Possible causes of injury

Although the exact circumstances of Walimah’s injury and loss of her infant can never be positively determined, we can evaluate both the possible and the probable causes of these events. Given that the loss of an infant orangutan and a severe injury to a female are both extremely rare, they occurred very close in time, and neither has been seen in over 30 years of research at this site, we argue that it is most parsimonious, without any evidence to the contrary, that these events occurred at the same time, due to the same cause. However, we cannot rule out the possibility that this injury and infant loss were separate events.

Mechanical injury

We ruled out the possibility that Walimah’s injury was caused by a mechanical injury such as being struck by a falling tree or branch or falling out of a tree. While such things are possible, but unlikely, events for orangutans, such an injury would lead to a fracture wound, not the loss of a large chunk from the middle of her foot. There are also no known cases of other kinds of mechanical injuries to orangutans caused by environmental hazards.

Sunbear

Gunung Palung National Park hosts a population of sun bears (Helarctos malayanus). These are the smallest bears in the world, weighing 25–65 kg60,61. They are opportunistic omnivores, primarily eating fruit, and augmenting their diet with stingless honey bees, termites, ants, larva, honey and small mammals62,63,64. Sunbears travel on the ground and are able to forage arboreally60. Although the mean width of sun bear canines (6.08 cm)65 is large enough to deliver the wound we observed, a sun bear attack seems highly unlikely for the following reasons. First, there are no known attacks of sunbears on orangutans61,62,66,67,68. In fact, we were unable to find any accounts of sunbear attacks on any large animals except for humans, either on the ground or in the trees61,62,66,67,68. Sun bears are normally passive, but there have been occasional attacks on humans when surprised69,70,71. Second, this kind of wound is not consistent with a sun bear attack. They have poor eyesight and attacks on humans typically happen when they are startled at close range69,70,71. One such attack on a human occurred at our research site in 2000 and involved a canine puncture wound. Walimah showed no puncture injuries. Furthermore, attacks typically also involve scratches from the sun bears’ sharp claws, and scratches were not present on Walimah. Third, an orangutan that did encounter a sun bear could easily escape vertically, being a far superior climber. Although they are arboreal, sun bears claw their way up and down tree trunks vertically60,72. They are unable to swing or jump between trees73. Orangutans, however, are extremely adept arboreal climbers and are easily able to move between trees. Thus, an orangutan confronted by a sun bear in the canopy could easily escape. Therefore, we conclude that the nature of the injury, the lack of any prior attacks on orangutans, and the typical behavioral patterns observed in both sun bears and orangutans do not support a sun bear as a likely cause of this injury.

Clouded leopard

The largest feline predator in Borneo is the clouded leopard (Neofelis diardi borneensis)74. Clouded leopards are medium-sized felids, ranging from 11 to 23 kg in weight75,76, that typically prey on small animals, such as juvenile bearded pigs, small deer, pangolins, monkeys and squirrels. Clouded leopards, like most cats, kill by stalking their prey, and jumping on them from behind73,77. Prey are dispatched by delivering one killing bite to the neck or back, with their long canines severing the spinal cord78,79,80. Once a bite is made, the cat typically holds on until the animal dies73,80. This is opposed to canids that deliver multiple, slashing bites79. Clouded leopards have the longest canines for their body size of any cat and their canines have the highest breaking point79,80,81. Their small size and slender canines give them the weakest bite force (344.2 N) of any of the medium to large-sized felids79,80,81. Large cats have much greater bite forces (e.g. 1234.3 N in the tiger, Panthera tigris)80,82. Clouded leopard attacks involve puncture wounds on the spine, at the back of the neck, as well as claw scrapes75,77. The puncture wounds on one animal, known to have been killed by a clouded leopard, had an inter-canine width of 3 cm75. Clouded leopard attacks on infant and juvenile proboscis monkeys (Nasalis larvatus) consist of bites to the necks, delivered from behind83. Another reported clouded leopard attack involved a juvenile, 3.7 kg, siamang (Symphalangus syndactylus) with a severed vertebrae at C284. There are no reported cases of clouded leopard attacks involving wounds other than on the neck or back73,75,76,77,78,85,86.

There are no observed cases of clouded leopards attacking orangutans, but there are several suspected cases. One juvenile orangutan died of injuries that were suspected of being caused by a clouded leopard87. This attack was not witnessed, but the authors argue that a clouded leopard is implicated due to two puncture wounds on the back87. At Tuanan Research Station, an adult female orangutan is suspected of having been killed by a clouded leopard18. However, this was an atypical female who lost her home range due to mining, logging, and fires and regularly traveled on the ground88. Her unusually high level of ground travel would have made her vulnerable to such an attack. The nature of the injuries that led to this suspicion have not been described. Additionally, Rijksen89 reports that 7 juvenile, ex-captive, rehabilitant orangutans on Sumatra, each weighing less than 10 kg, were apparently killed by a clouded leopard while walking on the ground around the feeding station. Given the nature of the attacks, Rijksen89 concluded that clouded leopards are too small to successfully prey on larger orangutans and that juveniles accompanied by their mothers would be protected from attack. He also attributes these deaths to one individual clouded leopard that had discovered the vulnerability of these rehabilitant juveniles at the feeding station. We could find no other reports of attempted or successful clouded leopard attacks on orangutans73,76,77,78,85,86.

