CONTEXTS AND PATTERNS OF INJURIES IN FREE-RANGING
MALE BABOONS (PAPIO CYNOCEPHALUS)
CARLOS DREWS 1 ,2)
(Department of Zoology, University of Cambridge, Cambridge, UK)
Injury in male baboons (Papio cynocephalus) was investigated as an indicator of damaging fights in order to provide a framework for analyses of conflict resolution and dynamics of agonistic competition in primates. The vast majority of wounds were canine slashes resulting from intraspecific face-to-face combat. Wounds were more common in males than females. In males they concentrated on the right side of anterior parts of the body, principally the head. Wounds took on average three weeks to heal. Aggressive conflicts represented 10% of all interactions between males. Less than 1% of aggressive contests led to injury. The individual rate of injury from fights with other males was on average once every 1.5 months. The winner of damaging fights was sometimes the wounded indi vidual. The number of wounds per damaging fight was not related in a simple way to the presence of proceptive females or to recent immigration events. Four fights yielding the
1) Present address: Programa Regional en Manejo de Vida Silvestre, Universidad Nacional, Apdo. 1350 - 3000 Heredia, Costa Rica, e-mail: email@example.com 2) I am thankful to the Government of Tanzania, Tanzanian Commission for Science and Technology, Tanzanian National Parks and Serengeti Wildlife Research Institute for permis sion to study baboons in Mikumi and Gombe National Park. The Mikumi Baboon Project, co-directed by R. Rhine, S. Wasser, and G. Norton, and the Gombe Baboon Project, coor dinated by A. Collins and J. Goodall, facilitated the study of habituated baboons and hosted the author at the respective study sites. The field assistance of A. Sindimwo in Gombe and of C. Kidung'ho, W. Marwa and A. Njalale in Mikumi was invaluable. I am most grateful to A. Schmidl-Drews, who collected half of the data for this study. Previous versions of this manuscript benefited greatly from comments by K. Eltringham, P.C. Lee, G. Norton, D. Hawkins, A. Whiten, G. Cowlishaw and an anonymous referee. This study was funded by Kings College Cambridge, Bedford Fund, Durham Fund, Bartle Frere Exhibition Fund, Gordon Wigan Income Fund, Mary Euphrasia Mosley Fund, Cambridge Philosophical So ciety, Sigma Xi, Leakey Foundation, and the Harry Frank Guggenheim Foundation. The preparation of this manuscript was funded by the Max-Planck Gesellschaft.
© E. J. Brill, Leiden, 1996
Behaviour 133, 443-474
highest number of injuries, however, involved recent immigrations or attempts to immigrate by adult males in their prime. Contexts of male injury observed during infliction include challenges to the resident alpha male by newcomers, intertroop encounter, fights over pro ceptive females or unusual foods, redirected aggression, defense of a female and a fight unrelated to any obvious resource. This study and anecdotal reports from the literature point at various implications of injury to male baboons, including physical impairments which can constrain feeding efficiency, limit access to resting sites and safe retreats, cause a drop in dominance rank, jeopardize mating success and even result in death. Severely injured males typically reduce interaction rates, retreat to the periphery of the troop or emigrate temporarily. Although most wounds are small and heal well, the potentially high costs of injury probably exercise strong selection pressure on contestants for means of peaceful conflict resolution, given that during fights both baboons risk injury irrespective of their competitive abilities. The potential fitness consequences of inflicted injury can explain the evolution of the formidable canine weaponry of some male primates. Keywords: aggression, sexual selection, trauma, competition, mortality, laterality, primates.
Most studies on animal fighting have focused on the determinants of out come and on the pattern of information exchange during the interaction (see Huntingford & Turner, 1987). Surprisingly little is known about the con sequences of wounds resulting from intraspecific fight, given that the risk of injury and its associated costs are a central component in game-theory analyses of animal conflict (e.g. Maynard-Smith & Price, 1973; Maynard Smith, 1974; Parker, 1974; Huntingford & Turner, 1987, p. 277 if; Enquist & Leimar, 1990). There is evidence of death resulting from escalated, intra-specific fights in a variety of taxa including molluscs, crustaceans, insects, spiders, amphibians, birds and mammals (examples in Huntingford & Turner, 1987, Table 3.1 therein). In general, therefore, injuries are as sumed to be costly in view of their potentially lethal consequences. Little is known about the non-lethal implications of injury sustained in fight, how ever. In red deer Cervus elaphus stags, recovery from injury is associated with loss of dominance and antler mass in the subsequent rutting season (Vogt, 1948), and can lead to a considerable reduction in reproductive suc cess (Clutton-Brock et al., 1982, p. 134). There are few accounts from field studies concerning the pattern, context and implications of lesions. During escalation animals risk to suffer a potential fitness reduction as a consequence of injury. There can be direct costs of injury, such as
INJURIES IN MALE BABOONS
e.g. a greater energetic expenditure from limping or the mating opportuni ties missed due to a reduction in competitive ability. In addition there are stochastic costs which mayor may not be incurred, and arise e.g. from an increased risk of falling prey to predators in the case of a locomotory hand icap. In principle, however, damaging fights, defined as contests leading to injury to any or both participants, need not necessarilly reduce the fitness of the victim because injury can be minor and may heal rapidly. Thus, the type of injury, its severity and its healing time largely determine the kind and magnitude of the handicaps attached to it. The aims of this report are (1) to present field data on lesions in male savannah baboons (Papio cynocephalus), (2) to bring together the anecdotal information about male injuries scattered in the vast literature about baboon behaviour and ecology, and (3) to evaluate the implications of injury to the victim. The theory of animal contests has been applied to agonistic competition in primates (e.g. Popp & DeVore, 1979), but studies of fights are missing in this order, which thus lacks the empirical data required in some models of aggressive competition. An insight into pattern and context of damaging fights can be gained from analyses of injuries, in a similar way to the use of scars as indicators of aggression levels in rodent populations (e.g. Christian, 1971; Turner & Iverson, 1973; Rose & Gaines, 1976; Rose, 1979). Primatologists report on the incidence of wounds and at the same time on the lack of direct observations of wound inflictions (e.g. Boelkins & Wilson, 1972; Symons, 1978, p. 168). The field worker is more likely to observe the result of aggression, i.e. injuries, than the aggression itself, because fights resulting in injury are brief and relatively rare, whereas injuries can be still recognized several days after the incident. It is necessary to know how animals fight and the nature of their weap onry in order to assess the risk of injury to the combatants (see Geist, 1966, 1978; Packer, 1983; Lincoln, 1994). Fights have been described, for example, in crustaceans (e.g. Hyatt & Salmon, 1978; Dingle, 1983), insects (e.g. Davies, 1978; Parker & Thompson, 1980; Thornhill, 1984; Marden & Waage, 1990), fish (e.g. Laudien, 1965; Simpson, 1968; Dow et al., 1976; Beaugrand et al., 1991), birds (e.g. Smith & Hosking, 1955; Stout, 1975), pinnipeds (Le Boeuf, 1971; Haley, 1994), ungulates (e.g. Geist, 1971; Walther, 1974; Wilkinson & Shank, 1977; Clutton-Brock et al., 1979; Fryxell, 1987), carnivores (e.g. Poole, 1973; Havkin & Fentress, 1985), and
mammals in general (Harrison Matthews, 1964). Little has been written about fights in primates. Two studies have specifically addressed fights and injuries in baboons. Bramblett (1967) did an osteological analysis of baboon injuries and diseases. Owens (1975) compared aggression during play with other aggressive episodes among juvenile and adult olive baboons (P. c. anubis), and included information on fight and wounding patterns in adult males. The most common movement pattern in aggressive episodes between adult males is chasing, lasting on average 12.5 s, about three times longer than chases between females or between juveniles. The second most common behaviour is sparring, i.e. partners stand facing each other, grapple with the arms and hit one another about the head. Less common behaviours include, mutual and non-mutual biting, non-mutual mauling and wrestling. Several field studies of baboons make marginal reference to fights and injuries. This information is cited in the relevant sections below. Analyses in this report are based on wound records and some direct observations of damaging fights. Canines: the baboon s weaponry During contact fights, male baboons utilize their canines as the main weap on to inflict wounds to the opponent. The remarkable degree of sexual dimorphism in canine length in the baboon is typical of its multi-male social organization (Harvey et al., 1978; but see Martin et al., 1994). The exposed shaft of a male's upper canine can measure 2.3 em (Ransom, 1981). The anterior edge is rounded, while the posterior edge and the tip are very sharp (pers. obs.). Males are believed to sharpen their canines prior to combat by grinding their teeth (Brain, 1992). The canines are effective weapons in antipredatory behaviour, for male baboons are known to kill dogs (Canis familiarisi and attack leopards (Panthera pardus) (see review of baboon responses to predators in Altmann & Altmann, 1970, p. 170 fj). In addition, male canines are responsible for injuries on females (Smuts, 1985, 1987; pers. obs.) and juveniles (e.g. Altmann & Altmann, 1970, p. 46; pers. obs.). Injuries to juveniles inflicted by males can be lethal (Altmann, 1980, p. 203; pers. obs.). Broken canines are not uncommon and are probably a consequence of clashes between the teeth of both contestants (Paterson, 1973; Packer, 1979b; pers. obs.). It is conceivable that the large upper canines of males have structural adaptations to the lateral impacts
INJURIES IN MALE BABOONS
suffered when parrying the opponent's blows (see description of fights below). Such adaptations are found in the horns of male antelopes (Packer, 1983). The nails of baboons are small and assumed to playa minor role in the causation of wounds, with the exception perhaps of injuries to the sensitive skin of the swollen perineum of proceptive females.
