Human–Wildlife Interactions 5(2):173–176, Fall 2011 Commentary [Editor’s note: the following articles are responses to Valerius Geist’s article “Wildlife habituation: advances in understanding and management application”, appearing in Human–Wildlife Interactions 5:9–12. Geist's rebutt al follows.] Misconceptions about black bears: a re- sponse to Geist (2011)
LYNN L. ROGERS, Wildlife Research Institute, 1482 Trygg Road, Ely, MN 55731, USA [email protected] SUSAN A. MANSFIELD, Wildlife Research Institute, 1482 Trygg Road, Ely, MN 55731, USA
We read with interest the commentary Dian Fossey did the same with great apes by Valerius Geist on habituation (Geist (Hominidae) years before. 2011). Dr. Geist is a world authority on To support his contention that habituation ungulate behavior, but his statements about leads to att acks, Geist erroneously used the bears refl ect misconceptions that he supported case of Timothy Treadwell who was killed by with anecdotes rather than with systematic a brown bear (Ursus arctos) in Katmai National observations that characterized his ungulate Park, Alaska, during 2002. In reality, Treadwell research. When someone of his stature att acked the bear as much as the bear att acked uncritically extrapolates from ungulates to him, and he did it fi rst (more below). I [Rogers] bears in this way, he sets back bear management, have watched Treadwell with bears many times promotes the sensationalized image of bears, as I led groups of bear-viewers. As long as and makes people unwilling to coexist with Treadwell behaved as usual, the bears tended to animals that they fear. ignore him. For 13 summers, Treadwell waded Habituation is a waning of response to next to the bears as they fi shed, approached a repeated, neutral stimulus (Thorpe 1956, them as they mated, and sat with them as they Whitaker and Knight 1998, Gilbert 1989, Smith grazed or as mothers 3 m away played with their et al. 2005, Herrero et al. 2005, Stringham 2009). cubs. The occasional young bear approached Bears that are fully habituated to humans ignore him. Sometimes they touched, but it was not the them (Whitaker and Knight 1998). Geist’s use of beginning of an att ack, as Geist implied. Guides the word habituation was confusing because he and tourists had similar experiences. Guides oft en used it to mean bears that are conditioned recognized the situations for what they were— or att racted to humans, which is the opposite of true habituation—and correctly judged the its true meaning. safety of it. They were not att acked, even when Geist’s main point was that “habituation” can I watched as 2 tourists approached within 2 m lead to bear att acks. There is danger in anything, of a large, sleeping bear that opened an eye and of course, but if habituated bears were as Geist went back to sleep. says, we and our co-workers could not do the Why did Treadwell get killed? It had nothing close-up black bear (Ursus americanus) studies to do with habituation. A bear investigated his that we have been doing for decades. Habituated camp when Treadwell had his gear and food individuals do not view us humans with packed up ready to be fl own out. Treadwell “unconsummated interest” and att ack. They probably burst out of his tent and went aft er the behave as if we are of litt le consequence. We bear in his “samurai” mode, as he mentioned are neither friends nor enemies. We are neither in the movie “Grizzly Man” (Herzog 2005). Did signifi cant food-givers nor competitors. Bears Treadwell know the bear? Was it habituated? No forage, nurse, and sleep with hardly a look in one knows. A sparse salmon run had brought our direction, thus, providing insights into bear new bears out of the interior, according to Clint life that we would not have thought possible. Hlebechuk (personal communication), who This is not new, of course. Jane Goodall and owned Hallo Bay Bear Camp. Offi cials killed a 174 Human–Wildlife Interactions 5(2) big bear that had fed on Treadwell’s body, but big use trust rather than tranquilizers to radio- bears take over kills from smaller bears. Geist collar black bears, including mothers with cubs mentioned none of the above. His only citation and males up to 578 pounds. These kinder and was an Anchorage Daily News article by Craig gentler research methods eliminate injury and Medred (2003), titled “Wildlife author killed, cause far less stress than traps and tranquilizers eaten by bears he loved.” The article fi t Geist’s (Catt et et al. 2003, 2008). point, and he cited it. Geist stated, “When large mammals show In his section on the theoretical basis for an interest in the observer, or perform the fi rst, habituation, Geist used the word habituation faint dominance displays, it is high time for the correctly and gave an excellent overview of how observer to leave.” In truth, if I had taken that animals function, citing his good work from the advice a quarter century ago, I never would 1970s. But, in the section on danger signals, have remained with bears long enough to discussing signals that show anxiety (Herrero et learn much. The same black bear displays that al. 2005), Geist followed the common practice of Geist and others call threats, warnings, and calling them threats. While it looks threatening dominance displays, I call harmless bluster. when a nervous black bear lunges, slams its feet Instead of leaving when I see bluster, I feel down, blows explosively, and clacks its teeth, it safe. Bluster means a black bear is apprehensive is a stretch to label these behaviors as signs of and wants to talk about it. Communication is a danger. In my 44 years of working with wild step toward trust. black bears, I have seen these ritualized displays Geist included the common advice that retreat hundreds of times and have never had one turn should not be at a run because “fearfulness and into an att ack. These displays are not predictors timidity can trigger att acks!” This may be true of black bear att acks. They merely express with some dogs and big cats, but I know of no nervous apprehension, as is shown in the bear support for that statement with black bears. The language videos on the North American Bear warning not to run is perhaps the most common Center’s website (
Literature cited Cattet, M. R., K. Christison, N. A. Caulkett, and G. B. Stenhouse. 2003. Physiologic responses of grizzly bears to different methods of capture. Journal of Wildlife Diseases 39:649–654. Cattet, M. R., G. Stenhouse, and T. Bollinger. 2008. Exertional myopathy in a grizzly bear (Ursus arctos) captured by leg-hold snare. Journal of Wildlife Diseases 44:973–978. Geist, V. 2011. Wildlife habituation: advances in understanding and management application. Human–Wildlife Interactions 5:9–12. Gilbert, B. K. 1989. Behavioral plasticity and bear– human confl icts. Pages 1–9 in M. Bromley, editor. Bear–people confl icts: proceedings of a symposium on management strategies. North- west Territories Department of Renewable Resources, Yellowknife, Northwest Territories, Canada. Herrero, S., A. Higgins, J. E. Cardoza, L. I. Hajduk, 176 Human–Wildlife Interactions 5(2)
LYNN L. ROGERS spent many years trap- ping, tranquilizing, and radio-collaring black bears as a U.S. Forest Service research scientist. In the mid-1980s, he adapted the trust-based research methods of Jane Goodall to black bears in the forests of Minnesota and began accompanying wild bears for 24 hours at a time. Research topics include diet, habitat use, social relations, care of cubs, hibernation, vocalizations, body language, causes of death, and causes of bear–human confl ict.
