Social Mammal Species Research Articles

Mechanisms of equality and inequality in mammalian societies.

The extent of (in)equality is highly diverse across species of social mammals, but we have a poor understanding of the factors that produce or inhibit equitable social organizations. Here, we adopt a comparative evolutionary perspective to test whether the evolution of social dominance hierarchies, a measure of social inequality in animals, exhibits phylogenetic conservatism and whether interspecific variation in these traits can be explained by sex, age or captivity. We find that hierarchy steepness and directional consistency evolve rapidly without any apparent constraint from evolutionary history. Given this extraordinary variability, we next consider multiple factors that have evolved to mitigate social inequality. Social networks, coalitionary support and knowledge transfer advantage to privilege some individuals over others. Nutritional access and prenatal stressors can impact the development of offspring, generating health disparities with intergenerational consequences. Intergenerational transfer of material resources (e.g. stone tools, food stashes, territories) advantage those who receive. Nonetheless, many of the same social species that experience unequal access to food (survival) and mates (reproduction) engage in levelling mechanisms such as food sharing, adoption, revolutionary coalitions, forgiveness and inequity aversion. Taken together, mammals rely upon a suite of mechanisms of (in)equality to balance the costs and benefits of group living. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Adolescence and the development of social behaviour in giraffes

All mammals experience different life stages as they develop, each of which is characterised by particular physical and behavioural changes. Despite the emergence of sophisticated behaviour analysis techniques, the ways in which social behaviour varies by life stage, and how this is influenced by an individual’s sex, is relatively understudied in most social mammals other than primates and elephants. Understanding the social requirements of mammals should be a central and critical component to their conservation, captive management and welfare. Here, we apply social network analysis techniques to understand how social behaviour differs with life stage in the giraffe, a gregarious fission–fusion mammal. We studied two wild populations of giraffes in Kenya and found that adolescents have significantly stronger associations with adolescents of their own sex first and foremost, then adults of their own sex. Other associations were significantly lower than would be expected, or non-significant. Our results suggest that adolescence in both male and female giraffes shares similar features to adolescence in other social mammal species. We discuss how the application of such knowledge might improve the management and welfare of captive giraffes.

Social integration predicts survival in female white-faced capuchin monkeys.

Across multiple species of social mammals, a growing number of studies have found that individual sociality is associated with survival. In long-lived species, like primates, lifespan is one of the main components of fitness. We used 18 years of data from the Lomas Barbudal Monkey Project to quantify social integration in 11 capuchin (Cebus capucinus) groups and tested whether female survivorship was associated with females’ tendencies to interact with three types of partners: (1) all group members, (2) adult females, and (3) adult males. We found strong evidence that females who engaged more with other females in affiliative interactions and foraged in close proximity experienced increased survivorship. We found some weak evidence that females might also benefit from engaging in more support in agonistic contexts with other females. These benefits were evident in models that account for the females’ rank and group size. Female interactions with all group members also increased survival, but the estimates of the effects were more uncertain. In interactions with adult males, only females who provided more grooming to males survived longer. The results presented here suggest that social integration may result in survival-related benefits. Females might enjoy these benefits through exchanging grooming for other currencies, such as coalitionary support or tolerance.

Social contact behaviors are associated with infection status for Trichuris sp. in wild vervet monkeys (Chlorocebus pygerythrus).

Social grooming in the animal kingdom is common and serves several functions, from removing ectoparasites to maintaining social bonds between conspecifics. We examined whether time spent grooming with others in a highly social mammal species was associated with infection status for gastrointestinal parasites. Of six parasites detected, one (Trichuris sp.) was associated with social grooming behaviors, but more specifically with direct physical contact with others. Individuals infected with Trichuris sp. spent significantly less time grooming conspecifics than those not infected, and time in direct contact with others was the major predictor of infection status. One model correctly predicted infection status for Trichuris sp. with a reliability of 95.17% overall when the variables used were time spent in direct contact and time spent grooming others. This decrease in time spent grooming and interacting with others is likely a sickness behavior displayed by individuals with less energy or motivation for non-essential behaviors. This study emphasizes the possible links between host behavior and parasitic infections and highlights the need for an understanding of a study population's parasitic infections when attempting to interpret animal behavior.

