Orangutan infanticide may occur even though it has never been reported in the wild. It is often suggested that insufficient sampling is the reason for the lack of observations (van Schaik 2004
; Mitra Setia and van Schaik 2007
; Stumpf et al. 2008
). This raises the question of whether we have studied orangutans long enough to know whether male infanticide is a regularly occurring male reproductive strategy. Although the absence of evidence is not evidence of the absence of infanticide, the longer orangutan behavioral observation continues, the less likely it becomes that failure to observe infanticide is the result of insufficient sampling effort.
At research sites with the most detailed available data for chimpanzees and mountain gorillas, there is a strong positive correlation between study site duration and the number of infanticides observed for four out of six long-term chimpanzee study sites (one-tailed Pearson correlation: Budongo r
0.001; Gombe r
0.001; Mahale r
0.001; and Ngogo r
0.001) and for mountain gorillas (Karisoke r
0.001), yet no long-term orangutan study sites have reported an infanticide (Fig. ). The other two long-term chimpanzee sites considered, Kanyawara and Tai, have one and zero confirmed infanticides respectively. This comparison between species must be made cautiously given the differences in social systems, group size, and number of females followed between the species. Nevertheless, despite well over 80,000 h of long-term behavioral observation at multiple study sites (Knott et al. 2008
; Morrogh-Bernard et al. 2009
), no observations of wild male orangutans attacking or killing unweaned infants have been reported.
Fig. 1 Study site duration and all cumulative infanticides (i.e., male or female, within or between groups) reported for chimpanzees (C), mountain gorillas (G), and orangutans (O). Four out of six long-term chimpanzee study sites show a strong positive correlation (more ...)
To assess further the role of sampling effort in explaining the lack of observed infanticide in wild orangutans, we calculated the probability of zero infanticides having been observed at a site based on the study site’s duration. At full confidence, the observed annual infanticide is 0:
is the study site duration in years, and F
is the infanticide frequency resulting in the zero infanticides given N
. We reduced our confidence for the actual frequency of infanticides for the duration of the study site to 95% and 99% (c
0.05 and 0.01):
We then calculated the maximum potential frequency of infanticides per year (Fmax
) for each orangutan study site (Table ):
Maximum orangutan infanticide frequencies
quantifies the decreasing likelihood of zero infanticide observations over time. It is not an estimate of infant survival, but rather a benchmark to which infant survival can be compared to assess whether infanticide might be a substantial source of infant mortality. We are aware that this is a rough proxy because it does not include the number of infants observed per year at each study site, but maximum infanticide frequencies are a quantitative starting point since to date no estimations of orangutan infanticide frequencies have been previously calculated (Mitra Setia and van Schaik 2007
Maximum potential infanticide frequencies at orangutan research sites with 7–10 years of observations (range 0.26–0.35 for Suaq Balimbing, Gunung Palung, and Kinabatangan, Table ) are comparable to those reported for chimpanzees or mountain gorillas (Table ), but maximum potential infanticide frequencies for the longest running orangutan study sites are much lower (range 0.08–0.09 for Ketambe and Tanjung Puting, Table ).
Observed infanticide frequencies in chimpanzees and mountain gorillas
High orangutan infant survival in the wild may be indicative of the absence of infanticide. Indeed, infant survival is higher in orangutans than in other great apes. Although published data on orangutan infant mortality are currently only available for two Sumatran sites (Wich et al. 2004
), these data indicate that infant mortality in the first year of life is approximately 8%, which is far lower than rates for mountain gorillas (26%) or chimpanzees (20%; Harcourt and Stewart 2007
). It is interesting to note that maximum infanticide rates and infant mortality in the first year of life are approximately equal for Ketambe. However, of the two reported infant deaths within the first year (out of a total of 29 observed infants), one death occurred because the infant’s mother died. No deaths were reported for infants between ages 1 and 3 years (Wich et al. 2004
). The smaller life history data set from Suaq Balimbing includes zero infant deaths in the first year of life and four infant deaths between ages one and two; however, two of these deaths occurred after heavy illegal logging began (Wich et al. 2004
), and the possibility of illegal hunting or capture for the pet trade cannot be ruled out as causes of mortality. These data indicate that less than half of the reported infant mortalities in the wild could potentially have been caused by infanticide. We note, however, that high infant survival would be expected if conditions during the observation periods were not those expected to result in infanticide (e.g., no turnovers in dominant males).
