Coyote Foraging Ecology and Vigilance in Response to Gray Wolf Reintroduction in Yellowstone National Park

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Coyote foraging ecology and vigilance in response to gray wolf reintroduction in Yellowstone National Park

T. Adam Switalski

Abstract: Coyotes (Canis latrans) in Yellowstone National Park (YNP) have lived in the absence of wolves (Canis lupus) for over 60 years. I examined whether wolf reintroduction in 1995 and 1996 in YNP influenced coyote vigilance and foraging ecology. From December 1997 to July 2000, my co-workers and I collected 1708 h of coyote activity budgets. Once wolves became established in the Park, they once again provided a continuous source of carrion in the Lamar Valley and we found that coyotes began feeding on carcasses throughout the year. Although we documented that wolves killed coyotes, it also became clear that surviving coyotes quickly adjusted their behaviors when wolves were present. When coyotes were near wolves or in areas of high wolf use, they fed on carcasses much more; however, they increased the amount of time spent in vigilance activities and decreased rest. There appears to be a trade-off in which wolf kills provide a quick source of food that is energetically advantageous to coyotes; however, attendant costs included increased vigilance, decreased rest, and a higher risk of being killed. Changes in the behavior of coyotes in response to the reintroduction of this large carnivore may ultimately have wide-ranging cascading effects throughout the ecosystem. Résumé : Les coyotes (Canis latrans) du Parc national de Yellowstone (YNP) ont vécu pendant plus de 60 ans en l’absence de loups (Canis lupus). Il s’agit ici d’examiner si la réintroduction de loups dans le parc en 1995 et en 1996 a influencé la vigilance et l’écologie de la quête de nourriture chez les coyotes. De décembre 1997 à juillet 2000, mes collaborateurs et moi avons calculé des bilans d’activités des coyotes pour un total de 1708 h. Une fois établis dans le parc, les loups sont devenus à nouveau des sources régulières de charogne dans la vallée de la Lamar et nous avons observé les coyotes se nourrir de carcasses tout au cours de l’année. Bien que nous ayons établi que les loups tuent des coyotes, il est clair que les coyotes survivants ont rapidement ajusté leur comportement à la présence des loups. Lorsque les coyotes sont à proximité des loups ou dans des zones fortement utilisées par les loups, ils se nourrissent beaucoup plus de carcasses; cependant, ils consacrent plus de temps à la vigilance et moins au repos. Il semble s’établir un compromis dans lequel les proies des loups procurent une source immédiate de nourriture, un avantage énergétique pour les coyotes; en contrepartie, les coûts imposés aux coyotes incluent l’accroissement de la vigilance, la diminution du repos et le risque plus élevé d’être tué. Les changements de comportement du coyote en réaction à la réintroduction de ce grand carnivore peuvent éventuellement se répercuter dans tout l’écosystème par des effets en cascade étendus. [Traduit par la Rédaction] 993 Introduction Switalski Mech (1966, p. 160) postulated that wolves were responsi- ble: “Since coyotes and wolves are closely related and since As early as 1937, Leopold addressed the effects of gray wolves are strongly territorial, it is not unlikely that on a wolf (Canis lupus) presence on coyotes (Canis latrans). In limited range, such as Isle Royale, wolves would chase, and his essay “Conservation in Mexico”, he questioned whether probably kill, every coyote encountered.” Direct killing of the absence of coyotes in the Chihuahuan Mountains was coyotes by wolves has been documented in Minnesota (Berg due to the presence of the once common Mexican wolf. and Chesness 1978), Alaska (Thurber et al. 1992), Manitoba Since then, several studies have addressed coyote–wolf co- (Carbyn 1982; Paquet 1991a, 1991b, 1992), Montana (Arjo existence. In 1957, when Mech began studying the ecology and Pletscher 1999), and Wyoming (Wigglesworth 2000). In of wolves on Isle Royale, just 8 years after their coloniza- many areas, however, coyotes and wolves live sympatrically. tion, coyotes had already been extirpated from the island. Coyote and wolf coexistence can be facilitated through spatial avoidance (Berg and Chesness 1978; Fuller and Keith Received 6 January 2003. Accepted 23 April 2003. Published 1981; Dekker 1989; Paquet 1992; Thurber et al. 1992), tem- on the NRC Research Press Web site at http://cjz.nrc.ca on poral separation (Carbyn 1982; Arjo and Pletscher 1999), or 11 July 2003. a low degree of diet overlap (Thurber et al. 1992). T.A. Switalski.1 U.S. Geological Survey, Utah Cooperative Historically gray wolves and coyotes were sympatric in Fish and Wildlife Research Unit, Forestry, Range, and Yellowstone National Park (YNP) (Murie 1940; Schullery Wildlife Sciences Department, College of Natural Resources, and Whittlesey 1992). A federal predator-removal program, Utah State University, 5210 Old Main Hill, Logan, established in 1872, succeeded in extirpating wolves from UT 84322-5210, U.S.A. the park by 1933. For 60 years since that time, coyotes have 1Present address: Wildlands CPR, P.O. Box 7516, Missoula, thrived in YNP without wolves. On 12 January 1995, 14 MT 59807, U.S.A. (e-mail: [email protected]). wolves were translocated from Canada and reintroduced into

