THE PREDATORY SEQUENCE AND THE INFLUENCE OF INJURY RISK ON HUNTING BEHAVIOR IN THE WOLF A THESIS SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL

THE PREDATORY SEQUENCE AND THE INFLUENCE OF INJURY RISK ON HUNTING BEHAVIOR IN THE WOLF A THESIS SUBMITTED TO THE FACULTY OF THE GRADUATE SCHOOL OF THE UNIVERSITY OF MINNESOTA BY DANIEL ROBERT MACNULTY IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE May 2002

Daniel Robert MacNulty 2002

i ACKNOWLEDGMENTS The privilege of writing this thesis would not have been possible without the commitment, encouragement, and patience of many individuals at many levels. In 1996 while I was working as a volunteer for the Yellowstone Wolf Project, Dr. David Mech suggested I summarize the early observations of wolves hunting elk in the park's Northern Range. Dr. Mech subsequently became my faculty advisor at the University of Minnesota and continued to encourage me to study the hunting behavior of wolves in YNP. Throughout my research Dr. Mech gave me the freedom to pursue my ideas, while providing important guidance at critical junctures in the research process. Dr. Douglas Smith, Yellowstone Wolf Project leader, was instrumental in conceiving and supporting the idea of a study of wolf hunting behavior. Dr. Smith handled administrative affairs to facilitate field research, and directed the Wolf Project s biannual winter study, which included the study on wolf hunting behavior. Mike Phillips also encouraged the study and helped secure vital funding during his early tenure as Wolf Project leader. Deborah Guernsey, administrative assistant, Yellowstone Wolf Project, patiently endured my endless requests for information. Ms. Guernsey also tended to many small but critical details that allowed field research to occur. Wolf Project volunteers were the heart and soul of the data collection process. Since 1995 many dedicated volunteers passed through the Wolf Project field program and provided the bulk of the observations that comprise this thesis. Without their hard work and dedication this study would not have been possible. I owe a special thanks to Wolf Project volunteers Nathan Varley, Kevin Honness, Daniel Stahler, and Paul Frame for going the extra mile (literally) to watch wolves hunt bison in Pelican Valley. Also, without the interest and support of Lake District Rangers John Lounsbury and Lloyd Kortge our research in Pelican Valley would not have been possible. Robert Landis, Landis Wildlife Films, generously shared with me his film footage of wolves hunting in Yellowstone. Bob s films played a key role in clarifying my understanding and interpretation of wolf hunting behavior. Dr. Thomas Drummer, Michigan Technological University, provided important statistical expertise early in the study, and generously provided statistical advice at various times throughout the study. Dr. Lynn Eberly, University of Minnesota, instructed me in statistical methods for analyzing correlated data, and thus opened my eyes to a new and indispensable area of statistics. Dr. Eberly patiently responded to every email and every question without exception. I am also indebted to Dr. James Halfpenny for initially introducing me to Yellowstone National Park, and the Yellowstone Wolf Project, shortly after wolves were restored to the park in 1995. Funding for this project was provided by the National Geographic Society, Yellowstone National Park Foundation, Dayton-Wilkie Natural History Fund, and the Department of Ecology, Evolution, and Behavior at the University of Minnesota. Housing and transportation in Yellowstone were provided by the Yellowstone Center for Natural Resources, Yellowstone National Park. Finally, Cory Counard provided valuable input and criticism throughout my research, and provided essential moral support during preparation of the thesis.

ii ABSTRACT To study the hunting behavior of the wolf (Canis lupus) in Yellowstone National Park (YNP), I first define the wolf predatory sequence as consisting of six distinct behaviors: travel, approach, watch, attack, target, and capture. These behaviors are organized into three nested groups: predation attempt, prey encounter, and hunting bout. Using this framework, I first evaluate general patterns of wolf hunting behavior and estimate success rates for wolves hunting various prey in YNP. I then compare reported success rates for wolves hunting various prey species in North America to demonstrate the general relationship between hunting success and prey size. Next I show that prey are dangerous to wolves and that risk of prey-caused injury is related to prey size. Finally, I evaluate the influence of injury risk on patterns of wolf hunting behavior. From May 1995 to March 2000, 62 hunting bouts, 267 prey encounters, and 565 predation attempts were observed in their entirety. The typical hunting pattern involved a brief hunting bout (< 60 min.) including at least one prey encounter (< 15 min.) and at least one predation attempt (< 4 min.). Wolves encountered prey within 25 minutes of hunting, and approximately once every 20 minutes thereafter (3.00 ± 0.42 encounters/hour/bout N = 62). Multiple prey encounters during hunting bouts were neither a prominent nor important feature of hunting behavior patterns. Overall, the estimated rate of success was 0.21 ± 0.03 kills per encounter, and bison (Bison bison) were more difficult to kill (0.04 kills/encounter) than elk (Cervus elaphus) (0.24 kills/encounter). Comparisons with other studies indicate a broad association between hunting success and prey size. In general, prey that confronted wolves were more aggressive, and therefore less likely to be killed than prey that fled. In YNP, bison confronted wolves more frequently than elk (79% vs. 55% of encounters; χ 2 = 8.60, d.f. = 1, P < 0.01) and charged wolves more frequently than did elk (62% vs. 26% of encounters; χ 2 = 22.20, d.f. = 1, P < 0.001), suggesting that elk are less dangerous and more vulnerable to wolf predation than bison. Wolf hunting behavior differed between encounters with bison and elk. During bison encounters, wolves made fewer predation attempts (60% vs. 80%; χ 2 = 8.50, d.f. = 1, P < 0.01) and shorter predation attempts (2.90 ± 0.51 min. vs. 4.00 ± 0.38 min.; t = 4.04, d.f. = 165, P<0.001) than during elk encounters. Wolf encounters with bison also included periods of watching from within 10 m. Difference in wolf hunting behavior between bison and elk encounters suggest that wolves assess their risk of injury and incorporate this information into their foraging decisions. The tendency for wolves to attack elk more often than bison suggests that wolf preference for vulnerable prey is an adaptive strategy to acquire food while minimizing the risk of prey-caused injury.

