Ryne A. Palombit

Factors Affecting Reproduction and Mortality Among Baboons in the Okavango Delta, Botswana

We present results of a 10-year study of free-ranging gray-footed chacma baboons (Papio ursinus griseipes) in the Okavango Delta of Botswana. The majority of deaths among adult females and juveniles were due to predation, while infants were more likely to die of infanticide. There were strong seasonal effects on birth and mortality, with the majority of conceptions occurring during the period of highest rainfall. Mortality due to predation and infanticide was highest during the 3-mo period when flooding was at its peak, when the group was more scattered and constrained to move along predictable routes. The reproductive parameters most likely to be associated with superior competitive ability—interbirth interval and infant growth rates—conferred a slight fitness advantage on high-ranking females. However, it was counterbalanced by the effects of infanticide and predation. Infanticide affected high- and low-ranking females more than middle-ranking females, while predation affected females of all ranks relatively equally. As a result, there were few rank-related differences in estimated female lifetime reproductive success.

Infanticide and the evolution of pair bonds in nonhuman primates

Social relationships between adult males and females vary widely among mammals. In general, interactions between the sexes, particularly those of an affiliative nature, are associated with and, indeed, often limited to the period of copulation or female estrus.1 Nevertheless, cohesive male‐female bonds persist beyond estrus in some species, particularly nonhuman primates,2 for reasons that remain largely obscure. Protection from male infanticide has been offered as a potential benefit to females of bonds with males in a variety of primates, including mountain gorillas and gibbons. Here I evaluate this hypothesis within a comparative framework that considers alternative costs and benefits of social relationships between the sexes.

Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments

Close association between an anoestrous female at the time of lactation and adult male(s) is relatively rare in mammals, but common in baboons (Papio hamadryas subsp.). The functional significance of these “friendships” remains unclear, however. In chacma baboons (P. h. griseipes), friendships are a counter-strategy to infanticide by immigrant males. Experimental playback of female distress calls in chacma baboons revealed that male friends are more motivated to protect females and infants than are control males. Olive baboons (P. h. anubis) also exhibit friendships, but infanticide is rare, suggesting that friendships provide females with protection from non-lethal aggression (anti-harassment hypothesis) or serve to promote male–infant bonds that later benefit the maturing juvenile (future male caretaker hypothesis). We replicated these playback experiments on a group of olive baboons to test between these hypotheses and to evaluate if the lower costs of non-lethal harassment lessens male protective responsiveness relative to protection from (more costly) infanticide. Spatial data revealed that most lactating females had one to four friend males. Relative to non-friends, friend dyads were characterized by higher rates of allogrooming and infant handling, but less agonism. Female rank was correlated with the number of male friends. Just as in chacma baboons, playback of female screams elicited stronger responses from male friends than control males in support the anti-harassment hypothesis. Compared to the chacma baboon, male olive baboons appeared to exhibit similarly high levels of protective solicitude for female friends although they protect against non-lethal harassment rather than infanticide.

Inter- and intraspecific variation in the diets of sympatric siamang (Hylobates syndactylus) and lar gibbons (Hylobates lar)

Studies of the siamang (Hylobates syndactylus continentis) and the lar gibbon (Hylobates lar lar) where they co-occur in mainland Asia have demonstrated interspecific dietary segregation based on body size and have suggested that observed levels of frugivory represent metabolically based maxima for these species. I studied sympatric groups of siamang (H. s. syndactylus) and lar gibbons (H. l. vestitus) at Ketambe in northern Sumatra (Indonesia) in order to assess the magnitude of within- and between-species variation in diets. The insular subspecies are considerably more frugivorous (60-70% of feeding time) than mainland conspecifics (35-50%). This is primarily because Sumatran hylobatids spend about twice as much time (approx. 45% of feeding) eating fig fruits (Ficus spp., Moraceae). A higher density of figs at Ketambe (compared to Kuala Lompat) may account for this behavioral difference. Enhanced frugivory has been achieved at the expense of folivory, which is much reduced in Sumatra--especially in H. lar (4% of diet)- and is limited almost entirely to immature foliage. The expected decline in protein intake resulting from diminished folivory in Sumatra may be counterbalanced by observed increases in insectivory, which is especially pronounced in lar gibbons. Interspecific dietary segregation emerges most clearly in how individuals of each species supplement their similarly fig-dominated diets. Siamang rely more on immature foliage--primarily from lianas, which generate young leaves more reliably and abundantly than trees do. Conversely, lar gibbons exploit the pulpy fruit of trees and lianas more heavily than siamang do. This general pattern occurs where the two species coexist in Malaysia, thereby suggesting a substantive interspecific difference that is somewhat greater in the insular populations.