SUSAN A. MANSFIELD, M.S., has been a data analyst since 1983 and has studied black bears since 1999. She is a research biologist spe- cializing in black bear behavior and ecology at the Wildlife Research Institute in Ely, Minnesota. Human–Wildlife Interactions 5(2):177–191, Fall 2011
Aggressive body language of bears and wildlife viewing: a response to Geist (2011) STEPHEN F. S TRINGHAM, WildWatch LLC, 39200 Alma Avenue, Soldotna, AK 99669, USA [email protected]
Key words: attack, bear, behavior, broadside display, communication, curiosity, frontal display, human–wildlife confl icts, threat, Ursus, viewing Geist’s (2011) commentary has 3 main (Stringham 2008, Smith et al., in press). points: (1) habituation increases risk that Defensiveness is the major cause of serious or large-bodied wildlife will injure people; (2) an fatal injuries infl icted by brown bears (Ursus animal’s body language oft en provides reliable arctos) and a cause of lesser injury by black clues of impending assault; and (3) although bears (Ursus americanus) Herrero 1985, Herrero some of those clues are obvious, others are and Higgins 1995, 2003). easily overlooked by untrained people. Geist (1978) and Walther (1984) provide Whereas Geist’s emphasis is on ungulates, he much of the information on contexts for also suggests that similar behaviors by bears agonistic signals by ungulates; but litt le of it have the same signifi cance; this is an issue that has been published for bears, and that litt le requires clarifi cation. is widely scatt ered through the literature. In The importance of recognizing signals that this paper, I summarize that literature plus sometimes preface att ack is beyond questioning my own fi ndings. These are based on 22 fi eld for those of us who frequently encounter seasons observing bears and bear viewers—15 potentially dangerous wildlife, whether as seasons with brown bears in Alaska and 7 with professional or recreational observers. However, black bears in Alaska, New York, Vermont and as Geist agrees (personal communication), California. During 13 of these fi eld seasons, I that information is most valuable if one also worked part-time guiding bear viewers and knows of any benign contexts in which the observing the bears. As director of the Bear same or similar signals appear and their Viewing Association, I track and analyze broad- relative frequency in each context. Otherwise, scale patt erns in viewing. Analysis of my data a person is not only at risk from overlooking or has proceeded far enough to permit qualitative misinterpreting threats, but also from mistak- descriptions, ordinal comparisons, and order of ing benign behaviors for preludes to att ack. magnitude numerics. More precise quantitative This can cause people to overreact in ways results and methodological details will be that actually increase their likelihood of being published later. Unless otherwise stated, all assaulted, albeit defensively. references to “bears” herein refer just to Alaskan Craighead (1972) describes a classic example. brown bears and black bears. How well these Even a grizzly bear (Ursus arctos) that would fi ndings apply to other ursidae remains to be normally fl ee from a human will sometimes determined. approach. A person who does not realize that the bear is approaching out of curiosity may Viewing bears and other wildlife make the mistake of not alerting the bear (e.g., Over recent decades, viewing of wild by snapping branches or thrashing brush) ungulates, especially large carnivores, has while it is still far away, and instead try to grown from the pastime of an eccentric minority hide. This reaction increases the risk that the of North Americans to a major form of eco- bear would not recognize the situation until tourism that att racts visitors from around the it is within its att ack distance. In such a case, globe. No large carnivores are more accessible the bear’s approach, especially at a run, oft en or more charismatic than bears. The continent’s is misinterpreted as aggressive and may lead 4 most popular bear-viewing sites—Wolverine someone to run from the bear or to shoot it. Creek and Brooks River in Alaska, the North Shooting risks retaliation by the bear, a risk American Bear Center, and Vince Shute wildlife that is especially high for emergency shooting sanctuary in Minnesota—together amount to 178 Human–Wildlife Interactions 5(2)
Figure 1. At some popular viewing areas on the Alaska seacoast, viewers can legally approach brown and black bears to within 50 to 100 m. Viewers can also legally allow bears to approach as close as they want. The decision of “how close is too close?” is left to the guide. So long as viewers remain seated, bears learn to feel confi dent in approaching closely; and a guide standing up is often suffi cient to deter the bear from coming closer. roughly 70,000 viewer-days per year. Continent done from vehicles or platforms that minimize wide, the total is estimated at >100,000 viewer- exposure of humans to bears. At the >100 other days at sites where bears are reliably seen, North American sites, viewing is done on the in addition to Yellowstone and some other ground, oft en at distances of 5 to 100 m from national parks where bear sightings are much the bears, which is close enough for bears to more chancy (Stringham, unpublished report). reach the people at will (Figure 1; Stringham Whereas visitors can enjoy the Minnesota and 2007, 2008, 2009;
Figure 2. Body language associated with various combinations of competing motivations—aggression ver- sus reluctance for combat. Levels of aggression: Low (aL), Medium (aM), High (aH). Levels of reluctance: Low (rL), Medium (rM), High (rH). Top, left to right, from the upper left corner: in a confi dent, assertive, slightly aggressive mood, a bear commonly walks or stands with its face 30 to 45º below horizontal and its neck at an angle between 30 and 45º degrees above or below horizontal. As aggression increases, the mouth gapes more widely, the upper lip extends farther, and the upper canines are exposed to the oppo- nent’s view. Simultaneously, vocalizations become harsher and more prolonged until the bear is roaring. Bottom left: assuming that the function of threats is to win without chancing injury through fi ghting, a bear reduces risk that its escalating aggression will provoke attack by the opponent by aiming its jaws away from the opponent. I refer to this counter-signaling as reluctance. Bottom center: as reluctance increases, neck angle tends to drop farther below horizontal, and face angle drops towards vertical. Bottom right: aggres- sion and reluctance are both intense, signaling a highly unstable balance of motivations that can suddenly tip into either attack or submission. A bear eventually tries to de-escalate a confrontation by turning its head and jaws to the right or left, away from the opponent, watching the latter with peripheral vision only. Another form of reluctance is seen when mothers threaten cubs with lowered head to prevent them from nursing or stealing pieces of salmon. Assertive cubs respond with head-low threats.
Bear threats that even novices to fi ght, resulting in 9 combinations of the 2 can recognize motivations (Stringham 2008, 2009). Aggression Postures and gestures and likelihood of combat peak at cell aHrL (= Elements of body language commonly used aggression High, reluctance Low), where 2 by brown and black bears during agonistic bears face off with their nostrils <1 m apart, encounters with conspecifi cs have been each bruin’s head high above its shoulders, and described by Herrero (1970, 1983), Burghardt body weight centered on its legs to free its arms and Burghardt (1972), Stonorov and Stokes for grappling, swatt ing, clawing and fending (1972), Craighead (1972), Henry and Herrero off att acks. The upper lip puckers forward as (1974), Egbert and Stokes (1976), Pruitt (1976), the mouth gapes widely and is tilted upwards Pruitt and Burghardt (1977), Jordan (1974), far enough that the upper canines are exposed Jordan and Burghardt (1986), Ludlow (1976), to the opponent’s view. Each bear tilts its head Bledsoe (1987), and Stringham (2002, 2008, to the right or left so as to bett er grasp and 2009). Elements used toward fellow bears neutralize or damage the opponent’s jaws appear to be identical to those used towards (Geist 1972). Each bear may alternately raise humans. and lower its head momentarily as though Figure 2 shows a matrix of postures seeking an opening to bite the opponent’s neck manifesting low, medium and high levels of or cheek. Alternately, changes in relative head aggression and comparable levels of reluctance height may refl ect momentary changes in self- 180 Human–Wildlife Interactions 5(2) confi dence, with the currently more confi dent bear holding its head highest. Both bears typically roar loudly and continuously. As Jordan (1976), Egbert and Stokes (1976), and Bledsoe (1987) emphasize, the elements of threat behavior may be stereotyped, but the sequences, durations, and combinations of elements vary from instance to instance due in part to constant adjustment by each bear to its opponent. Only suites of actions can be grouped into relatively predictable stages (Pruitt 1976). Combat is usually preceded by head-high threats, which are usually preceded by head-low threats, which are very occasionally preceded by broadside displays. Likelihood of immediate combat is higher when Figure 3. Appeasement of a subordinate by a dominant bears face off with heads high and bear. (A) A subordinate brown bear, S1 (upper left in photo) jaws—their primary weapon—aimed threatened a higher-ranking adult male, D1, when D1 ventured too close, even though D1 did not overtly threaten at the opponent, than when their heads S1. S1’s fearful assertiveness is indicated by its moderate- are low, aiming jaws away from the aggression, low reluctance threat with head high, ears opponent, usually at the ground (Egbert back tightly against its skull, and fully gaping jaws aimed at D1. S1’s upper canines were not exposed, and much of and Stokes 1976, Jordan 1976). its weight was on its arms, rather than shifted to its legs, Lowering the jaws to ground suggesting that it was defensive and not ready to fi ght. D1 responded with combined displays of dominance and level (Figure 2, aHrH) while roaring reluctance to fi ght. D1’s dominance was indicated by its ears continuously or bellowing in rapid forward and head high, while it appeased S1 by holding his pulses can be thought of as extreme jaws at only half-gape and turned away from S1. D1’s head- high posture also kept its jaws in position to counterattack if ursine saber ratt ling. Aiming one’s S1 tried to bite. weapons away from an opponent (B) S1 was calming down, with its mouth now at only half- gape and its jaws lowered and turned aside, even though its allows one to express intense aggression body was still aimed at D1. (Photos courtesy T. Guzzi) with less risk of triggering att ack by the opponent. opponent may even sit down, likely facing Whereas head-high weapon threats normally away from the challenger. However, if the begin when the nostrils of the 2 bears are <1 opponent does not acknowledge subordinance, m apart, head-low threats may begin while the challenger may stiff en its gait, thereby the 2 bears are several meters away. Further, escalating its threat. If the opponent still fails to whereas head-high threats are virtually submit or counter threatens, then aggression is always made face to face, a head-low threat much more likely to escalate into more intense may be made from any angle from which the visible and audible threats, and, perhaps, into aggressor happens to approach its opponent. combat (Craighead 1972, Stonorov and Stokes 1972). Offensive challenges Whether or not combat occurs, confrontations When a brown bear walks deliberately typically end with gradual de-escalation of towards an opponent, escalation of aggression tensions. This culminates in each bear pointing is unlikely if the opponent acknowledges its jaws toward the ground and lowering its subordinance by backing up a few paces and head, with the loser’s head lowest. Then one turning its neck and head to the side. If the or both bears turn their head aside. If the rank approaching bear has made no overt threat diff erence is small, the loser usually turns its display (Figure 2, cells aLrL–aMrL), the head aside fi rst, perhaps aft er having backed Commentary 181
