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Group structure predicts variation in proximity relationships between male–female and male–infant pairs of mountain gorillas (Gorilla beringei beringei)
Abstract
Relationships between conspecifics are influenced by both ecological factors and the social organization they live in. Systematic variation of both—consistent with predictions derived from socioecology models—is well documented, but there is considerable variation within species and populations that is poorly understood. The mountain gorilla (Gorilla beringei) is unusual because, despite possessing morphology associated with male contest competition (e.g., extreme sexual dimorphism), they are regularly observed in both single-male and multimale groups. Both male–female and male–infant bonds are strong because males provide protection against infanticide and/or predation. Risk of these threats varies with social structure, which may influence the strength of social relationships among group members (including females and offspring, if females with lower infant mortality risk are less protective of infants). Here, we investigate the relationship between group structure and the strength of proximity relationships between males and females, males and infants, and females and offspring. Data come from 10 social groups containing 1–7 adult males, monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center in Volcanoes National Park, Rwanda. After controlling for group size and infant age, association strength was similar for male–female pairs across group types with both dominant and nondominant males, but male–infant relationships were strongest in single-male groups where paternity certainty was high and animals had fewer social partners to choose from. The male:female and male:infant ratios better predicted both male–female and male–infant associations than the absolute number of males, females, or infants did. The fewer the number of males per female or infant, the more both pair types associated. Dominant males in groups containing fewer males had higher eigenvector centrality (a measure of importance in a social network) than dominant males in groups with more males. Results indicate that nondominant males are an important influence on relationships between dominant males and females/infants despite their peripheral social positions, and that relationships between males and infants must be considered an important foundation of gorilla social structure.
... The study of primate social structure considers how individual relationships, that is the content, quality and patterning of interactions between individuals, contribute to groupings as a whole [1]. From a basic perspective this field of study has provided insights into how broad group demographics such as group size [2,3], sex ratios [4] and kinship [5][6][7][8] benefits such as fitness outcomes [9][10][11][12] and stress mitigation [13][14][15] and resource availability [16][17][18] shape primate societies. This line of research has expanded to additionally encompass more applied perspectives. ...
... In singlemale mountain and western lowland gorilla groups, females spend more time associated with the silverback than with other females and maturing males [26,27], and in multi-male mountain gorilla groups, females tend to associate with the highest ranking male over lower ranking males [28]. Interestingly, despite the heavy emphasis on male-female relationships, maleimmature mountain gorilla dyads have stronger association patterns than male-female dyads, highlighting that immature gorillas are an integral component of gorilla social structure [4]. Preferential associations have been observed amongst females, however, these relationships do not appear to last longer than two years, suggesting females do not form strong long-term relationships with other adult females [29]. ...
... In support of GRACE's operation and mission, we implemented an ongoing behavior monitoring program focused on the association patterns amongst the individual gorillas. This methodology was selected because associations are regularly used to define social relationships of gorillas in nature [4,29,36,37] and could be readily implemented by the animal care team as part of their day-to-day routine. ...
The study of individual social relationships and group structure provides insights into a species’ natural history and can inform management decisions for animals living in human care. The Gorilla Rehabilitation and Conservation Education (GRACE) center provides permanent sanctuary for a group of 14 Grauer’s gorillas (Gorilla beringei graueri), a critically endangered and poorly studied subspecies of the genus gorilla, in the Democratic Republic of the Congo. We monitored the association patterns of the gorillas at GRACE over eight months and here describe their individual relationships and group structure via multiple social network statistics. The group was highly connected but associations between individuals were weak on average. Social network metrics describe that an adult female was the most gregarious and socially central individual within the group. In fact, adult females were the most gregarious and socially central on average. Group level association patterns were significantly correlated over the study period and across observation types, suggesting the group was socially stable during the eight month study period. The data collected in this study were done so by GRACE caregivers as part of their daily husbandry routine and provided important insights into this group’s behavior, ultimately informing on their care, welfare and future release considerations. The methodological approaches implemented here are easily scalable to any primate sanctuary or care facility seeking to use data to inform husbandry and management procedures. Lastly, our study is the first social network analysis to be conducted on Grauer’s gorillas and provides tentative insights into the behavior of this poorly studied subspecies. Though more research is needed to evaluate if the findings here are reflective of this subspecies’ natural history or the idiosyncrasies of the group.
... Groups of mountain gorillas consist of one or more silverbacks (males aged ≥12 yr or older), multiple adult females (aged ≥8 yr), and juvenile offspring (Harcourt 1979;Harcourt et al. 1976;Robbins 1995;Rosenbaum et al. 2016b). Group size and composition can be highly variable, ranging from 2 to 40+ adults (Caillaud et al. 2014). ...
... Dyadic bonds between group members are maintained through interactions including grooming, playing, and other affiliative behaviors, while agonistic behaviors function to reinforce dominance and settle foraging location disputes (Grueter et al. 2016;Rosenbaum et al. 2016a, b;Watts 1994a;Wright and Robbins 2014). The strongest social relationships exist between silverbacks and 1) adult females and 2) infants, while bonds between same-sex adults are weak (Rosenbaum et al. 2016b;Watts 1994b). The silverback-female relationships are likely formed in response to external threats, primarily extragroup male competitors (Watts 1989). ...
... The silverback-female relationships are likely formed in response to external threats, primarily extragroup male competitors (Watts 1989). A lower ratio of silverback males to females results in stronger social bonds between group members because there is less competition between females for proximity to silverback(s) (Rosenbaum et al. 2016b). Thus, group size and structure play a large role in the strength of relationships between mountain gorilla group members, and perhaps in the extent of collective action during intergroup interactions. ...
Group-living animals face a number of threats from extragroup conspecifics: from individuals seeking mating opportunities to rival groups attempting to access limited resources. The consequences of intergroup interactions can therefore include loss of mates, increased energy expenditure, and injury or death. There is increasing evidence that aggressive intergroup interactions can affect subsequent intragroup behavior, and that such post-conflict behavior may be directly related to the threats posed by different opponent groups (e.g., familiar vs. unfamiliar). However, empirical evidence for changes in intragroup behavior following intergroup conflict in social animals is limited. We compared the proximity and behavior of group members before and after 84 aggressive intergroup interactions involving 14 study groups of wild, habituated mountain gorillas (Gorilla beringei beringei) in Volcanoes National Park, Rwanda. Intergroup conflict affected subsequent intragroup behavior in several ways. We found that immediate movement away from the opponent following intergroup conflict was less likely between familiar groups compared to unfamiliar groups. However, both winning and losing groups spent twice as much time moving post-conflict, and losing groups spent less time resting. There was an increase in female intragroup affiliative interactions and a decrease in male intragroup agonistic interactions post-conflict. These results demonstrate that such intergroup contests can influence intragroup dynamics beyond the immediate period of interaction.