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YNP. An additional 17 wolves were reintroduced the fol- nual average annual precipitation was 31.7 cm, falling lowing year. Their population increased quickly, and during mostly as snow (Houston 1982). 1996 and 1997 it had the highest fecundity ever recorded for Ungulate carcasses and small mammals are the primary the species (Smith 2000). By December 2001 there were 132 food source for coyotes in YNP. YNP is home to seven spe- wolves in YNP and 216 wolves within the Greater Yellow- cies of ungulates, including elk (Cervus elaphus), mule deer stone Ecosystem (D. Smith, National Park Service, personal (Odocoileus hemionus), pronghorn (Antilocapra americana), communication). bison (Bison bison), moose (Alces aces), bighorn sheep (Ovis Gray wolves have been reintroduced into several areas of canadensis), and white-tailed deer (Odocoileus virginianus). the Rocky Mountains, as well as red wolves (Canis rufus)in Small mammals present in YNP included but were not lim- North Carolina (Phillips et al. 1995; Bangs et al. 2001) and ited to microtines (Microtus spp.), mice (Peromyscus spp.), Mexican wolves into the American Southwest (Parsons northern pocket gophers (Thomomys talpoides), and Uinta 1998). Further, gray wolves are recolonizing many areas in ground squirrels (Spermophilus armatus). the Midwest and along the Canadian border (Mech 1995). The consequences of these reintroductions are beginning to be understood (e.g., Clark et al. 1999). Additionally, at the Methods time of writing, wolves were dispersing from existing reintroduction sites and were being considered for reintroductions Each coyote was classified as either a member of a resi- into the Olympic Mountains of Washington State (Ratti et al. dent pack or a transient. Resident packs, including resident 1999), Colorado (Bennett 1994), and the northeastern United pairs, actively defended well-defined territories, whereas States (Harrison and Chapin 1998; Mladenoff and Sickley transients were not associated with any pack or area and ex- 1998). Coyotes are present in all of the proposed reintroduc- hibited nomadic movements (modified from Bowen 1981). tion sites and in the areas to which the wolves have dis- Pack sizes were determined through repeated observations of persed. animals displaying affiliative behaviors that included traveling and resting together, as well as other social interactions. Before the reintroduction of wolves into YNP, researchers Based on observed dominance hierarchies within each resi- in other areas of North America rarely witnessed coyote– dent pack, individuals were classified as alphas (dominant wolf encounters in the field. Since reintroduction, however, breeding adult), betas (subordinate adults and yearlings), or hundreds of wolf–coyote interactions have been observed pups (young of the year) (Schenkel 1947, 1967; Rabb et al. and recorded in YNP. Taking advantage of this natural ex- 1967; Mech 1970). periment, I examined whether the reintroduction of wolves would influence coyote life-history strategies by altering From December 1997 to July 2000 we made observations their time–activity budgets. Gese et al. (1996a, 1996b) quan- of both radio-collared and unmarked coyotes and wolves in tified coyote behavior in the Lamar Valley of YNP before the Lamar and Soda Butte valleys of YNP. Ten coyote pack wolf reintroduction, creating a benchmark for gauging the members were either radio-collared or implanted with radio effects of this top predator on coyote behavior. I am not transmitters, while 18 were identifiable only from distinctive aware of any study in which direct observations have been physical characteristics (e.g., different-sized and -shaped used to assess behavioral changes in individual coyotes tails, bars, and markings). Observations were made during caused by the reintroduction of wolves. Using direct obser- daylight hours using 45× spotting scopes. We recorded wolf vations in the Lamar Valley, I was able to quantify behav- and coyote locations daily either by observations or with te- ioral time budgets of coyotes in the presence of wolves. I lemetry. We randomly chose which coyote packs to observe addressed the following questions: (i) Do coyotes living be- before going into the field. We identified a series of observa- tween wolf packs (“buffer zones”) partition their time differ- tion points from which each pack territory could be viewed. ently than coyotes living in high wolf use areas? (ii)Do From these observation points we attempted to locate the coyotes exhibit different behavioral time budgets when coyote highest on the priority list. If this search was unsuc- wolves are in close proximity in the immediate study area cessful, we searched for the animal next highest in priority. than when they are absent from the study area? Once a coyote was located, we continuously recorded all activities of that animal using focal-animal sampling (Lehner 1979). We recorded the types of behaviors, as well as the Study area time of day they were recorded, and entered the data into a spreadsheet. Simultaneously, we recorded travel routes and My co-workers and I conducted research in the Lamar behaviors on 7.5′ quadrangle maps. Attributes of the ob- River Valley in the Northern Range of YNP, Wyoming served animal, including gender, social status, age class (44°52′N, 110°11′E). The study area encompassed the (adult, yearling, or pup), pack name, and pack size were also 70-km2 study area delineated by Gese et al. (1996a, 1996b) entered into the spreadsheet. Identified behaviors (modified and was extended by an additional 30 km2 west of Lamar from Gese et al. 1996a, 1996b) included (i) rest/alert: the Canyon into what is known locally as Little America. The coyote was sitting upright or lying down with head raised; Lamar Valley is a high-elevation, open river valley at ap- (ii) rest/sleep: lying down with head lowered; (iii) travel: proximately 2000 m elevation that is bordered by very steep moving from one location to another; (iv) hunting small forested habitat to the south and more gradually rising, open mammals: the total time spent searching (looking or listen- sage–grassland habitat to the north. The climate in the study ing for prey) and orienting (looking or listening toward a area is characterized by long, cold winters and cool summers prey item), not including the amount of time spent traveling (Houston 1982). The mean temperature was 1.8°C and an- between predation attempts; (v) successful predation at-