Defensive challenges When a bear with its neck roughly level (Figure 2, aMrL) defensively threatens a much higher-ranking opponent, the dominant individual may refrain from chastising its challenger and instead try to appease it by facing away from the subordinate, while holding its head at a similar height (Figures 3a and 4a). Facing away simultaneous-ly signals the dominant’s imperturbability and its benign intent. Typically, neither bear has its head high enough to reveal its upper canines. As the aggressive subordinate calms down (Figures 3b and 4b), it will Figure 4. Subordinate appeasing a dominant. (A) Defensive eventually back up and turn aggression where an adolescent male S2 threatened adult male D2. Although much of the body language in this case is like that away from the dominant, perhaps in Figure 3, there are important differences. First, S2’s head was lowering its head even if the initially higher than D2’s, indicating a brief period of high self- dominant does not. confi dence before D2’s imperturbability unnerved S1. S1’s failing confi dence is manifest in the fl attening of his ears and the lifting of This scenario is common when his tail and then defecation. Even though D2 held his head lower a mother deters an adult male than S2, he clearly dominated the encounter, never becoming ex- cited. (B) When these bears began to de-escalate, they did so by from approaching her cubs, even both lowering their heads, before either bear turned away. (C) S2’s though the male is just passing by, subordinate status was confi rmed as he sat down with his head lowered and turned partly aside as he closely watched D2 who re- not hunting her cubs. Furthermore, sumed grazing and turned away from S2, as though unconcerned even during the most intense phase with S2 as a potential threat. (D) Finally, S2 lay down, still facing of roaring match with an adult D2. Although lying down can be an extreme form of submission, it is far less common in bears than in dogs or wolves, and occurs male, a mother may momentarily only when attack risk is low, not during a tense, close encounter. turn her head aside to check on her cubs without this acknowledging up ≥1 steps. However, if the rank diff erence subordinance. is large, the loser may not dare turn aside and A bear, especially the loser, can be so physical- increase its vulnerability; so, the dominant is ly and emotionally exhausted by a confronta- left to do so fi rst. Losers almost never challenge tion that it soon sits down and may even lie a winner even during these moments of down, while remaining wary of the winner vulnerability (Craighead 1972). At this stage of (Figures 4c and 4d). Although depression is a confl ict, the movements of a subordinate bear more typical of losers than of winners, I have oft en seem stiff er than those of a dominant, seen a mother who saved her cub from a preda- the ultimate expression of stiff ness being tory male soon lie down and hardly move for immobility. Perhaps a subordinate bear, like a >6 hours, providing no care to the injured cub human, can be too afraid to move lest it trigger and ignoring pleas by both her cubs to nurse. att ack. In any event, Stonorov and Stokes (1972) found that subordinates are 4-fold (n = Audible signals 12 versus 3) more likely than dominants to turn Ursid postures indicating low to medium ag- their head and neck broadside to an opponent. gression (aL to aM), combined with medium to In the uncommon event that an infant or high reluctance (rM–rH), are oft en accompan- yearling challenges an adult, it is likely to be ied by distinctive sounds. These include 1 or 2 ignored, even as the adult watches lest the explosive woofs, followed by a series of pant cub’s mother appear to back up its threats. huff s and by jaw popping (i.e., a combination of 182 Human–Wildlife Interactions 5(2) snapping the jaws together and popping the lips (Ewer 1968). Threats can also be used to as the mouth opens). These signals may precede manipulate a social partner (e.g., an infant that or accompany the bear hopping or running insists on nursing or that keeps biting in play) forward a few steps towards the opponent, without risk of injuring the partner. terminating with a single explosive woof as In the uncommon event that a bear is motivat- the bear slams one or both hands against a tree ed to att ack a person, the att ack is more likely to or the ground, much as some ungulates do be inhibited by fear of retaliation than by con- with their hooves. This is commonly followed cern for the human. Nevertheless, when a bear by further pant-huffi ng and jaw-popping. is in a benign mood, it may go to considerable trouble to deter a person without doing harm. Threats versus attacks On several occasions, I have had a captive Those signals can all be highly intimidating bear stop me from touching it by catching the to opponents, including humans. However, skin of my hand in its incisors, then lett ing go, only a minority of such displays leads to att ack, without breaking or bruising the skin. Kilham especially if the displaying bear is appeased by (2002) refers to restrained bites to a human or its opponent, that is, by a human giving it more fellow bear as message bites. Restrained swats, space or ceasing to threaten it (Leslie 1968, with claws lift ed so they do not make contact, Stringham 2009; Herrero 1972 a, b; Herrero et al. are also used to deliver messages. On occasion, 2011). Each summer for the past few years, Ann a wild black bear has deterred contact by my Bryant (director, BEAR League, Lake Tahoe, hand by directing its gaping mouth at me, even California, personal communication) and her though the bear was otherwise content have its assistants have chased black bears out of yards body within inches of me or sometimes pressed and homes at Lake Tahoe on the California- against me. Nevada border, without suff ering even slight In lieu of inhibition, an angry animal would injury, despite being threatened in the above theoretically just att ack without preamble ways on hundreds of occasions. Rogers, (Lorenz 1966). I have seen numerous instances Mansfi eld, and their colleagues have faced of a black or brown bear suddenly lash out these displays by black bears many times, none at a conspecifi c standing beside it feeding on of which has ever caused them even moderate an animal carcass or an insect laden log. If injury, although they have rarely suff ered any warning was given, it was not apparent scratches and bruises. Other biologists (e.g., to human eyes or ears. In each case, the bears Faro, personal communication) and guides (e.g., were siblings or constant companions. Where B. Josephs, B. Wilde and K. Fredriksson, guides, the 2 bears diff ered appreciably in size, it was Katmai Coastal Bear Tours, personal com- usually the larger that att acked the smaller. munication), myself included, have escaped According to the same theory, a fearful animal being att acked, despite having faced hundreds that is not inhibited from withdrawing (e.g., by of threats, sometimes including short rushes or its own aggression or by expectation of att ack hop-slams, by brown bears on the seacoasts of from the rear) would just fl ee. Some bears run Alaska and British Columbia. as soon as they detect a person nearby; others One reason that att acks so rarely follow threat approach and threaten a person, then stalk off displays is that threats are not announcements stiffl y, occasionally spinning back to face the that an animal plans to att ack, but att empts by person, threaten, and continue to move away the animal to achieve its goals by manipulating for a few hundred meters away before suddenly its opponent, without risking a fi ght (Geist accelerating into a run, sometimes continuing 1978). Although an off ensive threat does warn for miles and disappearing from sight (Russell that att ack is imminent if its goals are not met 1972). (e.g., unless a competitor retreats or surrenders There is no indication that bears so clearly food), the aggressor seldom follows through, reveal fear, anger or frustration during preda- perhaps out of fear. Att ack is even less likely tory att empts (Herrero 1985), despite the following a defensive threat, which warns that likelihood that each of these emotions sometimes the individual will, in theory, retaliate only if occurs while trying to kill powerful prey, such att acked, threatened, or otherwise provoked as moose (Alces americanus), caribou (Rangifer Commentary 183 tarandus) or a fellow bear. I have seen video Ungulates versus bears footage and photos of an adult male walking up to a distracted subordinate and att acking Cryptic displays without preamble. In a 1997 incident at Brooks Recall that the focus of Geist’s (2011) paper Falls, in Katmai National Park, the aggressor was not such obvious threats, but what he call- quickly began eating the subordinate, ripping ed “silent signals” that only trained observers fl esh from its back; the adolescent hardly resisted are likely to recognize as such. Three of the as though immobilized by terror and shock. In most common of these are broadside displays, a 2010 incident at the Russian River Falls, on the averted gaze, and deceptive grazing. Kenai Peninsula, the adult male tore off a patch Even novices are likely to recognize the threat of skin from the victim’s rump roughly 0.3 m implied when a cervid or bovid faces them and in diameter, then held on, as though trying directs its antlers or horns at them. However, to force the adolescent underwater. Again, according to Geist (1978, 2011) and Walther the victim did not fi ght back. This continued (1984), novices are less likely to recognize the several minutes before the adult male desisted signifi cance of a broadside display. When such and shift ed to fi shing on salmon. At no time did a display is performed by 2 ungulates, they the att acker make a detectable visible or audible walk parallel to one another or circle in reverse threat. parallel positions, with each animal’s head In any att empt to assess att ack risk, it is toward the opponent’s tail. critical to keep in mind that probability that Even when a broadside display is directed a threat display will be followed by att ack toward people, “the displayer does not ap- is NOT directly