Four well habituated troops of yellow baboons (P. c. cynocephalus) were observed in Mikumi National Park, Tanzania. These included the two Viramba troops which have been monitored in Mikumi since 1975 (see Rhine, 1986). The number of males in a troop varied from two to five during the study. Baboons in Mikumi were observed on 164 days in two periods spanning a total of 16 months, between May 1990 and November 1991. The habitat in Mikumi National Park is characterized by Miombo woodland on the hills, and open woodland and grassland in the valley. For details of the Mikumi habitat see Norton et al. (1987). In September and October 1991, one additional troop of habituated olive baboons (P. c. anubis) with seven adult males, the Beach Troop, was observed on 33 days spanning six weeks in Gombe Stream National Park, Tanzania. Common vegetation zones in the range of Beach Troop was the evergreen and the deciduous forest, as well as the beach on the shore of lake Tanganyika. For details of the Gombe habitat see Ransom (1981), Goodall (1986) and Collins & McGrew (1988). The data set collected corresponds to 1413 h of baboon observations. The methods and subjects of this study are described in more detail in Drews (l993b). All adult and subadult males of the study troops were examined by two observers (c. Drews and A. Schmidl-Drews) from 2-5 m distance on each observation day for recent lesions. Scars, mutilations and other permanent marks resulting from wounds past are not included in the sample of this study. Adult males are defined as fully grown immigrant males. Subadult males are males over six years, residing in their natal troop and not show ing consort behaviour. A total of 123 fresh lesions were recorded on 19 males belonging to study troops and several other males not individually identified. An additional four injuries on males were recorded in Gombe. Data for the Gombe olive baboons are only included in analyses where explicitly so stated. Lesions on adult and subadult females, as well as juveniles were also recorded. Each record included the bodily location of the wound, its shape (cut, tear, puncture, fracture, other), size, age in days or an estimate thereof if knowingly less than eight days old, healing stage, identity of the individual and the context of the injury if observed. Two size categories were used in the analyses, Small (i.e. less than 5 em) and Large (i.e. 5 ern or larger). These categories applied to cuts and tears; the depth of wounds was not recorded. A wound was considered as healed when it was closed, dry, free of flies and not groomed any longer. Fractures and other internal wounds on limbs were considered healed when limping ceased. Fight is used here to describe the section of an agonistic contest, in which aggressive, bodily contact occurs. The troop is defined spatially as the most coherent set of baboons containing 90% of troop members. The remaining 10% are considered with the troop if they are within one
troop diameter of the troop's periphery. Baboons were recorded as peripheral when they occupied corners of the largest imaginary polygon around the troop. Baboons located more than one troop diameter away from the periphery of the troop were considered outside the troop and not included in the polygon. Definitions of dominance status and rank follow Drews (1993a). Statistical tests are two-tailed, unless otherwise stated. Chi-square values were corrected for continuity (Yate's correction) in analyses with one degree of freedom.
The following description of fighting techniques is the result of direct ob servations of 91 instances of escalated aggression between male yellow baboons and frame by frame analyses of two video records. In fights, males use their canines in a slashing rather than biting motion. This con trasts with fights among females and juveniles were biting and holding the opponent with closed yaws was common. Males used their muzzle both to strike at the opponent and to fend off the opponent's blows. Contes tants remained quadrupedal during fights, but used single hands to slap the opponent, sometimes sweeping its forelimbs away thus inducing a loss of balance. Exchanges of canine blows and hand slaps, which can lead to injury to one or both contestants, generally did not last more than 5 s (also Owens, 1975; Brain, 1992). Complete fighting sequences, which may include brief grappling bouts, did not exceed 30 s. Although a male olive baboon was reported to have ridden on its fleeing opponent while directing bites to its neck region (Popp, 1978, p. 99), male fights in this study typically ended in either a chase or one male leaving the fighting ground. Superficially, male baboon fights resemble carnivore fights in that canines are also used as both an offensive and defensive structure and in that sweeping in a judo-like fashion is a component of the interaction (e.g. wolf pups Canis lupus: Havkin & Fentress, 1985).
Types and causes of injuries
The sample sizes differ between analyses below, due to some incomplete records during the initial stages of the study. Male injuries included cuts, tears, punctures, fractures and a swollen shoulder. Limping with no external sign of the cause represented 15% of 104 injuries. The majority of wounds
INJURIES IN MALE BABOONS
1. Types of injuries among adult and subadult male baboons
67 6 % 76 7
Type of injury Cut Tear*) Puncture Fracture Swollen shoulder Total
7 1 100%
*) In tears, as opposed to cuts, a piece of skin hangs from the wound exposing it.
2. Causes of injury among adult and subadult male yellow baboons
13 % 13
Cause of injury" Aggression confirmed Aggression suspected Predator attack suspected Hit by vehicle confirmed Total
1 1 101
1 1 100%
*) 'Aggression confirmed' is based on the appearance of wounds immediately after observed fights (typically cuts, tears and punctures). 'Aggression suspected' is based on the type of injury as known from observed aggression. 'Predator attack suspected' is an open wound in which a portion of muscle is missing, similar to wounds observed in ungulates during the study.
were cuts, tears and punctures (Table 1). In complete records, nearly all wounds (i.e. 98%) could be confidently attributed to canine action during intraspecific fights (Table 2). The sample of injuries attributed to agonistic encounters between males is composed of 92 injuries on 29 adults and seven on two subadults. The cause of injury was unknown in 22 cases (not computed in Table 2), twelve of which corresponded to limping. Where size was indicated (N = 82), large wounds made up 27% of the sample. In the main study troop (Viramba 2), adult and subadult males did not differ significantly from adult and subadult females in the proportion of large to small wounds (X 2 = 1.89, df = 1, p = 0.168).
Contexts of injury
The infliction of fifteen injuries, i.e. 12% of all lesions recorded in males, was witnessed during ten damaging encounters. Eight immediate contexts leading to injury were identified. Injury occurred (1) in two out of eight coalition attacks during competition over a proceptive female, (2) in one out of five dyadic fights over proceptive females, (3) once in a fight during an intertroop encounter, (4) once in a fight between an alpha male and a non-resident male attempting immigration (see also Results: Number of wounds per damaging fight), (5) twice in fights over unusual foods (i.e. banana offered by passengers from a vehicle and kitchen refuse at the pit of the tourist lodge, respectively), (6) once in a fight over no apparent immediate resource, (7) once when a male redirected an attack received by a consorting male against another male (olive baboons), and (8) once when an old male, whose upper canines were missing, was wounded as he defended a non-proceptive female from an attacking, higher ranking male (olive baboons). Injuries have sometimes preceded the emigration of male baboons (e.g. Harding, 1980). In this study, the disappearance of a newcomer male, who had recently taken over alpha status in the troop, was noticed on a day when two of the three resident males had several fresh slash wounds. Injury was neither observed resulting from any of 513 socio-sexual in teractions between male baboons nor from any of 345 supplantations over natural foods or resting places such as shade, suitable branches, stones, or bare area of ground. Thus, common resources of small relative value were usually not involved in contests resulting in injury. All witnessed inflictions of injuries on males were sustained during fights with other males. On two occasions the winner of the fight injured the loser. Conversely, in three cases the winner (i.e. the animal which obtained the contested resource) sustained a small injury while the loser remained unharmed. During an immigration attempt both contestants received large wounds. Thus, being the superior combatant in a fight is no guarantee against injury.
