Primate Strategies Research Articles

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.

Adult sex ratio as an index for male strategy in primates

The adult sex ratio (ASR) is defined as the number of fertile males divided by the number of fertile females in a population. We build an ODE model with minimal age structure, in which males compete for paternities using either a multiple-mating or searching-then-guarding strategy, to investigate the value of ASR as an index for predicting which strategy males will adopt, with a focus in our investigation on the differences of strategy choice between chimpanzees (Pan troglodytes) and human hunter–gatherers (Homo sapiens). Parameters in the model characterise aspects of life history and behaviour, and determine both dominant strategy and the ASR when the population is at or near equilibrium. Sensitivity analysis on the model parameters informs us that ASR is strongly influenced by parameters characterising life history, while dominant strategy is affected most strongly by the effectiveness of guarding (average length of time a guarded pair persists, and resistance to paternity theft) and moderately by some life history traits. For fixed effectiveness of guarding and other parameters, dominant strategy tends to change from multiple mating to guarding along a curve that aligns well with a contour of constant ASR, under variation of parameters such as longevity and age female fertility ends. This confirms the hypothesis that ASR may be a useful index for predicting the optimal male mating strategy, provided we have some limited information about ecology and behaviour.

Foraging strategies underlying bird egg predation by macaques: A study using artificial nests.

Bird egg predation is widespread in non-human primates. Although nest predation is often described as opportunistic, little is known about foraging strategies and nest detection in primates. Since it is the prevalent cause of nest failure in the tropics, birds select nest sites within specific microhabitats and use different nest types to increase nesting success. Identifying the nests targeted by the northern pigtailed macaques (Macaca leonina), an omnivorous cercopithecine species, and known nest predator, will shine light on nest foraging strategies in primates. The aim of this research was to reveal if nest predation is a selective or opportunistic feeding behavior. We studied, using artificial nests and camera traps, the influence of nest type (open-cup vs. cavity), microhabitat (i.e., understory density, canopy cover, canopy height, ground cover, and presence vs. absence of thorns and lianas), and nest height, on nest predation by a troop of northern pigtailed macaques in the Sakaerat Biosphere Reserve (Thailand), a degraded environment. In our study, macaque predation on artificial nests was high; out of the 200 nests that were set up, 112 were plundered by macaques. Although predation rates decreased with nest height, nest type, and microhabitat had no significant effect on predation by macaques. Nest detectability and accessibility did not affect predation rates. Macaques actively searched for nests in different microhabitats, suggesting that nest predation by this primate might be considered a selective feeding behavior in this degraded habitat. Consequently, nest predation by this primate might have important conservation implications on the population dynamics of forest-dwelling bird species. Behavior observation methods, such as instantaneous scan sampling, may underestimate nest predation by primates, a furtive and cryptic behavior.

Sneak peek: Raptors search for prey using stochastic head turns

The strategies by which foraging predators decide when to redirect their gaze influence both prey detection rates and the prey's ability to detect and avoid predators. We applied statistical analyses that have been used to study neural decision-making for gaze redirection in primates to 3 species of predatory birds with different sizes, visual systems, habitats, and hunting behaviors: the Northern Goshawk (Accipiter gentilis), Cooper's Hawk (A. cooperii), and Red-tailed Hawk (Buteo jamaicensis). The timing of head saccades was measured during visual searches using field video recordings of foraging raptors, and during a variety of behaviors using a miniature camera mounted on the head of a Northern Goshawk. The resulting statistical distribution of latencies (time between successive head saccades) was compared to predictions from various models proposed to describe visual search strategies. Our results did not support models that assume a constant probability of gaze redirection per unit time, a constant time for “giving up” on the visual search, or an initial setup time before visual search initiation. Instead, our data were fit best by a log-normal distribution, consistent with the raptors stochastically changing their gaze direction on the basis of accumulated environmental information. Specifically, this suggests that saccade initiation arises from a neural computation based on detection of a threshold level of a dynamically updated decision signal that encodes noisy sensory data, similar to the processes inferred from previous studies of visual search strategies in primates. The only significant between-species difference we found was a slower mean gaze-redirection rate for 2 larger species compared to the Cooper's Hawk, even though the latter has hunting behavior and maneuverability similar to that of the Northern Goshawk. Head-saccade latencies measured for a Northern Goshawk during different behaviors showed that the bird changed gaze direction significantly less frequently, on average, while perched than while in motion.