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tempt: the coyote captured a prey item; (vi) unsuccessful of the Soda Butte pack were observed for 168 h, 4 members predation attempt: the coyote was hunting but unable to cap- of the Jackson Ridge pack for 264 h, 4 members of the ture the prey item; (vii) feeding on a carcass: the coyote was Druid pack for 201 h, 4 members of the Bison pack for feeding on an ungulate carcass; (viii) howling: any audible 163 h, 2 members of the Amethyst pack for 156 h, 4 mem- sound; (ix) vigilance: the coyote looked repeatedly to distant bers of the Jasper pack for 98 h, 2 members of the Crystal stimuli, using visual and auditory senses; the muzzle was el- Bench pack for 130 h, 2 members of the Slough Creek pack evated or level and not oriented toward the ground (as is the for 109 h, 3 members of the Little America pack for 106 h, case in “orient”); this could occur while traveling, hunting, and transients for 313 h. or feeding on a carcass; (x) other: the coyote performed behaviors not adequately described by categories i–ix, includ- Coyote pack history ing urination, defecation, and intraspecific social interactions Since wolf reintroduction in 1995, the Lamar Valley coy- both affiliative and agonistic. The behaviors categorized as ote population has been reduced by an estimated 25–33% “other” composed <4% of the total activity budget. The ob- each winter (Crabtree and Sheldon 1999). Fatal interactions served behaviors were mutually exclusive and could be de- while they scavenged on wolf-killed carcasses appeared to termined unambiguously by field personnel. We calculated be the main cause of this decline (Crabtree and Sheldon the sum and frequency of each behavior and deleted from 1999). As of summer 2000, 9 packs with 24 adult coyotes the sample any period of time when the observed animal remained in the study area. was out of sight. Among the 9 packs studied, only 1 pack retained the same We determined approximate coyote territories through ra- alpha pair during all 3 years of this study (Slough Creek). diotelemetry, observations of activity, and scent marking. All other packs experienced at least one alpha turnover. The The National Park Service determined wolf territories using Bison pack had a new alpha pair each year and the Jasper aerial and ground-based telemetry of radio-collared individu- pack had a new alpha male twice during 2000. Interspecific als coupled with observations (Smith et al. 2000; U.S. Fish killing by wolves was assumed to be the main cause of the and Wildlife Service, Nez Perce Tribe, National Park Ser- high turnover; however, actual killing of alphas was rarely vice, and USDA Wildlife Service 2001 (USFWS et al. witnessed. We witnessed an alpha female of the Druid pack 2001); Mech et al. 2001). Additionally, the National Park killed by wolves in November 1998 and 2 members of the Service recorded snow depth and maximum and minimum Amethyst pack killed by wolves in February 1999. Because temperatures daily during the winter at the permanent of this high mortality, few animals were observed in all 3 weather station at the Lamar Ranger Station. years. The weather in YNP varies greatly from year to year. Winter severity can influence reproduction, survival of Wolf pack history young and old, and predation of ungulates (Houston 1982). To measure the annual variation in winter severity, we used Two wolf packs, Druid Peak and Rose Creek, lived in the an index of winter severity (IWS) that was calculated by study area. The Rose Creek pack (n = 3) was introduced into combining snow-water equivalent, accumulated minimum the study area in January 1995 from Alberta, while the temperatures below the effective critical temperature for Druid Peak pack (n = 5) was introduced the following win- ungulates (the temperature at which animals must increase ter, in January 1996, from British Columbia. After about their metabolic rate to maintain an adequate body tempera- 10 weeks in acclimation pens, the wolves were released and ture), and the availability of forage in the winter range after an exploratory period settled into territories (Phillips (Farnes et al. 1999). and Smith 1997). Throughout the study, the Druid Peak pack lived in the Lamar and Soda Butte valleys west to Slough I used SAS for our statistical analysis. I followed a facto- Creek, encompassing most of the study area (Smith et al. rial (split-plot) design with season as the repeated measure 2000; USFWS et al. 2001; Mech et al. 2001). The Rose (Littell et al. 1994). The sample unit for all statistical analy- Creek pack territory was also very stable, ranging from the ses was the individual coyote. I used analysis of variance Lamar Canyon area to Hellroaring Creek, a straight-line dis- (ANOVA) using PROC MIXED; least-squared means are re- tance of 15 km. The two wolf territories overlapped on the ported. I used the proportion of time each behavior was per- west side of the study area, creating a buffer zone formed relative to the animals’ total time budget. For (Hoskinson and Mech 1976; Mech 1977; Rogers et al. 1980; analysis, we identified three phenological seasons: dispersal/ Lewis and Murray 1993). Wolves were rarely observed in breeding (15 October – 15 February), gestation (16 February – the buffer zone and were only occasionally located by radio- 15 April), and pup rearing (16 April – 15 July). From telemetry in this area. Ripple et al. (2001) also reported few 16 July to 14 October, no fieldwork was conducted, owing to wolves using this buffer zone. Pack sizes ranged from 7 to 8 low visibility in high grass. adults in the Druid Peak pack and from 15 to 22 adults in the Rose Creek pack throughout the study (Smith et al. Results 2000; USFWS et al. 2001; Mech et al. 2001). Territory use by wolves varied spatially during the year From December 1997 to July 2000, we made 1243 obser- (D. Smith, National Park Service, personal communication). vations of coyotes and collected 1708 h of coyote activity During the gestation and pup-rearing seasons, the Druid budgets. We observed 28 resident coyotes from 9 packs, plus Peak wolf pack denned and produced litters every year transients. Of the known animals, 16 were male and 12 were within the Soda Butte coyote pack territory. In spring 2000, female. We observed 24 alphas and 4 betas. Three members however, a beta female from the Druid Peak wolf pack

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Fig. 1. Index of winter severity for elk during the winters of 1986–2000 in the Lamar River Range in Yellowstone National Park, Wy- oming (modified from Farnes et al. 1999). More negative values correspond to more severe winters.

denned within the Amethyst coyote territory. She denned Fig. 2. Mean snow depth for each week during the winters of there only until mid-May and then, after the alpha female 1998, 1999, and 2000 (November–April) in the Lamar Valley, was killed, moved her pups to the historic den site. The Rose Yellowstone National Park, Wyoming. Creek wolf pack, however, denned toward the northern border of the Park and was outside the study area during most of the gestation and pup-rearing seasons. During the dispersal/breeding season, both packs were less localized, and traveled, hunted, and made kills throughout the study area.