Frequency of injury
Demographic composition data from the main study troop was used to analyse the distribution of injuries among different sex and age classes
INJURIES IN MALE BABOONS TABLE
3. Proportional representation of injuries among sex/age classes in troop Viramba 2
Injuries observed 35 (45%) 7 (9%) males 42 (54%) 25 (32%) 4 (5%) 29 (37%) 7 (9%) Injuries expected 8.7 4.6 13.3 29.4 2.6 32.0 32.7 Mean daily % in troop"! ILl % 6.0% 17.1% 37.6% 3.4% 41.0% 41.9%
Sex/age class Adult males Subad. males Ad.
Adult females Subad. females Ad.
Ad. = adult, Subad. = subadult. For statistical analysis see text.
*) The contribution of each sex/age class to the troop's composition is expressed as the
mean daily percentage, since troop composition varied over the course of the study. This
value was used to calculate the number of injuries expected in each sex/age class.
(Table 3). The distribution of injuries departed significantly from that ex pected according to the respective proportions of adult and subadult males, adult and subadult females, and juveniles in the troop (X 2 = 82.01, df = 2, p < 0.0001). Adult and subadult male yellow baboons had proportionally more visible wounds than females and juveniles (Table 3). The difference in wounding incidence between males and females was still significant when juveniles were excluded from the analysis (X 2 = 30.26, df = 1, p < 0.0001). The exclusion of juveniles is justified on the grounds that observed wound frequencies are underestimated in this age class, since a probably large proportion of wounds are lethal (e.g. Altmann, 1980, p. 203; personal observation), and thus lead to the disappearance of the juvenile before the wound is noticed. Nineteen (83%) of 23 adult males belonging to the study troops sustained at least one injury attributed to agonistic encounters during the 16 months of the study. Since the residence time of the study males varied considerably (range 1 day to 5.5 years), the rate as victim in damaging fights was calculated from the observation time on each individual and its number of
4. Individual rates of damaging fights resulting in injury to six adult and two subadult males in troop Viramba 2
Rank alpha beta lr lr lr Jr lr lr D ays2) 213 213 163 40 65 61 194 213 Injuries 9 6 8 0 0 1 4 2 Fights 3 ) 3 6 8 0 0 1 3 2 Days per fight 71 35 20 Fights per day 0.014 0.028 0.049 Injuries per fight 3.0 1.0 1.0
Male vtctim!' HUZ ADU USI NDU NOV WIM sUTE sNAF
61 64 106
0.016 0.016 0.009
1.0 1.3 1.0
Adult males: Mean days/fight
23.4 (N = 4)
alpha = top ranking throughont study period, beta = second ranking throughout study period, lr = low ranking (rank anywhere below beta). 1) Only males observed for over one month are listed. These males were not necessarily simultaneous residents. 2) Days = days covered by observation regime, assuming that on any given observation day all injuries of the preceding six days would have been detected, given that the minimum healing time recorded was eight days (Table 7). 3) All fights in the table are damaging. Separate injuries were attributed to the same fight when dated equally, thus data in the table show independent wounding events.
independent wounding events (Table 4). That calculation took into account the fact that wounds were still recognizable with considerable certainty up to six days after the damaging fight (see legend for Table 4). Crudely, on average an adult male is injured in a fight with another male every 1.5 months, but variation between males is considerable. The alpha male experienced the highest number of wounds per damaging fight but its rate of damaging fights was comparatively low. One low ranking male showed the highest rate of damaging fights of the sample, acting as the scapegoat among higher ranking males who initiated most contests. The proportion of aggressive interactions between males which results in injury can be calculated only by indirect means, given the small sample size of wound inflictions witnessed during focal animal samples. The median proportion of aggressive interactions among 20 male dyads in the main study troop was 10.3%. These were interactions including at least one aggressive element (i.e. threats, attacks, chases and/or fights). Out of
INJURIES IN MALE BABOONS
91 aggressive interactions between males, only 5.5% resulted in escalation with high potential for injury (i.e. face-to-face combat, bites, grappling and/or contact during chases). This corresponds to 1% of all male-male interactions (N = 662). A male yellow baboon interacts with other males on average 2.4 timeslh (Drews, 1993b, p. 134). Thus, a male participates in escalation to potentially damaging levels about 0.024 timeslh, or once every 3.5 days (42 daylight hours). If a male is on average injured once every 47 days (Table 4), then the incidence of injury is about 13 times smaller than the frequency of escalated fights. This crude calculation suggests that about 8% of escalated contests result in injury, i.e. 0.4% of all aggressive interactions or 0.04% of all interactions between males.
Bodily location of injuries
In male yellow baboons, injuries concentrated on the anterior body parts, particularly on the head (Table 5), as expected from their face-to-face fight ing pattern. Wounds on the anterior body parts attributed to agonistic en counters were significantly biased towards the right side of the body (66%) of adult and subadult males (Fig. 1). The wounds of twenty adult males and two subadults were pooled in this analysis, with no single male contributing with more than 12% to the sample. In contrast to the anterior prevalence of wounds in males, most female injuries were found on their posterior body parts (Table 6, X2 = 34.17, df = 1, p < 0.0001). The respective proportions of wounds on swellings
5. Bodily distribution of injuries resulting from aggression between adult male baboons in Mikumi
Number of injuries 42
Body part Head Neck, shoulders and chest Arms Trunk Pelvic region Legs Tail Total
2 - tailed Binomial p<O.O 15
Fig. 1. Laterality of wounds in adult and subadult male baboons, illustrated in a frontal, schematic view of a male baboon showing the head, neck, shoulders, upper arms and chest. Incidence of wounds on lower arms are excluded because these could be moved to the opposite side during fights and could, therefore, obscure a laterality effect. For details of sample see text.
6. Anterior and posterior bodily distribution of injuries attributed to agonistic encounters in adult males, adult and subadult females in Mikumi
Body region"? Anterior: Head, Neck, Shoulders, Arms Posterior: Pelvis, Tail, Legs Sexual swelling Total
Males 84 (85%) 15 (15%)
5 (15%) 18 (53%) 34 (100%)
For statistical analysis see text.
*) No injuries were recorded on the trunk (dorsally or ventrally) of either males or females.
INJURIES IN MALE BABOONS
attributed to agonistic interactions (personal observation) and to scratches against vegetation and alike is unknown. At the sample size used above, the sex difference in bodily distribution of injuries due to aggression is statistically significant if a minimum of 11 % of swelling injuries resulted from aggression (X 2 = 5.62, df = 1, p < 0.02). Males were sometimes injured on their hindquarters (Table 5). Highest ranking males are not immune to injuries on their hindquarters. Three alpha males in different troops received four of the 14 posterior injuries recorded. Posterior injury of alpha males could happen for instance when running away from a coalition attack or when pursued by a screaming subordinate (see Packer, 1979b).
A remarkable healing capacity and ability to survive severe wounds is often commented on for monkeys (e.g. Schultz, 1969, p. 114) and baboons in particular (Bramblett, 1967). The severity of an injury and the duration of impairments associated with it are reflected in the healing time. Typically, fresh wounds dried up within 24 h of the wounding incident. All injuries in which the healing process was followed up were less than one week old when first noticed. Data for healing time are summarized in Table 7 and Fig. 2. The median healing time of injuries from the day that they were first noticed was about three weeks. There is a slight underestimate in healing time due to the fact that, on average, wounds were a few days old when first noticed. This slight bias, however, is compensated by the fact that due to the irregularity of visits to the troop, the wound was usually recorded as healed a few days after it had in fact healed.