Infant mortality is higher in captive populations than wild populations (Anderson et al. 2008
). This is most likely due to hybridization between orangutan species in captivity, which results in significantly lower infant survival (Cocks 2007
). Recent large-scale comparisons of captive orangutan infant mortality have not reported infanticide as a cause of infant death (Cocks 2007
; Anderson et al. 2008
), although it is unclear to what extent infanticide opportunities from the introduction of stranger males were available. We note a single report of infanticide in captive orangutans. A Bornean male orangutan housed with a female killed his own infant shortly after its birth (Mallinson 1984
). Infanticide is therefore part of the behavioral repertoire of captive orangutans, but details from this single report are limited. A comprehensive investigation of historical opportunities for captive infanticides using zoo records is needed to evaluate the potential relationship between captive and wild infanticide in orangutans.
Whether wild orangutan behavior has been sufficiently well studied to detect infanticide remains a somewhat open question, but the lack of observed infanticides despite continued accumulation of data from long-term study sites suggests that infanticide is not a regularly occurring male strategy. Based on our calculations, if infanticide did occur in orangutans, it would occur at rates that are much lower than those reported for chimpanzees or mountain gorillas. Indeed, Sumatran infant mortality rates indicate that orangutan infants rarely die from any cause (e.g., predation, disease, and falling). If future behavioral observations discover that infanticide does occur in wild orangutans, the critical question will become whether its occurrence can be determined to be a product of sexual selection.
Because detecting infanticide itself is difficult, it is important that we investigate whether strategies adapted to prevent infanticide are present in orangutans. If such counterstrategies are detected, it would indicate that infanticide has posed a selective pressure on female behavior. Japanese macaques (Macaca fuscata
), for example, were observed for decades before sexually selected infanticide was documented (Soltis et al. 2000
), but even the rare occurrence of infanticide led to the maintenance of female counterstrategies during intermittent periods. Therefore, following Ebensperger (1998
), we review the common mammalian counterstrategies against infanticide as they apply to orangutans: coalition formation for group defense, direct aggression by the mother against intruders, avoidance of infanticidal conspecifics, female promiscuity, and territoriality. Although coalition formation does not apply to this predominately solitary species, the others must be evaluated for orangutans (Table ) as, theoretically, females should exhibit counterstrategies to prevent or reduce the potential cost of infanticide posed by males (Hrdy 1979
Aggression by mothers against intruders
Although primate mothers in other species are aggressive toward stranger males (e.g., Lemur catta
, Pereira and Weiss 1991
), there are no reports of direct aggression by orangutan mothers against stranger males. Since male attacks on infants have never been reported in wild orangutans (van Schaik and Kappeler 1997
; Mitra Setia and van Schaik 2007
), female aggression against nonresident males appears unnecessary. Most male–female aggression occurs when males attempt to force copulations (Galdikas 1985a
; Mitani 1985a
; Fox 1998
). Because the cost of infanticide would be higher than the cost of an unwanted copulation, the lack of female aggression against intruders indicates either that infanticide is of little concern to orangutan females or that fighting is fruitless, as is suggested by low success rate of female resistance to forced copulation (Mitani 1985a
Avoidance of potentially infanticidal conspecifics
In species in which infanticide occurs, females with infants avoid stranger males and encounters with other groups (van Schaik and Kappeler 1997
; Ebensperger 1998
). There are anecdotal reports from Sumatra that females and infants occasionally exhibit “fearful” reactions to some long calls (Mitra Setia and van Schaik 2007
). Delgado (2003
) investigated the reactions of orangutans to playbacks of familiar and unfamiliar male long calls in Gunung Palung National Park in Borneo and at Ketambe in Sumatra. He found no evidence of individuals moving away from the call, either immediately or as a delayed response. These results, however, were based on only a few individuals and did not account for differences in sex or reproductive state. It appears that females are unable to completely avoid sexual coercion and forced copulations by nonresident males (Fox 2002
), which indicates that females would similarly be unable to effectively evade infanticidal nonresident males. Nevertheless, given the higher cost of infanticide than forced copulation, a test of avoidance using expected encounter rates (Hutchinson and Waser 2007
) is necessary before the hypothesis of evasion can be rigorously examined. It therefore remains unclear whether orangutan females with infants attempt to avoid nonresident males (Stumpf et al. 2008
A recent review of female promiscuity illustrates that paternity confusion is the most common of nine alternative explanations for multi-male mating (Wolff and Macdonald 2004
). Promiscuous mating has been hypothesized as a female mammalian strategy to reduce infanticide by confusing paternity (Hrdy 1979
). The major predictions of the paternity confusion hypothesis are that females
solicit matings with multiple males and males commit infanticide. The second most commonly supported hypothesis for female promiscuity is avoidance of sexual harassment. The major predictions of the sexual harassment avoidance hypothesis are that males
solicit matings with females, infanticide does not occur, and promiscuity occurs in seasonal breeders in which males do not guard females (Wolff and Macdonald 2004
). We suggest that currently available orangutan behavioral data supports the latter hypothesis that female promiscuity occurs in order to avoid sexual harassment.