... There are potential alternative explanations for the differences we observed in females' behavior in single versus multi-male groups, although we believe protection against infanticide, plus high paternity certainty, is the most compelling. In multi-male groups, females generally face higher levels of competition for space near males [59,92]. If space near males is indeed a resource females compete over, higher-ranking females could potentially exclude lower-ranking females from accessing preferred males when they have new infants. ...
... Despite this the increase in proportion of point samples in close proximity to 'most preferred' males was negligible. Finally, increased competition in multi-male groups is not associated with weaker relationships between the dominant male and adult females [92], and even if it were this would not necessarily preclude changes in female behavior after infant births. Females could theoretically compensate for the additional competition by e.g. ...
Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multi-male groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females' social partner choice than paternity. Older infants (2-3 years) in multi-male groups mirrored their mothers' preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle.
... By increasing their association, two new mothers may be able to negate some of these costs and risks to enhance infant survival. While the infants are young and less mobile, mothers may associate for their infants' socialization and a rapid decline in this partnering after 1 year could reflect the infants' increased mobility and preference to socialize close to the silverback [76]. Thus, mothers' close association is no longer necessary. ...
Affiliative relationships are a hallmark of social relationships in gregarious mammals, but what drives variation of association patterns when kin are absent remains unknown. Gorillas, where females may disperse multiple times in their lives, provide an interesting counterpoint to female philopatric species to examine the factors influencing variation in association patterns. We examined demographic and social factors that may predict association patterns of female western (Gorilla gorilla gorilla; Loango, Gabon) and mountain gorillas (Gorilla beringei beringei; Bwindi, Uganda). We looked at dyadic and individual strength scores of social proximity (37 group-years). For individuals, high dominance rank increased association scores while newly emigrated females had lower scores than resident females. For dyads, higher mean dominance rank and both partners having a dependent infant increased association scores, whereas a partner being an immigrant decreased scores. Furthermore, time-matched analysis of birth and immigration events confirmed the temporal nature of these associations. Overall, female gorilla association patterns show flexibility in strength based on real-time contingencies, namely social and demographic traits. Association patterns in species with female secondary dispersal may be governed by homophily, like that of modern humans. Understanding female gorilla social structure can enhance our knowledge of the evolutionary origins of sociality.
... Third, we examined patterns of proximity among the silverback-mother-infant triads employing the prediction that the 5 mHWI values for mother-infant pairs would be the highest, and those of the silverback-infant pairs would be higher than those for silverback-mother pairs, as observed by Rosenbaum et al. (2016b). Our samples for this analysis included two pairs of "senior female-natal infant" and three pairs of "immigrant female-immigrant infant." ...
In primates living in one-male groups, the sole resident male is often an important social partner for group immatures. For such groups, however, replacement of the male and subsequent disruptions of their relationships are almost inevitable. Here, we described social relationships of immature wild western lowland gorillas within a habituated group, where two natal and eight immigrant immatures lived with the resident silverback. We recorded 5 m proximities among group members as an indicator of social closeness. We found that natal immatures spent more time within 5 m of the silverback than immigrant ones. The social closeness between the silverback and the younger immigrant immatures sharply increased after 1 year, but these values were still below those of the natal immatures. Regarding the development of independence from the mother, we found no significant difference between natal and immigrant immatures. The socially preferred nonmother mature for natal immatures was the silverback, whereas many immigrant immatures preferred a paternal adult sister who had previously co-resided with them in a previous group. Our results suggest that familiarity may be an important determinant of the social closeness between the silverback and immatures, but 1 year of co-residence might be too short to construct sufficient familiarity. The paternal sister may have played a pivotal role in the assimilation of immigrant immatures into the non-natal group. Nonetheless, it is not negligible that the silverback and immigrant immatures formed day-to-day close proximities. His tolerance toward co-residence with immigrant immatures can be considered a reproductive tactic.
Supplementary Information
The online version contains supplementary material available at 10.1007/s10329-024-01149-1.
... In light of the nature of data gathered on apes, these species provide particularly strong opportunities to explore hypotheses linking early life social experiences to later outcomes. For example, great ape data contain extensive direct information on who interacts with whom and how, allowing for (among other things) fine-grained analysis of individual-level positions in social networks (Rosenbaum et al., 2016;Feldblum et al., 2018;Morrison et al., 2020;Thompson González, Machanda et al., 2021). Social networks and social support-or lack thereof-are believed to be important contributors to health outcomes in humans, in part via their ability to encourage resilience to early life adversity (e.g. ...
Early life experiences have a significant influence on adult health and aging processes in humans. Despite widespread interest in the evolutionary roots of this phenomenon, very little research on this topic has been conducted in humans' closest living relatives, the great apes. The longitudinal data sets that are now available on wild and captive great ape populations hold great promise to clarify the nature, evolutionary function, and mechanisms underlying these connections in species which share key human life history characteristics. Here, we explain features of great ape life history and socioecologies that make them of particular interest for this topic, and those that may limit their utility as comparative models; outline the ways in which available data are complementary to and extend the kinds of data that are available for humans; and review what is currently known about the connections among early life experiences, social behavior, and adult physiology and biological fitness in our closest living relatives. We conclude by highlighting key next steps for this emerging area of research.
... An intervention to remove males that brought the ASR back to parity reduced female mortality. In mountain gorillas (Gorilla berengii), male-female relationships were weaker, as measured by spending less time in closer proximity, in groups with more males (Rosenbaum, Maldonado-Chaparro & Stoinski, 2016). In olive baboons (Papio anubis), a female-biased ASR caused by the sudden death of half the males from tuberculosis led to a more relaxed dominance hierarchy and an increase in male-female affiliation (Sapolsky & Share, 2004). ...
In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.
... The group spread of mountain gorillas is greater when feeding than resting, as expected to mitigate the first mechanism of scramble competition, but the effects of group size have not been reported (Fossey and Harcourt 1977;Grueter et al. 2016). Studies of individual spacing have mainly focused on social relationships within and among the age-sex classes (Harcourt 1979a, b;Watts 1992Watts , 1994bRosenbaum et al. 2016). Female mountain gorillas compete for proximity to the dominant male, who provides protection from Grueter et al. 2018). ...
Two mechanisms have been proposed to explain why scramble competition can increase the travel requirements of individuals within larger groups. Firstly, individuals in larger groups may be more likely to encounter food sites where other group members have already eaten, leading to greater asynchronous “individual” travel to find fresh sites. Secondly, when food sites are aggregated into patches, larger groups may need to visit more patches to obtain the same amount of food per capita, leading to greater synchronous “group” travel between patches. If the first mechanism can be mitigated by increasing group spread, then we expect the second mechanism to be more sensitive to group size. Here, we examine the individual travel and group travel of the Virunga mountain gorillas, along with potential implications for the two mechanisms of scramble competition. Asynchronous individual travel accounted for 67% of the total travel time, and the remainder arose from group travel. Group spread increased significantly for larger groups, but not enough to prevent an increase in individual travel. Contrary to expectations, group travel decreased with size among most groups, and we found only limited evidence of patch depletion that would cause the second mechanism of scramble competition. Collectively, our results illustrate how the influence of group size can differ for individual travel versus group travel, just as it differs among species for overall travel. Studies that distinguish between the two mechanisms of scramble competition may enhance our understanding of ecological constraints upon group size, including potential differences between frugivores and folivores.
