High-ranking Males Research Articles

Patterns of male–male association in mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica: effects of dominance rank and age

Cooperative relationships among male primates are emerging as an important aspect of primate social behavior. What remains unclear is the extent to which male associations with coresident males vary within species, and what social and demographic factors drive these associations. This information provides an important contribution to our understanding of how cooperative relationships play an adaptive role in the evolution of male social and reproductive strategies. To examine the nature of male associations and the influence of social and demographic factors, including rank and age, we collected 1751 h of focal behavioral data on adult males in two large multimale–multifemale groups of mantled howlers (Alouatta palliata) at La Pacifica, Costa Rica. Both groups inhabited upland forest area, were of similar size and sex ratio, and exhibited strongly linear male hierarchies. Based on observed spatial associations within 3 m proximity, dyadic patterns varied from strongly preferred to strongly avoided associations that were largely consistent among dyads over the study period. In contrast to reports from other mantled howler study sites, neither rank nor age differences among males predicted whether dyads spent any time in proximity to one another, nor the amount of time in proximity. However, higher-ranked males within dyads were more likely to maintain close proximity than their lower-ranked counterparts. Our results provide important data on the nature of male associations within mantled howler groups with linear dominance relationships, and are suggestive of the adaptive value of cooperative relationships.

The oxidative cost of unstable social dominance.

High social rank is expected to incur fitness costs under unstable social conditions. A disruption of the oxidative balance may underlie such effects, but how markers of oxidative stress vary in relation to social rank and stability is unknown. We examined in mandrills whether the mating season characterized by social instability between males (but not between females) affected their oxidative balance differently according to their social rank. Outside the mating season, high-ranking males showed the lowest levels of oxidative damage, while during the mating season, they were the only males to experience increased oxidative damage. In contrast, the mating season increased oxidative stress in all females, irrespective of their social rank. These results support the hypothesis that the coupling between social rank and social stability is responsible for differential costs in terms of oxidative stress, which may explain inter-individual differences in susceptibility to socially induced health issues.

Effect of mating activity and dominance rank on male masturbation among free-ranging male rhesus macaques.

The adaptive function of male masturbation is still poorly understood, despite its high prevalence in humans and other animals. In non-human primates, male masturbation is most frequent among anthropoid monkeys and apes living in multimale-multifemale groups with a promiscuous mating system. In these species, male masturbation may be a non-functional by-product of high sexual arousal or be adaptive by providing advantages in terms of sperm competition or by decreasing the risk of sexually transmitted infections. We investigated the possible functional significance of male masturbation using behavioral data collected on 21 free-ranging male rhesus macaques (Macaca mulatta) at the peak of the mating season. We found some evidence that masturbation is linked to low mating opportunities: regardless of rank, males were most likely to be observed masturbating on days in which they were not observed mating, and lower-ranking males mated less and tended to masturbate more frequently than higher-ranking males. These results echo the findings obtained for two other species of macaques, but contrast those obtained in red colobus monkeys (Procolobus badius) and Cape ground squirrels (Xerus inauris). Interestingly, however, male masturbation events ended with ejaculation in only 15% of the observed masturbation time, suggesting that new hypotheses are needed to explain masturbation in this species. More studies are needed to establish whether male masturbation is adaptive and whether it serves similar or different functions in different sexually promiscuous species.

Male baboon responses to experimental manipulations of loud “wahoo calls”: testing an honest signal of fighting ability

