Production of food-associated calls in wild male chimpanzees is dependent on the composition of the audience

Chimpanzees produce acoustically distinct calls when encountering food. Previous research on a number of species has indicated that food-associated calls are relatively widespread in animal communication, and the production of these calls can be influenced by both ecological and social factors. Here, we investigate the factors influencing the production of food-associated calls in wild chimpanzees and examine whether male chimpanzees produce food-associated calls selectively in the presence of important social partners. Male chimpanzees form stable long-term social relationships with each other, and these social bonds are vital in enabling a range of cooperative activities, such as group hunting and territory defence. Our data show that males were significantly more likely to produce food-associated calls if an important social partner was nearby, regardless of the size of the audience or the presence of oestrus females. Call production was also mediated by the size of the food patch and by whether or not the food could be monopolised. The presence of important social partners explained most of the variation in male calling behaviour, indicating that food-associated calls are socially directed and serve a bonding function.     

Female gregariousness in Western Chimpanzees (Pan troglodytes verus) is influenced by resource aggregation and the number of females in estrus

Among social animals, group size is constrained by competition over resources. Because female reproductive success is limited by access to food resources, and that of males by access to fertile females, chimpanzee females are proposed to be less social than males and to maintain weak intrasexual relations. Findings from Taï National Park, Côte d’Ivoire, challenged this view, as chimpanzee females were described as generally gregarious, and close intrasexual bonds were common. Here, in a new analysis that focuses on the South Group of chimpanzees in Taï forest, we reevaluate the proposed differences in female association patterns between the Taï and East African populations. We find that mean party size and dyadic association index between females has decreased in Taï, although the level of dyadic associations remains high compared with East African chimpanzees. We attribute the decrease in female gregariousness to the decline in community size over the last 10 years. In addition, we use a multivariate approach to analyze social and ecological factors influencing party size in females. We show that female gregariousness increased when the fruit resources were more clumped and with increased number of females in estrus present. Party size of mothers with sons, however, was smaller with increasing number of sexually receptive females. The results of our model and the reviewed findings of other studies support the socioecological model because food distribution affects female gregariousness, but social and demographic aspects are equally influencing female grouping tendencies.     

Do male "long-distance calls" function in mate defense? A comparative study of long-distance calls in primates

Long-distance calls produced by males are common among vertebrate species. Several hypotheses have been proposed to explain features of male long-distance calls and their phylogenetic distribution in primates, but the putative functions of male long-distance calls have yet to be tested comprehensively. We used phylogenetic comparative methods to investigate hypotheses for the function of male long-distance calls. We focused on the mate defense hypothesis, which states that male long-distance calls function in intra-sexual competition for mates, but we also examined factors involving resource defense, mate attraction, and habitat. Phylogenetic reconstruction of male long-distance calls in 158 primate species indicates that the presence of male long-distance calls is the ancestral state. The carrying distance of male long-distance calls is correlated with the size of the home range, which is consistent with the role of male long-distance calls in defending mates, attracting mates, and defending resources. However, measures of male intra-sexual competition were not associated with the evolution of male long-distance calls. Evolutionary transitions were only partly correlated with factors related to mate attraction. Instead, the strongest correlates of male long-distance calls were activity period, body mass, home range, habitat and some measures of resource defense. Our results are consistent with long-distance call production as a costly signal, but detailed study within species is required to assess these costs and the functions of long-distance calls in individual cases. Electronic Supplementary Material is available if you access this article at http://dx.doi.org/10.1007/.     

Sexual exchange relationships in captive chimpanzees?

Summary In a group of captive chimpanzees (Pan troglodytes), we studied whether females received more social benefits from males when they were in oestrus than at other times and whether males distributed their beneficial acts especially to females with whom they mated more frequently. When in oestrus, females were groomed more frequently by males than at other times. There was an indication that females were groomed especially by those males with whom they mated more often. From the male point of view, the relationship between active grooming and copulation frequency held only in interactions with oestrous females. No difference was found in the male's tendency to share food with females in oestrous or anoestrous condition. Further, clear disadvantages were associated with being in oestrus: females received support from males less frequently and were more often involved in conflicts with males than in their anoestrous period. Higher ranking males did not mate more often. No relationship was found between the frequency with which a male copulated with a given female and her dominance rank, age or parity, nor did he support her or share food more often with her.     