Reproductive adaptations to high densities in social mammals

An overview of population density control in social mammals sets the framework for examining reproductive responses to increasing population densities. We begin by honoring John B. Calhoun who played a major role, starting about 70 years ago, in correcting the conventional wisdom of the time that population control was all about adjusting mortality rates. Reproduction was considered a constant, and emigration was viewed as a component of mortality. His research was mostly on domestic and feral populations of Rattus norvegicus and Mus musculus for which he built complex arenas that could house thousands of inhabitants. In addition, he constructed elaborate living quarters in the alleyways of Baltimore. For the captive populations, he would individually mark all the inhabitants so that he could identify them and observe their behavior. Eight examples of his research publications are described. He was able to document a list of reproduction related behaviors that are the main focus of this essay, and clearly demolish the simplistic notion that reproduction is a constant. A summary of some of the major issues that encompasses the science of population growth and regulation is provided. There follows a series of 19 examples of non-Calhoun publications that cover many more species of social mammals, including humans. A comprehensive list of the many negative adaptations involving reproductive processes are documented for the 27 publications reviewed confirming that in many species reproductive constraints are non-trivial. There follows a brief discussion that attempts to create a cohesive whole for this intellectual adventure.

Long-term movements and home-range changes: Rapid territory shifts in meerkats.

Territoriality and stable home ranges are a common space-use pattern among animals. These ranges provide its inhabitants with important resources and thus favourable territories are associated with an increased fitness. While the role of territory quality and changes of territory ownership have often been investigated, the changes of territorial boundaries have been less studied. Here, we investigated space-use changes in a social mammal species, applying a novel analytical approach, calculating long-term dissimilarity in space use using distancematrices based on periodic utilization distributions. This approach makes it possible to identify different space-use patterns, which cannot be distinguished by only considering changes between consecutive time periods. We analysed meerkat (Suricata suricatta) movements of a total of 24 different groups over a 16-year period, resulting in 134 group years. We then correlated the identified home-range changes to life-history events and possible environmental drivers. Groups had stable territories for several years before they abandoned their home range mostly to move quickly to new areas where they again remained for several years. Of 26 identified sudden shifts, 22 occurred in the summer months and often involved distances larger than the original home-range size. Home-range movements that were close together in time were often also spatially clustered and moved in a similar direction. These shifts were often preceded by more frequent interactions between groups, but did not seem to be a product of direct displacements by other groups. The normalized difference vegetation index as a measure of food production and social factors such as dominance changes did not correlate to changes. Against our expectation space-use changes were not accumulations of small changes, but more often involved long-distance moves into unknown ranges. This means that the groups enter areas where they cannot profit from local knowledge. The methods used identify episodes of long stability alternated by sudden changes in meerkats and in general provides insight into long-term space use. Our methods can be used to analyse long-term space use, either within or across species.

Social context hinders humans but not ravens in a short‐term memory task

AbstractUsing resources shared within a social group—either in a cooperative or a competitive way—requires keeping track of own and others’ actions, which, in turn, requires well‐developed short‐term memory. Although short‐term memory has been tested in social mammal species, little is known about this capacity in highly social birds, such as ravens. We compared ravens (Corvus corax) with humans in spatial tasks based on caching, which required short‐term memory of one's own and of others’ actions. Human short‐term memory has been most extensively tested of all social mammal species, hence providing an informative benchmark for the ravens. A recent study on another corvid species (Corvus corone) suggests their capacity to be similar to the humans’, but short‐term memory skills have, to date, not been compared in a social setting. We used spatial setups based on caches of foods or objects, divided into individual and social conditions with two different spatial arrangements of caches (in a row or a 3 × 3 matrix). In each trial, a set of three up to nine caches was presented to an individual that was thereafter allowed to retrieve all items. Humans performed better on average across trials, but their performance dropped, when they had to keep track of partner's actions. This differed in ravens, as keeping track of such actions did not impair their performance. However, both humans and ravens demonstrated more memory‐related mistakes in the social than in the individual conditions. Therefore, whereas both the ravens’ and the humans’ memory suffered in the social conditions, the ravens seemed to deal better with the demands of these conditions. The social conditions had a competitive element, and one might speculate that ravens’ memory strategies are more attuned to such situations, in particular in caching contexts, than is the case for humans.