Gibbon foraging decisions and the marginal value model

We use data from an observational field study of frugivory in two sympatric gibbons, lar (Hylobates lar) and siamang (H. syndactylus), to test assumptions and predictions of the marginal value model (MVM). A key prediction of the MVM is that marginal gain rates at the time of leaving the patch are equal across patch types. We found that this is not the case for gibbons: rates of energy intake at the end of feeding sessions were significantly different for different types of fruit, and we could not attribute this to temporal variation in fruit availability. Initial and final caloric intake rates were highly correlated. This suggests that gibbons do not adjust the time spent in patches in order to maximize the average rate of energy intake. Similar results were obtained for all other currencies considered. Gibbon foraging appears to satisfy several, but not all, assumptions of the MVM. As required by the model, fruit patches occur as discrete units, patches are encountered sequentially, travel time between patches exceeds search time between items within a patch, search for and search within patches are incompatible activities, and intake rates decline over time spent in a patch. However, the declining rates we detected may be an effect of satiation instead of patch depletion, patches probably are not encountered at random, and group members may not forage independently. Thus, our results suggest that the MVM is not an adequate model of gibbon foraging behavior, but they do not invalidate the MVM per se.

A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). II. Potential of calls to regulate intragroup spacing

This study is a preliminary assessment of the potential of long-tailed macaque (Macaca fascicularis) calls to operate in systems of within-group spacing. Covariation in the rate of occurrence of calls with party spread, size, and activity among wild individuals of one group suggested that four classes of calls may function in intragroup spacing. Two of them are “clear” calls of long duration and pronounced frequency modulation. Calling rate increased with party spread for low- and high-frequency variants of these calls during resting and feeding respectively, suggesting possible utility in maintenance of spatial relations over moderately long distances. A third “harsh” call was negatively correlated with party spread during foraging and may thus function to increase dispersion among foraging individuals. Another harsh call with a tonal onset was unique among all calls in the vocal repertoire in being more frequently performed by lone, isolated individuals than by macaques accompanied by others, suggesting a possible function in reestablishing contact that has been severed. The functional significance of these calls with respect to their acoustic structures is discussed. Macaques that use calls to regulate intragroup spacing can control communication distance and direction by their choice of acoustically different vocalizations. This choice may be affected not only by varying environmental constraints on sound transmission, but also by social and ecological factors such as intragroup competition.

Longitudinal patterns of reproduction in wild female siamang (Hylobates syndactylus) and white-handed gibbons (Hylobates lar)

I present the 6- year reproductive histories of three wild female siamang (Hylobates syndactylus)and four white-handed gibbons (Hylobates lar)at the Ketambe Research Station (Sumatra, Indonesia). Reproductive output varied considerably among females. Two females failed to gestate: both were nulliparous young adult H. lar,one of which remained unpaired for 4 years after dispersing from her group, while the other lost her recently acquired mate to another female. Only one- (a white-handed gibbon)- gave birth more than once, yielding interbirth intervals of 22 and 31 months. Pair bond stability or reduced interspecific feeding competition or both factors may have contributed to the brevity of these intervals. The other females- one H. lar,and three H. syndactylus-each gave birth once, suggesting minimum interbirth intervals exceeding 4–5 years (H. lar)and 3 years (H. syndactylus)in these individuals. Even given the pronounced variation observed among H. lar,these data suggest that interbirth intervals may often exceed the 2- to 3- year interval commonly attributed to these two species. Sources of reproductive failure were 1) maternal abandonment of the neonate due to impaired ability to provide maternal care (H. syndactylus,),(2) premature or stillbirth (H. syndactylus,),and (3) pregnancy termination (H. lar).These data and a review of information on longevity and age at menarche suggest that the actual lifetime reproductive output of a siamang or white-handed gibbon female may often fall far short of the 10 offspring/lifetime originally proposed for these species. Indeed, females may rear as few as five offspring to weaning in a lifetime, which is a figure reminiscent of the reproductive potential of some pongids. Finally, variance in female reproductive success is higher than expected in these monogamous species, which suggests that females (and males) are under strong selective pressure to exert mate choice, possibly through acquisition of (new) mates and extrapair copulations. Future research must clarify the availability of opportunities for paired adults to engage in these sociosexual behaviors.