iii TABLE OF CONTENTS ACKNOWLEDGMENTS i ABSTRACT. ii TABLE OF CONTENTS. iii LIST OF TABLES iv LIST OF FIGURES.. v INTRODUCTION 1 Components of the Predatory Sequence.. 8 A Framework for the Predatory Sequence... 14 METHODS... 16 Study Area... 16 Study Population.. 17 Hunting Observations.. 18 Statistical Methods... 21 RESULTS. 23 Hunting Bouts.. 23 Prey Encounters... 23 Predation Attempts.. 25 Hunting States.. 26 Hunting Success... 27 Anti-Predator Response and the Risk of Injury... 29 Hunting Behavior in Bison and Elk Encounters.. 30 Success Rates for Wolves Hunting Various North American Prey. 31 DISCUSSION... 31 The Predatory Sequence.. 31 General Patterns of Hunting Behavior. 33 General Patterns of Hunting Success... 37 Hunting Success and Prey Size 41 Risk of Injury and Prey Size 41 Wolf Behavioral Response to the Risk of Injury. 42 LITERATURE CITED. 47

iv Table 1. Table 2. Table 3. Table 4. Table 5. Table 6. Table 7. LIST OF TABLES Number of hunting bouts, prey encounters, and predation attempts observed in their entirety and partially observed (in parentheses) for various wolf packs in Yellowstone National Park, May 1995 March 2000. Results of General Linear Mixed Model (GLMM) evaluating the effects of hunting-state type and prey species on huntingstate duration (min.) in wolf encounters with elk and bison herds in Yellowstone National Park, May 1995 March 2000. Predicted mean hunting-state duration with 95% confidence intervals is shown in Figure 6. Success rates for wolves hunting various prey species in Yellowstone National Park, May 1995 - March 2000, based on known outcomes from completely observed prey encounters only, and on both complete and incompletely observed encounters (in parentheses). Age and sex of prey killed by wolves in Yellowstone National Park, May 1995 March 2000. The proportion killed in each age/sex class for each species is shown in parentheses. Results of General Linear Mixed Model (GLMM) evaluating the effects of hunting-state outcome, hunting-state type, and prey species on hunting-state duration (min.) in wolf encounters with elk and bison herds in Yellowstone National Park, May 1995 March 2000. Predicted mean hunting-state duration with 95% confidence intervals is shown in Figure 9. Results of General Linear Mixed Model (GLMM) evaluating the effects of hunting-state type on hunting-state duration (min.) in wolf encounters with bison herds in Yellowstone National Park, May 1995 March 2000. Predicted mean hunting-state duration with 95% confidence intervals is shown in Figure 11. Reported success rates for wolves hunting various North American prey species. 53 54 55 56 57 58 59

v LIST OF FIGURES Figure 1. The predatory sequence for wolves hunting herds of prey. 60 Figure 2. Figure 3. Figure 4. Figure 5. Study area and general location of study wolf packs, Yellowstone National Park, May 1995 - March 2000. Time of year wolf hunting bouts were observed in Yellowstone National Park, May 1995 - March 2000. Time of day wolf hunting bouts were observed during intensive winter study periods (mid-november to mid-december & March) in Yellowstone National Park, 1995-2000. Number of prey present during wolf encounters with various prey species in Yellowstone National Park, May 1995 - March 2000. 61 62 63 64 Figure 6. Predicted mean duration (min.) of hunting states with 95% confidence intervals in wolf encounters with elk and bison herds in Yellowstone National Park, May 1995 March 2000. Fitted means and confidence intervals are derived from GLMM results (Table 2). 65 Figure 7. Figure 8. Results of completely observed wolf encounters with elk herds and solitary elk in Yellowstone National Park, May 1995 - March 2000. Results of completely observed wolf encounters with bison herds and solitary bison in Yellowstone National Park, May 1995 - March 2000. 66 67 Figure 9. Predicted mean duration (min.) of hunting states with 95% confidence intervals in failed and successful wolf encounters with elk and bison herds in Yellowstone National Park, May 1995 - March 2000. Fitted means and confidence intervals are derived from GLMM results (Table 5). 68 Figure 10. The association between mean wolf hunting success (kills/encounter) and season (early winter: Nov 1 - Dec 31, midwinter: Jan 1 - Feb 28, late winter: Mar 1 - Apr 30, spring: May 1 - Jun 30) in wolf encounters with elk and bison in Yellowstone National Park, May 1995 - March 2000. 69

vi Figure 11. Predicted mean duration (min.) of hunting states with 95% confidence intervals in wolf encounters with bison herds in Yellowstone National Park, May 1995 - March 2000. Fitted means and confidence intervals are derived from GLMM results (Table 6). 70 Figure 12. The association between hunting success (kills/encounter) and prey size for wolves hunting various North American prey. 71

1 INTRODUCTION Previous attempts to observe the behavior of wolves hunting have been frustrated by a number of factors including dense vegetation, rugged topography, and logistical constraints such as access to remote study sites and fuel limitations during aerial observation (Mech 1966a; Clark 1971; Haber 1977; Carbyn et al. 1993). As a result, studies of wolf predation have depended largely on the examination of remains from wolf-killed ungulates for insight into wolf hunting behavior. Most studies have found that wolves kill mainly vulnerable prey (e.g., prey easily captured due to their circumstantial, behavioral, or physical condition) (Murie 1944; Mech 1970; Carbyn 1974; Peterson 1977; Mech et al. 1998). In general, predators kill vulnerable prey when prey are difficult to capture, and very difficult prey are aggressive and can injure a predator (Temple 1987). Therefore, for predators that rely on dangerous prey for food, vulnerable prey are probably safer to kill. Wolves feed mainly on ungulates that can injure (Mech 1966a; Rausch 1967; Phillips 1984; Carbyn and Trottier 1988) or kill them (Ballard et al. 1987; Pasitschniak- Arts et al. 1988; Mech and Nelson 1990; Weaver et al. 1992). Since failure to avoid injury or death greatly decreases fitness, the risk of prey-caused injury may be a strong selective force favoring wolf preference for vulnerable prey. If preference for vulnerable prey is an adaptive strategy to acquire food while avoiding injury wolves should be able to assess their risk of being injured or killed by prey and incorporate this information into their foraging decisions.

