Multiple Adult Males Research Articles

The impacts of management interventions on the sociality of African lions (Panthera leo): Implications for lion conservation

Abstract African lion (Panthera leo) populations normally consist of several neighbouring prides and multiple adult males or groups of males that interact competitively. In large, open systems, cub defence from infanticidal males and territory defence drive group living in lions. However, in smaller (<1000 km2), fenced wildlife reserves, opportunities for natural immigration and emigration are limited which means that the evolutionary drivers of lion sociality may collapse. Here, we use lion behavioural data collected from 16 wildlife reserves across South Africa to test how management‐induced ecological conditions alter lion social dynamics. The number of lionesses observed together was best predicted by pride size, prey biomass and biome. Lionesses were less likely to group together as pride size increased, but more likely to group together as prey biomass and habitat productivity increased. In addition, adult males were observed more frequently with prides that had young (<12 months) cubs in reserves that had unfamiliar adult males present compared to reserves without any unfamiliar adult males. Our results demonstrate how intraspecific competition between lions drives their sociality, and this may break down in small, fenced wildlife reserves where lions are actively managed. Although small, fenced reserves in South Africa have made a significant contribution to increasing lion numbers on the continent, our work highlights several important ecological implications of active lion management. For wildlife managers, mimicking the outcomes of different levels of intraspecific competition is likely a critical management tool for the persistence of lions in small reserves.

Repeated long-range migrations of adult males in a common Indo-Pacific reef shark

The grey reef shark, Carcharhinus amblyrhynchos, is one of the most abundant coral reef sharks throughout the Indo-Pacific. However, this species has been critically impacted across its range, with well-documented population declines of > 90% attributed to human activities. A key knowledge gap in the successful implementation of grey reef shark conservation plans is the understanding of large-scale movement patterns, along with the associated biological and ecological drivers. To address this shortfall, we acoustically monitored 147 adult and juvenile grey reef sharks of all sexes for more than 2 yr across the New Caledonian archipelago, West Pacific. Here, we document multiple adult males undertaking return journeys of up to nearly 700 km in consecutive years. This constitutes the first evidence of repeated long-range migrations for this species. Although only a limited number of adult males were definitively tracked undertaking migrations, similar timing in changes in the detection patterns of a further 13 animals, mostly adult males, suggests this behavior may be more common than previously thought. The paucity of evidence for juvenile migrations and timing of adult movements suggest that mating is the motivation behind these migrations. Our results have important implications for management, given the potential of mature individuals to recurrently travel outside managed or protected areas. Future management of this species clearly needs to consider the importance of large-scale migratory behaviors when developing management plans.

Multi-male groups positively linked to infant survival and growth in a cooperatively breeding primate

Cooperative breeding is a system where helper individuals care for breeding individuals’ offspring. As a result, social environment is likely to play a key role in regulating reproductive success. In primates, cooperative breeding is only found in the family Callitrichidae. Callitrichid males typically provide more infant care than non-breeding females, and in many callitrichid species, the presence of multiple males has been linked to infant survival. Leontopithecus chrysomelas (the golden-headed lion tamarin) is an endangered callitrichid found in the Atlantic Forest of Brazil. We used long-term data for wild L. chrysomelas to assess the influence of social group composition on reproductive success. Our survival model found that infant survival was negatively associated with group size, but this cost was mitigated by the presence of multiple adult males vs a single adult male. We also found that infants raised in groups with multiple adult males exhibited faster growth rates and higher adult weights than infants raised with a single adult male. This study adds novel evidence for the positive influence of adult males on callitrichid reproduction, demonstrating that adult males influence infant growth, as well as survival, in wild populations of cooperatively breeding primates. We suggest that social group composition, particularly the presence of adult males, be considered in future conservation strategies given its importance for reproductive success. In cooperatively breeding species, group members care for breeding individuals’ offspring. Due to this care, group composition may have a strong influence on infant success. In cooperatively breeding primates, males often provide more infant care than females. We investigated the influence of group composition on infant success in a cooperatively breeding primate, the golden-headed lion tamarin. Using long-term field data, we found that infant survival decreased as group size increased. However, this effect was reduced when multiple adult males were present in the group compared to a single male. We also found that infants grew faster and reached larger adult weights in the presence of multiple adult males compared to a single male. Our results demonstrate the importance of group composition for cooperative breeders and provide new evidence for the positive influence of adult males on cooperatively breeding primate infants.