Environmental conditions According to the index of winter severity for elk in the Lamar Valley winter range, the winter prior to the beginning of this study (1996–1997) was the most severe in decades (Fig. 1). A midwinter rain event created a thick ice crust, resulting in large numbers of winter-killed ungulates. The first winter of this study (1997–1998), however, was considered the mildest winter in decades. Snow depth reached a maximum of 41 cm and was >30 cm for only 64 days (Fig. 2). The second winter of this study was also relatively mild, with snow conditions similar to those in the first winter. Coyote activity budgets Snow depth reached a maximum of 40 cm and was >30 cm As expected, coyote activity budgets varied throughout the for 60 days. The third winter was the most severe of this year (Fig. 3). Overall, coyotes generally decreased traveling study (1999–2000) and was characterized by early snowfall and hunting, and increased rest during the winter months. and deep snowpack. Snow depth reached a maximum of When the snow melted and ground squirrels emerged in 66 cm and was >30 cm for 110 days. mid-April, coyotes decreased the time spent sleeping and in- In contrast to Gese et al.’s (1996a, 1996b) study from Jan- creased the time spent traveling and hunting. Contrary to uary 1991 to July 1993, there were very few winter-killed Gese et al. (1996a), however, carcass use did not vary dra- ungulates during this study, even though the degree of winter matically from November to July. Wolves now provide a severity was similar during 1999 and 2000 (Fig. 1). During year-round source of carrion for coyotes, and accordingly mild or moderately severe winters, the wolf predation rate we found that coyotes fed on carcasses throughout the year. and wolf pack size now determine the amount of carrion Additionally, vigilance did not appear to vary much through- available to coyotes (C. Wilmers, University of California– out the year (Fig. 3). Berkley, in preparation). Generally, wolf predation increased in late winter (Smith et al. 2000; USFWS et al. 2001; Mech Level of wolf activity et al. 2001); however, ungulate carrion is now available to We wanted to determine if the degree of wolf activity in- coyotes year-round. fluenced resident coyote activity budgets. Four coyote pack

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Fig. 3. Proportions of time coyotes were observed to spend resting, traveling, hunting small mammals, feeding on carcasses, and vigilant each week from November to June during three field seasons (1998–2000) in Yellowstone National Park, Wyoming.

Table 1. ANOVAs showing the influence of snow depth, degree of wolf activity, sex, and year (model 1) and the influence of wolf distance, sex, and snow depth (model 2) on the proportions of time spent on 5 behaviors by coyotes in the Lamar Valley, Yellowstone National Park, Wyoming, from December 1997 to July 2000. Feeding on Rest Travel Hunting carcass Vigilance Source of variation df FPFPF P F PF P Model 1 Degree of wolf activitya 1 5.61 0.02 0.71 0.40 0.08 0.77 13.28 <0.01 12.98 <0.01 Sex 1 1.17 0.29 3.87 0.06 1.63 0.21 0.33 0.57 2.74 0.11 Yearb 1 0.03 0.87 0.11 0.74 1.97 0.17 1.60 0.21 4.54 0.04 Snow depthc 1 0.72 0.40 2.39 0.13 10.42 <0.01 13.57 <0.01 0.01 0.92 Wolf activity × snow 1 0.19 0.67 0.00 0.97 0.73 0.40 3.03 0.09 1.28 0.27 Sex × snow depth 1 0.20 0.66 0.05 0.82 0.09 0.76 0.56 0.46 0.69 0.41 Year × snow depth 1 1.72 0.20 0.30 0.58 0.47 0.50 3.54 0.07 10.23 <0.01 Model 2 Wolf distanced 1 11.13 <0.01 1.69 0.20 0.00 0.97 4.20 0.05 12.54 <0.01 Sex 1 0.60 0.44 3.31 0.08 0.44 0.51 0.77 0.39 0.53 0.47 Snow depthc 1 3.17 0.08 5.51 0.02 3.49 0.07 4.07 0.05 4.46 0.04 Sex × wolf distance 1 0.01 0.91 0.07 0.79 2.35 0.13 0.27 0.61 0.51 0.48 Snow depth × wolf distance 1 0.00 0.95 0.09 0.76 1.44 0.24 0.10 0.76 0.45 0.51 aIn the buffer zone (Little America, Slough Creek, Crystal Bench, and Jasper coyote packs) or non-buffer zone (Amethyst, Bison, Druid, Jackson, and Soda Butte coyote packs). bEither 1998 and 1999 combined or 2000. cLow/none (<30 cm) or high (>30 cm). dWolves were present (within the study area) or absent (outside of the study area or on the opposite side of the study area from the focal coyote).

territories (Little America, Slough Creek, Crystal Bench, and casses less (2 vs. 8%), and were less vigilant (9 vs. 14%) in Jasper) were located within the buffer zone between the the buffer zone than in the non-buffer zone. We did not find Druid Peak and Rose Creek wolf packs. Wolves were ob- a significant difference in the amount of time coyotes trav- served and radiolocated in the buffer zone less frequently eled and hunted for small mammals. than in other parts of their range and few agonistic interactions between wolves and coyotes were observed. Presence and absence of wolves We used a multiway ANOVA and found a significant dif- The degree of wolf use influenced the activity budgets of ference in the amount of time coyotes spent resting (P = coyotes, so we examined whether the actual physical pres- 0.02), feeding on carcasses (P < 0.01), and being vigilant ence of wolves had similar effects. Wolves were considered (P < 0.01) in the buffer zone versus the non-buffer zone (Ta- present if they were within the study area and absent if they ble 1, Fig. 4). Coyotes rested more (50 vs. 39%), fed on car- were outside of the study area. Wolves were also considered

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Fig. 4. Proportions of time resident coyotes were observed to spend resting, traveling, hunting small mammals, feeding on carcasses, and vigilant in the wolf buffer zone and non-buffer zone, and when wolves were physically present and absent (see the text) in Yel- lowstone National Park, Wyoming, from December 1997 to July 2000.