Among male chacma baboons (Papio hamadryas ursinus), rank positions in the dominance hierarchy are fiercely contested. Physical fighting is costly but relatively rare in this species. Instead, disputes are frequently resolved using displays that include loud, repetitive “wahoo” (two-syllable bark) vocalizations. We previously found that males of all ranks adjust their contest behavior based on the relative fighting ability of opponents and that length of the second syllable (“hoo” duration), calling rate, and fundamental frequency reliably indicate fighting ability. To test whether males indeed attend to hoo duration when assessing opponents, we designed two sets of playback experiments in which call sequence pairs were identical except for this single modified feature. In experiment 1, we used calls recorded from high-ranking males unfamiliar to all subjects. In experiment 2, callers were familiar rivals that ranked one position below subjects in the dominance hierarchy. In paired analyses, subjects in both experiments responded more strongly to sequences with more intense signal features (most commonly associated with high-quality males) compared to sequences with relatively less exaggerated features (most often associated with low-quality males). Results suggest that males can use acoustic features to both indirectly evaluate strangers and to monitor the changing condition of those rivals that present the biggest intragroup threat to their position in the dominance hierarchy. Taken together with our previous research, baboons appear to follow a classic assessor strategy—signal features related to rank and condition are salient to males and directly affect their propensity to respond to rivals.

Male coalitions and female behaviour affect male mating success independent of dominance rank and female receptive synchrony in wild Barbary macaques

Dominant mammalian males should gain a reproductive advantage due to their greater fighting abilities. However, the extent to which they can monopolise access to females varies across species. In primates and recently other mammalian species, the Priority of Access (PoA) model is commonly used to measure the degree to which male rank and female receptive synchrony affect mating skew. Few studies have examined the factors which lead to deviations from the expectations of the model. Here, we investigate male mating skew in wild Barbary macaques (Macaca sylvanus). We examined four of the main factors which affect male mating success: the roles of male rank, female receptive synchrony, coalitionary activity and female behaviour. We found that male mating was skewed up the hierarchy, but there was a large deviation from the PoA model's expectations with high-ranked males not gaining as big a share as expected. Females frequently initiated sexual encounters, predominantly with mid-ranked males, increasing their mating success. Male coalitionary activity independently increased mating success. Frequent associations with females were costly to males as they were the targets of bridging coalitions, decreasing future mating opportunities for the targets. High-ranking males did not increase their mating success directly through bridging coalitions but acted to dilute the effects of female behaviour. By examining different factors affecting mating skew, we are able to show that alternative male and female mating strategies are effective in reducing the monopolisation potential of the dominant male.

Correlates of Male Consortship Rate in Free-Ranging Rhesus Macaques (Macaca mulatta)

Male–male competition for access to receptive females can take the form of nonrecurring fights and/or a sustained contest over mating opportunities. Male physical condition has been linked to dominance rank and reproductive success in species characterized by intrasexual fights for dominance and access to females. In group-living species characterized by endurance rivalry, however, factors contributing to male reproductive success are less well understood. In such species, particularly seasonally breeding ones with low sexual dimorphism and seniority-based rank, age and social factors other than rank may prove important. In the absence of genetic data, male mate guarding or consortship can serve as an indicator of male reproductive success. To evaluate the contribution of age and intragroup sociality to male consortship rate, I collected behavioral data during one nonmating and one mating season in two social groups of free-ranging rhesus macaques that experience no predation or food scarcity. Higher-ranking males, younger males, or males that exhibited lower rate of intrasexual aggression had higher consortship rates. Male–female dyads that groomed outside consortship did not form consortships as often as dyads that did not engage in nonconsort grooming. This is the first study to identify the significance of male–male aggression and male–female affiliation to male consortship rate in a species characterized by endurance rivalry, high male rank stability, and strong female mate choice. Social behaviors and male age may be particularly important in determining male reproductive success in populations experiencing high food availability and a lack of predation, which are typical of an increasing number of vertebrates in areas densely populated by humans.

Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk

1. Heterogeneity in host association patterns can alter pathogen transmission and strategies for control. Great apes are highly social and endangered animals that have experienced substantial population declines from directly transmitted pathogens; as such, network approaches to quantify contact heterogeneity could be crucially important for predicting infection probability and outbreak size following pathogen introduction, especially owing to challenges in collecting real-time infection data for endangered wildlife. 2. We present here the first study using network analysis to quantify contact heterogeneity in wild apes, with applications for predicting community-wide infectious disease risk. Specifically, within a wild chimpanzee community, we ask how associations between individuals vary over time, and we identify traits of highly connected individuals that might contribute disproportionately to pathogen spread. 3. We used field observations of behavioural encounters in a habituated wild chimpanzee community in Kibale National Park, Uganda to construct monthly party level (i.e. subgroup) and close-contact (i.e. ≤ 5 m) association networks over a 9-month period. 4. Network analysis revealed that networks were highly dynamic over time. In particular, oestrous events significantly increased pairwise party associations, suggesting that community-wide disease outbreaks should be more likely to occur when many females are in oestrus. 5. Bayesian models and permutation tests identified traits of chimpanzees that were highly connected within the network. Individuals with large families (i.e. mothers and their juveniles) that range in the core of the community territory and to a lesser extent high-ranking males were central to association networks, and thus represent the most important individuals to target for disease intervention strategies. 6. Overall, we show striking temporal variation in network structure and traits that predict association patterns in a wild chimpanzee community. These empirically-derived networks can inform dynamic models of pathogen transmission and have practical applications for infectious disease management of endangered wildlife species.

Grooming reciprocity in male Tibetan macaques

In several primate species, adult males are reported to compete for access to reproductive partners as well as forming affiliative and cohesive social bonds based on the exchange of goods or services. We hypothesized that among a broad set of fitness-maximizing strategies, grooming can be used by individual adult males to enhance social relationships through reciprocity and/or through the interchange of grooming for a different but equivalent good or service. We used focal animal sampling and continuously recorded dyadic grooming and agonistic interactions to test a series of predictions regarding male social interactions in a free-ranging group of Tibetan macaques (Macaca thibetana) at Huangshan, China. During the non-mating season or between males of similar rank throughout the year, grooming effort given was matched by grooming effort received. However, lower ranking males groomed higher ranking males at a greater rate and/or for a longer duration during both the mating and non-mating periods. We found that higher ranking males directed less aggression towards males with whom they formed a frequent grooming partnership, indicating that grooming received was interchanged for increased social tolerance. These data suggest that individual male Tibetan macaques employ alternative social strategies associated with grooming reciprocity or interchange depending on dominance rank and rates of aggression, and highlight the importance of both biological markets and grooming reciprocity as behavioral mechanisms used by resident adult males to form and maintain affiliative social bonds.

The energy cost of singing in wild rock hyrax males: evidence for an index signal

In many species individuals advertise their quality via vocal communication. Although sound production requires energy, it is still unclear to what extent vocalizing increases metabolic rate. A substantial energetic cost of vocalization may suggest that it serves as a handicap. In this study, we evaluated the energetic cost of vocalization in the context of other activities in a free-living mammal. In the rock hyrax, Procavia capensis, males produce loud complex songs that convey multiple types of information about the singer. We used the doubly labelled water method to estimate field metabolic rate (FMR), in males that were collar-fitted with miniaturized recorders. Higher-ranked males sang longer songs, which also featured higher sound energy. However, contrary to our predictions, the duration of singing was negatively correlated with FMR, whereas the duration of other social sounds, typically associated with social conflicts, had a positive effect on FMR. We suggest that higher-ranking males expend overall less energy due to lower intrinsic metabolism, and thus the singing duration effect on FMR is a reflection of social rank. Rock hyrax singing is therefore assessed as requiring a high effort over a short period but not as a lengthy activity, matching the category of index signals. Singing may also serve as a handicap to the signaller, not because of its energetic cost but because it exposes the singer to potential predation. Our study is the first to record the activities and vocalizations of a free-living mammal in such detail. We discuss the costs and benefits of hyrax songs, suggesting that singing males trade safety from predators for increasing their reputation.