Socio-genetic correlates of unbiased sex dispersal in a population of black capuchin monkeys (Sapajus nigritus)

Most social mammal species exhibit male-biased dispersal. Sex bias in dispersal leads to a higher degree of relatedness among individuals of the philopatric sex, thus an atypical dispersal pattern might lead to deviations in the typical within-group kinship structure. Kinship, in turn, influences patterns of social interactions, as widely evident by kin-biased behaviors. We investigated the link between dispersal, relatedness structure, and sociopositive interactions established by adult females of black capuchin monkeys (Sapajus nigritus) living in a population that experiences female dispersal, an unusual pattern for capuchin monkeys. The study was conducted in Parque Estadual Carlos Botelho (PECB), within the Brazilian Atlantic Forest. We addressed dispersal and relatedness patterns by genotyping 20 adults of 3 groups across 9 microsatellite loci. We also sampled the monkeys’ behavior and compared spatial association frequencies and rates of grooming among same- and opposite-sex dyads. There was no difference between males and females in genetic parameters; both males and females show low coefficients of relatedness indicating that neither sex is consistently philopatric. The mean pairwise coefficient of relatedness for co-resident females was not higher than that for co-resident males. Compared to other populations of capuchin monkeys, female bond was weak, as evident by lower spatial association frequencies, reduced rates of grooming and lack of correlation between coefficients of relatedness and measures of dyadic sociopositive interactions. Our findings thus confirm that female dispersal is a habitual process in the capuchin population of PECB, and that, as expected, dispersal by females strongly influences the relatedness structure of the population as well as the affiliative relationships among female groupmates.

Evidence of allomaternal nursing across one-male units in the Yunnan snub-nosed monkey (Rhinopithecus Bieti).

BackgroundAllomaternal nursing, common in several species of social mammals, also has been reported in nonhuman primates. However, the function of this behavior in enhancing infant survivorship remains poorly understood.Methodology and Principal FindingsThe study was conducted on a free-ranging group of the Yunnan snub-nosed monkey (Rhinopithecus bieti) in the Baimaxueshan Natural Reserve. Direct observation and ad libitum sampling were used to record allocare behavior during a 20 month field study. R. bieti exhibits a multilevel social organization in which a large single troop, consisting of over 100 individuals, is divided into many one-male units (OMUs: 6∼41). These OMUs coordinate their daily activities, and feed, forage, travel, and rest together. Here we report on one case of infant temporary adoption in which an adult female from one OMU engaged in allomaternal nursing and cared for an infant from a different OMU of the same troop. This event began when the mother and her five-month-old infant were found to became separated accidentally. The victim infant was observed staying in another OMU. Over the next several days we observed a lactating female in the new OMU to care for and nurse both her infant and the immigrant infant, who also was tolerated by and cared for by the harem male.Conclusions and SignificanceOur findings suggest that lactating primate females are primed to care for young infants and, that the misdirected parental care hypothesis may offer the strongest explanation for allomaternal nursing in R. bieti.

Role of maternal odors on foraging behavior during postnatal development in a solitary subterranean rodent Ctenomys talarum

We investigated the role of maternal odors emanating from excretory deposits and/or glandular secretions during the postnatal development of foraging and related behaviors in young Los Talas’ tuco-tucos (Ctenomys talarum), a solitary rodent, under seminatural conditions. During cafeteria tests, we offered them two of the grasses most preferred by adults of this species (bromegrass, Bromus unioloides and panicgrass, Panicum racemosum). We scent marked one dietary option in a treatment group, and the other option in a second treatment group, keeping a third group with no odors as control. Pups did not show to prefer a special grass in particular, and maternal odors showed no effect on the behavioral variables evaluated in this study. When they reached their weaning age, they showed an ontogenetic change in food preferences, where they preferred bromegrass, and maternal odors influenced negatively on the consumption of panicgrass. During dispersal, preference for bromegrass was expressed independently of the presence of maternal odors. Overall, their effect was less pronounced than age’s effect, and it was evident in only a subset of the conducted experiments. This study shows that the influence of maternal odors is not essential for the establishment of feeding or site preferences in this species in seminatural conditions, contrarily to what was observed in other studies performed with social mammal species (i.e., rats and rabbits). It is suggested that other factors (e.g., individual learning) might influence the observed preferences.