Median and range of healing times in days for baboon injuries
N Median 23.0 14.0 24.0 Minimum Maximum 120 114 120
Total sample» Small injuries « 5 em) Large injuries (> 5 em)
35 IS II
*) The sample is composed of 24 cuts, 4 punctures, I tear, I case of limping, I bruise, and 3 injuries of unspecified shape.
10 20 30 40 50 50
70 80 90 100110120130
DAYS TO HEAL
Fig. 2. Frequency histogram of healing times of 35 baboon injuries. For details of sample see Table 7.
The length of a wound is an insufficient indicator of its severity. The difference in healing time between small and large wounds (Table 7) was not statistically significant (Mann-Whitney test, Z = -1.461, N, = 15, N 2 = 11, p = 0.14). This difference was not significant either when only cut wounds were considered. The two wounds which took longest to heal were a 3 em vertical slash splitting the upper lip (114 days) and a 15 em vertical slash deep in the chest (120 days). Depth of the wound is probably an important determinant of healing time, but it was not recorded in this study.
Damaging fights and male immigrations
Escalated fights could be associated with the recent arrival of newcomer males to a troop, when knowledge about the competitive abilities of op ponents is lacking. The null hypothesis that the interval from male im migration to a fight resulting in injury among troop males is the product
INJURIES IN MALE BABOONS
20 18 16 14
w a w
12 10 8
15 30 45 60 75 90
105 120 135 150
DAYS SINCE IMMIGRATION
Fig. 3. Observed (solid bars) and expected (open bars) frequency distribution of intervals from immigration to the first fight resulting in injury. Expected values correspond to a negative exponential distribution and did not depart significantly from the observations (see text).
of chance, would predict a negative exponential distribution of interval frequencies (Fig. 3). Expected frequencies n were calculated from
for each observed interval length t, where N is the total sample size (47 in tervals), w is the width of the histogram categories (15 days) and T is the mean interval length observed (T = 46.2 days). The distributions of observed and expected frequencies of interval lengths did not differ significantly (Kolmogorov-Smimov Goodness-of-fit test, D max = 0.1477, N = 47, p > 0.2, Fig. 3), thus failing to reject the null hypothesis that time since immigration and the occurrence of damaging fights are not causally related.
Number of wounds per damaging fight
In this section, wounds per fight refers to the number of wounds suffered by one animal in a single fight, while fight refers to combats resulting in injury. Hence, the minimum possible value is one, since this analysis is based on wound records. Wounds on an animal, that were dated back to the same day are assumed to have happened during the same fight. In 95% of the fights resulting in injury, the number of wounds sustained by one individual did not exceed four (N = 67). The mode and median number of wounds per fight was one (74% of all cases) and the maximum six (Fig. 4). The null hypothesis that the number of wounds per fight is the product of chance would predict a negative exponential distribution of value fre quencies (Fig. 4). Expected frequencies n for each observed count x were
W 0:: 1.L.
WOUNDS PER FIGHT
Fig. 4. Observed (solid bars) and expected (open bars) frequency distribution of number of wounds, which resulted from fights causing injury. Expected values correspond to a negative exponential distribution and did not depart significantly from the observations (see text).
INJURIES IN MALE BABOONS
_ N -x/Ai n- Me ,
where N is the total sample size (69 fights) and M is the mean number of wounds per fight observed (M = 1.46). The distributions of observed and expected frequencies of wounds per fight did not differ significantly (Kolmogorov-Smirnov Goodness-of-fit test D max = 0.0956, N = 67,
The average number of wounds did not differ significantly between dam aging fights on days in which at least one proceptive female was consorted in the troop and those on days without consorted females (Mann-Whitney test, Z = -1.059, N I = 25, N2 = 22, P = 0.29). The proportion of damaging fights resulting in more than one wound (i.e. above the pop ulation median) did not differ significantly either between these groups (X 2 = 1.175, df = 1, p = 0.28). The number of wounds per damaging fight was not related in a simple way to the immigration of males into the troop. Damaging fights soon after the immigration did not yield significantly more wounds than later damaging combats (Spearman's r = -0.117, N = 47, p > 0.2). Although days during which proceptive females were consorted are unlikely to be a confounding element in this analysis (see above), such days were removed from the sample in an additional test but the correlation between wounds per fight and days since last immigration was still not significant (Spearman's r = -0.136, N = 19, p > 0.5). Although the time since immigration was not related to the number of wounds per damaging fight it should be noted that four independent cases of unwitnessed fights resulting in more than three wounds to one contestant were associated with recent male immigrations. These cases represent the upper end (6% of the sample) of the frequency distribution of wounds per fight, thus suggesting that the arrival of newcomer males leads to the highest escalation levels during damaging fights.
Implications of injury
Feeding impairment A male whose upper lip was slashed vertically, was unable to suck in water, the baboon's usual way of drinking, and had to resort to the more time
consuming lapping. The cheek pouch of another male was sliced open in a fight. Subsequently, food ingested (fruits of Strychnos madagascariensis) was seen coming out through the wound. Drop in dominance rank A one-step drop in dominance rank associated with injury was observed in the main study troop in Mikumi. The change in dominance status took place between the subadult male sUTE and the next ranking dominant male USI after the latter was noticed limping badly. Comparisons were made between interactions during the 30 days prior to the injury and the 30 days thereafter. Whereas USI won 43 out of 44 agonistic interactions against sUTE during the 30 days prior to the injury, sUTE won all 18 interactions recorded during the 30 days following the date on which USI sustained a leg injury (X 2 = 57.4, df = 1, p < 0.0001). All of 37 interactions recorded in focal samples prior to the injury were initiated by USI while eleven interactions recorded thereafter were invariably initiated by sUTE (X 2 = 48.0, df = 1, p < 0.0001). In this case it is unclear whether the injury was cause or effect of the change in dominance status because the wounding event was not observed. sUTE left the troop before USI's leg had healed, so, it is not known whether USI would have regained his dominant status over sUTE upon recovery. Changes in behaviour upon injury The rate of interactions initiated by adult male USI towards the lower ranking subadult male sNAF decreased significantly after the date of his leg injury (Binomial test, N = 14, p < 0.05), despite the fact that USI maintained his dominant status over that male after sustaining the injury. As a control, the alpha male HUZ and beta male ADU did not change significantly their rate of interactions towards sNAF during the same period. There was a significant tendency for male USI to appear in the periphery of the troop more often when he was limping than before (X 2 = 4.76, df = 1, p < 0.05). There was no such a significant tendency among control males HUZ and ADU. USI's time budget, however, was not affected significantly by his severe limping. The means for time resting, stationary feeding, feeding on the move, moving, socializing and time spent on the ground did not differ significantly between the periods before and after
INJURIES IN MALE BABOONS
the injury. Neither differed the distance of USI to the nearest adult male significantly between these periods.