Pattern of Social Interactions after Group Integration: A Possibility to Keep Stallions in Group

Horses are often kept in individual stables, rather than in outdoor groups, despite such housing system fulfilling many of their welfare needs, such as the access to social partners. Keeping domestic stallions in outdoor groups would mimic bachelor bands that are found in the wild. Unfortunately, the high level of aggression that unfamiliar stallions display when they first encounter each other discourages owners from keeping them in groups. However, this level of aggression is likely to be particularly important only during group integration, when the dominance hierarchy is being established, whereas relatively low aggression rates have been observed among stable feral bachelor bands. We investigated the possibility of housing breeding stallions owned by the Swiss National Stud in groups on a large pasture (5 stallions in 2009 and 8 stallions in 2010). We studied the pattern of agonistic, ritual and affiliative interactions after group integration (17–23 days), and the factors influencing these interactions (time after group integration, dominance rank, age or experience of group housing). We found that stallions displayed generally more ritual than agonistic and than affiliative interactions. The frequency of agonistic and ritual interactions decreased quickly within the first three to four days. The frequency of affiliative interactions increased slowly with time before decreasing after 9–14 days. A stable hierarchy could be measured after 2–3 months. The highest-ranking males had less ritual interactions than the lowest-ranking. Males had also less agonistic, ritual and affiliative interactions if they had already been housed in a group the previous year. Therefore, we found that breeding stallions could be housed together on a large pasture, because the frequency of agonistic interactions decreased quickly and remained at a minimal level from the fourth day following group integration. This housing system could potentially increase horse welfare and reduce labour associated with horse management.

The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses.

Social status primarily determines male mammalian reproductive success, and hypotheses on the endocrinology of dominance have stimulated unprecedented investigation of its costs and benefits. Under the challenge hypothesis, male testosterone levels rise according to competitive need, while the social stress hypothesis predicts glucocorticoid (GC) rises in high ranking individuals during social unrest. Periods of social instability in group-living primates, primarily in baboons, provide evidence for both hypotheses, but data on social instability in seasonally-breeding species with marked social despotism but lower reproductive skew are lacking. We tested these hypotheses in seasonally-breeding rhesus macaques on Cayo Santiago, Puerto Rico. We documented male fecal GC and androgen levels over a 10 month period in relation to rank, age, natal status and group tenure length, including during a socially unstable period in which coalitions of lower-ranked males attacked higher-ranked males. Androgen but not GC levels rose during the mating season; older males had lower birth season levels but underwent a greater inter-season rise than younger males. Neither endocrine measure was related to rank except during social instability, when higher ranked individuals had higher and more variable levels of both. High ranking male targets had the highest GC levels of all males when targeted, and also had high and variable GC and androgen levels across the instability period. Our results provide evidence for both the challenge and social stress hypotheses.

Supply and demand predict male grooming of swollen females in captive chimpanzees, Pan troglodytes

The notion of a biological marketplace as a framework for explaining cooperative acts among animals is well supported. However, direct evidence for a biological market in a mating context is limited to a handful of studies. We collected data over a 3-year period to test supply/demand predictions of male grooming of swollen females according to a biological market in captive chimpanzees while controlling for other potential interchange. Females received more grooming from and gave less grooming to males when swollen than when not swollen, with parous females receiving more grooming from males than nulliparous females. The central tenet of a biological market that the market value of a commodity should vary according to its availability was supported. Males groomed swollen females less as the availability of swollen females in the group increased. There was also an effect of male dominance rank such that higher ranking males groomed swollen females less than lower ranking males. Taken together, our findings provide evidence for male grooming of swollen females according to a biological market while controlling for potential confounds.

Male and female reproductive strategies and multiple paternity in the polygynandrous Alpine Accentor Prunella collaris