related to intensity of the proach directly, but at a tangent; that is, it display; sometimes just the opposite. This is circles onto the object of display” (Geist 2011). akin to the situation between 2 men or boys People could easily mistake this for the animal insulting one another, where the louder and just walking past them—a misinterpreted longer the harangue continues, the less likely impression augmented by the tendency of a it is to end with fi ghting. In fact, it can serve displaying ungulate to direct its gaze or at as an alternative way of lett ing off steam. At least its muzzle away from the conspecifi c least, that was my own experience as a youth, or human opponent, as though uninterested when fi stfi ghts occurred several times a day. in the opponent. Threat is particularly hard Rogers and Mansfi eld, thus, refer to intense to recognize when an ungulate grazes as it pant-huffi ng, jaw-popping and hop-charging approaches an opponent. as blustering. One hypothesis is that these The danger to someone who misinterprets a signals have become so ritualized that they, broadside display is greatest with species like like human cussing or dog barking, reveal less mountain goats (Oreamnos americanus) that about intentions than about emotions. normally att ack from a broadside position, Any att empt to determine how well a given rather than head to head, as with bighorn sheep display predicts assault should distinguish (Ovis canadensis; Geist 1964). A mountain goat how oft en assault is prefaced by the display lowering its head and turning it away from an versus how oft en the signal prefaces aggression opponent might just be cocking its neck and versus other behavior. Even if all assaults were shoulders in preparation for att ack. preceded by a certain gesture, this would not Geist suggests that broadside displays, avert- preclude that same gesture from preceding or ed gaze, and deceptive grazing have the same accompanying other actions. Indeed, elements signifi cance in bears as in ungulates. However, of aggressive body language are common even if those behaviors do occasionally precede during play (e.g., puckered upper lip, ears assaults—if only on a fellow bear—they are back against the skull, head tossing, biting, not diagnostic of pending assault. In situations and wrestling). The fact that a display is typical where Rogers and Mansfi eld (personal of aggression does not mean it is diagnostic communication), and I have observed black thereof. Diagnosis requires recognition of and brown bears, those behaviors are orders of entire gestalts of signals and of their contexts. magnitude more likely to accompany nonvio- 184 Human–Wildlife Interactions 5(2)
to head threats than broadside dominance displays. I have seen both dogs and wolves begin fi ghting while they stood head to head, but not while they were in full anti-parallel orientation, as each individual sniff ed the anus of its opponent. During thousands of bear encounters, I have experienced no more than 10 occasions when a black or brown bear has walked past me, gott en partly or fully behind me, then rushed toward me several paces before terminating the rush, sometimes by slamming its hands on the ground. There was no way to tell whether the bear would have made contact had I not turned to face it; but taking my eyes off the animal Figure 5. Old Snagletooth (right) and a second likely gave it confi dence, much as resuming eye male (not visible in photo) were strutting in circles contact halted its approach. However, in none of around one another, while an estrus female grazed these cases was the bear making a stereotyped nearby. Note how Snagletooth’s arms and legs are spread much wider than those of the female, who is broadside display. The only forewarning of the in a normal quadrupedal stance, with her right and impending threat was that, in each case, the left feet separated <0.5 m, whereas his extended 1.2 m. The male’s body, especially his hindquarters, bear walked toward me much more directly and are covered with mud from wallowing where he perhaps more stiffl y than normal, and with its had just urinated, such that he reeked of his own pheromones. eyes locked on me. A few colleagues have told me of similar experiences, and Jordan (1976) lent interactions with conspecifi cs or with reports one with a black bear. Seldom have I people. When att acks do occur, they are typically seen 1 bear att ack another that way, and it was prefaced by the overt displays described earlier; always with a single bite or swat that caused no or the bear charges without warning, whether visible injury. defensively or off ensively. Sudden att acks seem Bears make at least 2 forms of stereotyped more typical of brown bears than of black bears. broadside displays, both of which are highly distinctive and not readily mistaken for simply Broadside displays strolling past a person. Geist (2011) states: “In both ungulates and bears, the most important [cryptic] signal to Sumo strut watch for is the dominance display. … [T]he Judging from experiences with brown bears usual dominance display of large terrestrial in coastal Alaska, the most common form of mammals, primates excluded, is a broadside broadside display exhibited by this species display…..” Geist (1978) and Walther (1984) is the sumo strut. The bear walks forward, describe broadside displays by a spectrum of urinating. Urine fl ows onto its legs and runs ungulate genera. Except in those species, such down the fur, presumably picking up its scent, as mountain goats that fi ght standing side by which is then ground into the soil by a repeated side, a broadside display seldom leads directly twisting motion of the feet. Its arms and legs are to fi ghting. The uncertainty of whether it will do widely spread and its knee and perhaps elbow so adds to the display’s capacity to intimidate joints stiff ened (Figure 5), as in the ceremonial rivals. However, in the normal course of events, preface to human sumo wrestling. The jaws of if a dominance contest cannot be sett led with a sumo-strutt ing bear are aimed at the ground, broadside displays, the animals escalate to not toward the opponent. frontal weapon threats, and only if that fails to Sumo strutt ing is almost always made by establish a winner do they resort to fi ghting. pairs of rival adult males during the breeding One would likewise suspect that among season. Unlike ungulates and canids that circle carnivores, which normally fi ght head-to-head, one another within striking distance, sumo- combat is much more likely to follow head strutt ing bears are usually separated by 2 to 10 Commentary 185 body lengths. In the >100 cases of strutt ing that with each step. Her legs were not locked. But I have observed, never has a bear att acked from otherwise, as in sumo strutt ing, urine ran down a broadside position. Seldom has a bear gone her legs, and her body shook with each step. from a broadside display into a head-high, The goosestep and slide, which seems frontal threat and then begun fi ghting. transitional between stomp walking and All cases of sumo strutt ing that I observed sumo strutt ing, was frequently triggered by a have been performed by an adult male toward human, but was not obviously oriented at the another adult male, never by or towards any human. According to Jordan (1976), each bear’s other age-sex class, although an estrus female orientation relative to a person seemed random. is oft en nearby, raising the question of whether In some cases, the bear was in an enclosure and sumo strutt ing can serve a courtship role. was not free to circle the person or to walk far Only twice have I seen a female (in each case a in any direction; so, the appearance of random juvenile) perform something that resembled a orientation may have been an artifact. Or it may mild, truncated sumo strut, and then for just a simply be an advertisement of the bear’s mood few steps while retreating facing away from me. that is broadcast “to whom it may concern” S. Bryant (director, Bear League, Lake Tahoe, rather than to a specifi c opponent. This display California, personal communication) has twice was made by both males and females. It might seen 2 mother black bears sumo strutt ing at one be the same display that I earlier likened to a another. truncated sumo strut when I saw it made on 2 I know of only 3 cases of sumo strutt ing occasions by a juvenile female brown bear. being aimed at a person. V. Geist (personal When a brown bear sumo struts, it may communication) twice observed this when he occasionally produce slide tracks similar drove a large adult male black bear away from to those made by a stomp walking black him. Neither of those broadside displays was bear, further suggesting that sumo strutt ing followed by frontal threats, much less by att ack. and stomp walking may be polar forms In the third case, an adult male brown bear, of a display with several intergradations. Old Snagletooth (Figure 5), strutt ed directly towards me just aft er losing a confrontation Cowboy walk with a larger male over an estrus female. When Black bears and, possibly, brown bears also I spoke, “Don’t do that,” he immediately swung make a face-to-face display where the forearms sideways to me, continuing to strut only briefl y are lift ed only several centimeters before the before walking off in a normal gait. In some hands are slammed against the ground, step cases, strutt ing seems to be a way of enhancing aft er step, accompanied by pant-huffi ng. a bear’s self confi dence, as do the associated This display typically ends with a hop-slam, behaviors of wallowing or tree marking. accompanied by an explosive woof. This third form of stiff -legged gait is called cowboy walk Stomp walk because the elbows are sometimes turned Black bears also exhibit a second form of out so far that the arms resemble the legs broadside display, dubbed stomp walking of a bowlegged horseman. Each time I have by L. Rogers and S. Mansfi eld (personal seen this, it accompanied a head-low threat. communication). As a bear walks forward, with its head nearly level with its shoulders, Direct and diagonal charges each forearm is alternately lift ed to near When a bear makes a full-fl edged charge, it horizontal position; then that forepaw typically runs with its neck and spine aimed is slammed down against the ground, at the opponent. During some charges, the whereupon it may slide forward <1 m. spine remains fairly level. In other charges, the spine oscillates up and down in kind of a Goosestep slide rockinghorse motion; indeed, the bear may seem Jordan (1976) describes a related behavior by to be bouncing as much as running forward. a female, except that her forearms were locked, My impression is that the greater the degree and she moved forward in something like a of rocking, the less likely the bear is to make goosestep, with her hands sliding forward physical contact with its opponent. Indeed, 186 Human–Wildlife Interactions 5(2) rocking may serve to increase its apparent size, All of those behaviors, except perhaps the making it more intimidating to its opponent. An predatory crouch (Shelton 2001), are seen in even less assertive brown bear will sometimes other behavioral contexts. So distinguishing advance several paces with a rocking hop, instances of att empted predation from other during which its spine and neck are