Quasi-PSO Algorithm for Modeling Foraging Dynamics in Social Mammals

In this paper, the authors present a computational model of a fundamental social phenomenon in the study of animal behavior: the foraging. The purpose of this work is, first, to test the validity of the proposed model compared to another existing model, the flocking model; then, to try to understand whether the model may provide useful suggestions in studying the size of the group in some species of social mammals.

Cross-cultural and cross-ecotype production of a killer whale ‘excitement’ call suggests universality

Facial and vocal expressions of emotion have been found in a number of social mammal species and are thought to have evolved to aid social communication. There has been much debate about whether such signals are culturally inherited or are truly biologically innate. Evidence for the innateness of such signals can come from cross-cultural studies. Previous studies have identified a vocalisation (the V4 or 'excitement' call) associated with high arousal behaviours in a population of killer whales in British Columbia, Canada. In this study, we compared recordings from three different socially and reproductively isolated ecotypes of killer whales, including five vocal clans of one ecotype, each clan having discrete culturally transmitted vocal traditions. The V4 call was found in recordings of each ecotype and each vocal clan. Nine independent observers reproduced our classification of the V4 call from each population with high inter-observer agreement. Our results suggest the V4 call may be universal in Pacific killer whale populations and that transmission of this call is independent of cultural tradition or ecotype. We argue that such universality is more consistent with an innate vocalisation than one acquired through social learning and may be linked to its apparent function of motivational expression.

The Akela-effect – Is there an evolutionary benefit from senators in mammals?

A characteristic feature of the life history of humans and some other species of social mammals is a long post-reproductive period. This condition is of a physiological nature in females (menopause), whereas in males it is largely of a behavioral nature. We discuss the hypothesis that old, post-reproductive individuals in these species may act as repositories of acquired knowledge, thereby providing an evolutionary benefit for their group. According to this view, the group's investment into the care for their older members is overcompensated by the benefits gained from the experience of these individuals (“senators”). This phenomenon is suggested to be largely independent from the degree of genetic relatedness within the group. We put forward a list of several necessary preconditions for the senator phenomenon to evolve. The presence or absence of these preconditions can be studied empirically.

Pathology of Mycobacterium bovis Infection in Wild Meerkats ( Suricata suricatta)

Pathological lesions associated with Mycobacterium bovis infection (bovine tuberculosis; bTB) in free-living meerkats (Suricata suricatta) in the Kalahari Desert of South Africa are described. The pathology of bTB in meerkats was determined through detailed post-mortem examinations of 57 animals (52 meerkats showing clinical signs of bTB, and five not showing signs of disease). Lymph nodes and tissue lesions thought to be associated with bTB were cultured for mycobacteria. All 52 bTB-infected meerkats showed gross or microscopical granulomatous lesions, but M. bovis was cultured from only 42% (22/52) of these animals. The majority (96%, 50/52) of diseased meerkats had lesions in multiple sites, the pattern of which suggested haematogenous spread of M. bovis infection in this species. The histological characteristics of the tuberculous lesions, together with the gross pathology and the wide range of body systems affected, indicate that infection in meerkats is acquired principally via the respiratory and oral routes, whereas excretion is most likely via the respiratory tract and suppurating skin wounds. Urine and faeces appear to be unlikely sources of infection. The findings of this study provide information on the transmission, pathogenesis and epidemiology of bTB in meerkats that is likely to be relevant to the understanding of M. bovis infection in other social mammal species such as the European badger (Meles meles).

Spoiled Brats: Is Extreme Juvenile Agonism in Ring‐Tailed Coatis (Nasua nasua) Dominance or Tolerated Aggression?