Both the location and nature of Walimah’s injuries are thus inconsistent with a clouded leopard attack for the following reasons. First, clouded leopards stalk their prey and then attack from the back, delivering puncture wounds to the head, neck and upper extremities90,91. Previously known or suspected cases of clouded leopard attacks on orangutans involved such injuries. Walimah’s injury did not involve a puncture wound and was delivered to the foot. Second, the canine width of clouded leopards is significantly smaller than the estimated width of Walimah’s injury. The injury to Walimah’s foot was estimated to be a minimum of 5 cm wide, significantly larger than the 3 cm inter-canine width of a clouded leopard. Third, the clouded leopard is a small cat that kills successfully by using their extremely long canines to sever the spinal cord. They have a weak bite force and thus are unlikely to have the jaw strength to bite through and remove bone from an orangutan’s foot.

Human

Another possible source of attack is from a human. Humans do attack and kill female orangutans to take their infants92. However, we do not suspect that this was a human attack. First, all known cases of humans taking infants involve the use of guns of some sort93, and the mother is killed. Because the infant was being carried on her body, the only way a human would have been able to take this infant would have been by shooting the mother and then taking the infant after the mother fell from the tree. There is no evidence that Walimah had any injuries associated with being shot or having fallen. Hunters, or local people, may carry a parang (machete) into the forest. But, Walimah’s injury does not involve a cut or slice that could have been delivered by a parang. We also note that there are no metal animal snares found in this forest, as are seen in some African forests94,95 and thus we can also rule out a snare injury.

Orangutan

The only source of recorded injury for wild orangutans at this study site are adult male orangutans. Orangutan males are known to attack and wound other males96,97. In our review of orangutan wounding patterns at Gunung Palung59 we found that 81% of males, who had been followed for at least 5 days, had sustained orangutan-inflicted wounds. Of these, 35% were to the hands and feet. Male orangutans often are seen with bent or missing digits caused from bites delivered by other males96,97. Furthermore, caged male orangutans have been known to bite off the fingers of their human keepers. Thus, male orangutans regularly bite the hands and feet of other male orangutans and are capable of biting off pieces of flesh and bone. We suggest that this is what may have happened to Walimah as she fought with a male during an attack that was aimed at killing her infant.

The nature of the wound itself is also consistent with an orangutan attack. We estimated the wound as being at least 5 cm wide (Fig. 5), within the range of orangutan canine breadth (Table 2). An adult male orangutan would also have the strength and ability to deliver such a wound. Orangutan males, both flanged and unflanged, sometimes forcibly copulate with females25,37,98. Although forced matings are not known to result in serious injury to females25, they do indicate that both flanged and unflanged male orangutans are able to restrain and overpower females46. Finally, orangutans were calculated to have a bite force of 2560 N at the 2nd molar (the position where bite force was measured)99, an order of magnitude greater than the 344N bite force of the clouded leopard at the canine or 547 N at the carnassial (the 4th upper premolar and 1st lower molar)80,100. It is worth noting that the bite force of an orangutan is far greater than even a tiger. Orangutans have powerful bites because some of their foods, particularly seeds, are extremely hard and they feed by crushing these food items101. Cats on the other hand, kill by puncturing with their canines, and feed by tearing, not crushing their prey.

Walimah’s injury represents the first known wounding attack on a female orangutan at Gunung Palung. Attacks and injuries to female orangutans, in general, are very rare102. However, such attacks have been reported from Tuanan Research Station102 where it has recently been reported that there was a fatal coalitionary attack by a young female and an unflanged male on an older resident female who had a four-year-old offspring88. The authors argue that although the young female initiated the attack, it proved lethal when she was joined by an unflanged male, who delivered the most severe injuries, including a serious bite to the foot. The authors speculate that it was the presence of two individuals that led to the female’s death, as she couldn’t escape, and it was the male who delivered the fatal injuries. They also conclude that the attacking female could not have successfully carried out this attack alone.