A preliminary study of vocal communication in wild long-tailed macaques (Macaca fascicularis). I. Vocal repertoire and call emission

Vocal communication in wild long-tailed macaques (Macaca fascicularis) is described in terms of (1) a preliminary vocal repertoire and the situations in which calls occur in the natural habitat of this species and (2) quantitative measurement of the natural occurrence of calls in the field. Although a number of calls are relatively discrete (e.g., a male loud call), gradation is pronounced for both wide-spectrum (“harsh”) and narrow-spectrum (“clear”) vocal signals. Thirteen general types of harsh calls are identified provisionally as elements of the vocal repertoire. The exact number of discrete clear calls contributing to the vocal repertoire could not be ascertained precisely, but these calls were classified operationally into six broadly acoustically different classes in order to measure natural vocal behavior. Vocalizations tended to occur in temporal “clusters” during sample, periods. Narrow-band clear or “coo” calls were more frequently performed by macaques than wide-band harsh calls. The possible functional implications of the correlated occurrence of multiple vocal signals are discussed.

Reproduction, Mortality, and Female Reproductive Success in Chacma Baboons of the Okavango Delta, Botswana

Predation, food competition, and infanticide all negatively impact female reproductive success. Female dominance rank may mitigate these effects, if competitive exclusion allows high-ranking females to gain priority of access to critical food resources. It may also exacerbate them, if low-ranking females are forced to feed or rest in marginal habitats where they are at increased risk. In this chapter, we present data on reproduction, mortality, and female reproductive success from a 10-year study of free-ranging chacma baboons (Papio hamadryas ursinus) in the Okavango Delta of Botswana and examine the influence of predation, infanticide, and dominance rank on female reproductive success. Predation appeared to be the cause of most deaths among adult females and juveniles, whereas infanticide was the most likely cause of deaths among infants. Seasonality strongly affected both births and mortality: The majority of conceptions occurred during the period of highest rainfall. Mortality due to predation and infanticide was highest during the 3-month period when flooding was at its peak, most likely because the group was more constrained to move along predictable routes during this time. Those reproductive parameters most likely to be associated with superior competitive ability-interbirth interval and infant growth rates-conferred a slight fitness advantage on high-ranking females. This fitness advantage was counterbalanced, however, by the effects of infanticide and predation. Infanticide affected high- and low-ranking females more than middle-ranking females, while predation affected females of all ranks relatively equally. As a result, there were few rank-related differences in estimated female lifetime reproductive success.

Infanticide as Sexual Conflict: Coevolution of Male Strategies and Female Counterstrategies

One of the earliest recognized forms of sexual conflict was infanticide by males, which imposes serious costs on female reproductive success. Here I review two bodies of evidence addressing coevolved strategies of males and females. The original sexual selection hypothesis arguing that infanticide improves male mating success by accelerating the return of females to fertilizable condition has been generally supported in some taxa--notably, some primates, carnivores, rodents, and cetaceans--but not in other taxa. One result of recent research has been to implicate other selective benefits of infanticide by males in various taxa from insects to birds to mammals, such as acquisition of breeding status or improvement of the female breeding condition. In some cases, however, the adaptive significance of male infanticide remains obscure. The second body of data I review is arguably the most important result of recent research: clarifying the possible female counterstrategies to infanticide. These potential counterstrategies span diverse biological systems, ranging from sexual behavior (e.g., polyandrous mating), to physiology (e.g., the Bruce effect), to individual behavior (e.g., maternal aggression), to social strategies (e.g., association with coalitionary defenders of either sex). Although much remains to be studied, these current data provide compelling evidence of sexually antagonistic coevolution surrounding the phenomenon of infanticide.