Group-living Individuals Research Articles

Immune Stimulation via Wounding Alters Chemical Profiles of Adult Tribolium castaneum

Group-living individuals experience immense risk of disease transmission and parasite infection. In social and in some non-social insects, disease control with immunomodulation arises not only via individual immune defenses, but also via infochemicals such as contact cues and (defensive) volatiles to mount a group-level immunity. However, little is known about whether activation of the immune system elicits changes in chemical phenotypes, which may mediate these responses. We here asked whether individual immune experience resulting from wounding or injection of heat-killed Bacillus thuringiensis (priming) leads to changes in the chemical profiles of female and male adult red flour beetles, Tribolium castaneum, which are non-social but gregarious. We analyzed insect extracts using GC-FID to study the chemical composition of (1) cuticular hydrocarbons (CHCs) as candidates for the transfer of immunity-related information between individuals via contact, and (2) stink gland secretions, with analysis of benzoquinones as main active compounds regulating ‘external immunity’. Despite a pronounced sexual dimorphism in CHC profiles, wounding stimulation led to similar profile changes in males and females with increases in the proportion of methyl-branched alkanes compared to naïve beetles. While changes in the overall secretion profiles were less pronounced, absolute amounts of benzoquinones were transiently elevated in wounded compared to naïve females. Responses to priming were insignificant in CHCs and secretions. We suggest that changes in different infochemicals after wounding may mediate immune status signaling in the context of both internal and external immune responses in groups of this non-social insect, thus showing parallels to social immunity.

Sex, not social behavior, predicts fecal glucocorticoid metabolite concentrations in a facultatively social rodent, the highland tuco-tuco (Ctenomys opimus)

Social relationships may influence circulating glucocorticoid levels, particularly in group-living species in which individuals regularly engage in interactions with conspecifics. The effects of such interactions appear to vary, with greater social contact being associated with increased glucocorticoid concentrations in some species but decreased concentrations in others. These distinct responses raise intriguing questions regarding relationships among social behavior, individual phenotypes, and glucocorticoid physiology. To explore such relationships in a free-living mammal with a dynamic social organization, we quantified variation in baseline glucocorticoids in a population of highland tuco-tucos (Ctenomys opimus) from Jujuy Province, Argentina. These subterranean rodents are facultatively social, with lone and group-living individuals regularly occurring within the same population. To assess potential endocrine correlates of this behavioral variability, we examined differences in baseline fecal glucocorticoid metabolite (fGCm) concentrations as a function of social group size and composition as well as several metrics of social behavior derived from social network analyses. Despite marked variability in social relationships among the 37 (12 male, 25 female) free-living tuco-tucos sampled, none of the measures of social behavior examined were significant predictors of variation in fGCm concentrations. In contrast, individual variation in glucocorticoid metabolites was best explained by sex, with males having higher fGCm concentrations than females. These analyses provide the first characterization of the glucocorticoid physiology of highland tuco-tucos and underscore the potential importance of intrinsic phenotypic factors (e.g., sex) in shaping glucocorticoid variation in free-living mammals.

The cessation of contact calls does not provoke or modulate alarm behaviour in a social passerine

Abstract Vocalizations that signal predation risk such as alarm calls provide crucial information for the survival of group-living individuals. However, alarm calling may attract the predator’s attention and, to avoid this cost, animals can opt for alternative strategies to indicate danger, such as ‘adaptive silence’, which is the cessation of vocalizations. We investigate here whether abrupt contact call cessation would provoke alarm responses, or would reinforce the signal given by an alarm call. In an aviary setting, we conducted playback experiments with a group-living passerine, the Swinhoe’s white-eye, Zosterops simplex. We found that birds did not respond to a sudden call cessation, nor did they have a stronger response to alarm calls followed by silence than to alarm calls followed by contact calls. Confirming previous work investigating contact call rate, it appears that in this species contact calls encode information about social factors but not environmental conditions.

Multi-year assessment of variability in spatial and social relationships in a subterranean rodent, the highland tuco-tuco (Ctenomys opimus)

In some species, populations routinely contain a mixture of lone and group-living individuals. Such facultative sociality may reflect individual differences in behavior as well as adaptive responses to variation in local environmental conditions. To explore interactions between individual- and population-level variabilities in behavior in a species provisionally described as facultatively social, we examined spatial and social relationships within a population of highland tuco-tucos (Ctenomys opimus) at Laguna de los Pozuelos, Jujuy Province, Argentina. Using data collected over 5 consecutive years, we sought to (1) confirm the regular occurrence of both lone and group-living individuals and (2) characterize the temporal consistency of individual social relationships. Our analyses revealed that although the study population typically contained lone as well as group-living animals, individual spatial and social relationships varied markedly over time. Specifically, the extent to which individuals remained resident in the same location across years varied, as did the number of conspecifics with which an animal lived, with an overall tendency for individuals to live in larger groups over successive years. Collectively, these analyses indicate that population-level patterns of behavior in C. opimus are consistent with facultative sociality but that this variation does not arise due to persistent differences in individual behavior (i.e., living alone versus with conspecifics). Instead, based on changes in spatial and social relationships across years, we suggest that variation in the tendency to live in groups is shaped primarily by local ecological and demographic conditions.Significance statementCharacterizing variation in conspecific relationships is critical to understanding the adaptive bases for social behavior. Using data collected over 5 successive years, we examined temporal variation in spatial and social relationships within a population of highland tuco-tucos (C. opimus) from northern Argentina. In addition to providing the first multi-year assessment of the behavior and demography of this species, our analyses generate important insights into relationships between individual behavior and population-level patterns of social organization. The behavioral variability evident in our study population suggests that C. opimus is an ideal system in which to explore the causes and consequences of individual differences in social behavior.

