kills we located while snow-tracking or from kills of radio- for coyotes were 2 grouse, 1 flying squirrel, and 1 unknown collared hares between October and April. When we prey, and for lynx were 12 grouse, 2 muskrats, 2 flying squir- 1 1 located caches with substantial meat left on them, we rels, short-tailed weasel, 1 red fox, and unknown prey. disturbed the sites as little as possible, and set up monitoring radios. These each consisted of a beacon radio, low numbers by the winter of 1992-1993 (Fig. 1). The hung in a tree overhead so the site could be located cyclic amplitude was 26-44 fold, depending on wheth- again, and a second "cache radio," which was buried er fall or spring densities are considered (Boutin et al. in the snow near the cache. The cache radio had a steel 1995). Numbers of hares began to climb again in 1994. wire wrapped around its battery, and the batteries were Densities of coyotes and lynx fluctuated 6-fold and 7.5- left uncemented to the radio transmitters. The wire ran fold, as the abundance of hares cycled, under the snow, and was twisted around an accessible respectively, with a in the numerical responses (Fig. 1; see part of the cache (often a leg). When caches were dis- 1-yr lag turbed, the battery pulled loose from the radio, which also O'Donoghue et al. 1997). then stopped transmitting. The cache radios were mon- Diets of coyotes and lynx itored every 2 d; when we could not hear signals from them, we followed the signals of the beacons to the Coyotes.-We followed the tracks of coyotes for sites, and recorded data about the cause of the distur- 1897 km during the eight winters from 1987-1988 bance, how much of the cache was eaten, and details through 1994-1995 (mean [+1 SD] per winter, 237 ? of the cache retrieval. 100 km). We found 189 kills by coyotes, 47.1% of which were hares, 13.2% red squirrels, and 37.6% RESULTS small mammals (Fig. 2). Coyotes killed mostly hares Densities of hares and predators from 1987-1988 through 1991-1992, plus some red Densities of hares increased from 1986-1987 to a squirrels and small mammals from 1989-1990 through peak of ~-2/ha in 1989-1990, and then declined to very 1991-1992. Small mammals comprised most kills in June 1998 PREDATION BY COYOTES AND LYNX 1199

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Winter Winter FIG. 3. Percentage biomass of kills by prey species lo- FIG. 4. Relative frequency of occurrence of prey species cated along tracks of coyotes and lynx during winter, 1987- in the scats of coyotes and lynx during winter, 1987-1988 1988 through 1994-1995. Sample sizes (numbers of kills) through 1994-1995. Sample sizes (numbers of scats ana- are given above bars. lyzed) are given above bars. Relative frequency of occurrence is roughly equivalent to biomass ingested, although smaller sized prey species may be overestimated. Other prey species 1992-1993 and 1993-1994, while hares and red squir- for both predators included moose, Arctic ground squirrel, rels were killed more frequently in 1994-1995. In and unidentified prey remains in scats. terms of biomass, the diets of coyotes were composed largely of hares in all winters (Fig. 3). Small mammals made up a maximum of 9.5% of biomass in 1993-1994, Lynx.-We followed the tracks of lynx for 2232 km a winter of high vole density, and red squirrels made during the eight winters from 1987-1988 through up a maximum of 19.9% in 1994-1995 (Fig. 3). 1994-1995 (mean [L 1 SD] per winter, 279 + 85 km). Scat analyses suggest that coyotes used a greater We found 502 kills by lynx, 50.2% of which were hares, diversity of prey during the cyclic increase (1987-1988 34.7% red squirrels, and 11.0% small mammals (Fig. and 1988-1989) and low (1992--1993 and 1993-1994) 2). Lynx killed mostly hares from 1987-1988 through phases in numbers of hares than indicated by our snow- 1991-1992, plus some red squirrels in 1987-1988. Red tracking (Fig. 4). The relative frequency of occurrence squirrels comprised most kills from 1992--1993 through of small mammals (mostly Microtus) in scats ranged 1994-1995. In terms of biomass, the diets of lynx were from 18.0 to 42.2% during these years; we likely composed largely of hares from 1987-1988 through missed many of these kills while snow-tracking. Hares 1991-1992, but red squirrels became increasingly im- comprised most of the diets of coyotes from 1989- portant from 1992-1993 through 1994-1995 (20.4- 1990 through 1991-1992 (relative frequency of oc- 43.9%; Fig. 3). Small mammals made up a negligible currence 82.9-90.7%), but only 31.1-65.4% (based on proportion of the diet in all winters. scats) in other years. Red squirrels were a minor com- Scat analyses suggest that lynx used a greater di- ponent of the diet in all winters (relative frequency of versity of prey during the cyclic increase (1987-1988 occurrence 0.0-13.5%). and 1988-1989) and low (1993-1994) phases in num- 1200 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4 bers of hares than indicated by our snow-tracking (Fig. 2.5 88 4). The relative frequency of occurrence of small mam- 2.0 mals in scats ranged from 23.1 to 25.5% during these years. Hares comprised most of the diets of lynx from 1989-1990 through 1991-1992 (relative frequency of occurrence 84.6-94.4%), and 38.5-60.0% of diets 0~~~~~~~~~8 (based on scats) in other years. Red squirrels were an a)~~~~~~~~~~~~8 important component of the diets of lynx from 1992- .21 5 ------a) 1993 through 1994-1995 (relative frequency of occurrence 25.0-36.5%). 