2 In addition, if safer prey provide less food than dangerous prey, wolves cannot simultaneously maximize food intake and minimize injury risk. Therefore, wolf preference for vulnerable prey may represent a trade-off between food and safety. For example, assuming prey size is related to injury risk (i.e. large prey are more dangerous than small prey) (Weaver et al. 1992), wolves may prefer small prey at the expense of food intake in order to minimize injury risk. Trade-offs between food and safety have only been examined for foragers that attempt to maximize food intake while minimizing the risk of predation (Krebs 1980; Newman and Caraco 1987; Lima and Dill 1990). Predators that elicit a conspicuous fear response from prey (e.g. trade food for safety) are considered fierce (Brown et al. 1999). In this model system, fierce predators freely pursue timid prey and contend only with the risk of starvation. However, predators are known to respond to the risk of preycaused injury, either by avoiding dangerous prey or modifying their behavior while foraging on dangerous prey. For instance, piscivorous birds attack fish with dangerous spines less often, and handle them longer than fish without spines (Forbes 1989). The dangerous-prey hypothesis proposes that predators respond to an increase in injury risk by handling dangerous prey more carefully, leading to longer handling times (Forbes 1989). In this case, predators manage the trade-off between food and safety through adjustments in handling time that lower injury risk at the expense of prey profitability, since handling time and prey profitability (e.g., net energetic return) are inversely related (Stephens and Krebs 1986). Although the tendency for wolves to kill vulnerable prey suggests that wolves trade between food and safety, the difficulty of

3 observing wolves hunt has hindered a close examination of the influence of injury risk on their hunting behavior. To examine wolf response to injury risk, one must first clearly characterize and define their hunting behavior. In most studies, observations of wolves hunting are limited in number, lacking in detail, and many are incomplete because the beginning or end of the hunt was not observed. As a result, no single study has produced a definitive account of wolf hunting behavior. Rather, current knowledge of wolf hunting behavior is the result of information accumulated over several generations of field studies. Initial studies provided the first general descriptions of wolf hunting behavior, indicating that wolves engage in several different types of behavior while hunting (Murie 1944; Banfield 1954; Tener 1954; Crisler 1956; Kelsall 1957, 1960). However, these early studies neither identified the individual behaviors explicitly, nor examined the relationships among them. A second generation of studies identified and described several types of wolf hunting behavior, and recognized that the behaviors occur in a logical sequence (Mech 1966a, 1970; Gray 1983; Carbyn and Trottier 1987). Mech (1970) decomposed hunting behavior into five stages : travel, stalk, encounter, rush, and chase. Gray (1983) described the behavior of wolves hunting muskoxen (Ovibos moschatus) as a sequence of six events : approach, circle herd, attack herd, cut off single individual, contact individual, and kill individual. For hunts of bison Carbyn and Trottier (1987) described five categories : watch, trail, trail and follow-up, harass, and rush.

4 The three predatory sequences differ in three main respects. First, the three sequences do not share the same set of behaviors. Second, different definitions are assigned to the same behavior. For example, Mech (1970) described the rush as an initial charge toward prey when prey are first encountered, while Carbyn and Trottier (1987) considered the rush to be the point during the encounter at which wolves grab prey. Third, similar definitions are assigned to different behaviors. For instance, the initial period of movement toward prey preceding attack has been described as stalk (Mech 1970), approach (Gray 1983), and trail and follow-up (Carbyn and Trottier 1987). Lack of consensus on the type and definition of behaviors that constitute the wolf predatory sequence hinders further study of wolf hunting behavior, and highlights the need for further clarification and explanation. In addition, the exact relationship between behaviors in the predatory sequence and more general types of wolf hunting behavior is uncertain. Specifically, studies that describe sustained periods of hunting activity in which wolves travel from one prey to another in succession, and make one or more attempts to kill prey during each encounter (Murie 1944; Mech 1966a, b; Haber 1977; Carbyn and Trottier 1987; Carbyn et al. 1993; Huggard 1993; Mech et al.1998), imply that behaviors from the predatory sequence are components of more general types of hunting behavior (e.g., hunting bouts, prey encounters, and predation attempts). These general types of hunting behavior and their relationship with specific behaviors of the predatory sequence have not been explicitly defined.

5 General patterns of wolf hunting behavior have been considered mainly in terms of the behavior necessary to locate uncommon and widely dispersed vulnerable prey. For instance, to increase the probability of locating vulnerable prey, wolves are believed to encounter and attack several different sets of prey during a hunt (Murie 1944; Mech 1970; Mech et al. 1998), and to prefer prey herds to solitary prey (Huggard 1993; Hebblewhite 2000). As a result, long hunts should have more prey encounters than short hunts, and successful hunts should be marked by higher prey encounter rates than unsuccessful hunts. Also, where prey herds are available, wolves should encounter prey herds more frequently than solitary prey. Multiple prey encounters during a hunt might occur simultaneously or consecutively (Murie 1944; Mech 1966a, b; Clark 1971; Haber 1977; Gray 1983; Mech et al. 1998). It is unknown whether the outcome of an encounter has any influence on the occurrence, or outcome, of a consecutive encounter. Prey encounters can also involve prey individuals that wolves encountered previously in the hunt (Clark 1971), or during a different hunt (Fuller 1962; Mech 1966a; Carbyn et al. 1993). The various types of prey encounter have not been defined, nor has the frequency of their occurrence been measured. Multiple attempts to kill prey during a single prey encounter have also been observed. Multiple attempts can occur simultaneously (Murie 1944, Mech 1966a, b, 1988; Clark 1971; Carbyn 1974; Mech et al. 1998) or consecutively (Fuller 1957; Mech 1966a, b; Miller and Gunn 1977; Miller et al. 1985; Carbyn and Trottier 1987; Gray 1987; Carbyn et al. 1993; Mech et al. 1998). It is also unknown whether the outcome of a