Significance statement
Feeding competition provides insight into how group size can influence the foraging patterns of social animals, but two key mechanisms are not typically compared. Firstly, larger groups may visit more patches to access the same amount of food per capita (group travel). Secondly, their individuals may also need to move past more spots where another member has already eaten (individual travel). Contrary to expectations, we found that group travel decreased with size for most groups of mountain gorillas, which may reflect extra travel by smaller groups to avoid larger groups. Individual travel increased with size in most groups, even though gorillas in larger groups compensated by spreading out over a broader area. The two mechanisms revealed patterns that were not apparent in our previous study of overall travel. Our approach may help to explain potential differences between folivores and frugivores.
... While gorilla familial groups are mainly based on adult male-female bonds(Harcourt & 12 Stewart, 2007), relationships between the silverback and its offspring play a significant role in13 group structure. As already shown in different studies, the close bonds between the adult male14 and the immature males(Rosenbaum et al, 2016;Stewart, 2001;Yamagiwa, 1983) are best15 explained as paternal care (protection and tolerance of proximity) rather than a significant16 investment in their offspring (resting in contact, grooming, play) (Rosenbaum et al, 2011).17 The "positive" behaviours that intact immature males performed at preference proximity of 18 the silverback and the mother decreased significantly when they reached maturity. ...
... While gorilla familial groups are mainly based on adult male-female bonds (Harcourt and Stewart, 2007), relationships between the silverback and its offspring play a significant role in group structure. As already shown in different studies, the close bonds between the adult male and the immature males (Rosenbaum et al., 2016;Stewart, 2001;Yamagiwa, 1983) are best explained as paternal care (protection and tolerance of proximity) rather than a significant investment in their offspring (resting in contact, grooming, play) (Rosenbaum et al., 2011). The "positive" behaviours that intact immature males performed at preference proximity of the silverback and the mother decreased significantly when they reached maturity. ...
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... We do, however, wish to highlight that studies quantifying social networks for species of conservation concern represent an important advance in our understanding that behaviour is relevant in a conservation context (e.g. mountain gorillas, Gorilla beringei: Rosenbaum, Maldonado-Chaparro, & Stoinski, 2015). The use of biologgers may also be facilitated if species already require capture for other purposes, such as genetic sampling, relocation or tagging. ...
The increased popularity and accessibility of social network analysis has improved our ability to test hypotheses about complex animal social structures. To gain a deeper understanding of the use and application of animal social network analysis, we systematically surveyed the literature and extracted information on publication trends from articles using social network analysis. We synthesize trends in social network research over time and highlight variation in the use of different aspects of social network analysis. The use of social network analysis in empirical articles has increased over time. In the context of social network methods, we found that many studies did not use an association index to account for missing individuals or observations of individuals; that the number and type of social network metrics calculated in a given study varied substantially (median = 2); and that focal observation was by far the most common method used to generate social networks, although the use of biologging devices increased over time. We also observed that most species studied using social networks are mammals (55%) or birds (23%), and that the majority are species of least concern (59%; International Union for the Conservation of Nature, IUCN, www.iucn.org). Based on our findings, we highlight four key recommendations for future studies: (1) the use of association indices is almost always necessary; (2) the a priori selection of specific network metrics and associated hypotheses increases transparency; (3) combination of focal observation with biologging devices could improve our understanding of remotely sensed behaviours; and (4) because most studies rarely study species of conservation concern, it may be practical to generate networks for similar species or populations, which could help inform management decisions. We highlight emerging trends in social network research that may be valuable for distinct groups of social network researchers: students new to social network analysis, experienced behavioural ecologists interested in using social network analysis and advanced social network users interested in trends of social network research. Our findings also shed light on past research and provide guidance for future studies using social network analysis.
... These groups are either one-male or multi-male (Robbins, 2001;Stewart & Harcourt, 1987). The strongest social bonds within these groups are formed between females and the male(s) (but see also Rosenbaum, Maldonado-Chaparro, & Stoinski, 2016). Females have weaker relationships with other females, but some female dyads (particularly relatives) are characterized by friendly and tolerant relations (Harcourt, 1979a(Harcourt, , 1979bWatts, 1994Watts, , 2003. ...
Objectives
Infant handling describes cases in which youngsters are temporarily removed from the care of their mothers and “taken care of” (held, carried, etc.) by other conspecifics. Handlers may gain indirect fitness benefits from these actions and can practice mothering skills, thereby improving the odds of survival of their own infants. Great apes are notable for displaying little infant handling. Apart from anecdotal observations, no published data exist on infant handling in wild mountain gorillas. We tested two of the most pertinent explanations (“kin selection” and “learning to mother”) in a wild population of mountain gorillas in Rwanda. We predicted that (a) nulliparous females would exhibit infant handling (i.e., carrying) more than parous females and (b) maternal kin would exhibit more infant handling than nonkin.
Methods
We collated 8 years of data on infant carrying behavior collected in 13 groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center.
Results
Infant handling is an infrequent behavior (1,783 instances over 25,600 observation hours). A strong positive effect of relatedness and handler parity on the frequency of infant handling emerged.
Conclusions
While the nature of handler–infant interactions (affiliative, abusive, etc.) remains unstudied, they could constitute alloparental care and could therefore attenuate maternal energetic burden and ultimately allow increased birth rates. However, the rarity of this behavior makes it an unlikely contributor to mountain gorillas' relatively short interbirth intervals.
... Adult males are often tolerant of the close proximity of these infants, and show contact behaviors that may indicate paternal care (Rosenbaum et al. 2016a). This tolerance is an important aspect of group structure (Rosenbaum et al. 2016b). Differential investments by males to both related and unrelated juveniles may be related to the mother's age and reproductive history ). ...
Gorilla beringei Matschie, 1903 is a great ape commonly called the eastern gorilla. Highly sexually dimorphic, this diurnal knuckle-walking quadruped is 1 of 2 species of Gorilla, the largest living primates. It is endemic to northwest Rwanda and southwest Uganda as G. b. beringei, and to eastern Democratic Republic of the Congo as G. b. beringei and G. b. graueri. G. beringei is known to both highland and lowland montane forests and subalpine environments, though only G. b. beringei is called the “mountain gorilla.” Those inhabiting higher elevations are more folivorous than those at lower elevations. Groups are highly cohesive polygamous social units, varying in size and composition. G. b. beringei and G. b. graueri are both listed as “Critically Endangered” by the International Union for the Conservation of Nature and Natural Resources.