Five breeding groups of the Alpine Accentor were studied in a Swiss alpine region. The studied groups showed a polygynandrous mating system and each group was formed of 1–4 females and 3–5 males. The females had exclusive territories, while the males cooperated in defending their group territory. Among the males of one group, a linear dominance relationship was usually well established among the alpha, beta and subordinate male S 1. Both frequent copulation and mate guarding strategies were applied. Females advertised their fertility, solicited most of the copulations and mated multiple times with several males. With approximately 350 matings during the short fertile period of 10 days, the Alpine Accentor is one of the bird species with the highest copulation frequency. Intensity of mate guarding and copulation frequency were highest starting 1 day before egg-laying and throughout the egg-laying period. The alpha male guarded a fertile female closely during the ovulation period, while the beta and other subordinate males (S 1, S 2 and S 3) were restricted in their access to fertile females by the alpha male’s mate guarding ability. In most cases, they did not guard mates and solely performed the frequent copulation strategy. Accordingly, higher ranking males got more solicitations from females, maintained a higher copulation frequency, but also refused a greater portion of all mating offers. Sperm competition was intense with 81.8 % of the broods having multiple paternity. The share of matings during the ovulation period best reflected the achieved share of paternity. Alpha, beta and S 1 sired most of the young, while S 2, S 3 and extra-group males were seldom fathers of offspring. At one nest, up to 4 males helped to feed the young, however, usually at a low rate and the overall male help (28 %) was smaller than the female contribution (72 %). In this polygynandrous mating system, females of the studied population lacked full male help but might have benefited from the greater genetic variation of their young, while males have a large individual variance in their lifetime reproductive success with higher ranking males raising their fitness to above average.

Mortal combat: an apparent intraspecific killing by a male Black-capped Chickadee

ABSTRACT Much theory about communication in aggressive contexts hinges on the assumption that injury or death is a potential outcome of fighting. However, published accounts of intraspecific killings during competitive interactions between songbirds are extremely rare. Here, we report an observation where one adult Black-capped Chickadee (Poecile atricapillus) appeared to kill another. The two opponents were high-ranking males that had been in the same winter flock, consistent with the prediction that mortal combat is most likely between evenly matched individuals. The interaction occurred when birds were defending territories and had begun nesting activities. A female that had previously been paired with the victim was also present during the interaction. Our observations suggest that the male chickadees were fighting for access to territorial resources or to a female, and indicate that aggressive interactions between songbirds can be costly and potentially fatal. Mucha de la teoría sobre la comunicación en el contexto de agresión gira entorno a la suposición que una pelea puede resultar en una lesión o la muerte de uno de los individuos. Sin embargo, registros publicados de muerte intraespecifica durante interacciones competitivas entre paseriformes son extremadamente raras. Aquí, reportamos una observación en donde un adulto de Poecile atricapillus aparentemente mato a otro. Los dos oponentes eran machos de alto rango que estuvieron en la misma bandada durante el invierno, esto es consistente con la predicción que combates mortales son mas probables entre individuos en igualdad de condiciones. Las interacciones ocurrieron cuando los individuos estaban defendiendo territorios y habían empezados actividades de anidación. Una hembra que previamente había conformado una pareja con la victima estuvo presente cuando ocurrió la interacción. Nuestra observación sugiere que los machos de P. atricapillus estaban peleando por acceso a recursos territoriales o por una hembra e indica que interacciones agresivas entre paseriformes pueden ser costosas y potencialmente fatales.

Adolescent Male Chimpanzees at Ngogo, Kibale National Park, Uganda Have Decided Dominance Relationships

Dominance relationships are common among primates, and are usually the result of resource competition. Adult male chimpanzees have pronounced dominance relationships, and can be ranked relative to one another in dominance hierarchies. Adult male chimpanzees achieve, and maintain, high rank through a combination of physical size, strength and political ability. Dominance in male chimpanzees has very real benefits as high-ranking males have priority access to resources and potential mates, and father more offspring than do low-ranking conspecifics. Previous research has suggested that adolescent male chimpanzees do not have dominance relationships with each other. Here, I report the first evidence of decided dominance relationships and a linear dominance hierarchy in adolescent male chimpanzees from an unusually large community of wild chimpanzees at Ngogo, Kibale National Park, Uganda.

Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques?

In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogen-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30–40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females' fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.

Evidence for scent marking in vervet monkeys?