The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire

Male–male competition has historically been considered the major force driving sexual selection. However, female choice and inter-sexual conflict are increasingly recognized as important influences affecting differential mating and reproductive success. Many females exhibit preferences for particular males; however, male strategies may conflict with females’ ability to obtain their mate preferences. To influence paternity, females must affect both (1) whether or not sexual interactions occur, particularly during the periovulatory period (POP) and (2) the outcome of sexual interactions. This study focuses on the effectiveness of female choice in wild chimpanzees (Pan troglodytes verus). Over 2,600 h of data were collected on two habituated chimpanzee communities in the Taï National Park, Côte d’Ivoire. Female mate preferences were measured by quantifying proceptive and resistance behavior toward males in both the periovulatory period and non-POP phases of estrus. The efficacy of female preference was measured both (1) by measuring success rates of female proceptivity and resistance behaviors and (2) by determining how well measures of female mate preference (proceptivity and resistance rates) predict male mating success. Though male chimpanzees are clearly dominant to females, the results indicate that females could effectively resist male solicitations and, in most cases, unwanted copulations were averted. Both female proceptivity and resistance rates correlate (positively and inversely, respectively) with male mating success in POP. Outside POP, female proceptivity rates corresponded with male mating success, but resistance rates did not. Males (irrespective of rank) that were preferred by females obtained higher mating success compared to other males during the POP, suggesting that females were effective in their mate choice and that, despite clear male dominance, female choice influences paternity in wild chimpanzees.     

Evolution of male mating behavior: male spadefoot toads preferentially associate with conspecific males

The evolution of male breeding aggregations is difficult to explain because males may reduce their reproductive success by associating with their closest competitors. We examined aggregative behavior by male New Mexico spadefoot toads, Spea multiplicata, which form breeding choruses in rain-filled pools. We specifically asked whether males are attracted to conspecific calls and, if so, whether they preferentially associate with those male calls that are also attractive to females. Field observations revealed that males showed significant clustering with conspecifics within breeding ponds, whereas laboratory phonotaxis experiments revealed that males preferentially associated with conspecific male calls. Moreover, when males were presented with conspecific calls that differed in call rate, smaller males associated with the stimulus preferred by females (average call rate). Thus, males appear to evaluate the attractiveness of competitors using the same trait employed by females to assess potential mates, and males adjust their positions relative to competitors depending on their size. We discuss these results in the light of several current hypotheses on the adaptive significance of male breeding aggregations. Received: 20 December 1999 / Accepted: 18 March 2000     

Intersexual food transfer among orangutans: do females test males for coercive tendency?

Tolerated transfer of food among adults is rare among primates, except in humans. Here, we present data on a consistent pattern of tolerated intersexual transfer of food (held in hand, foot, or mouth by the owner) among adult orangutans, in two different natural populations (Pongo abelii and Pongo pygmaeus wurmbii), based on ca. 9,000 h of focal observation per site. Although rare, intersexual food transfers were disproportionately from males to sexually active females and involved food that was equally available to both sexes. There was no evidence for direct trading of food for social favors (mating, grooming, or agonistic support) or for sharing under pressure of harassment. However, females frequently protested with loud screams when males, especially unflanged ones, attempted to take food they possessed, and also when males responded aggressively to their taking attempt. Since associations ended sooner when the female emitted noisy calls, a male who did not allow a female to take food from him risked losing the association. These findings support the hypothesis that by taking food, a sexually active female may test the male's tendency toward violence. Thus, intersexual food taking in orangutans is based on female leverage, resulting in a species-wide female entitlement to male “generosity”. The inhibition of food defense required for this kind of transaction may also form the basis for sharing patterns among species in which nutritional benefits have become important, such as chimpanzees and perhaps human foragers.     