Adult-adult social play in captive chimpanzees: Is it indicative of positive animal welfare?

Play is sometimes considered as an indicator of positive animal welfare. However, it is not yet sufficiently understood whether or not social play among adults can be considered as such an indicator because it is rare in adult animals. This study investigates the factors that influence social play in adult captive chimpanzees in order to discuss its function and use as a welfare indicator. The subjects were 37 adult chimpanzees (17 males and 20 females) living in Kumamoto Sanctuary, Kyoto University, Japan. We completed 367h of behavioural observation of mixed-sex and all-male groups of chimpanzees between June and July 2014, and December 2014 and March 2015, respectively. We collected data on social play, social grooming (mutual and unilateral grooming), aggressive interactions, self-directed behaviours and abnormal behaviours. We checked the relationship between social play and age, sex, timing, social group formation and different social behaviours. The results reveal that social play increased in males of all-male groups compared to those of mixed-sex groups. Furthermore, we analysed behaviours in individuals from all-male groups and found that social play increased before feeding. In addition, although mutual social grooming showed a negative correlation with aggressive interactions, social play did not show such a relationship. Furthermore, social play and mutual social grooming were negatively correlated. These results suggest that social play may be used as a means to reduce social tension and that it does not necessarily indicate that the individuals formed affiliative social relationships such as mutual social grooming indicates. Therefore, although social play is important to enable the coexistence of multiple adult males who do not always get along well, we need to be cautious when interpreting social play from the view of animal welfare.

The Evolution of Eulemur Social Organization

Recent comparative studies on the evolution of mammalian sociality came to opposite conclusions regarding the direction and drivers of evolutionary transitions in social organization, particularly concerning the evolution of pair-living among primates. Because the genus Eulemur is one of the few exceptional primate genera that contain both group- and pair-living species, eulemurs offer a rare opportunity to illuminate the processes driving social diversity among species with very similar life histories and ecologies. The aims of our study were therefore 1) to reconstruct the evolution of social organization in eulemurs with new demographic and phylogenetic data and 2) to evaluate several hypotheses about the evolution of pair-living with data from our long-term study of Eulemur rufifrons and published data on other eulemurs. Our review of published data confirmed that E. mongoz and E. rubriventer are pair-living, whereas the 10 other species of Eulemur live in groups with multiple adult males and females. Furthermore, pair-living evolved at least once among eulemurs from group-living ancestors. The available comparative evidence indicated that this evolutionary transition was probably not driven by male infanticide, social instability, or singular ecological factors. Instead, we propose that female competition has favored small female group size and that this effect may have been exacerbated by interspecific competition with sympatric congeners in the ancestors of the pair-living species. In conclusion, we confirmed that the evolution of pair-living from group-living ancestors among true lemurs is exceptional, but not unique, among mammals, and that commonly invoked hypotheses for the evolution of pair-living do not appear to be supported for this genus.

Complex cooperative breeders: Using infant care costs to explain variability in callitrichine social and reproductive behavior.

The influence of ecology on social behavior and mating strategies is one of the central questions in behavioral ecology and primatology. Callitrichines are New World primates that exhibit high behavioral variability, which is widely acknowledged, but not always systematically researched. Here, I examine the hypothesis that differences in the cost of infant care among genera help explain variation in reproductive traits. I present an integrative approach to generate and evaluate predictions from this hypothesis. I first identify callitrichine traits that vary minimally and traits that are more flexible (e.g., have greater variance or norm of reaction), including the number of males that mate with a breeding female, mechanisms of male reproductive competition, number of natal young retained, and the extent of female reproductive suppression. I outline how these more labile traits should vary along a continuum of infant care costs according to individual reproductive strategies. At one end of the spectrum, I predict that groups with higher infant care costs will show multiple adult males mating and providing infant care, high subordinate female reproductive suppression, few natal individuals delaying dispersal, and increased reproductive output by the dominant female -with opposite predictions under low infant costs. I derive an estimate of the differences in ecological and physiological infant care costs that suggest an order of ascending costs in the wild: Cebuella, Callithrix, Mico, Callimico, Saguinus, and Leontopithecus. I examine the literature on each genus for the most variable traits and evaluate a) where they fall along the continuum of infant care costs according to their reproductive strategies, and b) whether these costs correspond to the ecophysiological estimates of infant care costs. I conclude that infant care costs can provide a unifying explanation for the most variable reproductive traits among callitrichine genera. The approach presented can be used to generate predictions and motivate researchers to unravel complexity in callitrichine social and reproductive behavior.