diagonal to motivations relies on gestalts of actions plus the opponent, sometimes at just a slight angle contextual cues, which are beyond the scope of and at other times at >45º angle. Stonorov and this paper. Stokes (1972) interpret angling of the body as a Some forms of predatory approach by a sign of ambivalence. Perhaps the angle increases carnivore might indeed be mistaken as benign along with strength of the motivation to fl ee, or at searching or curiosity, exemplifi ed by coyotes least to display broadside. A frustrated bear will (Canis latrans; Baker and Timm 1998) and wolves sometimes hop in place without approaching (Canis lupus; Geist 2007, 2011). Geist notes that its opponent, perhaps while fl inging its head predatory curiosity is commonly manifest in back and forth and casting saliva far and wide. “att ention to and following” or approaching another animal or person. This may culminate Predatory body language in physical contact and perhaps licking or None of that body language is seen during nipping potential prey, eventually followed by predation except for running, with or without att ack (Geist 2007). However, he provides no a rocking motion. Bears that run through a other clues for distinguishing predatory versus stream to capture salmon move with a litt le nonpredatory curiosity among wolves or any rocking motion through water that is less than other large bodied carnivores, or how oft en belly deep. But as depth increases, so does the each occurs. height with which a bear lift s its forequarters In the thousands of times that I have observed before landing on its forefeet. Elevation of people, including myself, being followed or the forequarters not only lessens the eff ort of approached and investigated by a brown or plowing through the water, but it may provide black bear, none of those bears has ever made bett er visibility without having to stop and a recognizable att empt to test the focal person stand bipedally. The higher the angle from as prey. The only bears that mouthed any which a bear or person looks into water, the less person were playful cubs. So long as a person visibility is impaired by surface refl ections. does not try to touch a bear, injuries have been When hunting elk or moose calves, a bear rare and usually limited to scratches; touching may search by standing upright to see farther sometimes triggers more intense bite or clawing, and to catch airborne scent, or by walking but seldom prolonged mauling (Herrero 1985). quadrupedally while following scent in the air People who want to avoid a potentially or on the ground. Once prey is located, it may dangerous animal should indeed be especially be circled or stalked, as the bear hides behind wary if the animal stares at them >30 seconds available cover with its gaze locked on the prey without sign of being alarmed or if it approaches until the bear is close enough to att ack. In rare or follows them with its eyes locked on them. cases, a bear will stalk prey in a crouched posture However, no one should overreact by jumping reminiscent of an African lion (Panthera leo; to the conclusion that this reveals either Pezzenti 2001) or crawl forward on its forearms agonistic or predatory aggression. There are with its chest against the ground, as observed many reasons besides aggression for a bear on Kodiak Island on 2 occasions by deer hunter walking or even running toward a person or B. Garett (personal communication). There following the person. For example, I have had have also been numerous reports of polar bears run at me to initiate play or to take shelter bears (Ursus maritimus) crawling or swimming behind me from other bears. So, too, bears of toward seals; an example of this behavior can all ages sometimes walk up to within a few be seen in BBC footage on YouTube (
Which displays signal threat or some of these displays (e.g., pant huffi ng, dominance? woofi ng, and jaw popping) are made by bears I have interpreted virtually all behaviors of all ages and social ranks, whether they are described thus far as agonistic in the contexts facing an opponent or alone. It is not only adult considered. Jaw-popping seems to be an males, but also by adult females and adolescents intention movement to bite, comparable to jaw of both sexes that stomp walk, contrary to sumo snapping in some canids or perhaps to molar strutt ing and ungulate dominance displays. So, grinding in moose and some other ungulates, stomp walking and pant huffi ng may not, in even though these ungulates no long use teeth fact, be dominance displays. as weapons (Stringham 1974, Geist 1978). The fact that a display is associated with Rushing toward an opponent is intimidating agonistic activity does not prove that the display in a wide range of mammals because the itself is agonistic. This is illustrated by the aggressor is both coming closer and appears to exaggerated gait used by sumo wrestlers just suddenly increase in size (Geist 1978). When a prior to a match, the gait for which ursine sumo rush terminates with swatt ing the ground or a strutt ing is named. A naïve observer might tree, accompanied by an explosive woof, this jump to the conclusion that this is a dominance not only provides a sudden increase in noise, display. Actually, it is a religious purifi cation another widespread means of intimidation ceremony (Benjamin 2010). (Geist 1978), but it demonstrates the animal’s This issue is neither just academic nor power. Also, substrate slamming may draw semantic, but highly pragmatic. For if pant att ention to the bear’s hands and its claws, and huffi ng, woofi ng, jaw popping or scent it can be interpreted as an intention to swat marking are labeled as threats, which in the the opponent. For the same reasons, stomp broadest sense include dominance displays, walking and cowboy walking appear to signal then, any animal making them in the presence intention to slam an opponent. Furthermore, of a human might be condemned for daring to both sumo strutt ing and sometimes stomp threaten a human. Many bears have been killed walking display the bear in broadside, which for no worse crime. Rather than foster such maximizes its apparent size, similar to what misunderstandings, some biologists prefer one sees in the majority of mammals and some referring to these displays as signs of stress other vertebrates (Geist 1978, 2011). When a bear (e.g., Herrero et al. 2005). near me tensely claws the ground or chews on By far, the most thorough analyzes of bear a log while it stares at me, I likewise interpret att acks are those published by Herrero and those as threats to claw and bite me, even if his colleagues (Herrero 1980, 1985, 2002; those same bears, when later frightened by the Herrero and Higgins 1999, 2003; Herrero et appearance of a larger bear, then move behind al. 2011). These reports include cases where me for protection. This is perhaps reminiscent nonpredatory att acks followed frontal threats; of human adolescents who are aggressive but, no mention is made of att acks that followed toward adults, until need for adult assistance a broadside display. Again, predatory att acks shift s them into a more juvenile role. were not prefaced by any kind of display. Nevertheless, there is reason for caution in Geist’s statement that an ursine broadside labeling any of these displays as threats. First, display is a “signal of high danger” is certainly stomp walking and sumo strutt ing, along with true if “high” refers to severity of injury if the wallowing and tree rubbing, are also forms display is followed by att ack. However, in all of scent marking. Mammals commonly use contexts where I have seen it, it indicates low distinctive postures or gestures for drawing probability of att ack. That said, Geist is correct visual att ention to where and when they scent that any dominance display by a bear, either mark, for instance with urine or feces. L. Rogers frontal or broadside, warrants extra caution. and S. Mansfi eld (personal communication), If the bear is acting off ensively (e.g., to usurp thus, hypothesize that stomp walking and the space occupied by people or to steal their perhaps sumo strutt ing may have become so food), the people might best leave or dominate ritualized that they are no more threatening the bear by using appropriate body language. than the leg lift ing of a male dog or wolf. Second, A group of viewers oft en achieves dominance 188 Human–Wildlife Interactions 5(2) accidentally just by failing to react, if only out For example, at Wolverine Creek in Alaska, of ignorance that a bear is trying to intimidate both brown and black bears commonly rest them. A lone person can sometimes achieve the on shore or fi sh for salmon within 1 to 10 m of same thing by seeming imperturbable. But this several skiff s fi lled with people. These bears takes proverbial nerves of steel and does not are usually careful to avoid looking directly at always work, in which case one may have to people, much in the manner of submissive dogs rely on other tactics, such as those detailed by (Stringham 2008; Figure 6). At sites with fewer Stringham (2009) or by using pepper spray. visitors, bears commonly investigate people Withdrawal is also 1 option for appeasing a much as they investigate one another, grazing defensive bear (e.g., one defending an animal as they move ever closer. If they stare directly carcass or protecting small cubs). However, if a at people, they usually do so when alarmed and person’s goal is to observe the bear, a more use- from distances >50 m. ful tactic may be to assure the bear that it is in When a bear is approached by a higher- no danger. Viewers commonly appease bears by ranking opponent that makes no weapon kneeling, sitt ing down, or lying down (Figure 1; threat, the subordinate may turn its head aside Stringham 2009). Although a domineering bear (perhaps aft er sitt ing back on its haunches), can also sometimes be appeased, this should not watching the dominant with peripheral vision be done in a manner that rewards its bullying. (Stonorov and Stokes 1972). So, too, when peaceful bears pass one another, Eye contact either because they are walking in opposite Geist emphasizes the importance of main- directions along a trail or because of mutual taining eye contact with any potentially investigation, they commonly avert their gazes dangerous large mammal. He refers to att acks and watch each other peripherally. Averted during a lapse of eye contact when someone gaze is especially important when 1 bear runs thought that a passing ungulate was ignoring in the direction of another, perhaps to catch a them. I earlier described similar experiences salmon or to escape an enemy. When a rapidly with bears. I personally always try to maintain approaching bear aims its eyes away from direct eye contact with a domineering bear, another individual (thereby exposing a crescent but may avert my gaze if the bear is defensive of whitish sclera of the outside of the closest eye), (Stringham 2009). Loss of eye contact also seems this can signal that the approaching bear is not to be a factor triggering predatory att acks by threatening the other individual. I am not sure cougars (Puma concolor) and other large felids how oft en bears recognize this distinction, but I (Etling 2001). have found it reliable in hundreds of cases of a Geist notes that dominance displays by