The evolution of female copulation calls in primates: a review and a new model

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.

Male–female socio-spatial relationships and reproduction in wild chimpanzees

Recent research on primates and other taxa has shown that the relationships individuals form with members of the same sex affect their reproductive success. Evidence showing that intersexual relationships also influence reproduction, however, is more equivocal. Here, we show that male chimpanzees living in an exceptionally large community display long-term tendencies to associate with particular females. These association patterns are likely to arise because individuals of both sexes selectively range in specific areas of the communal territory, with males inheriting the ranging patterns of their mothers. These differentiated male–female socio-spatial relationships involved males of widely varying ranks, and their effect on reproduction is as strong as that of male dominance rank, which in turn is as strong a predictor of reproductive success at Ngogo as in other smaller chimpanzee communities. These results show that male–female socio-spatial relationships can play a large role in chimpanzee male reproductive strategies, although they probably neither weaken nor strengthen the relationship between male dominance rank and reproductive success. Our results linking male–female socio-spatial relationships to reproduction in chimpanzees suggest that the gap between the social and mating systems of humans and their closest living relatives may not be as large as previously thought.     

Male calling behavior,female discrimination and acoustic interference in the Neotropical treefrog Hyla microcephala under realistic acoustic conditions

Summary Anuran choruses are acoustically complex assemblages of calling males. Little is known about the behavior of males or females in such natural sound environments. I studied calling behavior of males of Hyla microcephala in nature by using an interactive computer-based system that allowed me to simulate call interruptions by a number of males. I also monitored the calling behavior of groups of four to six males. When a male is interrupted by the call of another frog, he increases the spacing between the notes of his call. Responses of this kind are strongest to the loudest neighbor, and some males may ignore interruptions by all but a single close male. Interruptions using synthetic calls with silent gaps indicated that males respond vocally to reductions in sound intensity as brief as 20 ms. This ability helps to explain how males can rapidly alternate notes during pairwise interactions. Amounts of acoustic overlap between pairs of males in the choruses were usually below 10% of an individual's total calling time during bouts. The time a male spent calling that was free of acoustic interference by any other male ranged from 34–92% of his total calling time. When group size was decreased, this unobstructed calling time increased. Previous research showed that females of H. microcephala discriminate against calls that overlap so that the call pulse-train structure is degraded. Here I show that a 6 dB difference in intensity between the overlapped calls is sufficient to reduce the degradative effect of call interference. Females were also given a choice between interfering calls broadcast from two adjacent and two widely separated speakers. An angular separation between speakers of 120° was insufficient to elicit a preference for the separated sources. Together, data on behavior of males and females indicated that males actively reduce acoustic interference with those loud individuals most likely to degrade seriously the temporal structure of their calls.     

Dominance,cortisol and stress in wild chimpanzees (<Emphasis Type="Italic">Pan troglodytes schweinfurthii</Emphasis>)

Field studies of endocrine function in a range of social mammals suggest that high dominance rank is commonly associated with elevated glucocorticoid production. This is puzzling, because in stable dominance hierarchies, high status is normally associated with social control and predictability, key predictors of low psychological stress. One solution to this problem may be that high rank is commonly associated with elevated energetic expenditure, leading to increased metabolic stress and glucocorticoid secretion. We conducted behavioural observations and non-invasive hormone sampling of male chimpanzees in Kibale National Park, Uganda, to examine the relationship between cortisol, dominance and stress in wild chimpanzees. Results indicate that male dominance rank positively correlated with urinary cortisol excretion in a stable dominance hierarchy. Cortisol excretion also correlated positively with rates of male aggression. We suggest that the relationship between cortisol and rank in chimpanzees may be driven by energetic factors rather than psychosocial ones. This interpretation is supported by the observation that urinary cortisol levels correlated negatively with food availability. These findings suggest that dominant chimpanzees experience significant metabolic costs that must be set against the presumed reproductive benefits of high rank. Metabolic stress may mediate the relationship between rank and cortisol in other social mammals.Communicated by L. Sterck     

Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale

For female chimpanzees (Pan troglodytes schweinfurthii) in the Mahale Mountains National Park, Tanzania, the most common mating pattern is opportunistic. In such opportunistic matings, females copulated promiscuously but not randomly. This study describes female mate choice during 1-year observation of six females who exhibited regular genital-swelling cycles. During the study period, 169 opportunistic matings and four restrictive matings were recorded over the course of 51 days. As female estrus progressed, mating frequency and the number of adult male mating partners increased, although the number of potential mating partners did not change. Criteria of female choice examined were the direction and consent/rejection of courtship, proximity maintenance, and female grooming. Adult-male courtships were successful more often than those of adolescent males. During the earlier phase of estrus, females copulated rather promiscuously with many males. But during the later phase of estrus when the likelihood of conception is expected to be highest, they copulated repeatedly with high-ranking adult males. There was a positive correlation between female grooming frequency and mating frequency when the likelihood of conception was greatest. Female chimpanzees are thought to choose high-ranking males as fathers of their offspring. Moreover, female chimpanzees may adopt one or both of two mating strategies, i.e., a many-male strategy and a best-male strategy. Received: 23 November 1998 / Received in revised form: 12 April 1999 / Accepted: 26 April 1999     

The relative value of call embellishment in túngara frogs

Facultative traits that have evolved under sexual selection, such as the acoustic ornaments present in the advertisement signals of male túngara frogs (Physalaemus pustulosus), offer a unique opportunity to examine selection for trait exaggeration with a focus on individual differences amongst signalers. By contrast, many studies of mate choice use experimental designs that obscure the inter-individual variation amongst signalers available for selection to act on—through the use of “typical” or average signals from the population. Here, we use dichotomous female phonotaxis choice tests to determine how the value of male call embellishment varies across 20 individual males frogs recorded from the wild—a sample which captures the acoustic diversity present in the population. We tested 20 females for each male call pair (i.e., 400 females). The results show widespread preference amongst females for ornamented calls (“whine–chucks”) over simple calls (“whines”), yet also demonstrate substantial variation in the relative benefits for individual male frogs—some males enjoy appreciable benefits by using ornaments while others (30% of males in this study) do not. We also show that the relative amplitude of the chuck to the whine correlates positively with the value of call elaborations across these 20 males. Finally, by manipulating the relative amplitude of whines and chucks using both natural and synthetic calls, we demonstrate directly that this single call parameter is key to determining the relative value of call elaborations across males.     

Female mate choice in the gray treefrog (Hyla versicolor) in three experimental environments

We studied female mate choice by Hyla versicolor in three venues to examine how acoustic and spatial complexity, background noise, and the calling behavior of males might influence preferences manifest in previous laboratory two-stimulus choice tests. Our laboratory-based two-stimulus choice tests with and without broadcasts of chorus noise demonstrated that females prefer long calls relative to short calls when calling efforts of alternatives are equivalent. Background noise impaired the ability of females to discriminate in favor of longer over shorter calls, but the magnitude of the effect was small. Captures of females at eight speakers broadcasting 6- to 27-pulse calls at the edge of a pond revealed strong discrimination against only the shortest call variant. In natural choruses, females may only rarely encounter males using such unattractive vocalizations. Female phonotaxis at an artificial pond with caged and electronically monitored calling males also indicated that consequences of female preferences for temporal aspects of calling observed in two-stimulus choice tests are much attenuated in choruses and explain only small portions (<10%) of the variation in male mating success. Nevertheless, relatively high call duration and calling effort increased male attractiveness. Acoustic interference emerged as another significant factor influencing male mating success and possibly the differences in female choice observed in laboratory and chorus settings. We suggest that the bias of females against both overlapped and very short calls may help explain why males lengthen their calls but lower their rate of delivery in response to increases in chorus size.     