absent if they were on the opposite side of the study area be- packs. Several of the coyote pack territories were located cause a small canyon and surrounding forested hills ob- within the overlap between these wolf territories. Wolves scured all visual and olfactory cues. We determined tended to avoid intraspecific interactions in the areas where presence or absence by telemetry and visual observations of their home ranges overlapped with those of other wolf wolves. We realized that scent marks remained even when packs, creating a “buffer zone”. Wolf buffer zones have wolves were not present. When wolves were within the been found to have higher deer survivorship (Hoskinson and study area, coyotes could use visual cues to determine their Mech 1976; Mech 1977; Rogers et al. 1980; Lewis and presence. When wolves were distant from coyote home Murray 1993) and provide refuge for coyotes (Berg and ranges, coyotes relied only on previous experiences and ol- Chesness 1978; Fuller and Keith 1981; Arjo and Pletscher factory cues to make behavioral decisions regarding wolves. 1999). Similarly, red foxes (Vulpes vulpes) that occurred We obtained 398 observations where wolves were present sympatrically with coyotes disproportionately used the pe- and 164 observations where wolves were absent. Because of riphery of coyote home ranges (Voigt and Earle 1983; Major our small sample size, we did not include yearly variation in and Shelburne 1987; Sargeant et al. 1987; Harrison et al. our ANOVA model as in the previous analysis. 1989; Fuhrmann 1998). In the buffer zone between the Coyotes exhibited different time budgets when wolves Druid Peak and Rose Creek wolf pack territories, we ob- were present from when they were absent (Fig. 4). We found served few agonistic interactions between wolves and coy- a significant difference in the amount of time coyotes rested otes. In fact, the only alpha pair to survive throughout the (P < 0.01), fed on carcasses (P = 0.05), and were vigilant (P < study (Slough Creek) lived in the buffer zone. In non-buffer 0.01) when wolves were present versus absent (Fig. 4). Coy- areas, however, more frequent encounters with wolves were otes rested more (54 vs. 36%), fed on carcasses less (4 vs. observed, and accordingly coyotes exhibited different behav- 9%), and were less vigilant (10 vs. 17%) when wolves were iors than coyotes within the buffer zone. absent than when wolves were present. We did not find a Prior to wolf reintroduction, Gese et al. (1996a) did not significant difference in the amount of time coyotes traveled find a significant difference in the amount of time different and hunted for small mammals when wolves were present coyote packs rested or fed on carcasses. Our results, how- versus absent. ever, suggest that coyote packs within the buffer zone fed on carcasses less and rested more than coyote packs in the high Discussion wolf use non-buffer zone. In the non-buffer zone, coyotes had more wolf-killed carcasses available, but slept less, pos- Studies of canid sympatry have been the topic of several sibly because they were wary of potentially fatal interac- reviews (Carbyn 1987; Litvaitis 1992; Peterson 1995; John- tions. son et al. 1996). However, because carnivores are rare, wide Predation plays a major role in natural selection and in the ranging, and difficult to observe, most studies have used te- evolution of the ecology and behavior of animals (Dawkins lemetry and scat analysis to examine the diet, space use, and Krebs 1979). Predators kill large numbers of both prey habitat, and temporal overlap of these sympatric carnivores. and competing species and in some cases can be the leading The reintroduction of wolves into the Lamar Valley of YNP source of mortality (Caro and Fitzgibbon 1992; Palomares in 1995 allowed us to use direct observations to document and Caro 1999). Interspecific killing of coyotes by wolves is the behavioral adaptations that coyotes use to allow coexis- well documented (Berg and Chesness 1978; Carbyn 1982; tence with wolves. Our results showed that coyotes have lo- Paquet 1991a, 1991b, 1992; Thurber et al. 1992; Arjo and cally adjusted their behaviors in response to the presence of Pletscher 1999; Wigglesworth 2000). wolves. “Naïve” prey and competing carnivore populations may All of the coyote packs examined in this study were reduce their vulnerability to reintroduced predators through within the territories of the Druid Peak or Rose Creek wolf behavioral changes. Behavioral responses may include mini-