... In mountain gorillas, male-female associations were weaker in groups with more males [187], suggesting that association patterns are also sensitive to variation in ASR. A sudden change in ASR in a baboon group due to the death of half of the adult males from tuberculosis also led to a more relaxed dominance hierarchy and an increase in male-female affiliation [188]. ...
Theoretical models and empirical studies in various taxa have identified important links between variation in sex roles and the number of adult males and females (adult sex ratio (ASR)) in a population. In this review, I examine these relationships in non-human primates. Because most existing theoretical models of the evolution of sex roles focus on the evolutionary origins of sex-biased behaviour, they offer only a general scaffold for predicting variation in sex roles among and within species. I argue that studies examining sex role variation at these more specific levels need to take social organization into account to identify meaningful levels for the measurement of ASR and to account for the fact that ASR and sex roles mutually influence each other. Moreover, taxon-specific life-history traits can constrain sex role flexibility and impact the operational sex ratio (OSR) by specifying the minimum length of female time outs from reproduction. Using examples from the primate literature, I highlight practical problems in estimating ASR and OSR. I then argue that interspecific variation in the occurrence of indirect forms of paternal care might indeed be linked to variation in ASR. Some studies also indicate that female aggression and bonding, as well as components of inter-sexual relationships, are sensitive to variation in ASR. Thus, links between primate sex roles and sex ratios merit further study, and such studies could prompt the development of more specific theoretical models that make realistic assumptions about taxon-specific life history and social organization.
This article is part of the themed issue ‘Adult sex ratios and reproductive decisions: a critical re-examination of sex differences in human and animal societies’.
Low-density social networks can be common in animal societies, even among species generally considered to be highly social. Social network analysis is commonly used to analyse animal societal structure, but edge weight (strength of association between two individuals) estimation methods designed for dense networks can produce biased measures when applied to low-density networks. Frequentist methods suffer when data availability is low, because they contain an inherent flat prior that will accept any possible edge weight value, and contain no uncertainty in their output. Bayesian methods can accept alternative priors, so can provide more reliable edge weights that include a measure of uncertainty, but they can only reduce bias when sensible prior values are selected. Currently, neither accounts for zero-inflation, so they produce edge weight estimates biased towards stronger associations than the true social network, which can be seen through diagnostic plots of data quality against output estimate. We address this by adding zero-inflation to the model, and demonstrate the process using group-based data from a population of male African savannah elephants. We show that the Bayesian approach performs better than the frequentist to reduce the bias caused by these problems, though the Bayesian requires careful consideration of the priors. We recommend the use of a Bayesian framework, but with a conditional prior that allows the modelling of zero-inflation. This reflects the fact that edge weight derivation is a two-step process: i) probability of ever interacting, and ii) frequency of interaction for those who do. Additional conditional priors could be added where the biology requires it, for example in a society with strong community structure, such as female elephants in which kin structure would create additional levels of social clustering. Although this approach was inspired by reducing bias observed in sparse networks, it could have value for networks of all densities.
Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male–female relationships in social mammals, especially outside of the mating context. Here, we investigate the effects of genetic ancestry on male–female affiliative behaviour in a hybrid zone between the yellow baboon, Papio cynocephalus, and the anubis baboon, Papio anubis, in a population in which male–female social bonds are known predictors of life span. We place our analysis within the context of other social and demographic predictors of affiliative behaviour in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behaviour we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with a subtle, but significantly higher, probability of opposite-sex affiliative behaviour, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behaviour as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behaviour partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Furthermore, they suggest that affiliative behaviour may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively.
Opposite-sex social relationships are important predictors of fitness in many animals, including several group-living mammals. Consequently, understanding sources of variance in the tendency to form opposite-sex relationships is important for understanding social evolution. Genetic contributions are of particular interest due to their importance in long-term evolutionary change, but little is known about genetic effects on male-female relationships in social mammals, especially outside of the mating context. Here, we investigate the effects of genetic ancestry on male-female affiliative behavior in a hybrid zone between the yellow baboon ( Papio cynocephalus ) and the anubis baboon ( P. anubis ), in a population in which male-female social bonds are known predictors of lifespan. We place our analysis within the context of other social and demographic predictors of affiliative behavior in baboons. Genetic ancestry was the most consistent predictor of opposite-sex affiliative behavior we observed, with the exception of strong effects of dominance rank. Our results show that increased anubis genetic ancestry is associated with subtly, but significantly higher rates of opposite-sex affiliative behavior, in both males and females. Additionally, pairs of anubis-like males and anubis-like females were the most likely to socially affiliate, resulting in moderate assortativity in grooming and proximity behavior as a function of genetic ancestry. Our findings indicate that opposite-sex affiliative behavior partially diverged during baboon evolution to differentiate yellow and anubis baboons, despite overall similarities in their social structures and mating systems. Further, they suggest that affiliative behavior may simultaneously promote and constrain baboon admixture, through additive and assortative effects of ancestry, respectively.
HIGHLIGHTS
Opposite-sex social relationships can have important fitness consequences.
In hybrid baboons, genetic ancestry predicted male-female affiliative behavior.
Both an individual’s genetic ancestry and that of its social partner mattered.
Male-female affiliation was assortative with respect to genetic ancestry.
Dominance rank and group demography also influenced male-female social affiliation.
Written by leading theorists and empirical researchers, this book presents new ways of addressing the old question: Why did religion first emerge and then continue to evolve in all human societies? The authors of the book-each with a different background across the social sciences and humanities-assimilate conceptual leads and empirical findings from anthropology, evolutionary biology, evolutionary sociology, neurology, primate behavioral studies, explanations of human interaction and group dynamics, and a wide range of religious scholarship to construct a deeper and more powerful explanation of the origins and subsequent evolutionary development of religions than can currently be found in what is now vast literature. While explaining religion has been a central question in many disciplines for a long time, this book draws upon a much wider array of literature to develop a robust and cross-disciplinary analysis of religion. The book remains true to its subtitle by emphasizing an array of both biological and sociocultural forms of selection dynamics that are fundamental to explaining religion as a universal institution in human societies. In addition to Darwinian selection, which can explain the biology and neurology of religion, the book outlines a set of four additional types of sociocultural natural selection that can fill out the explanation of why religion first emerged as an institutional system in human societies, and why it has continued to evolve over the last 300,000 years of societal evolution. These sociocultural forms of natural selection are labeled by the names of the early sociologists who first emphasized them, and they can be seen as a necessary supplement to the type of natural selection theorized by Charles Darwin. Explanations of religion that remain in the shadow cast by Darwin's great insights will, it is argued, remain narrow and incomplete when explaining a robust sociocultural phenomenon like religion. © 2018 Jonathan H. Turner, Alexandra Maryanski, Anders Klostergaard Petersen, and Armin W. Geertz. All right reserved.