bear walking or running toward me (Stringham ungulates are commonly made with the eyes 2009). Poulsen (2009) reports that a captive bear averted; the opponent is viewed through the uses the direction of its gaze to direct keepers rear of the eye. His description does not reveal to the focus of its att ention, perhaps food or whether the averted gaze is a consequence of a toy that the bear cannot reach or something antler or horn orientation. For example, if these that the bear wants removed from its cage. weapons are pointed toward an opponent, is the chin necessarily pointed away? Deceptive grazing The eyes of a cervid or bovid are oriented Geist notes that mountain sheep rams somewhat to the side of the head, enabling these sometimes att ack just aft er grazing up to a rival, animals to see behind themselves. Bears, of as though grazing, like averting its gaze, were course, do not. They cannot watch an opponent a deception that allowed the att acking animal if their head is averted much past broadside to to approach and catch its opponent off guard. the opponent. In that position, the opponent By contrast, in thousands of cases of bears is seen peripherally. The mere fact that a bear feeding near one another, I have never seen averts its eyes is not an indication that it is grazing immediately precede att ack. At most, making a dominance display. On the contrary, when the movements of 2 bears bring them this is normally a sign of appeasement in all uncomfortably close to one another, one may situations where I have observed bears, except make a short rush (perhaps only 1 or 2 steps) for sumo strutt ing and stomp walking. Commentary 189 toward the other bear, which is more likely to retreat than to reciprocate. In other cases, where 2 grazing bears tolerate a mutual approach, they may pass within a few meters of each other without ceasing to feed; or they may raise their heads, walk together, and begin sniffi ng one Figure 6. Adult female brown bears fi shing for salmon avoided looking another’s faces. In the directly at boats fi lled with people a few meters away. In photo B, the bear is case of adolescents or watching the people peripherally while facing away from them. pre-adolescents, this may eventually lead to in fact it is rarely followed by aggression, is mouthing each other’s cheeks, then to playful easily discredited in the public eye. Even if one wrestling. Accordingly, when a bear grazes up to cannot provide a precise numerical estimate of me, while watching me peripherally, I interpret risk (e.g., 1 att ack per 500,000 viewer days), one this as a sign that it is curious or playful. Cases might provide comparisons with equally severe where the bear just goes through the motions injury from more familiar hazards (e.g., playing of feeding, seldom biting off vegetation or Russian Roulett e versus slipping and falling ingesting it, suggest that the behavior is either versus driving without a seatbelt fastened). a ritualized or insightful means of signaling Through guilt by association, crying wolf benign intent, not veiled aggression. can also discredit other warnings and safety recommendations as mere superstitions, as Risk the late Timothy Treadwell and many other An unfortunate trait of hazard analysis viewers, hunters, and anglers have voiced based on scant information is that one ends to me. This is but one more example of the up emphasizing the possibility of tragic constant challenge safety advisors face in try- consequences without being able to quantify ing to protect the public against low frequency their probability even ordinally, much less on but high consequence hazards. an interval scale. Interval analysis also is limited People seldom respect warnings contradicted to a narrow range of conditions from which it is by their own experience, however limited. One diffi cult to extrapolate. For example, consider tactic for curbing skepticism is to become much Herrero et al.’s (2011) fi nding that of 36 black bett er at identifying the conditions that govern bear att acks that killed a person, 92% of the the degree of risk, as Matt son et al. (2011) have killers were adults or adolescent males. What done with particular sophistication regarding does that reveal about the relative risk of being cougars. For example, what environmental, injured by male versus female black bears in social, or physiological factors (e.g., stage of the regions where they are especially shy towards reproductive cycle) might enable an observer people, perhaps because shy bears have been to distinguish instances where a broadside the most likely to survive hunters? Again, the display, averted gaze, or grazing represents mere fact that some trait is commonly associated high att ack risk versus negligible risk? Suppose with agonistic or predatory aggression does not hypothetically that sumo strutt ing toward a mean that it is diagnostic of aggression or even human were followed by att ack only 1 in 10,000 most commonly seen in that context. times when all cases are considered, but in 10% Even if one cannot yet quantify how well a dis- of those cases where the bear is a previously play or situation predicts att ack, one should be dominant male who has just lost a fi ght with cautious of advising people on the consequences another male in competition for an estrus of this vagueness. Any implication that some female. The latt er generality could be more factor is a good predictor of aggression, when readily tested than the former. As uncertainty 190 Human–Wildlife Interactions 5(2) narrows, credibility rises. The more we know, Literature cited the more closely management can be tailored Baker, R. O., and R. M. Timm 1998. Management to avoid high-risk situations without unduly of confl ict between urban coyotes and humans constraining public freedom to enjoy wildlife in southern California. Pages 229–312 in R. O. and wildlands. For example, in national forests Baker and A. C. Crabb, editors. Procceedings where bears abound, is risk of att ack on bicyclists of the Vertebrate Pest Conference. University or people walking dogs high enough to warrant of California, Davis, California, USA. managers forbidding those activities? Benjamin, D. 2010. Sumo: a thinking fan’s guide to Japan’s national sport. Tuttle, North Claren- Conclusions don, Vermont, USA. The intensity of research on body language Bledsoe, W. T. 1987. Brown bear summer: life that characterized early ethology has, among Alaska’s giants. Dutton, New York, New unfortunately, waned in the face of newer York, USA. theoretical priorities. Until recently, few Burghardt, G. M., and L. S. Burghardt. 1972. researchers or wildlife managers recognized Notes on the behavioral development of two the pragmatic value of ethological knowledge female black bear cubs: the fi rst eight months. for people viewing large, potentially dangerous Ursus 255–273. wildlife, much less that viewing would become Craighead, J. 1972. Comment during a panel dis- so popular. At least occasionally, viewer safety cussion on bear behavior. Ursus 2:245. may depend critically on being accompanied by DeBruyn, T. D., and T. S. Smith. 2009. Manag- a specialist (e.g., interpretive guide or ranger) ing bear viewing to minimize human impacts who understands enough about the behavior on the species in Alaska. Chapter 7 in J. Hill, of each species to distinguish a wide range of editor. Ashgate Publishing, Farmham, Surrey, motivations and who knows how to respond United Kingdom. appropriately to each. We should not wait Egbert, A. L., and A. W. Stokes. 1976. The social until more viewers are mauled before we begin behavior of brown bears on an Alaskan salmon elevating the qualifi cations of viewing guides stream. Ursus 3:41–56. and managers to the levels of professionalism Etling, K. 2001. Cougar attacks: encounters of the long since achieved for hunting guides and worst kind. Lyons Press, Gilford, Connecticut, managers. Biologists should compile knowledge USA. on behavior of charismatic wildlife into Ewer, R. F. 1968. Ethology of mammals. Plenum, multimedia safety manuals, with elementary New York, New York, USA. versions for casual viewers as well as detailed Geist, V. 1964. On the rutting behavior of the moun- volumes for professionals (e.g., Stringham tain goat. Journal of Mammology. 45:551–568. 1974, 2002, 2008, 2009;
tation in American black bears (Ursus ameri- nication in terrestrial carnivores: mustelidae, canus) and brown and grizzly bears (U. arctos). procyonidae, and ursidae. Pages 767 –793 in Ursus 2:221–231. T.A. Sebeok, editor. How animals communi- Herrero, S. 1972b. Comment during a panel dis- cate. Indiana Univiversity Press, Bloomington, cussion on bear behavior. Ursus 2:247. Indiana, USA. Herrero, S. 1983. Social behavior of black bears Poulsen, E. 2009. Smiling bears: a zookeeper ex- at a garbage dump in Jasper National Park, plores the behavior and emotional life of bears. Ursus 5:54–70. Greystone, Vancouver, British Columbia, Can- Herrero, S. 2002. Bear attacks: their causes and ada. avoidance. Lyons and Buford. New York, New Russell, R. 1972. Comment during a panel discus- York, USA. sion on bear behavior. Ursus 2:248. Herrero, S., and A. Higgins 1999. Human injures Shelton, J. G. 2001. Bear attacks II: myth and re- infl icted by bears in British Columbia 1960– ality. Pallister, Hagensborg, British Columbia, 1997. Ursus 11:209–218. Canada. Herrero, S., and A. Higgins 2003. Human injuries Smith, T. S., S. Herrero, C. S. Layton, R. Larsen infl icted by bears in Alberta 1960–1998. Ursus and K. R. Johnson. (in press). Effi cacy of fi re- 14:44–54. arms for bear deterrence in Alaska. Journal of Herrero, S., A. Higgins, J. Cardoza, L. I. Hajduk, Wildlife Management. and T. Smith. 2011. Fatal Attacks by American Stringham, S. F. 1974. Mother–offspring relations black bear on people: 1900–2009. Journal of in moose. Naturaliste Canada 101:325–369. Wildlife Management 75:596–603. Stringham, S. F. 2002. Beauty within the beast. Herrero, S., T. Smith, T. D. DeBruyn, K. Gunther, Seven Locks Press, Santa Anna, California, and C. A. Matt. 2005. From the fi eld: brown USA. bear habituation to people—safety, risks and Stringham, S. F. 2007. Bear viewing in Alaska. benefi ts. Wildlife Society Bulletin 33:362–373. Falcon Press, Helena, Montana, USA. Jans, N. 2005. The grizzly maze: Tim Treadwell’s Stringham, S. F. 2008. Alaska magnum bear safe- fatal obsession with Alaskan bears. Dutton, ty manual. WildWatch, Soldotna, Alaska, USA. New York, New York, USA. Stringham, S. F. 2009. When bears whisper, do Jordan, R. H. 1976. Threat behavior of the black you listen? WildWatch, Soldotna, Alaska. bear (Ursus americanus). Ursus 3:57–63. Walther, F. R. 1984. Communication and expres- Jordan, R. H., and G. M. Burghardt. 1986. Employ- sion in hoofed mammals. Indiana University ing an ethogram to detect reactivity of black Press, Bloomington, Indiana, USA. bears (Ursus americanus) to the presence of humans. Ethology 73:89–115. Kilham, B., and E. Gray. Among the bears: raising STEPHEN F. STRINGHAM is an adjunct professor at the University of Alaska–Anchorage, orphaned cubs in the wild. Holt, New York, New director of the Bear Viewing York, USA. Association, and president of WildWatch, a consulting Leslie, R. F. 1968. The bears and I. E.P. Dutton, and research fi rm. He has New York, New York, USA. studied communication, Lorenz, K. 1966. On aggression. Bantam, New aggression, and human– wildlife interactions with York, New York, USA. bears and ungulates since Ludlow, J. C. 1976. Observations on the breeding 1969. His broader interests include the role of cognitive of captive black bears. Ursus 3:65–69. innovation in adaptation by Mosolov, V., and T. Gordienko. 2004. In memory of wildlife to changing environ- rd ments. (Photo courtesy K. Vitaly Nikolayenko—his 33 fi eld season. Inter- Fredriksson) national Bear News 13:6. Pezzenti, J. 2001. Shooting bears: the adventures of a wildlife photographer. Rizzoli, New York, New York, USA. Pruitt, C. H. 1976. Play and agonistic behavior in captive black bears. Ursus 3:79–86. Pruitt, C. H, and G. M. Burghardt. 1977. Commu- Human–Wildlife Interactions 5(2):192–196, Fall 2011