Monogamy and Nonmonogamy: Evolutionary Considerations and Treatment Challenges.

Few topics generate such controversy and emotional reactivity as the nature of human mating behavior. Unfortunately, and potentially to the detriment of good patient care, sexual medicine practitioners havelargely avoided this matter. An understanding of the scientific literature can empower practitioners to moreeffectively confront the inevitable monogamy and nonmonogamy challenges present in research and clinicalpractice. To review and summarize relevant scientific literature as a context to evaluate the more common myths and misunderstanding relating to the practice of monogamy and nonmonogamy in humans. This review also is intended to promote a discussion of the ways human mating strategies may impact sexual function and dysfunction for the individual and couple. A review of English written peer-reviewed evolutionary, anthropological, neuropsychiatric, zoological research, and other scholarly texts was conducted. Work published between 2000 and 2016 concentrating on evolutionary theory, long- and short-term mating strategies in primates and most specifically in humans, and consensual nonmonogamy was highlighted. Main outcomes included a brief explanation of evolutionary theory and a review of relevant literature regarding long- and short-term mating behaviors and consensual nonmonogamy. Serial sexual and social monogamy is the norm for humans. Across time and cultures, humans have adapted both long- and short-term mating strategies that are used flexibly, and sometimes simultaneously, based on unique personal, social, and environmental circumstances. Human mating behavior is individualistic, the result of numerous biopsychosocial influences. The clinician cannot assume that an individual presenting as a patient maintains a monogamy-valued view of his or her intimate relationship. Patients may experience conflict between the cultural monogamous ideal and their actual sexual behaviors. This conflict may be critical in understanding a patient's sexual concerns and in treatment planning. Awareness of these issues will aid the practitioner in sexual medicine.

The effects of plant nutritional chemistry on food selection of Mexican black howler monkeys (Alouatta pigra): The role of lipids.

Understanding the nutritional basis of food selection is fundamental to evaluate dietary patterns and foraging strategies in primates. This research describes the phytochemical composition of the foods consumed by two groups of Mexican black howler monkeys (Alouatta pigra) during a 15-month field study, and examines how plant nutritional chemistry affected food choice. Based on indices of selectivity that reflected seasonal changes in the amount of different phenophases of the most consumed plant species and their availability in the environment, we found that, in general, howlers did not preferentially select food items based on their concentrations of protein, sugar, energy, or their protein-to-fiber ratio. During only one season of the year, the nortes (October-January), there was evidence for selectivity. During this period, selectivity indices correlated positively with the lipid content of foods ingested. However, a strategy of selecting fruits high in lipids (21-41% dry matter) coincided with the consumption of a leaf-based diet (based on estimates of the dry weight of food ingested), suggesting that during this season howlers interchanged lipids with sugars to obtain energy and possibly to balance the higher protein intake obtained by the increased leaf consumption. Overall, these data did not support the prediction that food choice in this howler population was strongly correlated with particular nutrients, and suggest that balancing a suite of nutrients by consuming plants that vary widely in their composition may be an important strategy for howler monkeys. Am. J. Primatol. 79:e22524, 2017. © 2015 Wiley Periodicals, Inc.

Contributions of sarah blaffer hrdy

Contributions of sarah blaffer hrdy

Mating strategies in primates: A game theoretical approach to infanticide

Infanticide by newly immigrated or newly dominant males is reported among a variety of taxa, such as birds, rodents, carnivores and primates. Here we present a game theoretical model to explain the presence and prevalence of infanticide in primate groups. We have formulated a three-player game involving two males and one female and show that the strategies of infanticide on the males' part and polyandrous mating on the females' part emerge as Nash equilibria that are stable under certain conditions. Moreover, we have identified all the Nash equilibria of the game and arranged them in a novel hierarchical scheme. Only in the subspace spanned by the males are the Nash equilibria found to be strict, and hence evolutionarily stable. We have therefore proposed a selection mechanism informed by adaptive dynamics to permit the females to transition to, and remain in, optimal equilibria after successive generations. Our model concludes that polyandrous mating by females is an optimal strategy for the females that minimizes infanticide and that infanticide confers advantage to the males only in certain regions of parameter space. We have shown that infanticide occurs during turbulent changes accompanying male immigration into the group. For changes in the dominance hierarchy within the group, we have shown that infanticide occurs only in primate groups where the chance for the killer to sire the next infant is high. These conclusions are confirmed by observations in the wild. This model thus has enabled us to pinpoint the fundamental processes behind the reproductive decisions of the players involved, which was not possible using earlier theoretical studies.