Association indices have been a mainstay of social behaviour analysis for decades. However, researchers have long recognized that these indices can be biased under certain conditions. In this paper, I develop a process map of the steps necessary to transform social behaviour into estimates of association rates. This helps to distinguish the subject population's behaviour from the researcher's data collection protocol. By doing this, we can isolate the sources of bias. I also show that bias in association indices is often a function of the true association rate. This means that while bias does not affect the ordering of associations, it can impact analysis in unpredictable ways. Performing network analysis with biased association indices can lead researchers to arrive at different conclusions than if they had used unbiased estimators. To simplify the mathematical task of deriving unbiased estimators, I introduce three properties of maximum likelihood estimators that allow one to treat association data as output from a multinomial distribution, then use the functional invariance property of maximum likelihood estimators to solve for estimators. I apply these properties to a selection of common data collection protocols to show that there is no single association index that is appropriate for all cases. Instead, each of the commonly used indices is unbiased under appropriate conditions. Furthermore, when it is possible that some of the individuals are not identified, I introduce some new unbiased estimators. I close with a discussion of nontraditional techniques of collecting data that provide an opportunity to increase the number of outputs from the data collection process. These techniques may ultimately make it possible to specify association behaviour more carefully by allowing for more parameters in the data generation process.
As in other highly sexually dimorphic, group-living animals, reproduction in gorillas has been largely viewed as the outcome of competition among males. However, females may exert choice via dispersal decisions or choice of partner in multimale groups, and males may also mate selectively. Here, we examine the paternity of 79 wild mountain gorilla offspring born into four groups characterized by stable dominance hierarchies and the presence of mature offspring of the dominant male. We found that on average the dominant male sires the majority (72 %) of the offspring in stable multimale groups and subordinate males also produce offspring, particularly when dominant males become older or the number of competing males increases. Although expected to disperse to avoid inbreeding, only half of the maturing daughters of dominant males left the group in which their father maintained dominance. However, in all five cases of reproduction by a resident daughter of a dominant male, a subordinate male was the sire of the offspring. As females commonly initiate and end copulations, and dominant males may prefer mating with fully mature females, both male and female mate preferences in addition to male competition apparently play a role in reproductive patterns in multimale groups, emphasizing the complexity of social dynamics in one of our closest living relatives.
Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2-3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.
Socio-ecological models aim to predict the variation in social systems based on a limited number of ecological parameters. Since the 1960s, the original model has taken two paths: one relating to grouping patterns and mating systems and one relating to grouping patterns and female social structure. Here, we review the basic ideas specifically with regard to non-human primates, present new results and point to open questions. While most primates live in permanent groups and exhibit female defence polygyny, recent studies indicate more flexibility with cooperative male resource defence occurring repeatedly in all radiations. In contrast to other animals, the potential link between ecology and these mating systems remains, however, largely unexplored. The model of the ecology of female social structure has often been deemed successful, but has recently been criticized. We show that the predicted association of agonistic rates and despotism (directional consistency of relationships) was not supported in a comparative test. The overall variation in despotism is probably due to phylogenetic grade shifts. At the same time, it varies within clades more or less in the direction predicted by the model. This suggests that the model's utility may lie in predicting social variation within but not across clades.
This paper introduces a Theme Issue presenting the latest developments in research on the interplay between flexibility and constraint in social behaviour, using comparative datasets, long-term field studies and experimental data from both field and laboratory studies of mammals. We first explain our focus on mammals and outline the main components of their social systems, focusing on variation within- and among-species in numerous aspects of social organization, mating system and social structure. We then review the current state of primarily ultimate explanations of this diversity in social behaviour. We approach the question of how and why the balance between behavioural flexibility and continuity is achieved by discussing the genetic, developmental, ecological and social constraints on hypothetically unlimited behavioural flexibility. We introduce the other contributions to this Theme Issue against this background and conclude that constraints are often crucial to the evolution and expression of behavioural flexibility. In exploring these issues, the enduring relevance of Tinbergen's seminal paper 'On aims and methods in ethology', with its advocacy of an integrative, four-pronged approach to studying behaviour becomes apparent: an exceptionally fitting tribute on the 50th anniversary of its publication.
For the past three decades the mountain gorillas of Karisoke Research Center have been the subject of many studies focusing on their behaviour and ecology. Long-term observations on known individuals, from birth to death, and data on social behaviour within and between groups have led to an understanding of many aspects of gorilla social structure. The findings have made significant contributions to models of comparative primate behavioural ecology. Mountain gorillas have also been the focus of intense conservation efforts, which have become a model for conservation programs elsewhere. While most research has focused on mountain gorillas, data on the other two recognised subspecies have increased over the past twenty years. This book highlights and summarises some of the behavioural, ecological and conservation work on mountain gorillas, and makes comparisons with findings from other study sites. It represents the most up-to-date and diverse collection of information available on this endangered ape.
For the past three decades the mountain gorillas of Karisoke Research Center have been the subject of many studies focusing on their behaviour and ecology. Long-term observations on known individuals, from birth to death, and data on social behaviour within and between groups have led to an understanding of many aspects of gorilla social structure. The findings have made significant contributions to models of comparative primate behavioural ecology. Mountain gorillas have also been the focus of intense conservation efforts, which have become a model for conservation programs elsewhere. While most research has focused on mountain gorillas, data on the other two recognised subspecies have increased over the past twenty years. This book highlights and summarises some of the behavioural, ecological and conservation work on mountain gorillas, and makes comparisons with findings from other study sites. It represents the most up-to-date and diverse collection of information available on this endangered ape.
For the past three decades the mountain gorillas of Karisoke Research Center have been the subject of many studies focusing on their behaviour and ecology. Long-term observations on known individuals, from birth to death, and data on social behaviour within and between groups have led to an understanding of many aspects of gorilla social structure. The findings have made significant contributions to models of comparative primate behavioural ecology. Mountain gorillas have also been the focus of intense conservation efforts, which have become a model for conservation programs elsewhere. While most research has focused on mountain gorillas, data on the other two recognised subspecies have increased over the past twenty years. This book highlights and summarises some of the behavioural, ecological and conservation work on mountain gorillas, and makes comparisons with findings from other study sites. It represents the most up-to-date and diverse collection of information available on this endangered ape.