20~~~~~~9 Travel speed of coyotes and lynx Between 1989 and 1995, we successfully completed measures of the travel rates of coyotes 7 times (average (D duration 46 range 15-150 min), and of lynx 16 min, 1 5 times (average duration 99 min, range 11-274 min). 99 0.50 _1S9- Coyotes traveled at 2.49 ? 0.39 km/h (?1 SD, range 1.77-3.06 km/h), while lynx traveled at 1.09 ? 0.21 km/h (? 1 SD, range 0.75-1.46 km/h). t93 Activity of coyotes and lynx Coyotes.-We used radio telemetry to monitor the 0 50 100 150 200 250 activity of three coyotes in 1990-1991 (522 h), three in 1991-1992 (279 h), one in 1992-1993 (73 h), and No. hares/i100 ha two in 1993-1994 (468 h). The percentage time active FIG. 5. Functional responses of coyotes and lynx (kills averaged 46.7%, and varied little among years (range per day per predator) to the density of snowshoe hares from 44.3-49.7%) and animals (mean cv = 2.4%). Like- 1987-1988 through 1994-1995. The solid lines represent the wise, the number of beds of coyotes that we found best fits of the disc equation (Holling 1959a) and, in the case of coyotes, a linear functional response curve, plotting kill while snow-tracking was approximately the same in all rates against the mean over-winter densities of hares. Num- years (range 2.5-4.3 beds/10-km trail). bers next to each point indicate the year starting each winter Lynx.-We used radio telemetry to monitor the ac- (e.g., 87 =1987-1988). For comparison, functional responses tivity of five lynx in 1990-1991 (1595 h), four in 1991 - of predators were also calculated using fall densities of hares 1992 (181 h), six in 1992-1993 (195 h), five in 1993- and kills by predators from October to December (long- dashed lines), and late winter densities of hares and kills from 1994 (845 h), and six in 1994-1995 (1441 h). The January to March (short-dashed lines). percentage time active averaged 41.5%, and varied little among years (39.2-43.5%) and animals (mean cv = 4.8%). Unlike coyotes though, the number of beds measurements from 1990-199 1 were used for the three of lynx that we found while snow-tracking increased previous winters, and those from 1993-1994 were used over three-fold from 1989-1990 (5.1 beds/10-km trail) for 1994-1995, to calculate the kill rates in those win- to 1993-1994 (18.4 beds/10-km trail). The frequency ters in which no measurements of activity were made.) of resting beds was more stable (range 1.9-5.0/10-km The disc equation (type-2 curve) was fitted to these trail) than that of ambush and short beds (range 3.2- data for the purpose of description (fitted parameters 13.4/10-km trail) during this period. a = 0.021, h =0.418), but its fit (r2 = 0.83) is little Accuracy of method.-We listened to the signals of better than the fit of a linear functional response (r2 = three coyotes (122 h) and nine lynx (295 h) during the 0.80). When functional responses are plotted separately winter of 1991-1992 to assess the accuracy of inferring for the early and late winter, the early-winter curve is activity patterns from the output of the automatic re- nearly linear, while the late-winter response approaches ceiver. Coyotes were judged to be active 47.4% of the an asymptote over observed prey densities (Fig. 5). The time based on this monitoring, compared to 48.1% of maximum over-winter kill rate per coyote suggested by the time from the automatic receiver, and lynx were the disc equation is 2.4 hares per day, which is close judged to be active 41.9% of the time, compared to to what we observed in 1988-1989 (2.3 hares/day). Kill 40.0% of the time from the automatic receiver. Ana- rates peaked in 1988-1989, a year before hare numbers lyzing the output of the automatic receiver therefore peaked, and they were generally higher during periods seems to be an accurate method of assessing activity of increase in density of hares (1987-1988 through 1988-1989, and 1994-1995) than during the peak, de- of predators. cline, and low phases of the cycle (1989-1990 through Functional responses of coyotes and lynx 1993--1994). Coyotes.-Coyotes showed a strong functional re- Lynx.