AbstractRing‐tailed coatis exhibit an extreme form of juvenile agonism not found in other social mammals. Two groups of habituated, individually recognized, coatis were studied over a 2.5‐yr period in Iguazu National Park, Argentina. Dominance matrices were divided by year and group, resulting in four dominance hierarchies which were analyzed using the Matman computer program. Strong general patterns were seen in both groups during both years. Adult males (one per group) were the highest ranking individuals, followed by male juveniles, female juveniles, adult females, and male and female subadults. The pattern in which young, physically inferior individuals were able to outrank larger adults is different from other social mammal species in that the juvenile coatis aggressively defended food resources and directed aggression towards older individuals. These agonistic interactions may not reflect ‘dominance’ in the traditional sense, and appear to be a form of ‘tolerated aggression.’ This tolerated aggression leads to increased access to food, and should help juveniles during a period in which they need to rapidly gain weight and grow. Because this tolerance of juvenile aggression is reinforced through coalitionary support of juveniles by adult females, agonistic patterns are also consistent with the hypothesis that juvenile rank is being influenced by high degrees of relatedness within coati groups. Although some interesting parallels exist, there is little evidence indicating that these dominance patterns are the same as those found in other social mammals such as hyenas, lions, meerkats, or Cercopithicine primates.

Chronic social stress: Changes in behavioral and physiological indices of emotion

Subordination constitutes a natural and often chronic stress condition for males of virtually all species of social mammals. Subordinate male rats of mixed-sex groups maintained in visible burrow systems show high-magnitude changes in adrenal and gonadal steroid hormones and, in a subpopulation, disruptions in hypothalamic pituitary adrenal axis function. Changes in brain serotonin systems have been extensively documented in both colony subordinates and colony dominants, with other regional neurotransmitter system changes also indicated. The group experience seems to change a variety of behaviors both inside the colony situation and in tests run outside the colonies and may disrupt the relationship found in controls between hypothalamic pituitary adrenal response to an acute stressor and defensive behavior. Comparisons of these patterns of stress response with those of other chronic stress models such as learned helplessness and chronic mild stress suggest that, in terms of adrenal and gonadal steroid hormone response, subordination constitutes a more severe stressor. Some involvement of the serotonin system has been demonstrated for both subordination and more traditional models, and other systems may prove to be involved in both. However, a central feature of both learned helplessness and chronic mild stress paradigms is a specific criterion behavior or behaviors, emphasized as models for particular psychopathologies. Thus, learned helplessness and chronic mild stress studies have tended to emphasize the effects of pharmacological agents on these models, whereas work with subordination has been focused on analysis of the biobehavioral stress process itself.

Chronic social stress: Changes in behavioral and physiological indices of emotion

Subordination constitutes a natural and often chronic stress condition for males of virtually all species of social mammals. Subordinate male rats of mixed-sex groups maintained in visible burrow systems show high-magnitude changes in adrenal and gonadal steroid hormones and, in a subpopulation, disruptions in hypothalamic pituitary adrenal axis function. Changes in brain serotonin systems have been extensively documented in both colony subordinates and colony dominants, with other regional neurotransmitter system changes also indicated. The group experience seems to change a variety of behaviors both inside the colony situation and in tests run outside the colonies and may disrupt the relationship found in controls between hypothalamic pituitary adrenal response to an acute stressor and defensive behavior. Comparisons of these patterns of stress response with those of other chronic stress models such as learned helplessness and chronic mild stress suggest that, in terms of adrenal and gonadal steroid hormone response, subordination constitutes a more severe stressor. Some involvement of the serotonin system has been demonstrated for both subordination and more traditional models, and other systems may prove to be involved in both. However, a central feature of both learned helplessness and chronic mild stress paradigms is a specific criterion behavior or behaviors, emphasized as models for particular psychopathologies. Thus, learned helplessness and chronic mild stress studies have tended to emphasize the effects of pharmacological agents on these models, whereas work with subordination has been focused on analysis of the biobehavioral stress process itself. Aggr. Behav. 24:307–321, 1998. © 1998 Wiley-Liss, Inc.