Male rank, not paternity, predicts male–immature relationships in mountain gorillas, Gorilla beringei beringei

Kin discrimination mechanisms are expected to evolve when they provide fitness benefits. To date, evidence for kin discrimination is mixed across taxa and mating systems even when it would apparently be beneficial. In animals with promiscuous mating systems, males were long believed to abstain from parenting behaviours partly because the costs of offspring misidentification outweighed the benefits of dual parenting. Conversely, males in monogamous systems could parent because of high paternity certainty. However, recent work has shown that in some species males parent despite high false paternity rates, and males in some promiscuous systems discriminate between their own and other males' offspring. Here we evaluate the impact of male dominance rank, paternity and age on maleeimmature relationships in wild mountain gorillas. Mountain gorillas provide an interesting context for assessing paternal kin discrimination because (1) maleeimmature relationships are strong, and (2) while their morphological characteristics suggest an evolutionary history of single-male groups, a substantial fraction contain multiple adult males. In our sample of 21 males and 49 genotyped immatures living in multimale groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center, we found that male rank was the primary predictor of maleeimmature relationship strength. There was little evidence that paternity or age were related to relationship patterns. Maleeimmature dyads were closer social partners in 2011e12 when groups were smaller and reproductive skew lower, than comparable dyads in 2003e04 when groups were larger and skew higher. Gorillas' lack of paternal kin discrimination provides further behavioural evidence that the species' multimale social structure is evolutionarily novel. However, patterning of maleeimmature relationships and genetic paternity suggest a persistent minority of two-male groups throughout G. beringei's evolutionary history. This may help explain their ability to live in multimale, multifemale social units despite possessing morphological characteristics typical of harem systems.

Foraging range movements of the endangered Hawaiian hoary bat,Lasiurus cinereus semotus(Chiroptera: Vespertilionidae)

We documented nightly movements of Hawaiian hoary bats (Lasiurus cinereus semotus) on the island of Hawai'i. Based on data from 28 radiotagged individuals mean foraging range (FR) was 230.7 ± 72.3 ha, core-use area (CUA) was 25.5 ± 6.9 ha (or 11.1% of mean FR), and the mean long axis (LAX) across the FR was 3,390.8 ± 754.3 m. There was almost no overlap in CUAs among 4 adult males having overlapping foraging areas and tracked simultaneously or within a 90-day window of each other. CUAs of subadults partially overlapped with multiple adult males or with one other subadult. High variance in FRs, cores use areas, and LAX across the FR perhaps reflect localized stochastic variables such as weather, habitat, and food resources. Hawaiian hoary bats use moderately large FRs among insectivorous bats studied with comparable methodologies; however, foraging activity indicated by documentation of acoustic feeding buzzes is concentrated within one or a few disjunct areas cumulatively forming the 50% fixed kernel of C...

Female competition in chimpanzees.

Female chimpanzees exhibit exceptionally slow rates of reproduction and raise their offspring without direct paternal care. Therefore, their reproductive success depends critically on long-term access to high-quality food resources over a long lifespan. Chimpanzee communities contain multiple adult males, multiple adult females and their offspring. Because males are philopatric and jointly defend the community range while most females transfer to new communities before breeding, adult females are typically surrounded by unrelated competitors. Communities are fission-fusion societies in which individuals spend time alone or in fluid subgroups, whose size depends mostly on the abundance and distribution of food. To varying extents in different populations, females avoid direct competition by foraging alone or in small groups in distinct, but overlapping core areas within the community range to which they show high fidelity. Although rates of aggression are low, females compete for space and access to food. High rank correlates with high reproductive success, and high-ranking females win direct contests for food and gain preferential access to resource-rich sites. Females are aggressive to immigrant females and even kill the newborn infants of community members. The intensity of such aggression correlates with population density. These patterns are compared to those in other species, including humans.