-Lynx also showed a functional response to sponse to changes in density of hares (Fig. 5). (Activity changes in density of hares (Fig. 5). (Activity mea- June 1998 PREDATION BY COYOTES AND LYNX 1201 surements from 1990-1991 were used for the three 30 previous winters to calculate the kill rates in those winters in which no measurements of activity were made.) The disc equation was fitted to these data for the pur- 20 Killsof hares pose of description (fitted parameters a = 0.031, h = 0* 0.756), and it fits the observed kill rates quite closely 1 -U- - Aftempted kills,' (r2 = 0.96, compared to r2 = 0.88 for a linear functional response). Type-2 functional responses in the early- (I) winter and late-winter periods are similar in shape to 0- i that calculated for the whole winter, and, as with coyotes, the early-winter asymptote is higher (Fig. 5). The maximum kill rate per lynx suggested by the disc equa- ? 30 tion is 1.3 hares per day, which is close to what we 0) observed in 1990-1991 (1.2 hares/d). Kill rates peaked in 1990-1991, the year after hare numbers peaked, and 20 -.* Killsof hares , unlike coyotes, they were lower during periods of in- . -U- - Attempted kills,' '. crease in density of hares (1987-1988 through 1988- 1989, and 1994-1995) than during the peak, decline, 10 and low phases of the cycle (1989-1990 through 1993- 1994). 0 Components of the functional responses of coyotes 1987- 1989- 1991- 1993- and lynx 1988 1990 1992 1994 Holling (1959a, 1966) considered that there were Winter three basic components of functional responses of pred- FIG. 6. Lengths of chases of hares in successful (coyote, ators to prey: the rate of successful search (determined n = 59; lynx, n = 193) and unsuccessful (coyote, n = 149; by the reactive distance of the predator to its prey, the lynx, n = 623) attempts by coyotes and lynx from 1987- rates of movements of both the predator and prey, and 1988 through 1994-1995. Mean coefficient of variation of chase lengths = 103% (error bars are omitted for the sake of the predator's capture success), the time the predator clarity). was exposed to the prey, and the handling time (the sum of time spent pursuing, subduing, eating, and di- gesting prey). These parameters were constants in Holl- sity, we can only evaluate changes in travel rates during ing's disc equation (Holling 1959a), but it is likely they the hare cycle for lynx. The mean travel rate of lynx vary with changing densities of prey (Abrams 1990). did not differ between periods of higher numbers of We briefly examine our data here for evidence of hares (1989-1990 through 1991-1992; travel rate changes in these components with hare density; other (mean ? 1 SD) = 1.02 ? 0.23 km/h and periods of behavioral changes of predators are considered in lower numbers (1992-1993 through 1994-1995; travel O'Donoghue et al. (1998). rate (mean + 1 SD = 1.13 ? 0.16 km/h; t test, t = Rate of successful search.-The only measures that 1.63, df = 14; P = 0.13). We gathered no data on the we made of the reactive distances of coyotes and lynx travel rates of hares. to hares were the lengths of their chases, and we use Hunting success of coyotes preying on hares was these here as indices of the actual reactive distances relatively constant from 1989-1990 through 1993- (although they are invariably longer, due to the prey 1994 (range 26.8-37.5%; Fig. 7), but considerably being flushed). Chases of hares made by both coyotes higher in the cyclic increase years of 1988-1989 and lynx were considerably longer during the low and (57.4%) and 1994-1995 (68.8%, although the sample early increase phases of the hare cycle (1992-1993 size was quite small that year). Success rates of lynx through 1994-1995) than during the late increase, preying on hares were less variable than those of coy- peak, and decline winters (1987-1988 through 1991- otes (range 20.0-38.8%); the lowest success rates were 1992) (Fig. 6; ANOVA on log-transformed data, Effect in the last three winters of the study (20.0-21.9%; Fig. of Year, F = 32.26, df = 7, 990, P = 0.000; Tukey's 7). HSD for coyote and lynx data pooled, [1987-1988 = Time exposed to prey.-As previously noted, the per- 1988-1989 = 1989-1990] < [1989-1990 = 1990- centage of time active by both coyotes and lynx was 1991 = 1991-1992] < [1992-1993 = 1993-1994 = fairly constant from 1990 through 1995. For lynx, how- 1994-1995]). Unsuccessful chases were significantly ever, the percentage of time active may not be a good longer (F = 98.77, df = 1, 990, P = 0.000) than chases measure of time exposed to prey. Lynx often used am- at successful kills. bush beds, and use of ambush and short beds increased Since six of seven of our measures of rates of travel over four-fold during the cyclic decline of hares (see by coyotes were made during years of high hare den- also O'Donoghue et al. 1998). 1202 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4

100 5 E o 4 80 -6

C 60 - 47 (I) U) (a) 2 g\ a () ]~~~~~608 40 1 * 2 2 C/) -556/''1 ] 63 4 138,~ 20 ! 14| 78 55i "' 1 " /\ 0) U)~~~~~~~~* '

1987- 1989- 1991- 1993- 1987- 1989- 1991- 1993- 1988 1990 1992 1994 1988 1990 1992 1994