6 predation attempt has any influence on the occurrence, or outcome, of a consecutive predation attempt. The frequency of multiple predation attempts during prey encounters is not known. Overall, detailed information requiring extended and uninterrupted observations of wolves hunting is scarce. For instance, no observational data are available describing prey search time or prey encounter rate. In the absence of a clearly defined predatory sequence, estimates of wolf hunting success have involved a variety of measures defined differently for different studies. As a result, comparisons of hunting success across studies can be confounded if the type of measure and its definition are not taken into account. Previous measures of wolf hunting success based on direct observation include: (1) number of kills per prey animal tested (Mech 1966a; Haber 1977; Peterson 1977; Mech et al. 1998), (2) number of kills per encounter (Carbyn et al. 1993; Mech et al. 1998), (3) number of kills per chase (Clark 1971; Carbyn et al. 1993; Nelson and Mech 1993), and (4) number of successful behaviors per behavior of the same type (e.g., number of approaches resulting in an attack per approach) (Mech 1970; Peterson 1977; Carbyn and Trottier 1987). Confusion also arises over the term 'test'. A test can be a prey encounter where wolves pursue or hold an individual prey at bay (Mech 1966a; Peterson 1977; Mech et al. 1998), or a prey encounter where wolves simply move towards an individual prey without necessarily pursuing or holding it at bay (Haber 1977). A 'test' can also apply to entire herds of prey where hunting success is expressed as the number of kills per herd

7 tested, such that if a herd split into several smaller groups the encounter is still treated as a single test (Haber 1977). Similarly, estimates of success measured as kills per encounter score the outcome of the overall encounter rather than the outcome of each predation attempt that might comprise an encounter. In this case an encounter is considered to occur when wolves watch prey (Carbyn et al. 1993), or at least approach prey (Mech et al. 1998). Where success is estimated as the proportion of all chases that resulted in a kill, it is uncertain whether chases included predation attempts when prey were only held at bay (e.g., when pursuit did not occur). Here I first review and clarify the predatory sequence for wolves to establish a general framework within which to analyze their hunting behavior. I apply this framework to a highly observable population of gray wolves recently restored to YNP to (1) elucidate general patterns in wolf hunting behavior that have been difficult to quantify previously, and (2) estimate rates of hunting success for various prey in YNP. I compare reported rates of success among several different prey in North America to determine if wolf hunting success is generally related to prey size. Next I examine the influence of injury risk on patterns of wolf hunting behavior during encounters with bison (350-1000 kg) and elk (75-340 kg). First, I demonstrate that (1) prey in general are dangerous to wolves, and (2) bison are more dangerous than elk. Second, I evaluate whether wolves (1) make foraging decisions based on injury risk, and (2) trade food for safety. If elk are more vulnerable than bison, wolves should attempt to

8 kill elk more frequently than bison, and spend less time in elk encounters than bison encounters. Components of the Predatory Sequence A review of all available published accounts of wolf hunting behavior indicates that the predatory sequence in wolves is composed of six general hunting states which I describe as: travel, watch, approach, attack, target, and capture. In general, hunting states can be characterized according to the type of gait, or lack thereof, used by the wolves. All hunting states are defined in terms of the behavior of the wolves, independent of prey behavior. Although wolves may engage in each hunting state in a predatory sequence, they may also skip or repeat one or more hunting states. For instance, during encounters with bison in Wood Buffalo National Park, wolves sometimes go directly from the watch state to the attack state, or begin at the attack state, or even the capture state (Carbyn and Trottier 1987). As a result, I refer to the components of the predatory sequence as hunting states, where a state is considered to be any distinct behavior with a measurable duration (Martin and Bateson 1993). I use the term state to avoid the implication that components necessarily follow a definite order as suggested by stage. Travel State The need to locate vulnerable prey requires that wolves travel widely (Murie 1944; Mech 1966a); therefore wolves are considered hunting anytime they are traveling

9 (Murie 1944; Kelsall 1960; Mech 1966a, 1970; Haber 1977; Mech et al. 1998). Traveling involves wolves using any type of gait to move across the landscape without an obvious intention to move toward a particular prey. While traveling, wolves locate prey either by sight, direct scent, chance encounter, or tracking (Mech 1970). Although there are no reports on the duration of travel necessary before encountering prey in general, Mech (1966a) reported one case in which wolves traveled 100 km or more before encountering vulnerable moose (Alces alces). Watch State Watching involves intent staring at prey (Clark 1971; Haber 1977; Nelson and Mech 1994; Mech et al.1998), and has been described by some as surveillance (Clark 1971; Carbyn and Trottier 1988; Carbyn et al. 1993). Watching is believed to be a means by which wolves assess the vulnerability of prey and thereby their chance for success (Murie 1944; Mech et al. 1998). Wolves may assess prey by identifying a strategic advantage (Mech et al. 1998). For example, wolves hunting bison have been observed to wait until bison flee before they attempt to capture a calf (Carbyn and Trottier 1988), and wolves hunting muskoxen are known to wait until a calf moves outside the protective ring of the adults before attacking (Tener 1954). When wolves are seeking a strategic advantage, they may appear to sleep while watching prey, but are quick to strike when an opportunity presents itself (Carbyn and Trottier 1988; Mech 1988). In addition, Murie's (1944) observation that wolves approach caribou (Rangifer tarandus) and then watch them flee suggests that wolves may assess the physical condition of prey by observing