Paternity and relatedness in a polyandrous nonhuman primate: testing adaptive hypotheses of male reproductive cooperation

Male reproductive cooperation is rare in nature: expectations from evolutionary theory suggest that males should be competitors for reproductive opportunities and provide little parental care. Counter to this expectation, in cooperatively polyandrous mating systems, multiple adult males mate with a single breeding female and subsequently cooperate to rear her young. This raises the question of the fitness benefits of parental care, as males may be providing care to offspring that are not their own. Here, I use genetic and demographic data from a multiyear field study of Geoffroy’s tamarin, Saguinus geoffroyi ,t o test predictions of the indirect and direct fitness benefits hypotheses. I found that polyandrous males within a group were related at levels consistent with filial or fraternal relationships (r ¼ 0.36e0.44) and could also share paternity (40% of groups had >2 male sires). Sharing of paternity occurred both within litters and over multiyear associations that remained stable throughout the study period of 2e3 years. However, remaining groups had a single sire, perhaps owing to the ability of males to prevail in sperm competition. These results suggest the joint role of indirect and direct fitness benefits in maleemale cooperation in tamarins, in contrast to other cooperatively polyandrous species. The high average relatedness of polyandrous males may be consistent with fraternal cooperative polyandry in this species, as observed in certain human societies, providing a novel example that should enhance comparative studies of the evolution of maleemale cooperation in reproduction.

Preliminary Data on the Behavior, Ecology, and Morphology of Pygmy Tarsiers (Tarsius pumilus)

We here present the first behavioral, morphological, and ecological data on a living group of highland pygmy tarsiers, Tarsius pumilus, and compare them with the lowland tarsier species of Sulawesi. Pygmy tarsiers were previously known only from 3 museum specimens and had not been seen alive since the first specimens were collected in 1917 and 1930. As part of a 2-mo exploratory study, we recently located a group consisting of ≥4 pygmy tarsiers in the mossy cloud forest of Lore Lindu National Park, Central Sulawesi, Indonesia. We captured 1 adult female and 2 adult male group members. The tarsiers weighed a mean of 50 g, less than half the weight of adult lowland tarsiers. Our behavioral observations indicate that these tarsiers live in small groups that return to the same sleeping tree each morning. Though our data are preliminary, pygmy tarsier body proportions appear to differ from the lowland Sulawesian tarsier species, with relatively long hind limbs compared to total body length. We also observed differences in grouping and communication behaviors. Unlike lowland tarsiers, pygmy tarsiers possess multiple adult males per group and rarely vocalize or scentmark. These differences may correlate with variables unique to their high altitude habitat, especially a reduction in food and tree resources, given that tree density declined sharply along an altitudinal gradient. Our preliminary study identifies the importance of altitudinal ecological gradients to tarsier behavioral ecology in Central Sulawesi, providing questions and predictions for future research directions.

Molecular genetic evidence for social group disruption of wild vicuñas Vicugna vicugna captured for wool harvest in Chile

Since 1994 wild vicuñas have been captured and shorn for their wool, yet, there remains a noticeable lack of data regarding the possible influence of capture and shearing upon vicuña biology. Therefore, we assessed post-capture group composition, genetic relatedness, and paternity among animals that were captured for live shearing and release. We captured twenty-six groups (134 animals) on the Chilean Altiplano. Seventy-three percent of Male Groups (designated prior to chase) contained exclusively adult males upon capture, whereas remaining “Male Groups” contained crias and/or adult females and crias. Forty-seven percent of Family Groups (designated prior to chase) contained 1 adult male, adult females, and the number of crias ≤ the number of adult females. Remaining Family Groups contained no or multiple adult males, and more crias than adult females. Average relatedness among all vicuñas was −0.007. Paternity analysis revealed that 35% of crias were captured with their biological mother and that only 1 cria was captured with both biological parents. Based on previous observations of group composition in the wild, animals from different groups may separate and/or mix during the chasing stage. Improvement of the chasing technique and instituting a post-capture monitoring program may aid in the detection of medium- and long-term impacts regarding group stability, cria survival, and ultimately wool production.