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mizing encounters with predators and (or) decreasing the areas, coyote numbers have been suppressed and surviving success of the attacking predator (Endler 1986; Caro and coyotes have switched prey from small mammals to more Fitzgibbon 1992). These species can reduce encounters with wolf-killed carcasses. Although wolves will supplement predators by adjusting their spatial or temporal use patterns. their prey with small mammals during the summer (Murie For example, when reintroduced wolves hunted near the Na- 1944; Mech 1970; Carbyn and Kingsley 1979; Fuller 1989), tional Elk Refuge in Wyoming, elk routinely dispersed to populations of small-mammal prey should locally increase other feeding grounds, where they congregated in larger in the near future. Singer and Mack (1999) predicted that numbers and may have had better visibility and warning of this trophic cascade would result in more food for badgers approaching predators (USFWS et al. 2001). Additionally, (Taxidea taxus), weasels (Mustela spp.), and foxes (V. coyotes in northwestern Montana spatially and temporally vulpes). avoided wolves, became more nocturnal, and avoided high In conclusion, the reintroduction of wolves in YNP has re- wolf use areas seasonally (Arjo and Pletscher 1999). sulted in changes in coyote behavior. There appears to be a If prey and competing carnivores remain in risky areas, trade-off between vigilance and feeding in coyotes. Wolves they can lower the success rate of attacking predators by may provide a quick source of food and be energetically ad- scanning the environment. Many predators rely on surprise vantageous to coyotes; however, costs include increased vig- for a successful attack, and early detection by a potential ilance, decreased rest, and a higher risk of getting killed. victim of predation may allow escape. This vigilance behav- Furthermore, the amount of carrion available to coyotes may ior can aid in the detection of predators and may also play a be negatively related to wolf pack size, and as pack size in- role in observation of conspecifics, acquisition of food, and creases, a threshold may be reached in which wolf kills will prevention of kleptoparasitism (Quenette 1990). While feed- provide less energetic benefit to coyotes and other scaven- ing on carcasses, coyotes were at greatest risk of getting gers. In 2001, there were as many as 37 wolves in the Druid killed by wolves and were often chased off the carcass. In Peak pack and most carcasses were completely consumed by fact, most coyotes we observed to be killed by wolves (n = the wolf pack (Smith 2002). Interspecific killing is a major 3) were scavenging wolf-killed carcasses, and all recovered selecting force and surviving coyotes have quickly adjusted coyote carcasses (n = 8) were in the periphery of a wolf- their behaviors when wolves are present or in high-risk ar- killed carcass. Accordingly, coyotes were most vigilant eas. Changes in the behavior of coyotes in response to the while feeding on carcasses. Vigilance related to antipredator reintroduction of this large carnivore may ultimately have behavior in mammalian carnivores has been observed in the wide-ranging cascading effects throughout the ecosystem. meerkat (Suricata suricata; Moran 1984), cheetah (Acinonyx jubatus; Caro 1987), dwarf mongoose (Helogala undulata Acknowledgments rufula; Rasa 1989), and eastern quoll (Dasyurus viverrinus; I thank John Bissonette, Eric Gese, Jim MacMahon, and Jones 1998). For these carnivores there is a trade-off be- Bill Adair for review of the manuscript and helpful com- tween increased vigilance and a reduced risk of getting ments. I thank Jennie Sheldon, Bob Crabtree, Keith killed; however, the amount of time available for foraging is VanEtten, Kim Sager, Kerry Halligan, Dave Bope, and all also reduced. In the extreme, dwarf mongoose may be vigi- the volunteers who helped with fieldwork. Their countless lant for 20–35% of their total possible foraging time in order hours under freezing conditions made this research possible. to reduce their risk of getting killed (Rasa 1989). Coyotes I thank Susan Durham for statistical advice and Tom Ed- within the buffer zone were less vigilant than those in the wards for all of his help. Funding was provided by the U.S. non-buffer zone. Similarly, when wolves were absent, coy- Geological Survey Utah Cooperative Fish and Wildlife Re- otes were less vigilant than when they were present. This search Unit and Yellowstone Ecosystem Studies. clearly suggests that coyotes are using vigilance to detect wolves, and when exposed to wolves are quickly learning to adjust their behavior in order to avoid wolf predation. Coy- References otes were vigilant for 9% of their overall time budget, and as Arjo, W.M., and Pletscher, D.H. 1999. Behavioral responses of much as 14% in the high-risk non-buffer zone. coyotes to wolf recolonization in northwestern Montana. Can. J. Behavioral changes resulting from increased vigilance Zool. 77: 1919–1927. may reduce the overall fitness of certain prey species. An in- Bangs, E., Fotaine, J., Jiminez, M., Meier, T., Niemeyer, C., Smith, crease in vigilance in elk (Laundré et al. 2001; Smith and D., et al. 2001. Gray wolf restoration in the northwestern United Berger 2001) and moose (Berger et al. 2001) has been ob- States. Endangered Species Update. Vol. 18. University of Mich- served since wolf reintroduction in 1995. For example, igan, Ann Arbor. pp. 147–152. Laundré et al. (2001) predicted that increased vigilance in Bennett, L.E. 1994. Colorado gray wolf recovery: a biological fea- elk may ultimately lead to reduced fat content and lower sibility study. University of Wyoming Fish and Wildlife Cooper- body mass of females, lower survival rates during the winter ative Research Unit, Laramie, and U.S. Fish and Wildlife and other stressful periods, and calves being born at lower Service, Washington, D.C. body mass. An increase in vigilance in response to predators Berg, W.E., and Chesness, R.A. 1978. Ecology of coyotes in northern Minnesota. In Coyotes: biology, behavior, and management. coupled with a decrease in the number of helpers at the den Edited by M. Bekoff. Academic Press, New York. pp. 158–172. may also influence coyotes by reducing the survival of pups. Berger, J., Swenson, J.E., and Persson, I. 2001. Recolonizing carni- Behavioral changes may also result in a numerical re- vores and naïve prey: conservation lessons from Pleistocene ex- sponse of prey and be a driving force behind trophic cas- tinctions. Science (Wash., D.C.), 291: 1036–1039. cades. We found an increase in the number of Uinta ground Bowen, W.D. 1981. Variation in coyote social organization: the in- squirrels in high wolf use areas (unpublished data). In these fluence of prey size. Can. J. Zool. 59: 639–652.