10 their locomotion, similar to the function of watching behavior described for spotted hyena (Crocuta crocuta) (Kruuk 1972; Holekamp et. al 1997) and wild dog (Lycaon pictus) (Fitzgibbon and Fanshawe 1988) hunting Thompson's gazelle (Gazella thomsonii). Wolves may watch when they first encounter prey (Haber 1968; Carbyn 1974; Carbyn & Trottier 1987), after an initial approach (Murie 1944; Kelsall 1960; Haber 1968; Clark 1971; Carbyn 1974; Mech 1988; Nelson and Mech 1994), or following a failed attack (Murie 1944; Tener 1954; Mech 1966a; Gray 1983, 1987; Carbyn and Trottier 1988; Mech 1988). Except for an observation by Murie (1944) of a solitary wolf watching Dall sheep (Ovis dalli) after a failed attack, all reported watches following an attack have involved large, formidable prey, including moose (Mech 1966a), muskoxen (Tener 1954; Gray 1983, 1987; Mech 1988), and bison (Carbyn and Trottier 1987, 1988; Smith et al. 2000). In general, the distance at which wolves watch prey tends to be greatest for medium-size prey such as elk and caribou, and least for large prey such as moose, bison, and muskoxen. Wolves have been reported to watch medium-size prey from 23 to 410 m (Murie 1944; Kelsall 1960; Haber 1968; Clark 1971; Carbyn 1974) and large prey from 3 to 200 m (Tener 1954; Mech 1966a; Haber 1977; Carbyn and Trottier 1988; Mech 1988). However, in one exceptional case three wolves watched an adult white-tailed deer from 25 m prior to an approach, and from 5 m following an approach (Nelson and Mech 1994). The distance at which wolves watch prey also tends to be greatest prior to initial attack. Prior to initial attack, wolves have been reported to watch prey from 3 to 410 m

11 (Murie 1944; Kelsall 1960; Haber 1968; Clark 1971; Carbyn 1974; Haber 1977; Mech 1988), and following an initial attack from 23 to 200 m (Tener 1954; Mech 1966a; Carbyn and Trottier 1988). Approach State An approach involves wolves walking (Murie 1944; Banfield 1954; Crisler 1956; Kelsall 1957, 1960; Haber 1968; Mech 1970, 1988; Clark 1971; Carbyn 1974; Gray 1983, 1987; Miller et al. 1985; Carbyn and Trottier 1988) or trotting (Murie 1944; Banfield 1954; Haber 1968, 1977) toward prey. In one observation, Gray (1970) characterized the approach of one wolf toward an adult male muskox as a gallop. When wolves walk toward prey, they may do so casually with no attempt at concealment (Murie 1944; Kelsall 1960; Carbyn 1974; Gray 1983, 1987; Miller et al. 1985; Carbyn & Trottier 1988; Mech 1988; Nelson and Mech 1994) or they may stalk prey by walking either upright, slowly and deliberately (Banfield 1954; Crisler 1956; Kelsall 1957, 1960; Haber 1968; Mech 1970, 1988) or in a crouch, using topography (Clark 1971; Mech, USGS, unpublished) or vegetation to conceal themselves (Haber 1977). Reports of wolves stalking prey tend to be more common for encounters with medium-size prey such as caribou (Banfield 1954; Crisler 1956; Kelsall 1957, 1960; Haber 1968, 1977; Clark 1971) and Dall sheep (Murie 1944; cf. Haber 1968), than for encounters with large prey such as moose (Mech 1966a) and muskoxen (Mech 1988), although they do stalk the latter (Mech, USGS, unpublished). Wolves might stalk medium-size prey to reduce the chance that they flee (Mech 1970). However, Murie

12 (1944) found that without stalking, wolves could approach to within a few hundred meters of caribou. If wolves do not leave prey, an approach can be followed by either a period of watching (Murie 1944; Banfield 1954; Mech 1966b, 1988; Haber 1977; Carbyn and Trottier 1988), or by some form of attack (Murie 1944; Banfield 1954; Crisler 1956; Kelsall 1957; Mech 1966a, b, 1988; Haber 1977; Peterson 1977; Gray 1983, 1987; Miller et al. 1985; Carbyn and Trottier 1988; Mech et al. 1998; Mech and Adams 1999). Attack State An attack involves wolves pursuing (Murie 1944; Banfield 1954; Crisler 1956; Kelsall 1957, 1960; Mech 1966a, b, 1988; Haber 1977; Peterson 1977; Gray 1983, 1987; Miller et al. 1985; Carbyn and Trottier 1987, 1988; Carbyn et al. 1993; Nelson and Mech 1993; Mech et al. 1998; Mech and Adams 1999) and/or holding prey at bay (Tener 1954; Mech 1966a, 1988; Gray 1970; Miller and Gunn 1977; Peterson 1977; Gray 1983, 1987; Carbyn and Trottier 1987, 1988; Carbyn et al. 1993; Mech et al. 1998; Mech and Adams 1999). Elsewhere, the term attack has also been used to describe wolves and coyotes biting and grabbing prey (Mech 1966a; Gese and Grothe 1995) or pursuing an individual prey (Lingle 2002). The gait of wolves pursuing prey is usually a gallop (Murie 1944; Crisler 1956; Kelsall 1960; Miller et al. 1985; Carbyn and Trottier 1988) or trot (Murie 1944). If a prey herd fragments into several smaller groups during a pursuit, wolves may move from one group to another in succession (Murie 1944; Gray 1987), presumably to locate a