Does Estradiol Modulate Sexual Solicitations in Female Rhinopithecus roxellana?

Studies of the relationship between sexual behavior and reproductive endocrinology in females offer critical insight into sexual selection, mate choice, and female reproductive strategies in primates. We examine the relationship between sexual solicitations and urinary estradiol in female Sichuan golden monkeys (Rhinopithecus roxellana) living under semiwild conditions at the Shanghai Wild Animal Park, China. We collected data on the frequency of sexual solicitations and urinary samples on 4 adult females during 2 mating seasons. We determined urinary estradiol levels via radioimmunoassay. Our results indicate that during the ovarian cycle, solicitation focused on the periovulatory period around the estradiol peak. The frequency of female solicitations rose to a peak after the peak of estradiol level, suggesting that ovarian steroids modulate sexual behavior during the fertile phase of the ovarian cycle. We also found that females frequently solicited matings during pregnancy, most of which the α male accepted and that resulted in copulations. During pregnancy, however, there was no obvious relationship between sexual solicitation and urinary estradiol. We conclude that in Rhinopithecus roxallana, sexual behavior and estradiol production do not strictly correlate during different parts of the reproductive cycle. We discuss additional relationships between social interactions, dominance, sexual behavior, and endocrine function.

Are Kirindy sifaka capital or income breeders? It depends

The capital and income breeding framework has only recently been used to explain variation in female reproductive strategies in primates. The application of this framework to primates and other mammals with long reproductive cycles has not been consistent. We evaluated data on Verreaux's sifaka (Propithecus verreauxi verreauxi) in the Kirindy Forest of western Madagascar to determine whether they are capital or income breeders. We found that Verreaux's sifaka can be classified as either capital or income breeders, depending on how these concepts are operationalized. These conflicting findings highlight why the capital/income framework is currently problematic and must be standardized if it is to be a useful framework for primatologists.

Learning and decision making in monkeys during a rock–paper–scissors game

Game theory provides a solution to the problem of finding a set of optimal decision-making strategies in a group. However, people seldom play such optimal strategies and adjust their strategies based on their experience. Accordingly, many theories postulate a set of variables related to the probabilities of choosing various strategies and describe how such variables are dynamically updated. In reinforcement learning, these value functions are updated based on the outcome of the player's choice, whereas belief learning allows the value functions of all available choices to be updated according to the choices of other players. We investigated the nature of learning process in monkeys playing a competitive game with ternary choices, using a rock–paper–scissors game. During the baseline condition in which the computer selected its targets randomly, each animal displayed biases towards some targets. When the computer exploited the pattern of animal's choice sequence but not its reward history, the animal's choice was still systematically biased by the previous choice of the computer. This bias was reduced when the computer exploited both the choice and reward histories of the animal. Compared to simple models of reinforcement learning or belief learning, these adaptive processes were better described by a model that incorporated the features of both models. These results suggest that stochastic decision-making strategies in primates during social interactions might be adjusted according to both actual and hypothetical payoffs.