Even adult sex ratios in lemurs: Potential costs and benefits of subordinate males in Verreaux's sifaka (Propithecus verreauxi) in the Kirindy Forest CFPF, Madagascar

Optimal group size and composition are determined by both the costs and benefits of group living for the group's members. Verreaux's sifakas (Propithecus verreauxi), a diurnal lemur, form multimale multifemale groups with the tendency toward even adult sex ratios despite a small average number of females per group. The unexpected presence of multiple adult males may be explained by tolerance of other group members if subordinate males provide benefits to the group that outweigh the costs associated with their presence. Results based on both demographic data collected over a 13-year period and behavioral observations suggest that subordinate males provide no benefits in terms of infant survival and defense against group takeover by outside males. Although groups with more males are more likely to win intergroup encounters, subordinate males do not participate in these encounters more often than expected. Subordinate males are not costly to other group members in terms of direct intragroup feeding competition, but aggression rates between dominant and immigrated subordinate males increase in the mating season. Even though subordinate males provide very few benefits to the group, they are not very costly either and thus may be tolerated by resident females and dominant males. This tolerance may help to partially explain the tendency towards their unusual adult sex ratio.

The influence of captive adolescent male chimpanzees on wounding: management and welfare implications

Adolescence, the period lasting from the onset of puberty to the emergence of physical and sexual maturity, is a period of social change for many species including chimpanzees. Several reports have implicitly linked the physiological changes that occur during male chimpanzee adolescence to significant disruption in the social group, which in turn may result in serious agonism and wounding. To assess the association between adolescent males and wounding rates, 38 institutions housing 399 chimpanzees among 59 social groups, recorded all wounds incurred by chimpanzees over a 6-month period. The rate of wounding did not differ between groups with or without adolescent males. Adolescent males received the most wounds, but were no more likely to cause wounds than group members of any other sex-age class. Social groups with multiple adult males experienced lower wounding rates than those with a single adult male. Results indicate that (1) adolescent male chimpanzees may receive, but not inflict, more wounds than chimpanzees in other sex-age classes; and (2) management strategies that support natural social groupings may control and limit group agonism.

Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population

We investigated patterns of relatedness and reproduction in a population of striped hyenas in which individuals are behaviourally solitary but form polyandrous spatial groups consisting of one adult female and multiple adult males. Group-mate males were often close relatives, but were unrelated or distantly related in some cases, indicating that male coalitions are not strictly a result of philopatry or dispersal with cohorts of relatives. Most male-female pairs within spatial groups were unrelated or only distantly related. Considering patterns of relatedness between groups, relatedness was significantly higher among adult males living in non-neighbouring ranges than among neighbouring males. Mean relatedness among male-female dyads was highest for group-mates, but relatedness among non-neighbouring males and females was also significantly higher than among dyads of opposite-sex neighbours. Female-female relatedness also increased significantly with increasing geographic separation. These unusual and unexpected patterns may reflect selection to settle in a nonadjacent manner to reduce inbreeding and/or competition among relatives for resources (both sexes), or mates (males). Finally, resident males fathered the majority of the resident female's cubs, but extra-group paternity was likely in 31% of the cases examined, and multiple paternity was likely in half of the sampled litters.

Bonobos

Bonobos

Social organization and variation in cooperative alliances among male lance-tailed manakins

In species where males form cooperative alliances for the purposes of reproduction, there may be considerable variation in the strength and size of alliances observed within one population. Male lance-tailed manakins, Chiroxiphia lanceolata, form long-term cooperative alliances to court females on group-occupied display areas. I investigated male status and alliance structure in a colour-banded population. Each display area was a group territory attended by multiple adult and subadult males. Alpha males were present at display areas more often than other males, performed solo courtship displays for females, and vocalized distinctively in paired displays. Alpha–beta pairs had high duetting association index values and performed two types of paired courtship displays for females. I combined these characteristics in a predictive logistic regression model to assess male status probabilistically when not all key behaviours were observed. Typically, one alpha and one beta male occupied each display area, but males also formed multiple alliances (one alpha paired with multiple high-ranking subordinates) or were solitary, with no distinct alliances. Both alliances and solitary alphas attracted females for courtship displays. Alphas were generally older than their beta partners, but age did not absolutely predict status. Individual alpha males were involved in different alliance types in different years, showing that alliance variation is not the result of fixed differences in individual strategies. Instead, variation apparently results from changing opportunities for partnership formation and territory acquisition.