A detailed account of more than a year's close study of the African gorilla. It "describes, tabulates, analyzes, and evaluates every aspect of a gorilla's life: its habits of eating, nesting, mating, playing; its methods of communication; and its expressions of emotion, such as the chest-beating display. There are sections on population dynamics, including mortality factors, on group dynamics, and on the gorilla's response to weather, to other animals, and to man." (PsycINFO Database Record (c) 2012 APA, all rights reserved)
In order to explain the variation in primate social systems, socio-ecology has focussed on the role of ecological factors to explain female associations and relationships and on the spatio-temporal distribution of mating opportunities to explain male associations and relationships. While this approach has been quite successful, it ignores male-female associations and relationships and ignores the possibility that male behaviour modifies other aspects of the social system. In this paper, the ecological approach is complemented by consideration of a social factor found to limit fitness, namely infanticide by males. Infanticide risk is proposed to have selected for male-female associations and relationships, and to have modified female-female relationships in some cases. It is also hypothesized to have selected for the unusual male bonding by species such as chimpanzees. Finally, its possible impact on between-group relations is examined. The findings suggest that infanticide is of equal importance to ecological factors, with which it may interact in sometimes complex ways, in shaping primate social systems.
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 male–immature relationships in wild mountain gorillas. Mountain gorillas provide an interesting context for assessing paternal kin discrimination because (1) male–immature 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 male–immature relationship strength. There was little evidence that paternity or age were related to relationship patterns. Male–immature dyads were closer social partners in 2011–12 when groups were smaller and reproductive skew lower, than comparable dyads in 2003–04 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 male–immature 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.
We offer suggestions to avoid misuse of information-theoretic methods in wildlife laboratory and field studies. Our suggestions relate to basic science issues and the need to ask deeper questions (4 problems are noted), errors in the way that analytical methods are used (7 problems), and outright mistakes seen commonly in the published literature (5 problems). We assume that readers are familiar with the information-theoretic approaches and provide several examples of misuse. Any method can be misused-our purpose here is to suggest constructive ways to avoid misuse.
We give suggestions for the presentation of research results from frequentist, information-theoretic, and Bayesian analysis paradigms, followed by several general suggestions. The information-theoretic and Bayesian methods offer alternative approaches to data analysis and inference compared to traditionally used methods. Guidance is lacking on the presentation of results under these alternative procedures and on nontesting aspects of classical frequentist methods of statistical analysis. Null hypothesis testing has come under intense criticism. We recommend less reporting of the results of statistical tests of null hypotheses in cases where the null is surely false anyway, or where the null hypothesis is of little interest to science or management.
Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species.
Since the 1980s, the Virunga mountain gorilla population has almost doubled, now reaching 480 individuals living in a 430-km(2) protected area. Analysis of the gorillas' ranging patterns can provide critical information on the extent and possible effects of competition for food and space. We analyzed 12 years of daily ranging data and inter-group encounter data collected on 11 gorilla groups monitored by the Karisoke Research Center in Rwanda. During that period, the study population increased in size by almost 50% and the number of groups tripled. Groups had small yearly home ranges compared to other known gorilla populations, with an average 90% kernel density estimate of 8.07 km(2) and large between-group variations (3.17-23.59 km(2) ). Most groups had consistent home range location over the course of the study but for some, we observed gradual range shifts of up to 4 km. Neighboring groups displayed high home range overlap, which increased dramatically after the formation of new groups. On average, each group used only 28.6% of its 90% kernel home range exclusively, and in some areas up to six different groups had overlapping home ranges with little or no exclusive areas. We found a significant intra-group positive relationship between the number of weaned individuals in a group and the home range size, but the fitted models only explained 17.5% and 13.7% of the variance in 50% and 90% kernel home range size estimates, respectively. This suggests that despite the increase in size, the study population is not yet experiencing marked effects of feeding competition. However, the increase in home range overlap resulting from the formation of new groups led to a sixfold increase in the frequency of inter-group encounters, which exposes the population to elevated risks of fight-related injuries and infanticide. Am. J. Primatol. © 2014 Wiley Periodicals, Inc.
Monitoring changes in the population dynamics of endangered species is crucial to effective conservation strategies. The mountain gorilla population of the Virunga Massif has been the subject of intensive conservation efforts, research and several censuses over the last 40 years, but the region has also been affected by political instability and war. Here we present results from the 2010 census, which was the first to utilize genetic analyses of fecal samples for the entire population. The genetic analyses improved the accuracy of the population estimate by identifying several instances in which gorillas otherwise would have been undercounted or double-counted. The population was estimated to be 480 individuals; including 349 individuals found in 24 groups that were habituated for research and tourism, 101 individuals found in 12 unhabituated groups, fourteen solitary males, and a correction factor of sixteen for undetected infants. The population has increased by 26% since 2003 (an annual rate of 3.7%) and it has almost doubled since 1981. Nearly all of the increase can be attributed to a relatively higher growth rate in the habituated groups from 2003 to 2010, and in all five of the previous intervals between consecutive censuses. Nonetheless, it would be imprudent to habituate additional groups due to the concomitant risks of disease transmission from humans, behavioral disturbance and potential vulnerability to poaching. The results show that it is possible for conservation efforts to succeed even under difficult conditions, while highlighting the continuing challenges of managing a wild population of both habituated and unhabituated gorillas.
We examined demographic and behavioural influences on the dispersal decisions of 31 male mountain gorillas living in mixed-sex groups. Approximately half (45%) of silverback males dispersed from the groups in which they matured. Mean dispersal age corresponded with the age of physical maturity. For two-thirds (64%) of males, dispersal was a one time decision. The remaining individuals made repeated visits to their natal groups before permanently dispersing. Of dispersing males, 43% left with females. The remaining individuals dispersed alone, despite the presence of similar-aged male dispersal partners in their group. Dispersal decisions appeared voluntary; there was no evidence of increased aggression by the dominant silverback or peripheralization in the months prior to dispersal. Instead, dispersal decisions were influenced by limited opportunities to copulate within the group and the absence of a male's mother. Dispersing did not provide increased access to females, at least in the short term; only three dispersing males were observed to form groups whereas the remaining eight for whom data were available remained solitary (range 1–112 months) at the end of the study. The question remains why males choose to disperse rather than remain philopatric. Inbreeding avoidance seems unlikely, as all groups contained unrelated females. It may be that dispersal decisions are the result of several factors acting in combination, and thus dispersal is a more appropriate option for some males. Alternatively, dispersal decisions may actually be disadvantageous and reflect an incomplete adaptation to the ecological extremes of the Virunga region.
Social relationships between adult males and females in two groups of wild mountain gorilla are described. Each group contained about five, largely unrelated sub-adult and adult females, a peripheral near-adult male, and one fully mature male. Females were clearly attracted to the dominant male, and those with young offspring spent the most time near him. Also, when a female came into oestrus her time near the dominant male increased temporarily. Not all females engaged in grooming with this male, and those that did were judged to have the less stable, i.e. less potentially long-lasting, relationships with him. The relevance of affinitive behaviour to acquisition of benefits and to establishment and maintenance of relationships, plus the influence of competition on maintenance of relationships are discussed.