Patterns of injury The vast majority of wounds in male baboons are canine slashes resulting from intraspecific aggression. Fractures and other cases of limping can at least in part be attributed to agonistic encounters resulting in falls from trees (also Bramblett, 1967). Drops from as high as 12 m during chases (but none resulting in injury) were observed in this study. In some cases, while the screaming victim was hanging from the thinnest twigs the attacker shaked the branch vigorously with a hand, inducing the fall. Harding (1980) saw an olive baboon male fall off a cliff upon being pursued by another male. The victim was stunned for 10 min upon impact. Bramblett (1967) reports from a sample of 61 baboon skeletons, that most fractures occur in the phalanges of fingers and toes, but fractures on limbs, vertebrae, clavicles, ribs and skull (mainly on the face) are also common. In agreement with this study, in olive baboons the wounds on females (and aggressive bites between juveniles of both sexes) concentrate on the back and tail, whereas the wounds on adult males are mostly on anterior body parts, particularly on the face (Owens, 1975; also rhesus macaques Macaca mulatta: Hausfater, 1972). The proportion of wounds on the head of male yellow baboons (42%) was similar to that found in olive ba boon males (51 %, Owens, 1975). In contrast to yellow baboons, however, wounds on the back and body flanks were not uncommon in adult male olive baboons (Owens, 1975). The location of injuries in male hamadryas baboons (Papio hamadryas) differs from that of yellow baboons, in that most injuries are inflicted on the hands and forearms despite the fact that most bites in that species are aimed at the neck (Kummer, 1968, p. 49). The high incidence of wounds on the head of yellow baboon males could suggest that canine blows are targeted mainly at the head. This distribu tion, however, results more likely from the fact that blows are fended off with the muzzle, thus exposing the head to injury. In aggressive play, male juvenile baboons (but not female juveniles) bite the neck of the opponent more than any other region of the body (Owens, 1975), suggesting that
adults may as well be targeting their blows principally at the neck region. Analogously, although fights in most ungulates involve frequent head to head contact, blows are typically aimed at the neck, flanks and haunches (Geist, 1966, 1986). There was a right side bias in the lateral distribution of wounds on male baboons. Behavioural side biases in animals have received attention in research from the perspective of brain lateralization theory (e.g. Ward & Hopkins, 1993). Most reports and experiments have addressed asym metries in hand use in primates (review in Marchant & McGrew, 1991; Bradshaw & Rogers, 1993; Ward & Hopkins, 1993; yellow baboons: Post et al., 1980; Guinea baboons Papio papio: Fagot, 1993; Vauclair & Fagot, 1993) or derivatives thereof, such as the left nipple preference in suckling chimpanzees Pan troglodytes (Nishida, 1993). Overall, very few cases are known of limb independent behavioural asymmetries, such as that of successful slashes during baboon combat reported here. This lateralization of injuries could be related to an asymmetrical use of the field of vision during contests, in the way hypothesized for gelada baboons Theropithecus gelada (Casperd & Dunbar, in prep.). In contrast to antlers or horns (Geist, 1966), canines are an inefficient defensive organ when used to parry the opponent's slashes. In baboons simultaneous injury is likely because at the instant of striking, the attacker exposes itself to counter-attack, but also because the higher the intensity of attack the greater the likelihood of retaliation and retaliation increases the likelihood of intensification of further attacks (game-theory: Maynard Smith & Price, 1973; polecats Mustela sp.: Poole, 1973; rhesus macaques: Bernstein & Gordon, 1974). In fights between olive baboon males, mutual biting is more common than non-mutual biting (Owens, 1975). Thus, both the winner and the loser are likely to be injured (also Smuts, 1985, p. 86 and p. 152), regardless of differences in competitive ability. This is an important reason for both contestants to avoid escalated fights. Accordingly, in male yellow baboons only 5.5% of aggressive contests led to high risk escalation and about 8% thereof resulted in wounds, whereas in red deer stags, a species with effective defensive organs, 24% of aggressive contests led to fights (Clutton-Brock & Albon, 1979) and only 2% of fights resulted in injury (Clutton-Brock et al., 1979). Similarly, severe wounding was observed in only 1.3% of fights between male white-eared kob Kobus kob
INJURIES IN MALE BABOONS
leucotis (Fryxell, 1987). Consistent with the nature of the weaponry, in the goat antelope Oreamnos, a species with short, straight and sharp horns, overt fighting is relatively rare, probably because the risk of injury to both participants is high (Geist, 1966). In male toque monkeys (Macaca sinica), another primate with large canines, only 0.6% of threats resulted in actual body contact (Dittus, 1977). Fights between elephant seal Mirounga angustirostris bulls, which almost invariably lead to injury, represent only about 2% of their aggressive conflicts (Le Boeuf, 1971). Baboon contests involve ritualized aggressive signals, such as eye-lid displays, ground slapping, audible chewing or teeth grinding, and canine displays, which probably contribute to an assessment of the opponent with out resorting to damaging escalation levels (Smuts, 1987; pers. obs.). The incidence of injuries shows that contests between male baboons are not fully ritualized, however. Among species capable of inflicting injury, the evolution of wholly symbolic conflict is not possible because a mutant that employed physical attack would have a reproductive advantage (Maynard Smith & Price, 1973). Similar to other species mentioned above, however, the overall frequency of damaging fights between male yellow baboons is low if expressed as a proportion of all aggressive incidents (less than 1%; also olive baboons: Owens, 1975). Conversely, damaging fights be tween male yellow baboons are relatively common, if frequency is based on time units, for each male is likely to be injured on several occasions each year. This wounding rate may not be uniquely high among primates. Each olive baboon female in Gilgil (Kenya) can be expected to receive at least one serious wound every year, almost invariably inflicted by adult males (Smuts, 1985, p. 87 ff). The individual rate of fights calculated for rhesus monkeys was one fight every 26 to 30 days (Symons, 1978, p. 166, using data from Southwick et al., 1974). In a squirrel monkey (Saimiri sp.) study all 15 males of the study troop were wounded at some point (C. Mitchell personal communication to Baldwin, 1992). For references to wounds in other primate species see Smuts (1987, Table 32.2 therein). Al though wounding rates of some ungulates can be similarly high (see Geist, 1986), red deer stags, for example, are wounded in fights only once in a lifetime (Clutton-Brock et al., 1979). The incidence of wounds was higher in male than in female yellow baboons, a sex difference found also in olive baboons (Smuts, 1987),
macaques and other primates (Wilson & Boelkins, 1970; Hausfater, 1972; Drickamer, 1975; Smuts, 1987). There is no sex difference in the overall frequency of fractures in baboons (Bramblett, 1967). Virtually all baboons older than 13 years show fractures (Bramblett, 1967). It should be noticed, however, that fractures are only a small proportion of the sample which revealed a difference between the sexes in this study. Overall, therefore, baboons fit the pattern of several animal taxa where severe aggression, based on wound frequencies, is more common in males than females (e.g. crustaceans: Jones, 1980; rodents: Christian, 1971; Rose & Gaines, 1976; Rose, 1979; ungulates: Geist, 1986; primates: Smuts, 1987). The median healing time for male baboon injuries was about three weeks. Smuts (1985, p. 93) reported an 8 ern gash inflicted by a male on the arm of a female which took two months to heal, the arm not being used for over one week. Limping from gashes can take several months (Packer, 1979b) and up to a year to heal when recovery is impeded by infection (Altmann, 1980, p. 210). Intensive grooming of wounds by other troop members was not uncommon during this study (pers. obs.). The wounds of adult males were usually groomed by females. This behaviour along with self-grooming and licking may foster the healing process (Bramblett, 1967). Clean cuts are reported to heal rapidly while dirty wounds in which a large pocket of loose skin collects debris are often fatal, partly because adequate cleaning through grooming is not possible (Bramblett, 1967).
Contexts offights resulting in injury
Hausfater (1975, p. 135 if) found that presence of proceptive females in creases the incidence of wounds in male baboons in Amboseli National Park. Here I analysed whether damaging fights in the presence of pro ceptive females resulted in more wounds than damaging fights in other contexts. This was not the case. The likelihood of injury and the number of wounds sustained in each damaging fight between male baboons were not related in a simple way to the time since male immigrations either. The null hypothesis that the number of wounds per fight merely reflects the result of chance events during the contest, instead of reflecting esca lation level, could not be rejected. It is noteworthy, nevertheless, that the four damaging fights yielding the highest number of injuries concerned re cent immigrations or attempts to immigrate by young males in their prime.