Although we cannot rule out the possibility that Walimah was attacked by another adult female orangutan, or that a female joined a male in an attack, we argue that this scenario is less likely than a solo attack by a male. First, female-female antagonism, and particularly direct contact, is rare in orangutans. In our study of female-female competition103 we recorded only 97 incidents of female-female aggression in 7041 orangutans follows (1.3%) and this was all non-contact aggression. Second, in the Tuanan case, the injured female had repeatedly been in antagonistic interactions with the attacking female88. We observed no cases of female harassment of Walimah in over 15,000 hours of observation. Third, no other injuries were found on Walimah. If the aim of the attack was lethal aggression against Walimah, rather than Walimah getting in the way of an attack on her infant, we would have expected additional injuries. While it is possible that Walimah herself was the victim of the attack and was unable to care for her infant after the injury, this seems unlikely due to the lack of additional injuries, such as seen in the Tuanan case. Infanticide by females is more common in mammalian species with intense resource competition104. While orangutans do experience some forms of resource competition103,105, it seems unlikely that a female orangutan was capable of carrying out this attack on her own. This is also apparently the case in chimpanzees where all cases of female infanticide have been carried out by a pair or group of females106,107. Fourth, as Marzec et al.88 found, instances of females attacking other females are very rare and are not known to cause severe injury, and they argue that a female would not have been able to deliver bites of the same force as a male. Indeed, the force of the bite needed to sever a portion of Walimah’s foot would have been substantial, but based on other orangutan injuries observed, is well within the capabilities of a flanged or unflanged adult male. Orangutans exhibit extreme sexual dimorphism, with flanged males being twice the size of adult females108,109,110. Unflanged males are closer to female size, but are still larger111. We also know from the regular occurrence of forced copulations that both types of male can easily overpower females25. Along with their larger bodies, males have substantially larger jaws and canines, with Bornean males having canines that are 1.48–1.63 times longer than those of females112,113. This evidence, combined with the semi-solitary nature of orangutans, makes it most likely that a single adult male orangutan carried out the attack.

We also argue that it is highly unlikely that Walimah was attacked by a male during a forced copulation. Orangutans have a mean inter-birth interval of 7.6 years17 and a mean interval of postpartum amenorrhea of 5.4 years19. This attack occurred 4 months after Walimah gave birth, many years before she would be expected to start ovulating again. Orangutan males typically avoid mating with females with very young infants, preferring to mate with reproductive females98. Furthermore, in an earlier review of forced copulations in wild orangutans, Knott25 found that although a male may attempt to restrain a female during forced copulations, which can include hitting and biting the female, there are no reports of bites ever breaking the skin. In fact, there are no reports of females receiving wounds of any kind, including soft tissue injuries.

However, injuries do sometimes occur in cases of sexually selected infanticide by males (Table 3), especially in great apes. Although in the majority of cases of primate infanticide mothers are not injured, this may be due to the fact that in some species males are more likely to attack infants who are not clinging to their mother’s body (e.g. Hanuman langurs, Semnopithecus entellus)114. However, Walimah’s infant was clinging 100% of the time before she disappeared, which is typical of ape infants less than 3 months of age115,116,117,118. In orangutan infants of 3–6 months of age, time spent off the mother’s body is minimal (21% of the time), always within the same tree and they are never more than 10 meters away116. Scott and Knott119 found that when males approach, the distance between mothers and infants also decreases, and no infant younger than 10 months was recorded out of contact with his or her mother when a male was present. Thus, an infanticide would have involved a very close association between the mother and the attacker, which would have increased the possibility of injury to the mother. Table 3 shows that when mothers are injured during successful infanticidal attacks, they are often injured on the extremities, consistent with the location of Walimah’s injury. Although rare, there are instances of male infanticide in primates where the male has taken an infant off of the female’s ventrum7,120. Based on the evidence, we conclude that the most probable cause of Walimah’s injury was a bite by a male orangutan during a successful infanticidal attack on her infant.

Infanticide risk in primiparous females

Promiscuous mating by females serves to establish a nonzero chance of paternity among multiple males, thereby decreasing the risk of infanticide2. We suggest that in species where females mate with multiple males, primiparous mothers are at increased risk of infanticidal attack due to the fact that nulliparous females are not preferred as mating partners by males121, and thus they are less successful at employing promiscuous mating for paternity confusion as a counter-tactic to infanticide. Muller et al.122 found that male chimpanzees prefer mating with older, parous females over both nulliparous and young parous females, and suggest that this may be a result of accumulated maternal experience leading to lower rates of infant mortality for these mothers, or the possibility that their advanced age signals higher genetic quality. Anderson121 argues that the lack of male mating interest in primiparous females, across many primate species, is due to lower birth rates and lower infant survivorship for these inexperienced mothers. Additionally, primiparous females often have long periods of adolescent subfecundity15,123,124,125. The low probability of conception by these females may make them less attractive122 which may explain why males are not interested in mating with them. Orangutans, have a 4 year period of adolescent subfecundity15, likely the longest of any of the primates. As documented in other primates (chacma baboons, Papio ursinus126; chimpanzees, Pan troglodytes127; ring-tailed lemurs, Lemur catta128; mandrills, Mandrillus sphinx129), male orangutans seem to have low interest in mating with young nulliparous females34,54,55. Thus, if female orangutans rely on promiscuous mating as an anti-infanticide tactic2,35, nulliparous females, being less attractive to males, would have little opportunity to wield this tactic effectively. Without being able to effectively employ this behavioral counter-tactic, primiparous females should be at a higher risk of infanticidal attack compared to multiparous females.