Literature data on 25 primate species were examined for correlations between measures of ejaculate quality and testes size and body size, respectively. Ejaculate volume and sperm concentration were positively correlated with body size in an interspecific analysis. In contrast, number of sperm per ejaculate, sperm motility, and number of motile sperm per ejaculate were not significantly correlated with body size. Data on interspecific variation in ejaculate quality showed that primate species with relatively large testes also produced ejaculates with relatively large volumes, high sperm counts, high sperm motility, and more motile sperm. Sperm motility and the number of sperm contributed independently to the number of motile sperm. Testes size, after controlling for the effect of body size, was related to breeding system in primates; species in which more than one male copulated with each oestrous female had larger testes than those with single-male breeding systems. Primate species with multi-male breeding systems produced ejaculates with relatively higher sperm motility and with relatively more motile sperm than did primates with single-male systems.
There are 2 main competing theories on the evolution of group living in diurnal non-human primates. 1) Predation avoidance favours group living; there are only disadvantages to feeding in a group and feeding competition increases with group size. 2) There is a feeding advantage to group living deriving from communal defence of high-quality food patches; predation is not important. A critical test is proposed: the theories differ in the predicted relationship between a female's birth rate and the size of the group in which she lives. An additional test is concerned with the predicted relationship between population density relative to food availability and average group size. Finally, a critical test is proposed of the hypothesis that increasing group size should lead to reduced predation risk by comparing demographic patterns between areas where predators are still present and where they have disappeared. In all 3 tests, results provide strong support for the predation-feeding competition theory and are clearly unfavourable for the theory postulating feeding advantages to group living. Such feeding advantages may, however, gain prominence under some conditions.-from Author
In multimale groups where females mate promiscuously, male-infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father's presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant's mother. Hence, infant care might provide fitness gain for males. Here, we investigate male-infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate-guarding. We combined behavioural data with genetic paternity analyses of one cohort of the semi-free-ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0-4 years) of focal subjects. Our results revealed that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male-infant interactions were affiliative, indicating the rareness of male-infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than nonsires with unrelated infants. This preference was independent of mother's proximity and emphasized during early infancy. Male-infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall, our results suggest that male-infant affiliation is also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low-cost paternal care.
The socioecological model is to date the best evolutionary model to explain variation in primate behaviour. Some species or populations, however, deviate from the predictions. These deviations may be due to a disequilibrium between evolutionary causes and behavioural adaptations, caused by recent human changes of the environment. The relationship between human habitat alteration and primate social behaviour is reviewed and investigated for langurs. Provisioning affects the spatial distribution of food. In these areas, but also in areas with natural monopolizable food sources, female dominance relationships are linear, but not nepotistic. This does not fit into the evolutionary model. Provisioning also affects the temporal distribution of food. This reduces the seasonality of mating, increases female monopolizability and gives rise to more one-male groups than in undisturbed areas. A human reduction of the number of predators leads to fewer males per group. It also results in female philopatry. Infanticide risk was higher in disturbed than in undisturbed areas. This was not caused by the lower proportion of one-male groups in disturbed areas, but by the lack of female dispersal. Thus, female behaviour was affected by human habitat disturbance in a way that does not fit the socioecological model. However, the extension of habitat disturbance does not explain all results. We could say that the model is refuted. Phylogenetic constraints, however, do explain the behaviour of despotic Hanuman langurs. Such phylogenetic constraints complement the socioecological model. To understand the evolutionary history of a current set of features, these two approaches should be studied simultaneously.
The current study examined skew in reproductive behaviour in male mountain gorillas under previously unstudied demographic conditions of large numbers of males. Subjects included 27 males eight to 30 years of age living in three groups in Parc National des Volcans (Rwanda) between June 2003 and January 2007. Rank was a significant predictor of copulations with both multiparous and nulliparous females, although copulations were more evenly distributed between the three top ranking males than previously reported. Copulations by non-alpha males were unaffected by the level of monopolization potential in the group and relatedness to the alpha silverback. Dispersing males copulated with cycling females prior to their dispersal significantly less than philopatric individuals. As compared to previous studies, we found decreased behavioural reproductive monopolization by the alpha silverback. Additionally, whereas previous studies suggested that patterns of reproductive skew may be best explained by limited control models, our results suggest that concession models should be reconsidered. However, paternity data are needed to determine the relationship between the observed behavioural patterns and changes in reproductive success.
Networks of social relations can be represented by graphs and socio- or adjacency-matrices and their structure can be analyzed using different concepts, one of them called centrality. We will provide a new formalization of a “node-centrality” which leads to some properties a measure of centrality has to satisfy. These properties allow to test given measures, for example measures based on degree, closeness, betweenness or Bonacich’s eigenvector-centrality. It turns out that it depends on normalization whether eigenvector-centrality does satisfy the expected properties or not.
Attempts to explain differences in the size and structure of primate groups have argued that they are a consequence of variation in the intensity of feeding competition caused by contrasts in food distribution. However, although feeding competition can limit the size of female groups, many other factors affect the costs and the benefits of sociality to females and contribute to differences in group size. Moreover, interspecific differences in social relationships between females, in female philopatry, and in kinship between group members appear to be more closely associated with variation in life-history parameters, reproductive strategies, and phylogeny than with contrasts in food distribution or feeding competition. The mismatch between predictions of socioecological theory and observed variation in primate social behavior has led to protracted arguments about the future of primate socioecology. We argue that future attempts to understand the diversity of primate societies need to be based on an approach that explores separate explanations for different components of social organization, combines ecological and phylogenetic information, and integrates research on primates with similar studies of other groups of mammals.
The mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes Range of Rwanda, Uganda, and the Democratic Republic of Congo are one of the most endangered ape populations in the world. Following a dramatic decline during the 1960s, and relative stability in the 1970s, the population steadily increased during the 1980s. Due to political instability and war, a complete census had not been conducted since 1989. Here we compare the results of a complete census using the ‘sweep method’ conducted in 2003 with those from a monitoring program, to estimate the size and distribution of the gorilla population. A total of 360 gorillas were counted from census measurements and known habituated groups. Based on quantitative assessments of the census accuracy, we calculated that an additional 20 gorillas were not counted, leading to an estimated population of 380 individuals, and a 1.15% annual growth rate since 1989. The Ranger Based Monitoring programme yielded similar results. The encouraging results must be viewed with caution, however, because the growth was concentrated almost entirely in one section of the Virungas. Additionally, the distribution of gorilla groups was negatively correlated with the frequency of human disturbances, which highlights the need to continue strengthening conservation efforts.