INJURIES IN MALE BABOONS
This suggests that the number of wounds per damaging fight could reflect escalation level at least in some contexts. Young adult males typically attempt to gain alpha status upon immigra tion (Altmann et al., 1988; Noe & Sluijter, 1990). Alpha rank is the most valuable social resource of young adult males, for their reproductive suc cess during this stage of their life depends entirely on holding top rank as long as possible (Altmann et al., 1988; Noe & Sluijter, 1990). Challenges for alpha rank are therefore very likely to result in high levels of escala tion, irrespectively of the immediate presence of proceptive females, since the benefits at stake are very high to both contenders. In addition, fights between young adult males are more likely to result in injury than contests with older foes partly because the canines of the latter are usually bro ken, worn, or both (Packer, 1979b; Smuts, 1985, p. 146). Also, while the frequency and severity of fighting over rank is expected to be minimized among close relatives (West-Eberhard, 1975), adult male baboons in a troop are unlikely to be closely related (Packer, 1979a) and thus, their aggression is usually not constrained by kinship. Hostility towards immigrant males sometimes even results in the eviction of the newcomer (Drews, 1993b, p. 312 jj). A similar pattern is found in other multi-male primate species, in which violent fights and severe wounds in adult males (and females) are associated with male immigrations (e.g. rhesus macaques: Lindburg, 1969; Vessey, 1971; squirrel monkeys: Baldwin, 1968). In captive rhesus macaques a newly arrived male may effectively join a group with high initial status if he can inflict a few quick injuries to the resident males (Bernstein et al., 1974). Injury in male yellow baboons was associated with immediate compe tition over proceptive females in three of the ten witnessed incidents of wounding. Injury to at least one of the contestants was caused in three (23 %) out of 13 aggressive consort take-overs witnessed, a proportion similar to that of male gelada baboons fighting over groups of females, whereby four (25%) out of 16 fights led to severe injury (Dunbar, 1984). Among the olive baboons studied by Bercovitch (1988) this proportion was smaller: four (9%) out of 46 aggressive take-overs included wound ing. None of the fights observed by Kummer (1968, p. 50) between male hamadryas baboons was over proceptive females, but rather over long term possession of a female in the harem. Competition over mating opportuni
ties is probably a relatively common context of damaging fights in other primates as well. Male macaques are wounded more frequently during the mating than during the non-mating season (Vandenbergh & Vessey, 1968; Wilson & Boelkins, 1970; Dittus, 1977; review in Symons, 1978, p. 173, 174), and 87% of male deaths (but not of females) occur during the mating season in Cayo Santiago (Wilson & Boelkins, 1970). Simi larly, in microtine rodents (Turner & Iverson, 1973; Rose & Gaines, 1976; Rose, 1979), pinnipeds (e.g. Le Boeuf, 1971) and ungulates (e.g. Wilkinson & Shank, 1977; Clutton-Brock et al., 1979,1982, p. 132jf), high levels of wounding in males are associated with the reproductive period. The proportion of damaging fights among combats associated with immediate reproductive competition is higher in baboons than in ungulates for which such proportions have been reported (less than 3%: Clutton-Brock et al., 1979; Fryxell, 1987). Challenges to the resident alpha male and fights over proceptive females are the contexts which most directly affect the reproductive success of male baboons and, therefore, escalation risking injury may payoff for both contestants in such situations (Enquist & Leimar, 1990). Fights over unusual foods (also Ransom, 1981), intertroop encounters, female defense, redirected aggression and some fights unrelated to any obvious resource also resulted in injury, however. The relative contributions of these contexts to the incidence of male wounds cannot be estimated with confidence from the small sample of ten witnessed inflictions of injury. This diversity of contexts can obscure a simple unifactorial effect in analyses of determinants of wounding incidence.
Implications of injury to male baboons
Wounds sustained in fights between male baboons can imply loss of eye sight (Packer, 1979b, two cases), bacterial infection (Bramblett, 1967; Alt mann, 1980, p. 210 and p. 214) and increased vulnerability to parasites. Feeding impairments result from injury in the mouth region (P.c. Lee, pers. cornm.; this study). Wounds on forelimbs can also impair feeding by constraining the rate at which food items are processed, since baboons use their hands to pick these items. Also, injury resulting in limping can hinder low ranking male baboons from their typical running ahead of the troop to utilize for some minutes a good feeding site, prior to the arrival
INJURIES IN MALE BABOONS
of higher ranking males (pers. obs.). Such locomotory handicaps imply additional energy expenditure, impaired flight response during predator at tack and impaired climbing ability limiting efficient access to food and safe retreats. Furthermore, injury can affect the social activity of male baboons, as shown in this study in the form of a reduction in the rate of interactions initiated. Similarly, injured olive baboon males generally avoid interacting with other males (Popp, 1978, p. 100; Harding, 1980; Ransom, 1981), whereas other troop males seek out repeatedly and aggressively the handicapped peer (Harding, 1980). As a consequence, some injured males become peripheral or emigrate temporarily (Harding, 1980; Collins, 1981, p. 336; this study). The costs of non-lethal injury in male baboons can be substantial. Such injury, particularly when impairing locomotion, can affect fitness directly by reducing the victim's competitive ability, causing drops in dominance rank and jeopardizing its mating success. Drops in dominance associated with injury to males as observed during this study have been reported from another population of yellow baboons (Altmann, 1980, p. 210) and for olive baboons (Popp, 1978, p. 100; Ransom, ] 981). A drop in dominance rank implies for the victim an increment in the number of potential supplanters and aggressors. Injuries have been found to reduce the reproductive activity of male baboons in at least six independent cases (Packer, 1979b; Collins, ]981, p. 336; Smuts, 1985, p. 133). In other male primates, injury or illness also results sometimes in drops in dominance (e.g. rhesus macaques: Kaufmann, 1967; Vandenbergh, 1967; chimpanzees: Bygott, 1979) and in a reduction in mating activity (e.g. squirrel monkeys: C. Mitchell pers. comm. to Baldwin, 1992; rhesus macaques: Conaway & Koford, 1965; Loy, 1971). Fights between male baboons can result in death to a combatant. Ransom (1981) reported that an old, adult olive baboon male in Gombe National Park sustained a slash wound on his inner thigh in a fight with another male over bananas. The femoral artery was severed and the male bled slowly to death. Another male at the same site is suspected to have died in a fight over a proceptive female (1. Goodall pers. comm. to Packer, 1979b). In Amboseli (Kenya), a high ranking male suffered a severe leg injury probably inflicted by an uprising natal male (Altmann, 1980, p. 205 and p. 214). The puncture wounds became badly infected until a month
later the male could hardly move and disappeared overnight. Two olive baboon males were killed as single combatants against coalition attacks on independent occasions in the Masai Mara, Kenya (Popp, 1978, p. 96). Popp inferred that approximately 20-30% of all adult males in this area die directly from injuries received from other males and that almost all of these lethal injuries are inflicted by coalitions. Bercovitch (1988), however, conjectures that baboon male coalitions in Gilgil, Kenya, are less likely to result in injury than dyadic fights, both on an absolute and a per capita risk basis. Canine gashes sustained during fights were the major cause of mortality in male chacma baboons Papio ursinus belonging to a desert troop (Brian, 1992). In that study, four males died and two disappeared after sustaining serious wounds during fights. These lethal fights occurred during male immigration and competition over reproductive females (Brian, 1992). Lethal injuries sustained in fights between males are known from other primates as well (e.g. rhesus macaques: Lindburg, 1971; chimpanzees: Goodall, 1986, p. 503 jf). Across anthropoid primates there is a positive association between fre quency and intensity of escalated aggression between males and the degree of canine dimorphism in the species (Plavcan & van Schaik, 1992). It is argued that selection has favoured large canines in male primates as a means to enhance the chances of winning fights (also Martin et al., 1994). This argument rests on the assumption that effective use of canines during escalated contests leads to injuries resulting in costs to the opponent. The evidence reviewed here shows that the handicaps resulting from damaging fights in male baboons and other primates can be substantial. In general, the balance between value of resource contested and future reproductive prospects is a major determinant of the likelihood of severe injury in fights (Enquist & Leimar, 1990). Although the implications of injury sustained in fights between male baboons can be considerable, it should be noticed that most wounds were small, healed well and did not seem to affect fitness in any direct way, for not uncommonly the victim of wounding was the winner of the fight (also in elephant seals: Le Boeuf, 1971). Thus, while the risk of injury attached to escalated contests be tween males can be a more or less constant value, the costs resulting from injury can vary considerably. It is likely that chance determines to some extent the severity of canine slashes inflicted in a fight, i.e. the depth of
INJURIES IN MALE BABOONS
the wound, organs affected, etc. Consequently, the decision to escalate a fight should incorporate a low predictability of injury costs in damaging encounters. In conclusion, the costs potentially associated with escalated aggression seem high enough to exert strong selective pressure to both possess highly damaging weaponry and to avoid escalated confrontations. Avoidance of escalated confrontations is seen in the very low percentage of such es calation from the total of aggressive contests between males. Although escalation is generally avoided, the high interaction rate between male ba boons results in a relatively high risk of injury. The intra-sexual selective pressure acting on males is reflected in the fact that male baboons are repeatedly injured in fights during their lifetime. The implications of in jury listed above are the basis to understand patterns of contest avoidance, peaceful conflict resolution, punishment (Clutton-Brock & Parker, 1995), as well as the dynamics of dominance relationships between male baboons and possibly other primates with similar patterns of reproductive competi tion.