(Editor’s note: Following is the author’s rebutt al of responses made by Lynn L. Rogers and Susan A. Mansfi eld (2011), and Stephen Stringham (2011) to his commentary, “Wildlife habituation: advances in understanding and management application”, which appeared in Human–Wildlife Interactions 5:9– 12.) Response to Rogers and Mansfi eld (2011) and Stringham (2011)
VALERIUS GEIST, P.O. Box 1294, St. M, Port Alberni, British Columbia, V9Y 7M2, Canada [email protected]
Three valued colleagues, extremely then let them touch and lick a piece of rock knowledgeable of bear behavior, have taken salt I held in hand. This they licked eagerly, at exception to some of my writing. I am grateful which time I placed my fi ngers on their nose to be able to reply. There are a number of and then proceeded to systematically touch points of contention. Regarding habituation, and stroke their faces till they allowed me to I am well aware of the defi nitions proposed, clear hair off the small aluminum ear-tags that but I fi nd them wanting. How does “a waning park wardens had placed there earlier, usually of responses to a repeated, neutral stimulus” when the sheep were lambs. They tagged adult diff erentiate adequately between habituation sheep by slipping the ear-tag over the lower and taming? Put another way: how could one ear and clamping down, releasing the pliers at disprove the claim of Rogers and others that once as the sheep bounded back, shook its head they are working not with habituated, but with and came back and resumed licking the salt. tame bears? Bears do tame, aft er all, quite easily. I tagged lambs by hunching beside a female But if they tame, then how does that diff er from while it licked salt. As the lamb approached, habituation? I touched it on the breast until it accepted the I experienced working not only with human hand, then it was gently lift ed up right habituated, and also with thoroughly tamed, but beside the female’s head. No lamb protested. free-ranging mountain sheep (Ovis canadensis). Tags were clamped into the ears, and the lamb Further, the animal may continue exploring the was slowly and gently released, the female observer not only when habituated, but also licking salt all the while. Thus, no drugs, traps, when tame. Therefore, even tameness may be or wrestling to the ground of panic-stricken a state of unconsummated exploration. I have animals was necessary. I could freely walk up observed free-roaming sheep in 4 stages of to the tame sheep and touch them. That is why acquaintance: (1) those that I saw at a distance I know, for instance, that bighorns are ticklish. with spott ing scope and binoculars; (2) those The tame sheep, otherwise, went about their that I habituated to my presence till they ignored daily business much as they had when merely me and went about their daily lives (very much habituated. as Rogers and Mansfi eld described it for their This continued for nearly 2 years, but, then, work with black bears [Ursus americanus]); (3) sheep began a new phase of interaction: they those that I tamed systematically; and (4) those started including me into their social system, that proceeded to address me as a conspecifi c. with the females treating me as a super-female, It may be worth examining this 4-stage and the rams as a rival. This last phase began progression, as it was unexpected. with females and lambs associating with me, First, the changeover from habituation to using me as a center of their activity. This taming was initiated always by the habituated was followed by them taking notice of my sheep. It began when the sheep, aft er observing departures from the herd in the evening, me noticeably, approached me and began followed by an old female running to me then to explore me physically. They sniff ed my blocking my further progress by body contact, clothing, touched it with their muzzle and very much like a lamb blocking a female before licked at it. I allowed this to happen and that suckling. I could play hide-and-seek with the Commentary 193 sheep and discover that they did not simply hop forward and at once continue grazing. follow where I disappeared, but, they had a Aft er that he was just fi ne all day long. Come conception of where I should reappear and they morning, the whole procedure was repeated. awaited me there. They were spatial strategists. This ram surprised and knocked one of my However, they would also track me—their colleagues unconscious. Fortunately, the ram nose to the ground—for hundreds of yards till soon disappeared, never to be seen again. they found my hiding place. Further, bands of Subsequently, I took pains to insure that none females followed me into the valley. Soon aft er of the animals I observed would be anything leaving the open hills, they clustered behind but habituated. There is no way to handle the me and assumed body contact. They could be att ack of any male deer, elk, moose, bison, etc. I, led anywhere, but they broke into a run when thus, do not counsel working with free-ranging, I returned them to within 100 m or so of their tame, large mammals. As an aside, I have no home range. doubt that the proclivity for taming by bighorn Then the fi rst ram addressed me suddenly sheep was known to native people, and this with its head high horn display, one of 2 horn allowed them to mange the sheep. Petroglyphs displays, dominance or status displays. This in the canyons of Utah and elsewhere att est to was a serious challenge. However, in mountain this. sheep, it can be easily terminated by stepping up Diff erent species end habituation diff erently. to the ram and sharply shoving him downhill In my experience, exploration by sheep and so that he stumbles. Stumbling is essential. In whiskey-jacks (i.e., Canada jays [Perisoreus dominance fi ghts, the ram who stumbles aft er canadensis]) was gustatory (how did I taste?). In a clash is the looser. He gives up by turning, free-ranging wolves (Canis lupus) and coyotes feeding, and accepting the full-fl edged, ongoing (Canis latrans), habituation may change to courtship procedure of the dominant, mounting an exploration of an alternative food source, included. A subordinate does not leave the band resulting in an att ack. This was originally aft er loosing status, but remains being treated discovered in coyotes targeting children in as a female by the dominants. urban parks by Baker and Timm (1998), and I was att acked once when I was surrounded independently discovered for wolves by myself by a large, rutt ing band of sheep on a steep (See Appendix B in Geist 2007). Woolpy and slope. I tried to disengage by suddenly turning Ginsburg (1967) found that wolves also did and running down hill and was at once struck their fi nal exploration as an att ack. In short, my by a large ram. My second escape att empt account of habituation is based on contrast with resulted in another att ack. I escaped injury as taming and its consequences. the clash is a twisting downward blow in which Rogers and Mansfi led (2011), and Stringham the horn edge acts much as a hand in a karate (2011) reported that in their professional blow. The horns brushed down my back and experience habituated bears are harmless. the ram slammed his head into the scree. I gave Unfortunately, bears are not always treated him a piece of salt that he could not readily spit with caution and skill as done by professional out, and as other sheep crowded in to partake of observers and viewing guides. Bears in the the salt, I escaped. However, that ram came for Canadian national parks where I worked me subsequently every morning from as far as were routinely molested, especially through nearly half a mile away. He would rear running photography, and had a very high rate of on his hind legs showing readiness to clash. I mortality (Nielsen et al. 2004). For example, a would then step behind a female, allowed the young female grizzly bear (Ursus arctos) showed ram to run past and then rear towards me on up in my study area in the back country of the downhill side. Now, however, I was taller Banff National Park. She did not fl ee from my than he, and I simply stared at him (rams cannot vehicle as other grizzlies did (habituated?). A clash uphill). He would blink, eventually, drop district warden and I were fi shing at a beaver to all fours, give me the head-high display—I pond when we were charged by this female. would not budge—then turn and start grazing She appeared suddenly across a narrows and (peace signal), at which point I stepped forward charged instantly, jumping into the water and and gave him a litt le swat on his bum. He would swimming for us. I escaped by climbing, the 194 Human–Wildlife Interactions 5(2) warden by diving. Shortly thereaft er, she treed 10 rules we follow in showing off our status. this same warden and a horse wrangler. When (Geist 1978b). she appeared a third time, the warden was Because dominance displays are species- carrying a rifl e. A student of mine also was specifi c and quite diff erent from species to treed when he surprised a large male grizzly species, its study in ungulates has the advantage on an elk kill. Years later he and a warden of many species to compare. Moreover, the were deep inside the wilderness of a newly- large size of the animals and visual orientation minted national park out in the wide open have fostered picture planes during the display when they were met by a an old female grizzly that closely follow artistic theory. Show and with a 2-year old cub. Aft er “dancing about” explain such to students of art, architecture, apparently examining the intruders, the female or design, and they instantly recognize the and cub charged. My former student shot both code and follow matt ers with enthusiasm, bears, one of which was on top of the warden. while biologists sit there with glum faces! (It, One bear att ack by a (habituated) black bear of course, suggests that large mammals use resulted in a kill-order to remove all habituated much the same neural mechanisms to evaluate black bears; 256 bears subsequently were killed. and interpret space). The trouble is that unlike The wardens who did the executions secretly primates, ungulates notoriously avert eyes informed me of this while we worked in the from the individual displayed to, so that we parks. Subsequently, colleagues in parks have may not even notice that we are being signaled. worked hard, and successfully, to reduce the A friend working in a zoo barely escaped with carnage. his life, though not without injury, when he Do bears terminate habituation with att acks? was att