Winter Winter FIG. 7. Hunting success rates (percentage of all chases FIG. 8. Frequency of signs of scavenging (visiting old that were successful) of coyotes and lynx preying on hares kills or caches) along trails of coyotes and lynx from 1987- from 1987-1988 through 1994-1995. Sample sizes (number 1988 through 1994-1995. of chases) are given next to the points. to 14 of them (51.9%), and ate an average of 74.0% Handling time.-We have no measures of the amount (37.0-97.7%, 95% ci) of each carcass retrieved. No of time necessary to digest hares, but we did record caches made by coyotes were eaten by lynx, 2 were the amount of prey eaten per kill for both predators. scavenged by red squirrels, and 11 were unused. Coy- The percentage of the carcasses of hares eaten by coyotes returned to caches an average of 56.1 ? 34.6 d otes and lynx remained fairly constant from 1987-1988 (? 1 SD, range 9-140 d) after they made the kill. through 1994-1995 (ANOVA on arcsine-transformed Lynx typically cached only portions of hare car- data, Effect of Year, F = 0.43, df = 7, 285, P = 0.886). casses (one of seven carcasses was of a whole hare; Coyotes ate 82.2-95.6% of carcasses in all years except mean percentage of prey body mass cached = 61.1% 1993-1994, when an average of only 62.1% per hare [32.9-85.7%, 95% ci] per kill). Of the seven caches carcass was eaten (but only five hares were killed in of hares, lynx returned to six of them (85.7%), and ate this winter). Lynx ate an average of 78.2-95.2% per an average of 99.5% (96.1-99.7%, 95% ci) of each carcass. The total amount of time devoted to chasing, carcass retrieved. No caches made by lynx were eaten subduing, and eating hares are likely very minor com- by coyotes, none were scavenged, and one was unused. ponents of the time budgets of coyotes and lynx. Lynx returned to caches an average of 0.9 ? 0.5 d (?1 SD, range 0-2 d) after they made the kill. and and Scavenging caching by coyotes lynx Most caches of hares made by coyotes were made Signs of scavenging (defined here as any feeding on early in the winter (85.2% of monitored caches were prey that was not killed at that time by the predator made in October and November), while those made by being followed) were noted frequently along the trails lynx were more evenly distributed over the winter of coyotes, and more scavenging was noted during win- (42.8% in October and November). Evidence from ters of high hare abundance (Fig. 8). We found less monitoring the survival of radio-collared hares sup- evidence of scavenging by lynx, and the increase in ports this pattern. Most kills of radio-collared hares by frequency of scavenging with hare abundance was less coyotes in winter were made in October and November pronounced. (77.3% of 141 kills; Fig. 9), while lynx kills occurred We used our monitoring of caches to infer whether more evenly across the winter. Coyotes cached the en- or not the coyotes and lynx were scavenging animals tire carcasses of 37.0% of all hares they killed; they that they had likely killed previously, as opposed to cached the carcasses of 41.4% of all kills made in Oc- finding caches opportunistically. From 1992-1993 tober and November, and none after January. Lynx through 1994-1995, we monitored 37 caches; 30 of cached the entire carcasses of only 1.6% of kills. these were made by coyotes (27 hares, 1 red squirrel, 1 flying squirrel, and one piece of a moose carcass), DISCUSSION and 7 by lynx (all hares). Coyotes and lynx showed clear functional responses Coyotes cached mostly entire hare carcasses (24 of to changing densities of snowshoe hares. Kill rates of 27 carcasses were of whole hares; mean percentage of hares by coyotes increased at a faster rate than those prey body mass cached = 99.3% [96.7-100.0%, 95% by lynx during the cyclic increases in hare abundance. CI] per kill). Of the 27 caches of hares, coyotes returned The functional response of coyotes is described equally June 1998 PREDATION BY COYOTES AND LYNX 1203

0 110 92 65 153 48 62 60= n measured in the field is typical (Boutin 1995), contrary 0- to theoretical expectations. Coyotes responded to increasing hare numbers, both in 1987-1988 through 80 -Other 1988-1989 and in 1994-1995, with kill rates that were FIG. 9. Unidentified higher than those at comparable densities of hares dur- given above bars.Predator ing the cyclic decline (Fig. 5). Lynx showed the op- -Q 60- posite pattern. This was not what we had expected 0 4 based on the simple contrast of coyotes as generalists and lynx as hare specialists; typically, specialists re- a) 40_ spond with kill rates increasing at a faster rate at low densities of their preferred prey than do generalists. In 20- Alberta, the functional response of lynx was stronger 0) than that of coyotes at low numbers of hares (type-2 vs. type-3 responses; Keith et al. 1977). The availability of alternative prey in the Yukon may be one reason for the difference in the relative re- rr ~~~Month sponses of coyotes and lynx. The main prey of coyotes in our FIG. 9. Percentages