Altmann, J. (1980). Baboons mothers and infants. - Harvard University Press, Cambridge. - - , Hausfater, G. & Altmann, S.A. (1988). Determinants of reproductive success in savannah baboons, Papio cynocephalus. - In: Reproductive success (TH. CIutton Brock, ed.). University of Chicago Press, Chicago and London, p. 403-418. Altmann, S.A. & Altmann, J. (1970). Baboon ecology: African field research. - University of Chicago Press, Chicago. Baldwin, J.D. (1968). The social behaviour of adult male squirrel monkeys (Saimiri sciureus) in a seminatural environment. - Folia primatol. 9, p. 281-314. - - (1992). Determinants of aggression in squirrel monkeys (Saimiri). - In: Aggression and peacefulness in humans and other primates (J. Silverberg & J.P. Gray, eds). Oxford University Press, New York, p. 72-99. Beaugrand, J., Goulet, C. & Payette, D. (1991). Outcome of dyadic conflict in male green swordtail fish, Xiphophorus helleri, effects of body size and prior dominance. Anim. Behav. 41, p. 417-424. Bercovitch, F.B. (1988). Coalitions, cooperation and reproductive tactics among adult male baboons. - Anim. Behav. 36, p. 1198-1209. Bernstein, I.S. & Gordon, TP. (1974). The function of aggression in primate societies. Am. Sci. 62, p. 304-311. - - , Gordon, TP. & Rose, R.M. (1974). Factors influencing the expression of aggression during introduction to rhesus monkey groups. - In: Primate aggression, territoriality and xenophobia (R.L. Holloway, ed.). Academic Press, New York, p. 211-240.
Boelkins, R.e. & Wilson, A.P. (1972). Intergroup social dynamics of the Cayo Santiago rhesus (Macaca mulatta) with special reference to changes in group membership by males. - Primates 13, p. 125-139. Bradshaw, J.L. & Rogers, L.J. (1993). The evolution of lateral asymmetries, tool use and intellect. - Academic Press, San Diego, California. Bramblett, e.A. (1967). Pathology in the Darajani baboon. - Am. J. phys. Anthropol. 26, p.33l-340. Brain, e. (1992). Deaths in a desert baboon troop. - Int. J. Primatol. 13, p. 593-599. Bygott, J.D. (1979). Agonistic behavior, dominance, and social structure in wild chim panzees of the Gombe National Park. - In: The great apes (D.A. Hamburg & E.R. McCown. eds). The Benjamin/Cummings Publishing Company, Menlo Park, p.405-427. Christian, J.1. (197]). Fighting, maturity, and population density in Microtus pennsylvanicus. - J. Mammal. 52, p. 556-567. Clutton-Brock, T.H. & Albon, S.D. (1979). The roaring of red deer and the evolution of honest advertisement. - Behaviour 69, p. 145-170. - - , - - , Gibson, R.M. & Guiness, F.E. (1979). The logical stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). - Anim. Behav. 27, p. 211-225. - - , Guiness, F.E. & Albon, S.D. (1982). Red deer. Behavior and ecology of two sexes. - Edinburgh University Press, Edinburgh. - - & Parker, G.A. (1995). Punishment in animal societies. - Nature 373, p. 209-216. Collins, D.A. (1981). Social behaviour and patterns of mating among adult yellow baboons (Papio cynocephalus cynocephalus L. 1766). - PhD thesis, University Microfilms International 8270026, Ann Arbor. - - & McGrew, W.e. (1988). Habitat of three groups of chimpanzees (Pan troglodytes) in Western Tanzania compared. - J. Human Evo!. 17, p. 553-574. Conaway, e.H. & Koford, e.B. (1965). Estrous cycles and mating behavior in a free-ranging band of rhesus monkeys. - 1. Mammal. 45, p. 577-588. Davies, N.B. (1978). Territorial defence in the speckled wood butterfly (Pararge aegeria): the resident always wins. - Anim. Behav. 26, p. 138-147. Dingle, H. (1983). Strategies of agonistic behaviour in crustacea. - In: Studies in adap tation. The behaviour of higher crustacea (S. Rebach & D.W. Dunham, eds). John Wiley, New York, p. 85-111. Dittus, W. (1977). The social regulation of population density and age-sex distribution in the toque monkey. - Behaviour 63, p. 281-322. Dow, M., Ewing, A.W. & Sutherland, I. (1976). Studies on the behaviour of cyprinodont fish. III. The temporal patterning of aggression in Aphyosemion striatum (Boulenger). - Behaviour 59, p. 252-268. Drews, e. (1993a). The concept and definition of dominance in animal behaviour. - Be haviour 125, p. 283-313. - - (1993b). Psychological warfare and the management of relationships between male baboons (Papio cynocephalus). - PhD thesis, University of Cambridge, Cam bridge. Drickamer, L.e. (1975). Quantitative observation of behaviour in free-ranging Macaca mulatta: methodology and aggression. - Behaviour 55, p. 209-236.
INJURIES IN MALE BABOONS
Dunbar, RI.M. (1984). Reproductive decisions: An economic analysis of ge1ada baboon social strategies. - Princeton University Press, Princeton. Enquist, M. & Leimar, O. (1990). The evolution of fatal fighting. - Anim. Behav. 39, p. 1-9. Fagot, J. (1993). Ontogeny of object manipulation and manua11atera1ization in the Guinea baboon: preliminary observations. - In: Primate laterality (J.P. Ward & W.D. Hop kins, eds). - Springer-Verlag, New York. FryxeIl, J.M. (1987). Lek breeding and territorial aggression in white-eared kobo - Ethology 75, p. 211-220. Geist, V. (1966). The evolution of horn-like organs. - Behaviour 27, p. 175-214. - - (1971). Mountain sheep: a study in behavior and evolution. - University of Chicago Press, Chicago. - - (1978). On weapons, combat and ecology. - In: Aggression, dominance and indi vidual spacing (L. Krames, P. Pliner & T. Alloway, eds). Plenum Press, New York. - - (1986). New evidence for high frequency of antler wounding in cervids. - Can. J. Zoo!' 64, p. 380-384. Goodall, J. (1986). The chimpanzees of Gombe. - The Belknap Press of Harvard University Press, Cambridge, MA and London. Haley, M.P. (1994). Resource-holding power asymmetries, the prior residence effect, and reproductive payoffs in male northern elephant seal fights. - Behav. Eco!. Sociobio!. 34, p. 427-434. Harding, RS.O. (1980). Agonism, ranking, and the social behavior of adult male baboons. - Am. J. phys. Anthropo!. 53, p. 203-216. Harrison Matthews, L. (1964). Overt fighting in mammals. - In: The natural history of aggression. Institute of Biology Symposium No. 13 (J.D. Carthy & F.J. Ebling, eds). - Academic Press, London. Harvey, P.H., Kavanagh, M. & Clutton-Brock, T.H. (1978). Sexual dimorphism in primate teeth. - J. Zoo!' Soc. Lond. 186, p. 475-485. Hausfater, G. (1972). Intergroup behaviour of free-ranging rhesus monkeys (Macaca mu latta). - Folia primato!. 18, p. 78-107. - - (1975). Dominance and reproduction in baboons (Papio cynocephalus): a quantitative analysis. - Contrib. Primato!. 7, p. 1-150. Havkin, Z. & Fentress, J.e. (1985). The form of combative strategy in interactions among wolf pups. - Z. Tierpsycho!. 68, p. 177-200. Huntingford, F.A. & Turner, A.K. (1987). Animal conflict. - Chapman & Hall, London. Hyatt, G.W. & Salmon, N. (1978). Combat in the fiddler crabs Uca pugilator and Uca pugnax: a quantitative analysis. - Behaviour 65, p. 182-211. Jones, A.R (1980). Chela injuries in the fiddler crab, Uca burgersi. - Mar. Behav. Physio!. 7, p. 47-56. Kaufmann, J.H. (1967). Social relations of adult males in a free-ranging band of rhesus mon keys. - In: Social communication among primates (S.A. Altmann, ed.). University of Chicago Press, Chicago and London, p. 73-98. Kummer, H. (1968). Social organization of hamadryas baboon, a field study. - Karger, Basel. Laudien, H. (1965). Untersuchungen tiber das Kampfverhalten des Mannchen von Betta splendens Regan (Anabantidae, Pisces). - Z. Wiss. Zoo!' 172, p. 134-178.