Loud calls as a mechanism of social coordination in a fission–fusion taxon, the white-bellied spider monkey (Ateles belzebuth)

Spider monkeys (Ateles spp.) live in social groups that exhibit high levels of fission–fusion dynamics, in which group members form subgroups of varying sizes and compositions. Within these fluid societies, how individuals establish contact with dispersed group members with whom they might choose to associate remains unclear. Long-range vocalizations might facilitate interactions between group members and provide a means of social coordination in fission–fusion societies. We evaluated this possibility for one spider monkey vocalization, the loud call, by examining calling behavior, the relationship between loud calls and changes in subgroup size, and the response of individuals to distant calls and playback experiments in a single study group. We found that 82 % of loud calls were emitted within 30 min of a call from a different location, suggesting that individuals frequently emit loud calls in response to the calls of distant group members. Subgroups that emitted loud calls, especially those that responded to distant calls, were much more likely to experience an increase in subgroup size within an hour after calling than those that did not. Animals also approached distant loud calls more than they avoided or ignored these calls. Finally, playbacks of male calls demonstrated that females respond preferentially to the calls of some individuals over others. Taken together, these results provide support for the hypothesis that spider monkey loud calls function to facilitate and initiate interactions between dispersed group members and suggest that vocal signals can play an important role in influencing social interactions in fission–fusion societies.     

Vocal competition in male Xenopus laevis frogs

Male Xenopus laevis frogs produce underwater advertisement calls that attract gravid females and suppress calling by male competitors. Here we explore whether groups of males establish vocal ranks and whether auditory cues alone suffice for vocal suppression. Tests of male–male pairs within assigned groups reveal linear vocal dominance relations, in which each male has a defined rank. Both the duration over which males interact, as well as the number of competitive opportunities, affect linearity. Linear dominance across the group is stable for about 2 weeks; rank is dynamic. Males engage in physical interactions (clasping) while paired but clasping and vocal rank are not correlated. Playbacks of advertisement calls suppress calling and calls from high- and low-ranking males are equally effective. Thus, auditory cues alone suffice to suppress vocal behavior. Playback intensities equivalent to a nearby male advertising effectively suppress calling while low-intensity playbacks are either ineffective or stimulate vocal behavior. X. laevis advertisement calls are biphasic, composed of alternating fast and slow click trills. Approximately half the males tested are more vocally suppressed by all slow than by all fast trills; thus, these males can distinguish between the two phases. The fully aquatic family Pipidae diverged from terrestrial ancestors approximately 170 mya. Vocal suppression in the X. laevis mating system may represent the translation of an ancient anuran social strategy to underwater life.     

Predation affects alarm call usage in female Diana monkeys (Cercopithecus diana diana)

Diana monkeys produce acoustically distinct calls to a number of external events, including different types of predators. In a previous study, we found population-wide differences in male alarm call production in Taï Forest, Ivory Coast, and on Tiwai Island, Sierra Leone, mostly likely originating from differences in predator experience. In Taï Forest, leopards (Panthera pardus) are common but on Tiwai Island they have been absent for decades, while the predation pressure from crowned eagles (Stephanoaetus coronatus) has been similar. To further evaluate the impact of predator experience, we here analyse the vocal behaviour of female Diana monkeys in both habitats. Female Diana monkeys produce predator-specific alarm calls, alert calls and contact calls in response to predators, suggesting that their calls serve in a broader range of functions compared to males. Results showed that females produced the same call types at both sites, despite the differences in predator fauna. Regarding call usage, leopard alarm calls were extremely rare on Tiwai Island, but not in Taï Forest, whereas we found no differences in eagle alarm call production. When comparing response latencies, Tiwai females were slower to respond to both predators compared to Taï females. Finally, we found no habitat-specific acoustic differences in the alert and predator-specific alarm calls, but significant differences in frequency-based parameters of contact calls. Overall, our results suggest that ontogenetic experience can affect primate vocal behaviour in both usage and acoustic structure but that the way in which particular call types are affected may be closely linked to function.     