acked by a rutt ing, white-tailed deer I suspect that, unless they are professionally (Odocoileus virginianus) buck that apparently handled, they occasionally do. And that is ignored him. Some captive stags approaching where the lesson resides, thanks to the dedicated with their eyes averted respond with an instant professional eff orts and successes of the likes of att ack into the fence if one looks away from Lynn Rogers, Susan Mansfi eld, and Stephen them. Looking away made a victim of a good Stringham. I counsel caution with animals that acquaintance of mine (also a zoo worker) who, do not fl ee, that look “habituated”, unless one while close to the wire fence, looked away from knows their history. an approaching bull elk (Cervus canadensis) Another bone of contention between my that appeared to ignore him. The elk’s fourth colleagues and myself was signaling by tine penetrated my friend’s chest just above his bears. Dominance or status displays are heart. Fortunately, he was saved. My late friend signals universal to vertebrates, and bears Fritz Walther, himself a former zoo director, and are no exception. Displays of status cannot a great student of ungulate communication, be understood in isolation from the subject talked of a number of similar happenings, some of aggression (Geist 1978a). Status displays with tragic outcomes because the eye-aversion vary considerably. In mammals, they tend to threw off the human victim. Unfortunately, I be body displays in their primitive form, but can go on with such war stories. Standing with may be weapon displays in other species. An friends, students, and colleagues in front of zoo individual thus signals its superiority and exhibits or showing them fi lms, I found again may back it up with an att ack. In humans, and again that they overlooked the displays dominance displays reach the highest diversity of ungulates, but quickly caught on once it of expression through the cultural elaboration of was explained. As primates, we understand the biological basis. We use art to enhance innate primates bett er. They look at us! display structures that we share with old world In 1963, I showed to graduate students at primates (face, head-hair, chest, penis, butt ) the University of British Columbia my fi rst followed by sophisticated cultural elaborations. fi lm, featuring mountain goats, including the Our displays express pride, humor, and also long, stiff dominance displays of big rutt ing the antithesis of dominance—courtesy—and males. Maurice Hornocker spoke up, pointing incorporate, among others Thorstein Veblen’s out that grizzly bears had a very similar “conspicuous consumption”. There are at least display. Hornocker had done a masters thesis Commentary 195 on grizzly bears. He was, of course correct, ethologists, pointed out that such a scheme falls as the dominance display of bears was later to pieces the moment one does an interspecifi c described in detail by Stringham (2010) and comparison of dominance displays, as even labeled “sumo display”. It is so similar to that closely related species may have greatly of primitive ungulates (broadside orientation, diff erent status displays. Secondly, emotions aversion of eyes, stiff motion, release of urine) are inferences, not observations as illustrated by that one might be forgiven looking for horn-on- the sentence “The ant stamps ifs feet in anger”. the-head of the displaying bears. As expected, We preferred to stick to observable phenomena, this is primarily a display of large males to one avoiding deliberately terms like anxiety, fear, another. Dominance displays signal intent to or nervous apprehension. Note the diff erence: dominate. They are not “harmless bluster” as Rogers and Mansfi eld describe beautifully the has been claimed. threat behavior of black bears. They then add Stringham (personal communication) related that from their experience, there is no follow to me that in all the years of his work with up with att acks, and even the threats diminish black and grizzly bears he has never been with time spent with bears—very important addressed with a “sumo display”. This speaks observations. However, the phenomenon legions about the tactful, careful approach in involved is still a threat as recognized by the observing bears used by this exceptionally universals of threat behavior, namely the capable scholar. I have been, however, address- orientation toward an opponent, intimating the ed with the “sumo display” by very large black use of weapons (mouth and paws), even if the bear males for perfectly logical reasons. For the chances of att ack are low. I concur that threats past 16 years, I have resided with black bears are mostly a defensive behavior. However, (and misbehaving wolves) in an agricultural one does not ignore them, even if there is low district on Vancouver Island. Two salmon danger, and I do not think that Rogers and streams pass through our acreage close to our Mansfi led counsel such. house, where we also have poultry, fruit trees, Ignoring threat signals (i.e., defensive ones) and grape arbors. These are great att ractants can be costly. For instance, one threat behavior for bears, and I set myself the task of keeping of moose (Alces americanus) is to lift a hind leg bears out, as shy bears avoiding humans are the slightly off the ground, cocking it, ready to only live bears hereabouts. A dog announces strike. A warden in Yellowstone National Park, the arrival of a bear, and at any hour of the day faced by a young bull blocking the plowed or night I respond, clatt ering the action of a snow road to snowmobilers, though the moose pump shotgun (super-teeth-clapping) moving was injured. He tried to haze the bull into at the bear till it fl ees. Young bears and most the deep snow. In vain. (When confronted by old male bears fl ed at once and usually stayed predators, moose seek out small areas of low away (although snowfalls revealed that they snow and hard footing, on which they can spin were constantly monitoring me). However, 2 around unimpeded striking with their front large males “objected” in their species-specifi c legs and lashing out with their hind legs. The ways and pushed back, which included sumo power is great and the aim very accurate). He displays! I have seen these displays performed managed to make the bull move to an edge, by large males in their interactions. Bears learned using bangers, upon which he signaled the quickly to avoid the vicinity of our house, but snowmobiles to proceed. The moose att acked continued making use of the salmon streams the fi rst snowmobile instantly, leaving 1 man and meadows close by. From our veranda, we with a broken neck. The court case against the can hear them fi shing. park was dismissed on the basis of sovereign The study of animal behavior is not a immunity. monolithic discipline, but it contains diff erent I am grateful to Lynn Rogers for elaborating lineages that evolved their own language and on the Timothy Treadwell case. I was aware of conceptions. Konrad Lorenz introduced the Treadwell’s “samurai” mode. I also practice it notion of expressions as resultants of diff erent, very frequently and have done so for 16 years, confl icting emotions, and bear biologists still with the aim of teaching black bears where they hang onto that. Others, in particular ungulate will be confronted and where not, where they 196 Human–Wildlife Interactions 5(2) can feed in peace (salmon stream, grazing or the ages. Detselig, Calgary, British Columbia, mousing in meadows) and where not (garden, Canada. chicken coops, apple trees close to house etc.). Nielsen, S. E., S. Herrero, M. S. Boyce, R. D. For years, very few large males did not accept Mace, B. Benn, M. L. Gibeau, and S. Jevons. being displaced without protest! I am well 2004. Modeling the spatial distribution of hu- aware that bears (and wolves) are, paradoxically, man-caused grizzly bear mortalities in the Cen- timid compared to ungulates and that assertive tral Rockies ecosystem of Canada. Biological behavior on our part is good protection from Conservation 120:101–113. harm. Large mammals that readily draw blood Rogers, L. L., and S. Mansfi eld. 2011. Misconscp- are, as a rule of thumb, unlikely to enter into tions about black bears: a resonse to Geist overt combat. Retaliation by the victim sees to (2011). Human–Wildlife Interactions 5:173– that (Geist 1966, 1978a). I think bears fall into 176. this category, especially black bears who are Stringham, S. F. 2002. Beauty within the beast. products of the competitive large predator Last Post Press, Falls Village, Connecticut, fauna in Pleistocene North America. I saw USA. Treadwell’s behavior on fi lm, and was appalled. Stringham, S. F. 2007. Alaska magnum bear safe- I am impressed that he lasted as long as he did. ty manual. Wild Watch Publications, Soldotna, The great achievement of Rogers, Mansfi eld, Alaska, USA. Stringham, and bear-viewing guides is to Stringham, S. F. 2009. When bears whisper, do demonstrate how knowledgeable habituation you listen? Negotiating close encounters with can result in safe bear viewing. This knowledge bears. Wild Watch Publications, Soldotna, needs to be spread (see Stringham 2002, 2007, Alaska, USA. 2009, 2010). In national parks, I have seen a lot Stringham S. F. 2010. Ghost grizzlies and other of misbehavior towards wildlife by tourists, rare bruins: the art and adventure of knowing as well as by park staff , which is not likely to wild bears. Wild Watch Publications, Soldotna, cease, nor are the dangers arising from this Alaska, USA. behavior. A good understanding of the body Stringham, S. F. 2011. Aggressive body language language of large mammals, bears included, of bears and wildlife viewing: a response to not only makes viewing more interesting, but Geist (2011). Human–Wildlife Interactions can save the lives of humans and wildlife. I do 5:177–191. not think we disagree on this point. As for the Woolpy, J. H., and B. E. Ginsburg. 1967. Wolf so- rest—I pass. cialization: a study of temperament in a wild species. American Zoologist 7:357–363. Literature cited Baker R. O, and R. M. Timm 1998. Management of VALERIUS GEIST (photo unavailable) is confl icts between urban coyotes and humans professor emeritus of environmental science in the Faculty of Environmental Design at the University of in southern California. Proceedings Vertebrate Calgary, Calgary, Alberta, Canada. He is an animal Pest Conference 18:299–312. behaviorist whose research focused on free-ranging Geist, V. 1966. The evolution of horn-like organs. ungulates and their habituation. His broader inter- ests include northern Pleistocene large mammals Behaviour 27:175–215. (humans included), their ecology, history, evolution, Geist, V. 1978a. Aggression. Pages 62–85 in V. and conservation. He also is interested in theory of health that is universal to all organisms, the North Geist. Life strategies, human evolution, envi- American Model of Wildlife Conservation, and court ronmental design. Springer-Verlag, New York, cases on various wildlife matters. New York, USA. Geist, V. 1978b. Dominance displays: the biology of art, pride, and materialism. Pages 86–115 in V. Geist. Life strategies, human evolution, envi- ronmental design. Springer-Verlag, New York, New York, USA. Geist, V. 2007. Appendix B. Pages 195–197 in W. N. Graves. Wolves in Russia: anxiety through