13 vulnerable individual (Murie 1944; Mech et al. 1998). Otherwise, if the herd continues to flee as a single group, wolves may keep to the rear of the herd and wait for a vulnerable individual to fall behind (Murie 1944; Crisler 1956; Kelsall 1960; Haber 1977; Carbyn and Trottier 1988). All reports of wolves holding prey at bay, except 2 involving white-tailed deer (Odocoileus virginianus) (Mech 1984; Nelson and Mech 1994), involve large prey including moose (Mech 1966a; Peterson 1977; Mech et al. 1998), muskoxen (Tener 1954; Gray 1970, 1983, 1987; Miller and Gunn 1977; Mech 1988; Mech and Adams 1999), and bison (Carbyn and Trottier 1987, 1988; Carbyn et al. 1993). If wolves attack more than one prey and single out an individual, the next hunting state in the predatory sequence would be target. If wolves attack a solitary prey and grab it, the next hunting state would be capture. Target State The target state involves wolves pursuing and/or holding at bay a specific individual from a prey group (i.e. 2 or more individuals) (Murie 1944; Banfield 1954; Crisler 1956; Fuller 1957; Kelsall 1960, 1968; Mech 1966a, b, 1988; Haber 1977; Miller and Gunn 1977; Gray 1983, 1987; Carbyn and Trottier 1987, 1988; Carbyn et al. 1993; Mech et al. 1998; Mech and Adams 1999). If wolves are in pursuit, their running speed typically increases from the attack state to the target state (Murie 1944; Crisler 1956; Kelsall 1960; Carbyn and Trottier 1987). Prey targeted by wolves are often young (e.g., < 12 months) (Murie 1944; Kelsall 1968; Haber 1977; Miller and Gunn 1977;

14 Carbyn and Trottier 1987, 1988; Mech 1988; Mech et al. 1998) or crippled (Mech and Frenzel 1971; Peterson 1977; Carbyn and Trottier 1987). Sometimes wolves target a prey that falls behind the herd (Crisler 1956; Haber 1977; Mech 1988) or stumbles (Kelsall 1960). The target prey can be pursued or held at bay repeatedly if wolves fail to initially subdue it (Fuller 1957; Mech 1966a; Carbyn et al. 1993). If wolves grab and restrain the prey, the next hunting state in the predatory sequence would be capture. Capture State The capture state involves wolves grabbing and restraining an individual prey (Murie 1944; Kesall 1960; Mech 1966a; Peterson 1977; Carbyn and Trottier 1987; Gray 1983, 1987; Carbyn and Trottier 1988; Carbyn et al. 1993; Nelson and Mech 1993; Mech and Adams 1999). The capture state results in wolves killing prey (Murie 1944; Kelsall 1960; Mech 1966a; Peterson 1977; Smith 1980; Carbyn et al. 1993; Mech and Adams 1999) or prey escaping wolves (Mech 1966a; Peterson 1977; Gray 1983; Carbyn and Trottier 1988; Nelson and Mech 1993; Mech and Adams 1999). A Framework for the Predatory Sequence To examine general patterns of wolf hunting behavior that involved one or more hunting states, I developed a framework that defined the relationship between the individual hunting states and three nested groups of hunting states: predation attempt, prey encounter, and hunting bout (Fig. 1). A hunting bout was a discrete period beginning when wolves began traveling or encountering live prey (whichever came first) and ending

15 when wolves stopped encountering live prey and rested (e.g., sat or laid down) or stopped traveling (whichever came last). A hunting bout could contain at least one hunting state (except watch, see below) or a continuous sequence of hunting states. Wolves often howl or socialize while hunting (Banfield 1954; Mech 1966a; Haber 1977), and I considered this to be part of the hunting bout, rather than marking its conclusion. One or more hunting bouts could occur per day. A prey encounter was a period during a hunting bout involving prey and containing one or more of the following hunting states: approach, watch, attack, target, capture. The unit of encounter during a hunting bout was either a solitary prey or herd of prey. An individual prey was considered to be in a herd if its nearest neighbor was 20 m away. I considered a prey encounter to begin when wolves sighted prey and walked or ran toward them. A prey encounter ended when wolves stopped staring at prey or otherwise ceased to pay attention to prey (e.g., traveled away from prey). Situations that involved wolves watching prey without initially walking or running toward them were not considered encounters by my definition. One or more prey encounters could occur per hunting bout. Prey encounters were categorized as new, consecutive, repeat, return, or simultaneous. A new encounter was the first encounter to occur in a hunting bout and involved prey not previously encountered earlier in the day or in preceding days. A consecutive encounter denoted the second, third, fourth, etc. encounter during a hunting bout, and involved prey not previously encountered in the hunting bout or during a different hunting bout earlier in the day or in preceding days. A repeat encounter

16 involved prey encountered earlier in the same hunting bout, while a return encounter involved prey encountered in a different hunting bout earlier in the same day or in preceding days. An encounter was simultaneous if it occurred at the same time as another encounter in the same hunting bout. A predation attempt occurred when wolves pursued, held at bay, or grabbed prey. It was a period during a prey encounter that involved the sequential occurrence of one or more of the following hunting states: attack, target (prey groups only), or capture. A predation attempt failed if (1) the sequence leading from attack to capture was interrupted or (2) a capture did not result in a kill. A subsequent attempt began when the sequence restarted at one of the three hunting states. Multiple predation attempts could be consecutive and/or simultaneous. A consecutive predation attempt was one that occurred following a preceding attempt, and a simultaneous attempt was one that occurred at the same time as another attempt in the same prey encounter. METHODS Study Area Yellowstone National Park extends across 891,000 ha of a primarily forested plateau in northwestern Wyoming (Fig. 2). Elevations range from 1,500 m to 3,300 m. Several large montane grasslands punctuate the Yellowstone plateau and provide unobstructed views of wildlife. However, continuous viewing can be inhibited by forests on the periphery of grasslands, by occasional trees within grasslands and by varied