of deprediatedradio-collared hares besides hares study area were small mammals killed by coyotes and lynx by monthduring winter from 1986 (Figs. 2-4). Populations of small mammals were high through 1995. Sample sizes (total numberof mortalities)are in 1987-1988 and from 1991-1992 through 1993- given above bars. Otherincludes avian predators,red foxes, 1994, and low in other years (Boutin et al. 1995). Based wolverines, wolves, and cases where the identity of the pred- on scat analyses (Fig. 4), they were the most important ator could not be determined. alternative prey of coyotes during years that they were abundant. The availability of small mammals during well by linear and type-2 curves, while that of lynx is winter, however, is limited by snow cover (Wells and well described by a type-2 curve. Both predators killed Bekoff 1982, Halpin and Bissonette 1988) and affected more hares than energetically required when hares were by species-specific vulnerabilities; Microtus, which are abundant. At lower densities of hares, coyotes preyed mostly confined to grassy meadows (which comprised more on small mammals, and lynx on red squirrels. only -7% of our study area), appear to be much more Coyotes frequently scavenged carcasses of hares, and vulnerable to predation than the more widespread many of these may be hares previously killed and Clethrionomys (Henttonen et al. 1987). cached by coyotes. Coyotes may have opportunistically taken advantage In the following discussion, we will discuss these of increasing numbers of hares because they had few main points in more detail, and finish with an evalu- alternatives. The most important prey of coyotes during ation of potential biases in our estimates of functional cyclic lows in other northern studies was either not responses. available (livestock carcasses in Alberta; Todd et al. 1981, Todd and Keith 1983) or available in low num- Functional responses of coyotes and lynx bers (moose carcasses in Alaska; Staples 1995) for coy- Our estimates of kill rates were based on measured otes in our study area. Coyotes were evidently not as numbers of kills per distance traveled, travel rates, and skilled at catching red squirrels as were lynx, since activity budgets of coyotes and lynx. The variance of they made few kills of this abundant potential prey. the latter two parameters was very low among radio- Alternatively, lower kill rates by coyotes during cyclic collared animals, but as we were unable to distinguish declines, and, in our case, at the cyclic peak of hare among tracks of individuals, we have no measures of abundance (1989-1990; Fig. 5), may reflect an in- variance of kill rates per winter. The functional re- creased proportion of inexperienced young animals in sponses calculated for predators therefore reflect over- the predator population, derived from the pulse of re- all trends among years, but we have no estimates of production from 1988-1989 through 1991-1992 their precision. We must be accordingly conservative (O'Donoghue et al. 1997). in the inferences we make based on these observed The main alternative prey of lynx during our study patterns. was red squirrels (Figs. 2-4). Populations of red squir- Although we had too few data points to accurately rels were relatively stable during the eight winters of determine the shapes of the functional responses of this study (Boutin et al. 1995). Behavioral data suggest coyotes and lynx, it is clear that the two predators that lynx increased active foraging for squirrels during responded differently to changing densities of hares in the cyclic low in hare abundance (1992-1993 and our study. The functional response of coyotes showed 1993-1994; O'Donoghue et al. 1998). Despite the in- no clear asymptote, especially in the early winter, while crease in hare numbers in 1994, lynx that had mostly that of lynx clearly had a decelerating slope (Fig. 5). hunted squirrels during the previous two winters, con- Lack of evidence for satiation in functional responses tinued to do so during the winter of 1994-1995. While 1204 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4 hunting success of lynx preying on hares declined from ing years of increasing densities of hares (Fig. 7). In- 1990-1991 through 1994-1995 (38.8% to 20.0%; Fig. creases in either of these parameters would lead to 7), it increased from 1992-1993 through 1994-1995 higher rates of successful search. Reactive distances of (30.5% to 50.5%; O'Donoghue et al. 1998) for lynx predators may be a function of hunger or environmental hunting red squirrels. factors (Holling 1965, Abrams 1990, Bell 1991), and These data suggest that lynx surviving into the low there is evidence from other field studies that satiated of the hare cycle became skilled at hunting squirrels, predators react to prey within smaller perceptual fields and these may have been less plastic than coyotes in (e.g., Wood and Hand 1985). The average hunting