Le Boeuf, B.J. (1971). The aggression of breeding bulls. - Nat. Hist. 80, p. 82-94. Lincoln, G.A. (1994). Teeth, horns and antlers: the weapons of sex. - In: The differ ences between the sexes (RY. Short & E. Balaban, eds). Cambridge University Press, Cambridge, p. 131-158. Lindburg, D.G. (1969). Rhesus monkeys: mating season mobility of adult males. - Science 166, p. 1176-1178. - - (1971). The rhesus monkey in North India: An ecological and behavioral study. - In: Primate behavior Vol. 2 (L.A. Rosenblum, ed.). Academic Press, New York, p.2-106. Loy, J. (1971). Estrous behavior of free-ranging rhesus monkeys. - Primates 12, p. 1-31. Marchant, L.P. & McGrew, W.C. (1991). Laterality of function in apes: a meta-analysis of methods. - J. Human Evol. 21, p. 425-438. Marden, J.H. & Waage, J.K. (1990). Escalated damselfly territorial contests are energetic wars of attrition. - Anim. Behav. 39, p. 954-959. Martin, RD., Willner, L.A. & Dettling, A. (1994). The evolution of sexual size dimorphism in primates. - In: The differences between the sexes (RY. Short & E. Balaban, eds). Cambridge University Press, Cambridge, p. 159-200. Maynard-Smith, 1. (1974). The theory of games and the evolution of animal conflict. J. theor. BioI. 47, p. 209-221. - - & Price, G.R (1973). The logic of animal conflict. - Nature, Lond. 246, p. 15-18. Nishida, T. (1993). Left nipple suckling preference in wild chimpanzees. - Ethol. Sociobiol. 14, p. 45-51. Norton, G.W., Rhine, RJ., Wynn, G.W. & Wynn, R.D. (1987). Baboon diet: a five year study of stability and variability in the plant feeding and habitat of the yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. - Folia primatol. 48, p. 78 120. Noe, R. & Sluijter, A. (1990). Reproductive tactics of male savanna baboons. - Behaviour 1J3, p. 117-170. Owens, N.W. (1975). A comparison of aggressive play and aggression in free-living ba boons, Papio anubis. - Anim. Behav. 23, p. 757-765. Packer, C. (1979a). Inter-troop transfer and inbreeding avoidance in Papio anubis. - Anim. Behav. 27, p. 1-36. - - (1979b). Male dominance and reproductive activity in Papio anubis. - Anim. Behav. 27, p. 37-45. - - (1983). Sexual dimorphism: the horns of African antelopes. - Science 221, p. 1191 1193. Parker, G.A. (1974). Assessment strategy and the evolution of fighting behaviour. - J. thcor, BioI. 47, p. 223-243. - - & Thompson, E.A. (1980). Dung fly struggles: a test of the war of attrition. Behav. Ecol. Sociobiol. 7, p. 37-44. Paterson, J.D. (1973). Ecologically differentiated patterns of aggressive and sexual behavior in two troops of Ugandan baboons, Papio anubis. - Am. J. phys. Anthropol. 38, p. 641-648. Plavcan, .T.M. & van Schaik, C.P. (1992). Intrasexual competition and canine dimorphism in anthropoid primates. - Am . .T. phys. Anthropol. 87, p. 461-477.
INJURIES IN MALE BABOONS
Poole, TB. (1973). The aggressive behaviour of individual male polecats (Mustela putorius, M. furo and hybrids) towards familiar and unfamiliar opponents. - J. Zool., Land. 170, p. 395-414. Popp, J.L. (1978). Male baboons and evolutionary principles. - PhD thesis, Harvard Uni versity, Cambridge, MA. - - & DeVore, I. (1979). Aggressive competition and social dominance theory: syn opsis. - In: The great apes (D.A. Hamburg & E.R McCown, eds). The Ben jamin/Cummings Publishing Co., Menlo Park, p. 317-338. Post, D.G., Hausfater, G. & McCuskey, S.A. (1980). Feeding behavior of yellow baboons (Papio cynocephalus): relationship to age, gender and dominance rank. - Folia pri matol. 34, p. 170-195. Ransom, TW. (1981). Beach troop of the Gombe. - Associated University Press. Rhine, RJ. (1986). Ten years of cooperative baboon research at Mikumi National Park. - In: Primate ontogeny, cognition and social behaviour (J.G. Else & P.C Lee, eds). Cambridge University Press, Cambridge, p. 13-22. Rose, RK. (1979). Levels of wounding in the meadow vole Microtus pennsylvanicus. 1. Mammal. 60, p. 37-45. - - & Gaines, M.S. (1976). Levels of aggression in fluctuating populations of the prairie vole, Microtus ochrogaster, in eastern Kansas. - J. Mammal. 57, p. 43-57. Schultz, A.H. (1969). The life of primates. - Universe Books, New York. Simpson, M.J.A. (1968). The display of the Siamese fighting fish, Betta splendens. - Anim. Behav. Monogr. 1, p. 1-73. Smith, S. & Hosking, E. (1955). Birds fighting, experimental studies of the aggressive displays in some birds. - Faber & Faber Ltd., London. Smuts, B.B. (1985). Sex and friendship in baboons. -- Aldine, New York. - - (1987). Gender, aggression and influence. - In: Primate societies. (B.B. Smuts, D.L. Cheney, R.M. Seyfarth, RW. Wrangham & TT Strushaker, eds). University of Chicago Press, Chicago, p. 400-412. Southwick, CH., Siddiqui, M.R, Farooqui, M.Y. & Pal, B.C (1974). Xenophobia among free-ranging rhesus groups in India. - In: Primate aggression, territoriality and xeno phobia (RL. Holloway, ed.). Academic Press, New York, p. 185-209. Stout, J.E (1975). Aggressive communication by Larus glaucescens. III. Description of the displays related to territoriality protection. - Behaviour 55, p. 181-208. Symons, D. (1978). Play and aggression: A study of rhesus monkeys. - Columbia Uni versity Press, New York. Thornhill, R (1984). Fighting and assessment in Harpobittacus scorpionflies. - Evolution 38, p. 204-214. Turner, B.N. & Iverson, S.L. (1973). The annual cycle of aggression in male Microtus pennsylvanicus and its relation to population parameters. - Ecology 54, p. 967-981. Vandenbergh, J.G. (1967). The development of social structure in free-ranging rhesus mon keys. - Behaviour 29, p. 179-194. - - & Vessey, S. (1968). Seasonal breeding of free-ranging rhesus monkeys and related ecological factors. - J. reprod. Fertil. 15, p. 71-79. Vauclair, J. & Fagot, J. (1993). Manual specialization in gorillas and baboons. - In: Primate laterality (J.P. Ward & W.D. Hopkins, eds). Springer Verlag, New York.
Vessey, S.H. (1971). Free-ranging rhesus monkeys: behavioural effects of removal, separa tion and reintroduction of group members. - Behaviour 40, p. 216-227. Vogt, F. (1948). Oas Rotwild. - Osterreichischer Jagd- und Fischerei- Verlag des N.-b. Landesjagdverbandes, Vienna. Walther, FR. (1974). Some reflections on expressive behaviour in combats and courtship of certain horned ungulates - In: The behaviour of ungulates and its relation to management, Vol. I (V Geist & FR. Walther, eds). IUCN, Morges. Ward, J.P. & Hopkins, W.O. (eds) (1993). Primate laterality: current behavioral evidence of primate asymmetries. - Springer-Verlag, New York. West-Eberhard, MJ. (1975). The evolution of social behavior by kin selection. - Q. Rev. BioI. 50, p. 1-33. Wilkinson, P.F. & Shank, c.c. (1977). Rutting-fight mortality among musk oxen on Banks Island, Northwest Territories, Canada. - Anim. Behav. 24, p. 756-758. Wilson, A.P. & Boelkins, R.c. (1970). Evidence for seasonal variation in aggressive behav ior by Macaca mulatta. - Anim. Behav. 18, p. 719-724.