CD70 Signaling Is Critical for CD28-Independent CD8+ T Cell-Mediated Alloimmune Responses In Vivo

The inability to reproducibly induce robust and durable transplant tolerance using CD28-B7 pathway blockade is in part related to the persistence of alloreactive effector/memory CD8(+) T cells that are less dependent on this pathway for their cellular activation. We studied the role of the novel T cell costimulatory pathway, CD27-CD70, in alloimmunity in the presence and absence of CD28-B7 signaling. CD70 blockade prolonged survival of fully mismatched vascularized cardiac allografts in wild-type murine recipients, and in CD28-deficient mice induced long-term survival while significantly preventing the development of chronic allograft vasculopathy. CD70 blockade had little effect on CD4(+) T cell function but prevented CD8(+) T cell-mediated rejection, inhibited the proliferation and activation of effector CD8(+) T cells, and diminished the expansion of effector and memory CD8(+) T cells in vivo. Thus, the CD27-CD70 pathway is critical for CD28-independent effector/memory CD8(+) alloreactive T cell activation in vivo. These novel findings have important implications for the development of transplantation tolerance-inducing strategies in primates and humans, in which CD8(+) T cell depletion is currently mandatory.

Fecal androgen levels in common marmoset (Callithrix jacchus) males living in captive family groups

In captive common marmoset groups, the reproductive inhibition observed in subordinate female seems to be a result of olfactory, visual and behavioral cues from the dominant female. However, few studies have examined the relationship among adult males living in the same social group. These studies have shown that reproductive failure among peer males seems to be based on hormonal and behavioral mechanisms. New insights on sexual strategies in primates have been shown using fecal steroids, but so far no information is available for common marmoset males. In the present study, we evaluated the influence of light-dark cycle, age and reproductive condition on the profile of fecal androgens in males living in the same family group. Feces were collected from six fathers and six sons for androgen determination during the light phase of the 24-h cycle for eight days randomly distributed over a 4-week period. Androgen levels were determined by enzyme immunoassay technique. Adult sons showed higher androgen levels (166.97 +/- 22.95 ng/g) than fathers (80.69 +/- 44.38 ng/g) and juveniles (49.06 +/- 23.15 ng/g; P < 0.05). No diurnal variation (P > 0.05) in fecal androgen profile was observed in adults or juveniles. No indication of androgen-mediated social competition between fathers and adult sons was demonstrable. These results provide basic information on fecal androgen profile useful to investigate the socioendocrinology of free-ranging common marmoset males and verify that, in contrast to daughters, the reproductive suppression of sons is not based on physiological inhibition of their gonads.

The interaction of male and female reproductive strategies and paternity in wild Japanese macaques, Macaca fuscata

Japanese macaques reside in large, mixed-sex social groups in which various reproductive strategies of both sexes operate simultaneously. This report represents the first study combining behavioural and genetic data to examine the interaction of male and female reproductive strategies in primates (N=15 adult males, N=15 adult females, Yakushima Island, Japan). During one mating season, socially dominant males monopolized most female matings. Furthermore, the six offspring sired by troop males were more likely sired by higher-ranking males than lower-ranking males. Nontroop males sired three additional offspring in the troop. Lower-ranking troop males avoided direct competition with higher-ranking males by engaging in sneak copulations with females outside of the presence of other males. Also, females expressed mate choice behaviour towards multiple males of various dominance ranks. Thus, the female strategy of attempting to mate with multiple males conflicted with the mate-guarding strategy of high-ranking males. Despite some female mate choice for mid- and low-ranking males and alternative male mating tactics by subordinate males, high-ranking males were able to monopolize most, but not all, within-troop mating and paternity. This result was due in part to the low number of females mating at the same time. The mean number of females displaying mating behaviour per day was 2.42 (range 1–5), and higher-ranking males more successfully monopolized females on days when fewer females were mating. The number of females mating simultaneously influences the outcome of reproductive conflicts between the sexes.

The Predator Deterrence Function of Primate Alarm Calls

It is generally assumed that alarm calls function in intraspecific communication, for example to warn close relatives about the presence of a predator. However, an alternative hypothesis suggests that, in some cases, signallers may also gain fitness benefits in directly communicating to the predator, for example by advertising perception and unprofitability to predators that depend on unprepared prey. In this study, we show that six monkey species in Taï forest, Ivory Coast, produce significantly more alarm calls to leopards than to chimpanzees, although both are notorious monkey predators. The conspicuously high vocalization rates to leopards had adaptive consequences for the monkeys. By following a radio‐collared leopard, we found that after detection and high alarm call rates the leopard gave up its hiding location and left the group significantly faster than would be expected by chance. We discuss these data with respect to the various functional hypothesis of alarm call behaviour and conclude that the high alarm call rates to leopards are part of an anti‐predator strategy in primates that may have evolved to deter predators that depend on surprise.

Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates

This study examines statistical correlations between socioecological variables (including measures of group composition, intermale competition, and habitat preference) and the ontogeny of body size sexual dimorphism in anthropoid primates. A regression-based multivariate measure of dimorphism in body weight ontogeny is derived from a sample of 37 species. Quantitative estimates of covariation between socioecological variables and this multivariate measure are evaluated. Statistically significant covariation between the ontogeny of dimorphism and socioecological variables, with the possible exception of habitat preference, is observed. Sex differences in ontogeny are lacking in species that exhibit low levels of intermale competition and are classifiable as species with monogamous/polyandrous mating systems. Among dimorphic species, two modes of dimorphic growth are apparent, which seem to be related to different kinds of group compositions. Multimale/multifemale species tend to become dimorphic through bimaturism (sex differences in duration of growth) with minimal sex differences in growth rate. Single-male/multifemale species tend to attain dimorphism through differences in rate of growth, often with limited bimaturism. Measures of intermale competition may also covary with these modes of dimorphic growth, but the relations among these variables are sometimes ambiguous. Correlations between dimorphic growth and behavioral variables may reflect alternative life history strategies in primates. Specifically, the ways in which risks faced by subadult males are distributed and the relations of these risks to growth rates seem to influence the evolution of size ontogenies. The absence of dimorphic ontogeny in some species can be tied to similar distributions of risk in each sex. In taxa that become dimorphic primarily through rate differences in growth, the lifetime distribution of risks for males may change rapidly. In contrast, males may face a pattern of uniformly changing or stable risk in species that become dimorphic through bimaturism. Finally, much variation recorded by this study remains unexplained, providing additional evidence of the need to specially examine female ontogeny before primate body size dimorphism can be satisfactorily explained.

Socioecologia delle strategie riproduttive nei Primati

The reproductive strategies of primates are explored from a socioecological and comparative perspective. This study shows that all Primates respond to food distribution and predation risk in a predictable manner. Reproductive strategies, are often the result of conflicting interest between the two sexes. Human reproductive strategies are then compared to those of non human primates. We conclude that humans have more resemblance to a multimale- multifemale social organization as opposed to that of solitary or monogamous primates. The human monogamous couple is but one of the solutions available to the human “deme”. We suggest it is a recent phenomenon which originated in neolithic agricultural societies, rather than in earlier hunting and gathering paleolithic society. Future human socio-ecology demands a reassessment of modern reproductive strategy and the eradication of biological xenofobia, to include all humans in a global “deme”.

Dominance-seeking strategies in primates: an evolutionary perspective

The thesis advanced in this paper is that there are basic social influence strategies and attendant principles that are characteristic of social primates. A model for analyzing and comparing social influence strategies in primates, with particular attention to dominance-seeking strategies, is advanced. The utility of the model is illustrated by reference to studies of social influence strategies in baboons, chimpanzees, and humans. Emphasis is placed on the role of communication as the vehicle for social competence. Speculation is offered about the importance of the evolution of symbolic communication in expanding the repertoire of dominance-seeking strategies in human primates.

Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis).

The seeds in fruits consumed by primates may be chewed and digested, swallowed and defecated intact, or separated from the flesh and spat out. We show by a combination of close field observations and experiments with caged animals, that long-tailed macaques (Macaca fascicularis) have a remarkably low threshold of 3-4 mm for swallowing seeds and also that wild macaques rarely break them. The seeds of 69% of the ripe fruit species eaten are spat out intact or cleaned outside the mouth and dropped. Seed-spitting significantly reduces the swallowed food bulk and may lessen the risk of releasing seed toxins during mastication. However, it requires that even small fruits are processed in the mouth one or a few at a time. We suggest that fruit storage in the cheek pouches of cercopithecine monkeys allows them to spit seeds individually without excessively slowing fruit intake while feeding on patchily distributed fruit. In contrast, Apes and New World monkeys apparently swallow and defecate most ripe seeds in their diet and colobine monkeys break and digest them, detoxifying seed defenses by bacterial fermentation.