suc- modifying their foraging behavior when hare numbers cess of coyotes preying on hares was 36.9% and of started to increase again. There is ample evidence from lynx 28.7% in our study; this was higher than previ- the literature that foraging decisions are more strongly ously reported success rates of 6-10% for coyotes influenced by recent feeding choices than those made (Ozoga and Harger 1966, Berg and Chesness 1978), over a longer time frame (Shettleworth et al. 1993), but within the range of 19-57% reported for lynx and this effect may be stronger in some predators than (Saunders 1963, Haglund 1966, Brand et al. 1976, Par- others. ker 1981, Major 1989). As in this study, hunting suc- The maximum kill rates of hares by coyotes (2.3 cess of lynx was not related to hare density in Alberta hares per day per coyote) and lynx (1.2 hares per day (Brand et al. 1976). The apparently higher hunting suc- per lynx) calculated in this study are higher than those cess by coyotes in 1988-1989 and 1994-1995 may reported in the literature, and those based on estimates have been partly due to the absence of young, inex- of energetic requirements. The energetic needs of coy- perienced coyotes in the population during these years. otes have been estimated to be from 0.7 to 0.9 hares We have no evidence that coyotes or lynx changed per day (Keith et al. 1977, Litvaitis and Mautz 1980), their rate of travel as densities of hares changed (we and those of lynx to be from 0.4 to 0.5 hares per day did not, however, have an adequate sample size of coy- (Nellis et al. 1972, Aldama et al. 1991). Estimated kill ote travel rates at low hare densities). Several studies rates by lynx have ranged from 0.5 hares/d in New- have noted that travel rates vary with density of prey foundland (Saunders 1963) to 0.8 hares/d in Alberta (e.g., Smith 1974, Bell 1991), but Holling (1966) con- (Brand et al. 1976, Keith et al. 1977) to -I hare/d in sidered hunting speed to be adaptive for specific prey, Nova Scotia (Parker 1981). The studies in both Alberta and unlikely to vary. and Newfoundland based their estimates of kill rates Our measures of the activity patterns of coyotes and on the assumption that the distance between two resting lynx showed that neither species increased their amount beds represented 1 d of travel by lynx. Several studies of active time in response to declining numbers of have noted though, that lynx may rest more than once hares. During times of food shortage, many arthropod per day (Haglund 1966, Parker 1981; M. O'Donoghue, predators decrease the amount of time they spend for- unpublished data), and estimates made with this as- aging (review in Bell 1991), but this is not true for all sumption are likely underestimates. predators; lions do not change foraging time even dur- Our estimates of kill rates of hares by lynx, and ing periods when cubs are starving (Schaller 1972). particularly coyotes, are likely conservative, due to po- While Ward and Krebs (1985) found that lynx increased tential biases in our field sampling (see Discussion: their daily movements during periods of low hare den- How accurate are our estimates of kill rates?). Ap- sity in the Yukon, this was not the case in studies in parently then, coyotes, and to a lesser extent, lynx, Alberta (Brand et al. 1976). As discussed previously, killed more than they energetically needed during years active time is not likely equivalent to foraging time for of high abundance of hares. Some of this excess food lynx. Lynx increased their use of hunting beds during was cached by coyotes, and some of these caches were the decline and low phases of the hare cycle lost to scavengers or not retrieved. Storing excess food (O'Donoghue et al. 1998), which likely represented an may guard against future periods of scarcity or losses increase in the amount of time they were exposed to of caches (review in Vander Wall 1990). While lynx prey. seldom cached food, our data suggest some wastage We have no evidence that the handling time of coy- (incomplete consumption) of prey by lynx during peak otes and lynx preying on hares changed significantly years of hare abundance (mean 78.2-83.0% consumed during our study. We did note, however, that coyotes per carcass from 1989 through 1991). scavenged (and possibly cached) more often, and lynx consumed slightly less of hare carcasses, during peri- Components of the functional responses of coyotes ods of high hare abundance. Partial consumption of and lynx prey may decrease handling time (Abrams 1990). Our data suggest that the reactive distances of coyotes and lynx to hares (as indexed by the lengths of Diets of coyotes and lynx chases) increased once hares had declined to low abun- Coyotes depended heavily on snowshoe hares during dance (Fig. 6), and they provide weaker evidence that most years of our study, and preyed on small mammals the average hunting success of coyotes was higher dur- during winters when voles were abundant (Figs. 2-4), June 1998 PREDATION BY COYOTES AND LYNX 1205