17 topography. Approximately 35,000 elk, 4,000 mule deer (Odocoileus hemionus), 3,000 bison, 700 moose, 200 pronghorn (Antilocapra americana), 200 bighorn (Ovis canadensis) and scattered mountain goats (Oreamnos americanus) reside in YNP during all or part of the year (D.W. Smith, National Park Service, unpublished data). Observations of wolves hunting were made primarily in a 100,000 ha complex of montane grasslands situated in the northern quarter of YNP referred to as the Northern Range (Fig. 2). The Northern Range is a series of open valleys, ridges, and minor plateaus linked by the Lamar and Yellowstone Rivers. Low elevations (1,500 m to 2,400 m) on the Northern Range create the warmest and driest conditions in YNP during winter. As a result, the Northern Range serves as the principal winter range for nearly 12,000 elk and 700 bison (D.W. Smith, National Park Service, unpublished data). Elk and bison occurred in singles or in herds of up to 800 and 75 animals, respectively. A single paved road runs the length of the Northern Range and provides year-round access. Wolves were routinely visible from observation points on or near the road. In winter, wolves were also observed from a hilltop observation point in Pelican Valley in the interior of YNP at approximately 2,500 m. Pelican Valley was accessed in winter by ski. Study Population A combined total of 31 radio-collared wolves were reintroduced to YNP in 1995 and 1996 (Bangs and Fritts 1996; Phillips and Smith 1996). Each subsequent year YNP personnel radio-collared 30-50% of the pups born (Smith et al. 2000). Wolves observed in the study were either members or descendents of the original reintroduced population.

18 From 1995 to 2000, 14-110 wolves comprised 2-7 packs of 2 to 27 wolves per pack (9.9 ± 1.0 wolves/pack, N = 37 pack-years). Approximately 20-60 of the wolves studied were radio-collared and 20-25 were individually recognizable by combination of color pattern, radio-frequency, and body conformation. Observations of wolves hunting were recorded from May 1995 to March 2000. During the study the number and location of packs changed. In 1995, the study population was limited to the three initial packs reintroduced to the Northern Range: Crystal Creek, Rose Creek and Soda Butte. The Soda Butte pack eventually moved outside YNP onto private lands, was returned to YNP, and was released in a remote southern region of the park. In early 1996, a female and male dispersed from the Rose Creek and Crystal Creek packs, respectively, and formed a third pack on the Northern Range called Leopold. Shortly after their release in 1996, the Druid Peak pack replaced the Crystal Creek pack on the Northern Range, and the Crystal Creek pack relocated to the more remote Pelican Valley. For the remainder of the study, the Rose Creek, Leopold, and Druid Peak packs were the focus of study because they inhabited the easily accessed, and sparsely forested Northern Range (Fig. 2). In 1996, the Nez Perce and Chief Joseph packs were also released, but they inhabited areas too forested and/or inaccessible to allow observation from the ground. Hunting Observations Wolves were mainly observed hunting during two annual 30-day intensive study periods in March and mid-november to mid-december (Fig. 3). In general, wolves on the

19 Northern Range were more easily observed during winter because they were attracted to ungulates concentrating on low elevation winter range that was easily accessed by observers. Observations were also made in April, May, and June during annual wolf-denmonitoring studies. Observations during other months were recorded opportunistically. During each study period, teams of two observers were assigned to daily monitor each Northern Range wolf pack from the ground from dawn to dusk. Observation effort per hour was generally constant throughout the day. Nighttime observation was attempted with night vision goggles but was ineffective due to long distances between wolves and observers. In the eight study periods from May 1995 to March 2000, observers on the Northern Range watched wolves for a total 1,901 hours. At least two observers monitored the Crystal Creek pack in Pelican Valley during March 13-19, 1999 and March 23-31, 2000. Observers in Pelican Valley watched wolves for a total of 80 hours. All packs were located daily from fixed-wing aircraft, weather permitting, during each study period. Outside study periods, wolves were located from the air weekly. Hunting behavior was observed from the aircraft as well as from the ground. Aerial observers recorded 24 wolfprey encounters, and ground observers recorded 560 wolf-prey encounters. To standardize data collection, each observer was trained to record wolf hunting behavior prior to each study period. Observers on the ground first located wolf packs with radio-telemetry to obtain a directional fix, and visually located and observed wolves with binoculars and spotting scopes. Observers watched wolves at distances of 0.1-6.0 km for as long as they remained in view and recorded hunting behavior using hand-held voice recorders and

20 digital stopwatches. Recorded observations were subsequently transcribed onto data forms. Some observations were also recorded on video. During each hunting state, observers recorded the following: duration of the hunting state, number, age, and gender of wolves, number and age/sex class of prey, and prey behavioral response. Wolf age and gender were determined during the annual effort to capture and radio-collar wolves (Smith et al. 2000). Sex of wolves not captured was determined by noting wolf body position while urinating (Mech 1970). Wolf age was also determined during den monitoring by noting when individuals were born. Hunting states that started or ended out of view were excluded from duration analyses. For this study only watch states that occurred at close range (< 10 m) were noted. Unless otherwise noted, all estimates of hunting success were based on prey encounters, predation attempts, and hunting states that were observed in their entirety. Estimates of hunting success included encounters involving both solitary and group hunts. Hunting success was measured at the level of prey encounter (kills/encounter), predation attempt (kills/attempt), and hunting state. For prey encounters and predation attempts, a success was considered to be the occurrence of a single ungulate kill. At the level of hunting state, success was measured according to whether the subsequent hunting state in the predatory sequence occurred. For example, the success of wolves approaching was measured as the proportion of approaches that resulted in an attack (i.e., number of attacks per approach). Data on the association between hunting group size and hunting success will be presented elsewhere.