Behavioural responses of Diana monkeys to male long-distance calls: changes in ranging,association patterns and activity

Although much is known about the relationship between vigilance, group size and predation risk, behavioural responses to predation risk and their resultant costs are less clear. We investigated the response of Diana monkeys to increased predation risk by looking at behavioural changes associated with male long-distance calls, which are reliably given to certain predators. After male long-distance calls, group spread and nearest-neighbour distance decreased whilst travel and association rates for the group increased. The average height and exposure level of individuals in the group did not change after calls. Individual Diana monkeys changed their behaviour and were more likely to be vigilant or travel and less likely to engage in social or resting behaviours after long-distance calls. In addition, movement rates increased with the number of species the Diana monkeys were associated with. Diana monkey long-distance calls facilitate the joining of groups of other species. Black and white colobus and lesser spot-nosed monkeys were more likely to be in an association following a long-distance call than before. Behavioural responses, such as increased travel or association rates, that reduce foraging efficiency are interpreted as evidence of a non-lethal impact of increased predation risk.     

Interactions in male baboons: the importance of both males’ testosterone

To date, research on testosterone and behavior has focused on individuals, even when studying social behaviors that necessarily involve multiple participants. Here, we explore male responses to other males of different dominance ranks and testosterone levels in a population of wild baboons. In chacma baboons (Papio hamadryas ursinus) of the Okavango Delta, a male’s testosterone is related to his rank trajectory and, therefore, the threat he poses to other males. To examine the effects of testosterone and rank on male–male interactions, we used playback experiments to measure how a target male responded to the simulated approach of another male, scoring responses by whether or not the subject moved away from the speaker in the first minute. High testosterone subjects did not move away from the speaker more often than low testosterone subjects, but high testosterone callers elicited a move more often than low testosterone callers. When the combined testosterone of the subject and caller was high, moves were most common. The rank relationship between subject and caller did not predict moves, but the effect of combined testosterone on moving was most pronounced in adjacently ranked males. Adjacently ranked, high testosterone males are the most likely to be competing for each others’ rank, and our experiments on these dyads elicited the most moves. Both behavioral and experimental observations indicate that testosterone may be more important than the rank relationship in predicting the outcome of male–male interactions. Furthermore, combined information on the testosterone of both males was the best predictor of results, highlighting the utility of dyadic analyses when relating testosterone to behavior.     

Advertisement call duration indicates good genes for offspring feeding rate in gray tree frogs (Hyla versicolor)

Indicator or ”good genes” models of sexual selection predict that mating preferences allow females to choose mates that are genetically superior. Female gray tree frogs (Hyla versicolor) prefer male advertisement calls of long call duration, which can be indicators of enhanced offspring growth performance. We tested the effects of father’s call duration and the presence of a caged predator (dragonfly naiad) on tadpole activity and growth in a factorial experiment, controlling for maternal and environmental effects. The effect of food availability (a repeated measure) on tadpole activity was also examined. Tadpoles responded to predator presence and to high food availability by decreasing activity and feeding. Tadpoles exposed to a caged predator were smaller after 14 days than those exposed to an empty cage, suggesting that spending less time feeding carries the cost of reduced growth. Offspring of males with long versus short calls responded similarly to the presence of a predator. Nonetheless, offspring of long-calling males spent more time feeding than did offspring of short-calling males, except when a predator was present but no food was available. Increased time spent feeding may contribute to enhanced offspring growth and, therefore, to the indirect benefit that a female may realize by selecting a mate with long calls. However, because the behavioral differences depended on the environment, and because the fitness consequences of such behavioral differences should also vary with the environment, the benefit of mating with a long-calling male may depend on the conditions encountered by the offspring. Received: 15 February 2000 / Revised: 24 September 2000 / Accepted: 16 October 2000