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Carbyn, L.N. 1982. Coyote population fluctuations and spatial dis- Johnson, W.E., Fuller, T.K., and Franklin, W.L. 1996. Sympatry in tribution in relation to wolf territories in Riding National Park, canids: a review and assessment. In Carnivore behavior, ecology, Manitoba. Can. Field-Nat. 96: 176–183. and evolution. Vol. 2. Edited by J.L. Gittleman. Cornell Univer- Carbyn, L.N. 1987. Gray wolf and red wolf. In Wild furbearer sity Press, Ithaca, N.Y. pp. 189–218. management and conservation in North America. Edited by M. Jones, M.E. 1998. The function of vigilance in sympatric marsu- Novak, G.A. Baker, M.E. Osbard, and B. Malloch. Ontario pial carnivores: the eastern quoll and the Tasmanian devil. Trappers Association, Ministry of Natural Resources, Toronto. Anim. Behav. 56: 1279–1284. pp. 358–376. Laundré, J.W., Hernández, L., and Altendorf, K.B. 2001. Wolves, Carbyn, L.N., and Kingsley, M.C.S. 1979. Summer food habits of elk, and bison: reestablishing the “landscape of fear” in Yellow- wolves with emphasis on moose in Riding Mountain National stone National Park, Can. J. Zool. 79: 1401–1409. Park. In Proceedings of the 15th North American Moose Con- Leopold, A. 1937. Conservationist in Mexico. Am. For. 43: 118–121. ference Workshop, St. John’s, Newfoundland. pp. 349–61. Lehner, P.N. 1979. Handbook of ethological methods. Garland Caro, T.M. 1987. Cheetah mothers’ vigilance: looking out for prey STPM Press, New York. or for predators. Behav. Ecol. Sociobiol. 20: 351–361. Lewis, M.A., and Murray, J.D. 1993. Modelling territoriality and Caro, T.M., and Fitzgibbon, C.D. 1992. Large carnivores and their wolf–deer interactions. Nature (Lond.), 366: 738–740. prey: the quick and the dead. In Natural enemies: the population Littell, R.C., Freund, R.J., and Spector, P.C. 1994. SAS system for biology of predators parasites and diseases. Edited by M.J. linear models. 3rd ed. SAS Institute Inc., Cary, N.C. Crawley. Blackwell Scientific Publications, Oxford. pp. 117– Litvaitis, J.A. 1992. Niche relations between coyotes and sympatric 142. Carnivora. In Ecology and management of the eastern coyote. Clark, T.W., Curlee, A.P., Minta, S.C., and Kareiva, P.M. 1999. Edited by A.H. Boer. Wildlife Research Unit, University of New Carnivores in ecosystems: the Yellowstone experience. Yale Brunswick, Fredericton. pp. 73–85. University Press, New Haven, Conn., and London. Major, J.T., and Shelburne, J.A. 1987. Interspecific relationships of Crabtree, R.L., and Sheldon, J.W. 1999. The ecological role of coyote, bobcats, and red foxes in western Maine. J. Wildl. coyotes on Yellowstone’s northern range. Yellowstone Sci. 7: Manag. 51: 606–616. 15–22. Mech, L.D. 1966. The wolves of Isle Royale. U.S. National Park Dawkins, R., and Krebs, J.R. 1979. Arms races between and within Service Fauna Ser. No. 7. U.S. Government Printing Office, species. Proc. R. Soc. Lond. B Biol. Sci. 205: 489–511. Washington, D.C. Dekker, D. 1989. Population fluctuations and spatial relationships Mech, L.D. 1970. The wolf: the ecology and behavior of an endan- among wolves, Canis lupus, coyotes, Canis latrans, and red gered species. Natural History Press, Garden City, N.Y. foxes, Vulpes vulpes, in Jasper National Park, Alberta. Can. Mech, L.D. 1977. Wolf-pack buffer zones as prey reservoirs. Sci- Field-Nat. 103: 261–264. ence (Wash., D.C.), 198: 320–321. Endler, J.A. 1986. Defense against predators. In Predator–prey re- Mech, L.D. 1995. The challenge and opportunity of recovering lationships: perspectives and approaches from the study of lower wolf populations. Conserv. Biol. 9: 270–278. vertebrates. Edited by M.E. Feder and G.V. Lauder. University Mech, L.D., Smith, D.W., Murphy, K.M., and MacNulty, D.R. of Chicago Press, Chicago. pp. 109–134. 2001. Winter severity and wolf predation on a formerly wolf- Farnes, P., Heydon, and Hansen, K. 1999. Snowpack distribution free elf herd. J. Wildl. Manag. 65: 998–1003. across Yellowstone National Park, Wyoming. Final Rep. Pro- Mladenoff, D.J., and Sickley, T.A. 1998. Assessing potential gray posal No. 97–447, National Park Service, Yellowstone National wolf restoration in the northeastern United States: a spatial pre- Park, Wyo. diction of favorable habitat and potential population levels. J. Fuhrmann, R.T. 1998. Distribution, morphology, and habitat use of Wildl. Manag. 62: 1–10. the red fox in the northern Yellowstone ecosystem. M.S. thesis, Moran, G. 1984. Vigilance behavior and alarm calls in a captive Montana State University, Bozeman. group of meerkats, Suricata suricata. Z. Tierpsychol. 65: 228– Fuller, T.K. 1989. Population dynamics of wolves in north-central 240. Minnesota. Wildl. Monogr. No. 105. Murie, A.M. 1940. Ecology of the coyote in the Yellowstone. Fuller, T.K., and Keith, L.B. 1981. Non-overlapping ranges of coy- United States National Park Service Fauna Ser. No. 4. U.S. Gov- otes and wolves in northeastern Alberta. J. Mammal. 62: 403– ernment Printing Office, Washington, D.C. 405. Murie, A.M. 1944. The wolves of Mount McKinley. United States Gese, E.M., Ruff, R.L., and Crabtree, R.L. 1996a. Foraging ecol- National Park Service Fauna Ser. No. 5. U.S. Government Print- ogy of coyotes (Canis latrans): the influence of extrinsic factors ing Office, Washington, D.C. and a dominance hierarchy. Can. J. Zool. 74: 769–783. Palomares, F., and Caro, T.M. 1999. Interspecific killing among Gese, E.M., Ruff, R.L., and Crabtree, R.L. 1996b. Intrinsic and ex- mammalian carnivores. Am. Nat. 153: 492–508. trinsic factors influencing coyote predation of small mammals in Paquet, P.C. 1991a. Scent-marking behavior of sympatric wolves Yellowstone National Park. Can. J. Zool. 74: 784–797. (Canis lupus) and coyotes (C. latrans) in riding Mountain Na- Harrison, D.J., and Chapin, T.G. 1998. Extent and connectivity of tional Park. Can. J. Zool. 69: 1721–1727. habitat for wolves in eastern North America. Wildl. Soc. Bull. Paquet, P.C. 1991b. Winter spatial relationships of wolves and coy- 26: 767–775. otes in Riding Mountain National Park. J. Mammal. 72: 397– Harrison, D.J., Bissonette, J.A., and Sherburne, J.A. 1989. Spatial 401. relationships between coyotes and red foxes in eastern Maine. J. Paquet, P.C. 1992. Prey use strategies of sympatric wolves and Wildl. Manag. 53: 181–185. coyotes in Riding Mountain National Park. J. Mammal. 73: Hoskinson, R.L., and Mech, L.D. 1976. White-tailed deer migra- 337–343. tion and its role in wolf predation. J. Wildl. Manag. 40: 429– Parsons, D.R. 1998. “Green fire” returns to the Southwest: reintro- 441. duction of the Mexican wolf. Wildl. Soc. Bull. 26: 799–807. Houston, D.B. 1982. The northern Yellowstone elk: ecology and Peterson, R.O. 1995. Wolves as interspecific competitors in canid management. Macmillan Publishing Co., Inc., New York. ecology. In Ecology and conservation of wolves in a changing