Walimah’s case fits this prediction as she was a primiparous mother and was only seen mating with two males during her peri-conceptive period. As described, Walimah had long, elaborate, extremely proceptive sexual interactions with one flanged male, Codet, and comparatively short and notably less proceptive and even non-receptive matings with one unflanged male. Walimah displayed 7 months of high interest in Codet, before they successfully mated. We argue that because she invested so heavily in mating with this flanged male (Table 1), she did not mate with more of the other males in the study site. Given these observations of Walimah, along with our observations of other nulliparous female mating events that were similar, and the description Schürmann54 provided of nulliparous female and flanged male mating events, it seems that nulliparous female orangutans put forth a great deal of effort to mate with individual flanged males – effort that we do not see matched in parous females. Galdikas34 also found that nulliparous females were much more proceptive than parous females. Nulliparous female orangutans may be unable to sufficiently confuse paternity because they are unable to mate with as many males as parous females are, due to a combination of a lack of male interest in mating with them, their focus on flanged males, and their lack of social confidence55. We suggest that more studies, in primates and other species, should compare the ability of nulliparous versus parous females to mate promiscuously, and thus further test the hypothesis that primiparous mothers are at increased infanticide risk compared to multiparous mothers.

An interesting case of chimpanzee intragroup infanticide fits this prediction130. In this case, two females with 3–3.5 year old infants were present but only the primiparous female and her infant were attacked. Additionally, the primiparous female and infanticidal male were seen mating in the past, but at very low frequencies, when the female was maximally tumescent. This case supports the hypothesis that primiparous mothers may be at a disadvantage in terms of using promiscuous mating to protect their infants from infanticidal attacks by males.

Infanticide in orangutans revisited

Although circumstantial, the evidence in this case points to an attack by a male orangutan, and is the first report of a suspected case of infanticide in wild orangutans. The circumstances also provide further evidence that although rare, infanticide may occur in orangutans. One of the arguments against the possibility of infanticide in orangutans has been that a male who killed a female’s offspring would be unlikely to have the opportunity to father subsequent offspring46. However, our data indicate that there is no reason to expect that a male would not be in the vicinity of a female several months after her infant’s death. Although we cannot say for certain who killed Walimah’s offspring, interestingly, she was seen with an unflanged male 23 days after she was found injured and without her infant. This male first appeared two weeks before she gave birth, was not present during Walimah’s peri-conceptive period and she had no known prior social interactions with him. During the month following the suspected infanticide, she was in almost continual consortship with this male. Matings were observed within 4 months of the suspected infanticide, although they may have occurred at an earlier date. Thus, the opportunity for a new male to enter the study area and then to kill an infant and subsequently sire the female’s next offspring existed. The assertion that a male who killed a female’s offspring would not have the opportunity to father future offspring with that female is not supported. Further, this timing of the return to mating after infant loss is comparable to the 2.5 month wait time reported by Galdikas34 after an ex-captive lost an infant, although ex-captive females may experience different energetic and social conditions. We have no way of knowing, if indeed Walimah and her baby were attacked by a male, if this was in fact that male. However, their subsequent consortship and mating demonstrate that a male of this species could have the opportunity to father a female’s offspring after infanticide, as predicted by the sexual selection hypothesis2,29,32.

Several other factors warrant the infanticide interpretation, and it fits the pattern observed in other great apes. Most intragroup infanticidal attacks by male chimpanzees occur during the first 6 months of an infants’ life130,131 and for gorillas, the mean age of infant victims was 358 days132. Walimah’s infant was approximately 4 months of age, consistent with when we might expect infanticide to occur. These first 6 months of lactation are also when we expect infant loss to have the greatest impact on female ovarian function, as it the most energetically demanding period for orangutan mothers18 and likely the most intense period of suckling. During this period Walimah may have been avoiding contact with conspecifics as she had no known social interactions during the period when she was with her new infant. Avoidance of potentially infanticidal conspecifics is another known anti-infanticide tactic employed by female mammals30. In a fission-fusion species such as orangutans, where individuals can choose whether or not to associate with others, this may be a preferred tactic. However, being alone also increases a female’s vulnerability, because of the lack of potential allies.

Our observations are thus consistent with the prediction that wild orangutan infants are vulnerable to infanticide13,35. It will be of some interest to see if further fieldwork produces additional data on this important topic in helping us to understand infanticide as a male reproductive tactic.