Occurrence and Evolution of Cooperative Breeding Among the Diurnal Raptors (Accipitridae and Falconidae)

Abstract Cooperative breeding, in which more than two individuals live in a group and raise offspring, usually in a single nest, is found in only 3% of avian species. On the basis of a review of the literature, we found reports of groups (usually trios) at nest sites in 42 species of diurnal raptors. At least one example of cooperative breeding was found in 29% of genera and 14% of species, distributed in both Accipitridae and Falconidae. Given the difficulty of obtaining behavioral observations necessary to detect cooperative breeding in most raptor species, combined with the large number of species that have been poorly studied, cooperative breeding in diurnal raptors may be more common than our data indicate. However, when data on the sex of the extra bird(s) or relationships among group members were available, patterns were quite varied. For 7 of 13 species, groups primarily contained multiple adult males, though three of those species also had groups formed from offspring that had delayed dispersal; three species had a low, but regular, occurrence of multiple females (females of groups laid eggs in the same nest); and the remaining three species were characterized by having extra birds that were yearlings or subadults. In over half of species, groups did not appear to be composed of related individuals, contrary to many cooperatively breeding passerine species where groups are primarily composed of offspring that have delayed dispersal. Our review suggests that the evolution of group living in many raptors may be independent of delayed dispersal, and that the factors important in explaining the evolution of that behavior depend upon the benefits of group living.

OCCURRENCE AND EVOLUTION OF COOPERATIVE BREEDING AMONG THE DIURNAL RAPTORS (ACCIPITRIDAE AND FALCONIDAE)

Abstract Cooperative breeding, in which more than two individuals live in a group and raise offspring, usually in a single nest, is found in only 3% of avian species. On the basis of a review of the literature, we found reports of groups (usually trios) at nest sites in 42 species of diurnal raptors. At least one example of cooperative breeding was found in 29% of genera and 14% of species, distributed in both Accipitridae and Falconidae. Given the difficulty of obtaining behavioral observations necessary to detect cooperative breeding in most raptor species, combined with the large number of species that have been poorly studied, cooperative breeding in diurnal raptors may be more common than our data indicate. However, when data on the sex of the extra bird(s) or relationships among group members were available, patterns were quite varied. For 7 of 13 species, groups primarily contained multiple adult males, though three of those species also had groups formed from offspring that had delayed dispersal; ...

Male Competition, Mating Success and Female Choice in a Seasonally Breeding Primate (Erythrocebus patas)

AbstractMammals with restricted breeding seasons often show brief but intense bouts of male competition for mates and male reproductive success has been attributed to male competitive abilities, with the most aggressively successful males able to control access to fertile females, or with females choosing to mate with such males. We studied male competition, mating behaviour and female mate selection in patas monkeys, a primate with a restricted breeding period. We observed two habituated patas groups in Laikipia District, Kenya, during Jun.‐Aug. 1983. During the study, one group had a single resident male while the other group had multiple adult males. Within the multimale group, experienced adult males were no more successful than the subadult male. The sole resident male had a significantly higher rate of fights won (p < 0.02) although he did not differ from the multimale group males in rate of aggression or initiation of fights. We found no significant differences in either mating success or female preference based on males' experience or residency. The rates at which males copulated with and were solicited by females were not significantly correlated. We found no evidence of stable dominance ranks among males in the multimale group and aggressive success was not significantly correlated with copulation rate for males in the multimale group. Subadult males were responsible for the majority of copulations observed during the final third of the breeding season. Our observations of this patas population showed a fluid number of males in groups, with the same groups able to shift rapidly from single to multimale structure. This fluidity may result from the large fluctuations in numbers of breeding‐age males and females observed over 4 yr of studying this population.