We used data from two troops of free-ranging vervet monkeys (Chlorocebus aethiops) to assess the proposition that the conspicuous chest rubbing observed in this species constitutes scent-marking behavior. Our data indicate that chest-rubbing behavior is associated with higher-ranking males who are more likely to do so during the breeding season in areas where territorial encounters occur. We found no indication that chest rubbing was triggered directly by encounters between troops. We conclude that these data, in conjunction with reports of chest rubbing from other Old World monkeys, are sufficiently suggestive of scent marking to warrant further, directed research and support the suspicion that olfactory cues remain important to catarrhines in a number of domains.

Impartial third-party interventions in captive chimpanzees: a reflection of community concern.

Because conflicts among social group members are inevitable, their management is crucial for group stability. The rarest and most interesting form of conflict management is policing, i.e., impartial interventions by bystanders, which is of considerable interest due to its potentially moral nature. Here, we provide descriptive and quantitative data on policing in captive chimpanzees. First, we report on a high rate of policing in one captive group characterized by recently introduced females and a rank reversal between two males. We explored the influence of various factors on the occurrence of policing. The results show that only the alpha and beta males acted as arbitrators using manifold tactics to control conflicts, and that their interventions strongly depended on conflict complexity. Secondly, we compared the policing patterns in three other captive chimpanzee groups. We found that although rare, policing was more prevalent at times of increased social instability, both high-ranking males and females performed policing, and conflicts of all sex-dyad combinations were policed. These results suggest that the primary function of policing is to increase group stability. It may thus reflect prosocial behaviour based upon “community concern.” However, policing remains a rare behaviour and more data are needed to test the generality of this hypothesis.

Stable fighting strategies to maintain social ranks in captive male Alpine musk deer (Moschus sifanicus)

This study was conducted at the XINGLONGSHAN Musk Deer Farm of China from July to September 2008. Results showed that captive male musk deer exhibit aggressive dominance behavior, by which a stable social ranking is established. Generally, there were three types of aggression in agonistic interactions among males: attacking, displacing and threatening. Threatening was more frequently observed than displacing and attacking. When in conflict with other deer, high-rank males exhibited significantly more attacking than displacing and threatening. Moreover, no attacking occurred in low-rank and middle-rank males, but these individuals initiated significantly more threatening displays than high-rank individuals. Among musk deer groups with different social ranks, there were no significant differences between threats received by middle-rank and low-rank groups, but attacks directed to high-rank males was significantly lower than displacing and threatening behaviors. On the basis of these results, it is suggested that when a captive male musk deer population is assembled, individuals should be diversified in fighting ability and level of aggression. In particular, deer with higher aggression should not be enclosed with deer with similar tendencies, but should be enclosed with individuals with lower fighting levels. This should maintain stable social structures within captive musk deer groups and improve the overall welfare of captive musk deer.

Mate competition, testosterone and intersexual relationships in bonobos, Pan paniscus

Variation in male testosterone levels across and within species is known to be related to mating systems, male dominance rank and aggression rates. When aggression enhances access to mates, dominance status and androgen levels correlate positively. Deviation from this pattern is expected when access to females is determined by factors other than male dominance or when high androgen levels interfere with nonaggressive forms of male reproductive strategies such as paternal care and pair bonding. Bonobos offer an interesting study species to test the relationship between male dominance, aggression and intersexual relationships. On the one hand, males form dominance hierarchies and compete for access to females and mating success varies with rank. On the other hand, males and females are equally dominant, male rank is not only the result of aggression, and strong intersexual relationships might be crucial to male reproductive success. We used behavioural and physiological data from wild bonobos to test relationships between behavioural correlates of mate competition and androgen levels. Aggression and rank were positively correlated, as were aggression and mating success. In the presence of potentially fertile females, male aggression increased but only low-ranking, less aggressive males showed increases in testosterone levels, which consequently tended to be negatively related to rank. High-ranking males who had lower testosterone levels and were less responsive in their testosterone increase were more often involved in friendly relationships with unrelated females. These results suggest that, in bonobos, amicable relationships between the sexes rather than aggressive interactions mediate males’ physiological reactivity during periods of mate competition.