J:\cjz\cjz8106\Z03-080.vp July 9, 2003 7:02:41 AM Color profile: Generic CMYK printer profile Composite Default screen

Switalski 993

world. Edited by L.N. Carbyn, S.H. Fritts, and D.R. Seip. Cana- wolves and related wildlife species in the Yellowstone National dian Circumpolar Institute, Occas. Publ. No. 35. pp. 315–323. Park area prior to 1882. In Wolves for Yellowstone? Vol. 4. Phillips, M.K., and Smith, D.W. 1997. Yellowstone wolf project bi- Edited by J.D. Varley and W.G. Brewster. National Park Ser- ennial report 1995 and 1996. National Park Service, Yellow- vice, Yellowstone National Park, Wyo. pp. 1–4 to 1–174. stone National Park, Wyo. Singer, F.J., and Mack, J.A. 1999. Predicting the effects of wildfire Phillips, M.K., Smith, R.C., Lucash, C.F., and Henry, V.G. 1995. and carnivore predation on ungulates. In Carnivores in ecosys- Red wolf reintroduction program. In Ecology and conservation tems: the Yellowstone experience. Edited by T.W. Clark, A.P. of wolves in a changing world. Edited by L.N. Carbyn, S.H. Curlee, S.C. Minta, and P.M. Kareiva. Yale University Press, Fritts, and D.R. Seip. Canadian Circumpolar Institute, Occas. New Haven, Conn., and London. pp. 189–237. Publ. No. 35. University of Alberta, Edmonton. pp. 157–168. Smith, D.W. 2000. The Yellowstone wolves: the first five years. In Quenette, P.Y. 1990. Functions of vigilance behavior in mammals: Abstracts from the 12th Annual North American Interagency a review. Acta Ecol. 11: 801–818. Wolf Recovery Conference, Pray, Mont. pp. 1–2. Rabb, G.B., Woolpy, J.H., and Ginsberg, B.E. 1967. Social rela- Smith, D.W. 2002. The Yellowstone wolves: an update. In Ab- tionships in a group of captive wolves. Am. Zool. 7: 305–311. stracts from the 14th Annual North American Interagency Wolf Rasa, O.A.E. 1989. The cost and effectiveness of vigilance behav- Recovery Conference, Boise, Idaho. pp. 1–2. ior in the dwarf mongoose: implications for fitness and optimal Smith, B., and Berger, J. 2001. Wolves in paradise?: some sur- group size. Ethol. Ecolog. Evol. 1: 264–282. prises at the National Elk Refuge. In Abstracts from the 13th Ratti, J.T., Weinstein, M., Scott, J.M., Avsharian, P., Gillesberg, A., Annual North American Interagency Wolf Recovery Confer- Miller, C.A., et al. 1999. Feasibility study on the reintroduction ence, Pray, Mont. p. 9. of gray wolves to the Olympic Peninsula. Department of Fish- Smith, D.W., Murphy, K.M., and Guernsey, D.S. 2000. Yellow- eries and Wildlife Resources and the Idaho Cooperative Re- stone wolf project annual report, 1999. National Park Service, search Unit, University of Idaho, Moscow. Yellowstone National Park, Wyo. Ripple, W.J., Larsen, E.J., Renkin, R.A., and Smith, D.W. 2001. Thurber, J.M., Peterson, R.O., Woolington, J.D., and Vucetich, J.A. Trophic cascades among wolves, elk, and aspen on Yellowstone 1992. Coyote coexistence with wolves on the Kenai Peninsula, National Park’s northern range. Biol. Conserv. 102: 227–234. Alaska. Can. J. Zool. 70: 2494–2498. Rogers, L.L., Mech, L.D., Dawson, D.K., Peek, J.M., and Korb, M. U.S. Fish and Wildlife Service, Nez Perce Tribe, National Park 1980. Deer distribution in relation to wolf pack territory edges. Service, and USDA Wildlife Services. 2001. Rocky Mountain Wolf J. Wildl. Manag. 44: 253–257. Recovery 2000 annual report. Available at http://www.r6.fws.gov/ Sargeant, A.B., Allen, S.H., and Hastings, J.O. 1987. Spatial rela- wolf/annualrpt00/ [accessed on 1 December 2001]. tions between sympatric coyotes and red foxes in North Dakota. Voigt, D.R., and Earle, B.D. 1983. Avoidance of coyotes by red fox J. Wildl. Manag. 51: 285–293. families. J. Wildl. Manag. 47: 852–857. Schenkel, R. 1947. Expression studies of wolves. Behaviour, 1: Wigglesworth, R.R. 2000. Habitat use, diet, social organization, 81–129. and seroprevalence of diseases in coyotes (Canis latrans)in Schenkel, R. 1967. Submission: its features and function in the Grand Teton National Park and suburban/agricultural areas of wolf and dog. Am. Zool. 7: 319–329. northwestern Wyoming. M.S. thesis, University of Wyoming, Schullery, P., and Whittlesey, L. 1992. The documentary record of Laramie.

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