It has recently been argued that female orangutans engage in multi-male mating to confuse paternity based on evidence that during nonconceptive periods, female orangutans exhibit prosexual behavior, which is defined as positive female sexual response irrespective of the initiating sex (Stumpf et al. 2008
). This interpretation, however, does not directly address the aforementioned predictions. If females engage in promiscuous mating as an anti-infanticide strategy to confuse paternity, then females are expected to solicit matings from potentially nonpreferred males when conception is unlikely (Hrdy 1979
; Wolff and Macdonald 2004
; Stumpf and Boesch 2005
). Nonpreferred males are defined as unflanged and past-prime flanged males (Stumpf et al. 2008
). A comparison of female orangutan sexual solicitations across study sites has shown considerable female solicitation toward preferred flanged males at some sites, but very little female sexual solicitation toward nonpreferred unflanged males at any site. Moreover, all matings during conceptive periods at Gunung Palung were with flanged males, and there were no significant differences in female sexual solicitations of nonpreferred males between conceptive and nonconceptive periods (Stumpf et al. 2008
). Lack of female proceptivity outside of the conception period at Gunung Palung is consistent with captive behavioral experiments (Nadler 1982
). Current evidence thus suggests that female orangutans do not solicit potentially infanticidal males when conception is unlikely.
Convenience polyandry predicts that females accept rather than resist matings when the costs of resisting outweigh the costs of mating (Rowe 1992
). Because of the exceptionally large female investment in offspring, impregnation by a nonpreferred male is expected to be the main potential cost of mating based on the good genes hypothesis (Knott and Kahlenberg 2007
). If females engage in multi-male mating because of convenience polyandry, females are expected to resist nonpreferred males less when conception is unlikely. Interestingly, female orangutan resistance toward unflanged males at Gunung Palung decreased significantly during nonconceptive periods (Stumpf et al. 2008
). Additionally, Sumatran females at Suaq have been reported to resist only 36% of copulations initiated by unflanged males (Fox 2002
). These data therefore indicate that orangutan females mate promiscuously to “make the best of a bad job” (Lee and Hays 2004
) and reduce sexual harassment (Wolff and Macdonald 2004
) rather than to confuse paternity.
One potential inconsistency in understanding female orangutan promiscuity as avoidance of sexual harassment is that Bornean females at Gunung Palung have been reported to solicit all types of males with the highest proceptivity rates during the early stages of pregnancy. It has been argued that the most likely explanation for orangutans mating during pregnancy is paternity confusion to reduce infanticide (Stumpf et al. 2008
). Indeed, mating during pregnancy is currently the strongest evidence in support of a female orangutan counterstrategy to infanticide.
Available orangutan genetic data (Utami et al. 2002
; Goossens et al. 2006
) have shown that paternity is not concentrated in any particular male at the two sites at which it has been measured (Table ). This indicates that whether or not females actively attempt to confuse paternity, the functional result of multi-male mating in orangutans is some degree of paternity confusion. Both studies reported that not all potential fathers in the populations were sampled, but neither study published the corresponding behavioral mating data that included the number of potential fathers or total males in the area. As a result, we do not know how many additional males had a zero chance of paternity and therefore might be potentially infanticidal for either site. To what extent paternity is confused across these populations and may thereby prevent infanticide remains an open question. Future approaches to address this question should determine the percent of resident males with whom females mate between weaning and conception as well as the probability of a nursing female encountering a nonresident male with whom she has not mated.
Orangutan male reproductive success
Orangutans have been described as a classically nonterritorial species (Mitani and Rodman 1979
). Competition between flanged males can be severe (Galdikas 1985a
), but flanged males are known to tolerate unflanged males (Galdikas 1985b
) and males have overlapping home ranges (Singleton and van Schaik 2002
). Territoriality is therefore not an anti-infanticide strategy in orangutans.