To visualize long-term social relationships among 12 gorillas in a captive breeding group at the San Diego Wild Animal Park, San Diego, CA, the multidimensional scaling (MDS) procedure was applied to proximity (within 5 m) values collected in five different periods over 2.5 years. The resulting two-dimensional representations clearly show that in samples taken during this 2.5-year period, the silverback male was surrounded by five adult females, while three infant or young juvenile females, gathered in a body, remained between the silverback male and adult females. Some adult females maintained proximity to the silverback male more frequently than other adult females throughout the five periods. Unlike mountain gorillas in the wild, females with dependent offspring did not tend to stay near the silverback male more frequently than other females, and related females did not tend to spend more time near each other than non-related females. Three older juvenile or young adult males were plotted the furthest from the silverback male, with gradual changes with increasing age. The usefulness of the MDS procedure, which can be used to visualize easily and clearly the social relationships among individuals, is discussed from the viewpoint of the management of breeding groups of captive gorillas. Zoo Biol 20:197–209, 2001. © 2001 Wiley-Liss, Inc.
A new measure of sexual dimorphism in tooth size (Relative Male Tooth Size) is estimated for a sample of 39 primate species and is used to test predictions concerning the adaptive significance of sexual dimorphism in primate tooth size. It is concluded that both sexual selection and predator defence are important selective forces producing marked sexual dimorphism in the teeth used for fighting.
Female transfer is common in mountain gorillas, but most adult females reside with female relatives for at least some of their lives. In four mountain gorilla social groups, co-resident relatives had higher rates of affiliative interaction and lower rates of aggressive interaction, and were more tolerant of each other, than non-relatives. These differences were greater for maternal than for paternal relatives. Non-relatives typically had few affiliative interactions, but some (mostly but not entirely long-term co-residents) had friendly relationships. Females showed reciprocity in affiliative behavior. Long-term residents in two groups maintained less tolerant relationships with more recent immigrants than with each other and than did most pairs of immigrants. The effects of relatedness and residence status on relationships may sometimes be complementary because both factors can lead to similar reproductive interests. A potential exists for some resemblance between female-female social relationships in mountain gorillas and those in female-bonded primate species. However, even female relatives usually spend little time interacting socially with each other, and the benefits of relationships with males outweigh those of relationships with other females. © 1994 Wiley-Liss, Inc.
“Squirrel-monkeys occur in a considerable number of slightly different forms, but all are built upon a similar body plan and have a basic color scheme. One of the larger races—from inner Perú—is also the most colorful and one of the brightest colored of all mammals. It may be taken as a point of departure. The top of the head and the upper and outer parts of the body and the upper side of the basal half of the tail are a vivid green, with a pepper and salt effect of yellow and gray. The face is pure white except for black spectacles, muzzle and chin; the throat, chest, underside, insides of limbs, and the underside of the basal half of the tail are brilliant daffodil yellow. The terminal half of the tail is jet black and rather bushy. The flesh of the hands is pale pink. Other races vary in the intensity of the green and yellow, so that some may be olive brown above and white below, and in the amount and arrangement of the black areas on the face and the tip of the tail. Some have almost naked ears, others have these organs clothed in short fur, and still others bear thereupon long tufts or fringes. All these variations seem to blend into the other geographically . . . some of these pure color variations may constitute valid regional subspecies or even species. . . .”I. T. Sanderson1 (p. 77).
Adult males are important social partners for all females in mountain gorilla social groups, but male-female relationships can vary in association with variation in female residence status, male age and mating status, and relatedness. Such variation occurred in a large group observed over a 3-year period. All females associated and interacted affiliatively relatively often with a young silverback with whom all mated. Long-term resident females also did so with an old, non-breeding male to whom most were related, but recent immigrants spent little time near him and had few non-aggressive interactions with him. The old male made agonistic interventions to support relatives; interventions in female conflicts by the younger male tended to ameliorate competitive differentials that immigrants faced and may have helped him to retain them as mates. Males aggression toward females was common, most probably served as a mating tactic, and did not involve resource competition. Extensive grooming by an adolescent male suggests that males may also use affiliative behavior to develop mating relationships. Females may have competed for proximity with and social access to the younger silverback; competitive success could influence how well females and their offspring are protected by silver-backs, but the extent of such competition was not clear. Large group size may have heightened differentiation of male-female relationships and competition among females, but comparative data from smaller groups generally corroborate the findings from the large group. © 1992 Wiley-Liss, Inc.
2In an influential paper, Freeman (1979) identified three aspects of centrality: betweenness, nearness, and degree. Perhaps because they are designed to apply to networks in which relations are binary valued (they exist or they do not), these types of centrality have not been used in interlocking directorate research, which has almost exclusively used formula (2) below to compute centrality. Conceptually, this measure, of which c(ot, 3) is a generalization, is closest to being a nearness measure when 3 is positive. In any case, there is no discrepancy between the measures for the four networks whose analysis forms the heart of this paper. The rank orderings by the
Variation in male dispersal and behavior patterns are components of intraspecific differences in social systems. A comparison of male behavior in different social settings can be useful for determining which behavioral mechanisms contribute to variability in social systems. Two heterosexual multimale groups and one all-male group of mountain gorillas (Gorilla gorilla beringei) were observed for over 1100 h at the Karisoke Research Centre, Rwanda. Data on proximity patterns, dominance relationships, aggression, agonistic interventions, affiliation, and homosexual behavior were compared among the males in these groups to examine the influence of female presence, sex ratio, group size, and kinship on male—male interactions. Males in the all-male group stayed closer together, affiliated more, exhibited more homosexual behavior, and were more aggressive toward each other than males in heterosexual groups. However, the males in heterosexual groups showed more wounding and more consistent dominance relationships. Kinship did not influence male-male relationships in the all-male group. The males in the heterosexual groups rarely interacted with one another; they may actively avoid close proximity to reduce aggression. Results suggest that the variable social system of mountain gorillas may be more strongly influenced by demographic factors, male-female social relationships, and male-male competition for mates than by any benefits of male-male relationships.
In gorillas (Gorilla gorilla beringei), male reproductive competition is manifested during inter-group encounters through displays and contact aggression with opposing males and through attempts to control the movement of females between groups. This paper documents the effect of within-group male reproductive competition on male-female relationships. In one-male groups, females are known to take the initiative in the maintenance of their relationships with males. In two-male units, because males face within-group reproductive competition, one can expect a reversed pattern of responsibility for proximity maintenance. Three measures were used to assess responsibility for proximity maintenance: Hinde's index of proximity: the proportion of ‘follows’ and ‘neighing’. The proportion of follows is the number of follows in relation to the number of departures within each dyad. Neighing is a vocalization emitted by males towards departing females. It is used as a measure of males' motivation to negotiate proximity with females. The data come from focal observations on the silverbacks and ad libitum data collected over 8 months (380 h in 1989) at the Karisoke Research Center. Results indicate that within-group reproductive competition in itself does not lead to a reversed pattern of responsibility in proximity maintenance between males and females, but that the stability of the dominance relationship between the males, and the quality of the relationship between males and females, might have a role to play as well. Results on the neighing vocalization suggest that males are eager to negotiate proximity with cycling females rather than with lactating or pregnant females.