21 Statistical Methods Means are reported with standard errors throughout, and for all analyses, results were considered significant at P < 0.05. P-values shown are for two-tailed tests. Frequency data, such as kills/encounter and kills/attempt, were evaluated with Pearson's chi-square test, or if more than one-fifth of fitted cells were sparse (e.g., frequency < 5), with Fisher's exact test. All continuous data were checked for normality prior to analysis. To satisfy normality assumptions, duration and count data (e.g., number of encounters and attempts) were log and square-root transformed, respectively. However, results were plotted in the original scale to aid interpretation. Prey encounter and predation attempt duration were evaluated with Student's t-test. Continuous data were analyzed with a Mann-Whitney U-test and Spearman s rank correlation coefficient if sample sizes were small (< 30), or transformations were not adequate. The relationship between prey mass and anatomical point of capture was evaluated using ANOVA. Assumed weights (kg) for elk were: cow, 226; yearling, 165; calf, 103 and bull, 266 (K. E. Murphy, National Park Service, unpublished data). Assumed weights (kg) for bison were: calf, 271; cow, 430; and bull, 679 (Meagher 1973). All the above tests assume independence of observations. Analyses of hunting-state duration were performed with general linear mixed models (GLMMs) (Verbeke and Molenberghs 2000) using the SAS 8.0 analysis package (SAS Inc. 2000). A mixed linear model is a generalization of the standard linear model (i.e. simple linear regression) which accounts for correlation and non-constant variance in the data. Hunting states were correlated if they occurred during the same hunting bout or prey encounter. In these models, an unstructured correlation matrix was used, which

22 allows for any level of correlation among hunting states within the same prey encounter and within the same hunting bout. Model parameters were estimated using maximumlikelihood estimation, and significance of effects was determined by an approximate t- test. Model reduction was performed using the likelihood-ratio test. Results were robust to other choices of correlation matrices. Predicted mean hunting-state duration was derived from the GLMM analysis and plotted with confidence limits to illustrate the significance of comparisons between different types of hunting state. Sample sizes varied considerably among tests because not all observations contained the same quality of information. For example, 267 prey encounters were observed in their entirety, but accurate duration data were only recorded in 175 of those encounters. Thus, analyses of encounter duration were restricted to those 175 prey encounters. The association between prey size and hunting success was examined by first summarizing reported rates of success for various North American prey species. Where more than one estimate was available for a particular prey species, estimates were compared within prey species, using Pearson s chi-square or Fisher s exact test, to identify if differences existed among studies. To quantify prey size, mean weights (kg) were estimated for each prey species based on Nowak (1999). Spearman's rank correlation coefficient (r s ) was used to test the association between success rate and mean prey weight.

23 RESULTS Hunting Bouts Observers watching the Rose Creek, Leopold, Druid Peak, and Crystal Creek packs recorded 62 hunting bouts in their entirety and portions of an additional 400 (Table 1). I personally observed and recorded 78 (17%) of those 462 hunting bouts. During intensive study periods, packs made on average 1.08 + 0.22 hunting bouts/observation hour (N = 181 pack-observation days), and hunting bouts were observed mainly in the morning and evening (Fig. 4). Wolf behavior immediately preceding a hunt was noted in 91 hunting bouts and included 36 (40%) resting, 21 (23%) sleeping, 12 (13%) feeding, 17 (19%) rallying (e.g., excited greeting), and 5 (5%) howling. The initial hunting state in 144 hunting bouts observed at the start included 101 (70%) travel, 36 (25%) approach, and 7 (5%) attack states. In 65 hunting bouts that began with travel, wolves encountered prey within 1 to 118 minutes (22.30 + 3.10 min., N = 65). Duration of hunting bouts was 3-594 minutes (48.10 ± 9.80 min., N = 62), and included 0-3 prey encounters (1.20 ± 0.09 encounters/bout, N = 62). Number of prey encounters/bout was not significantly associated with duration of hunting bout (Spearman rank correlation coefficient, r s = 0.22, N = 62, P=0.24). Prey Encounters Observers recorded 267 prey encounters in their entirety and portions of an additional 317. The initial hunting state among 336 prey encounters observed at the start included 291 (87%) approach, 44 (13%) attack, and 1 (0%) target states. Of the 584 total

24 prey encounters observed, 486 (83%) involved elk, 75 (13%) bison, 12 (2%) pronghorn, 6 (1%) bighorn sheep, 3 (0.5%) mule deer, and 2 (0.5%) moose encounters. Overall, wolves encountered prey at a rate of 3.10 ± 0.42 encounters/hour/bout (N = 62). Among 55 completely observed hunting bouts in the Northern Range where wolves encountered elk or bison, wolves encountered elk at a slightly higher rate (3.28 + 0.48 encounters/hour/bout, N = 49) than they encountered bison (3.18 + 0.80 encounters/hour/bout, N = 6) but the difference was not significant (Mann-Whitney U- test, z = 0.16, P = 0.68). Among 529 encounters involving elk or bison on the Northern Range, wolves did encounter elk more frequently 472 (89%) than bison 57 (11%). Data were unavailable to adequately determine whether wolves were encountering prey species proportionate to their occurrence in the study area. Overall, wolves encountered herds of prey more often (85% of N = 584 prey encounters) than solitary prey (15%; χ 2 = 267, d.f. = 1, P < 0.001; Fig. 5). Again, data were not available to determine whether wolves were encountering prey herds in proportion to their occurrence in the study area. Among 175 prey encounters for which duration data were available, duration of prey encounters ranged from < 1 to 553 minutes (12.40 ± 3.30 min., N = 175). Of 134 multiple encounters that occurred during hunting bouts, 118 (88%) were consecutive, 8 (6%) simultaneous, 4 (3%) repeat, and 4 (3%) unknown. Among 178 prey encounters observed at their finish, a consecutive encounter was more likely to occur after an unsuccessful encounter (34.2%, N = 105) than after a successful encounter (8.2%, N = 73; χ 2 = 16.23, d.f. = 1, P < 0.001). Among 123 consecutive prey encounters