which coincided with years of low hare densities. Al- Coyotes killed and cached most hares early in the though not quantified here, most small mammals killed winter (Fig. 9). This is also the time when snow is were Microtus (M. O'Donoghue, unpublished data). shallow, and travel is easier. Hares may also be more We likely underestimated the number of kills of small vulnerable at this time of year due to a higher propor- mammals from our snow-tracking because, while it was tion of young animals in their population. easy to distinguish attempted captures of voles by coyotes "mousing," it was often difficult to judge whether How accurate are our estimates of kill rates? they were successful. The results of our scat analyses There are a number of potential biases that could suggest that we missed many kills of voles. In Alberta have affected the accuracy of our estimates of kill rates (in the only other comparable study of diets of coyotes of hares by coyotes and lynx: during a cycle in abundance of hares), the proportion 1) In some winters, snow conditions were poor for of hares in the diets of coyotes ranged from 0% to 77% snow-tracking in October, so we could have missed during cyclic lows and highs, respectively (Nellis and some tracking during the time of year when kill rates Keith 1976, Todd et al. 1981, Todd and Keith 1983), by coyotes were highest. considerably lower than we observed (Figs. 2-4). 2) During the winters of peak densities of coyotes The preponderance of hares in the diets of lynx in and hares, the abundance of tracks often made snow- our study was consistent with all studies of North tracking in prime habitats difficult, due to confusion American lynx (e.g., Saunders 1963, Van Zyll de Jong caused by criss-crossing and obliterated tracks. Tracks 1966, Brand et al. 1976, Brand and Keith 1979, Parker were easier to follow when they were away from these et al. 1983, Staples 1995). However, extensive use of habitats. As a result, we may have tracked longer dis- red squirrels as the main alternative prey has not been tances outside of the best habitats where more kills noted previously. Only two other studies, one in Wash- would have been located. We attempted to avoid this ington (Koehler 1990) and one in Alaska (Staples by tracking right after fresh snows when tracks were 1995), have recorded squirrels as more than minor com- least confusing. ponents of the diets of lynx; in both these areas, pop- 3) Coyotes and lynx often circled many times in the ulations of hares were low. Our behavioral data show areas of kills, and made mazes of tracks that were con- that lynx actively hunted for squirrels from 1992-1993 fusing to follow. This was particularly true of coyotes. through 1994-1995, and may have switched (sensu We may have missed some kills because we were un- Murdoch 1969) from preying on hares to preying on able to follow some tracks to kills. We attempted to red squirrels during these years (O'Donoghue et al. avoid this by searching very carefully in any areas with 1998). Our scat analyses suggest that lynx also preyed frequent circling. on small mammals in significant numbers during win- 4) Coyotes were very skilled at hiding caches of ters when voles were abundant (Fig. 4). hares with minimal deviation from their trail and little The contrast between coyotes and lynx as generalists noticeable disturbance to the snow. We may have vs. hare specialists is obviously not appropriate at the missed some of these, although we searched very care- local scale in our study area. Where few alternative fully around any areas where coyotes broke stride. prey are available, coyotes may be as or more depen- 5) Coyotes and lynx that were the most successful dent on hares than are lynx. hunters may have moved less than unsuccessful predators, and therefore crossed our trails, where we started Scavenging and caching by coyotes and lynx snow-tracking, less frequently. The evidence from our monitoring of radio-collared 6) We may have overestimated the amount of active hares and caches suggests that many of the instances time of radio-collared coyotes and lynx. Activities such of scavenging of hares by coyotes, which we noted as eating or grooming, in which the animal frequently while snow-tracking, may have been of their own pre- moved its head up and down, were probably classified vious kills. Lynx seldom cached prey, and when they as active in our analyses, even though the animal was did, they usually retrieved it the next day. Coyotes, in not traveling. This bias would cause us to underesti- contrast, returned to about half of their caches, as long mate the total amount of time represented by our tracks, as 41/ mo after they were made. The wires and radios and therefore overestimate kill rates. We added in stan- that we attached to the caches may have discouraged dard times for each instance of a kill or scavenging some animals from retrieving their caches, so this re- that we observed, to account for active time spent at turn rate is a minimum estimate. This nevertheless sug- these activities. While we could not directly measure gests that coyotes have a long-term spatial memory that these standard times, the total amount of time spent allows them to remember the location of caches even feeding was a relatively small proportion (means of after they have been covered by a half meter of snow 10.0% [7.5-12.9%, 95% ci] and 4.1% [3.3-4.9%, 95% (review of spatial memory by other species in Vander ci] of the total estimated time budgets of coyotes and Wall 1990). This corresponds with our field observa- lynx, respectively), and we suggest that there was little tions of coyotes deviating well away from their travel error introduced by this potential bias. In Alberta, Bow- routes (sometimes >0.5 km) to retrieve caches. en (1982) estimated that coyotes were active 50% of 1206 MARK O'DONOGHUE ET AL. Ecology, Vol. 79, No. 4 the time during winter, and Bekoff and Wells (1981, Banfield, A. W. F. 1974. The mammals of Canada. University 1986) estimated that coyotes spent 46% of their time of Toronto Press, Toronto, Canada. Bekoff, M., editor. 1978. Coyotes: biology, behavior, and traveling and hunting during winter; these are quite management. Academic Press, New York, New York, USA. close to our estimates of 44-50% time active for coy- Bekoff, M., and M. C. Wells. 1981. Behavioral budgeting otes. by wild coyotes: the influence of food resources and social In summary, most of the potential biases in our meth- organization. Animal Behaviour 29:794-801. od of estimating kill rates would cause us to under- Bekoff, M., and M. C. Wells. 1986. Social ecology and behavior of coyotes. Advances in the Study of Behavior 16: estimate the true kill rates. We therefore consider the 251-338. calculated kill rates from this study to be conservative, Bell, W. J. 1991. Searching behaviour. Chapman and Hall, particularly for coyotes. London, UK. Berg, W. E., and R. A. Chesness. 1978. Ecology of coyotes CONCLUSIONS in northern Minnesota. Pages 229-247 in M. Bekoff, editor. Coyotes: biology, behavior, and management. Academic Coyotes and lynx both killed more hares per day at Press, New York, New York, USA. higher densities of this prey, but the patterns of their Boutin, S. 1995. Testing predator-prey theory by studying functional responses differed, contrary to our null hy- fluctuating populations of small mammals. Wildlife Re- pothesis. The functional response of coyotes showed search 22:89-100. no clear level of satiation, while that of lynx ap- Boutin, S., et al. 1995. Population changes of the vertebrate community during a snowshoe hare cycle in Canada's bo- proached a maximum kill rate of about 1.3 hares per real forest. Oikos 74:69-80. day. Second, although the kill rates of both predators Bowen, W. D. 1981. Variation in coyote social organization: differed between the increase and decline phases of the the influence of prey size. Canadian Journal of Zoology hare cycle, the direction of change was the opposite; 59:639-652. Brand, C. J., and L. B. Keith. 1979. Lynx demography during coyotes killed more hares, at comparable hare densities, a snowshoe hare decline in Alberta. Journal of Wildlife during the cyclic increase, while lynx killed more dur- Management 43:827-849. ing the decline. These data suggest mechanisms in the Brand, C. J., L. B. Keith, and C. A. Fischer. 1976. Lynx behavior (e.g., plasticity, caching) and relative abilities responses to changing snowshoe hare densities in Alberta. of the two predators in catching alternative prey that Journal of Wildlife Management 40:416-428. Crawley, M. J. 1992. Overview. Pages 476-489 in M. J. contribute to their different functional responses. Crawley, editor. Natural enemies. Blackwell Scientific Pub- ACKNOWLEDGMENTS lications, Oxford, UK. Douglas, G. W. 1974. Montane zone vegetation of the Alsek This paper is based on eight years of field work, as a part River region, south-western Yukon. Canadian Journal of of the Kluane Boreal Forest Ecosystem Many people Project. Botany 52:2505-2532. contributed their time, work, and ideas to the predator re- Dunbrack, R. L., and L. A. Giguere. 1987. Adaptive research. S. Antpoehler, C. Bell, J. Bishop, M. Blower, R. Buck, sponses to accelerating costs of movement: a bioenergetic E. Claus-Sinclair, M. Connor, T. Heakes, T. Hucal, A. Milani, basis for the type-III functional response. American Nat- S. Schweiger, I. Sinclair, P. Upton, and J. Wilmshurst tracked uralist 130:147-160. coyotes and lynx. V. 0. Nams developed the data entry pro- Elton, C., and M. Nicholson. 1942. The ten year cycle in tocols. C. Doyle, F Doyle, and S. Schweiger gathered much numbers of lynx in Canada. Journal of Animal Ecology 11: of the data on hare populations. W. 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