Social conformity in solitary crabs, Carcinus maenas, is driven by individual differences in behavioural plasticity

Group living is widespread in the animal kingdom and recent studies into the mechanisms underlying group cohesion and behavioural synchrony have highlighted the importance of between-individual behavioural differences (‘animal personality’). In group-living animals, social conformity occurs when animals compromise their own behaviour to the level of a certain behaviour displayed by another individual or a group, and the degree to which individuals conform can depend upon interindividual differences in behavioural types. Social conformity can increase group cohesion and ultimately predator avoidance and/or resource acquisition for group-living individuals. However, it remains unclear whether similar conformity effects exist in solitary species, many of which form temporary aggregations and, if so, whether changes in behaviour in the presence of conspecifics are dependent on individuals' personalities in solitary contexts. We studied the effects of social context (i.e. the presence of a conspecific) on behaviour in solitary shore crabs, using automated video tracking. Individuals differed consistently in their activity levels within and across contexts and were significantly more active in solitary than dyadic contexts. No differences in activity between same- and opposite-sex dyads were found. Crabs' activity levels were more similar when tested together than when tested alone, indicating a social conformity effect. Furthermore, more active behavioural types decreased their activity to a greater extent when paired with a conspecific. The sex composition of the dyad had no effect on changes in activity. Overall, our findings suggest that social conformity is moderated by individual behavioural differences in a solitary organism. It is often presumed that, over evolutionary time, the social structure of animal populations has important consequences for the evolution of personalities and vice versa. We suggest that studying solitary or facultatively social organisms may allow researchers to tease out causality between personality differences and socioecological dynamics.

Can outcomes of dyadic interactions be consistent across contexts among wild zebrafish?

Winner–loser relations among group-living individuals are often measured by the levels of aggressive interactions between them. These interactions are typically driven by competition for resources such as food and mates. It has been observed in recent studies on zebrafish that dominant males generally have higher total reproductive success than their less aggressive subordinate counterparts. This study aimed to test whether males who monopolized a food resource (winners) also displayed higher levels of aggression than the males who were unsuccessful (losers). Further, the study also tested whether the same ‘winner’ males were also able to monopolize interactions with females during courtship. The results from these experiments showed that while males monopolizing food resources (winners) demonstrated higher levels of agonistic interactions than the losers, the average number of courtship interactions initiated by either of the males (i.e. winners/losers) with a female was not significantly different. A significant relationship was obtained between the number of aggressive interactions and feeding latencies of males in the context of food monopolization. This indicated that there could be a linkage between boldness defined by feeding latency in a novel environment and agonistic responses. The probable role of nature of resources, resource availability and distribution in determining the outcomes of dyadic contests is discussed.

Solitary individuals in populations of the group-living lizard Ouroborus cataphractus: voluntary or forced?

We compared crevice fidelity among solitary and group-living individuals in a population of the group-living lizard Ouroborus cataphractus. We also compared the incidence of solitary individuals between the sexes and different seasons.We surveyed suitable rocky areas at two sites in the Graafwater district, South Africa, and all O. cataphractus individuals found, whether in groups or solitary, were marked and released back into their crevices. The areas were resurveyed after one month, three months and four months to compare crevice fidelity of solitary and group-living individuals. We found that solitary individuals were significantly less loyal to their rock shelters than individuals living in groups, and that solitary females appeared to be less loyal than solitary males. We found no significant difference in the frequency of solitary adult males in and outside of the mating season. Solitary adult males were significantly smaller in mean body size than group-living adult males, but did not have more scars or other deformities than the latter. We found no significant difference in the frequencies of solitary individuals during the wet and the dry seasons, or in the frequencies of solitary adult males versus solitary adult females recorded during any of the surveys. The significantly lower crevice fidelity displayed by solitary than group-living individuals supports the notion that being in a group must be the optimal situation for individuals of this relatively slow-moving cordylid. Our finding that solitary adult males were significantly smaller in mean body size than group-living adult males also suggests that the exclusion of less competitive males from groups may in part be responsible for the occurrence of solitary males.

Solitary Individuals in Populations of the Group-Living Lizard Ouroborus Cataphractus: Voluntary or Forced?

We compared crevice fidelity among solitary and group-living individuals in a population of the group-living lizard Ouroborus cataphractus. We also compared the incidence of solitary individuals between the sexes and different seasons. We surveyed suitable rocky areas at two sites in the Graafwater district, South Africa, and all O. cataphractus individuals found, whether in groups or solitary, were marked and released back into their crevices. The areas were resurveyed after one month, three months and four months to compare crevice fidelity of solitary and group-living individuals. We found that solitary individuals were significantly less loyal to their rock shelters than individuals living in groups, and that solitary females appeared to be less loyal than solitary males. We found no significant difference in the frequency of solitary adult males in and outside of the mating season. Solitary adult males were significantly smaller in mean body size than group-living adult males, but did not have more s...

Differences in social behaviour between group-living and solitary African striped mice, Rhabdomys pumilio

Little is known about the extent to which solitary individuals differ in their social behaviour from group-living ones within the same species. Using the socially flexible African striped mouse, we tested through a series of dyadic encounters in a neutral arena whether group-living mice that later became solitary differed from their philopatric conspecifics. We compared philopatric and solitary mice both before and after dispersal. We predicted striped mice that became solitary would be more aggressive, less amicable and more investigative than individuals that remained group living, and would change their social behaviour after changing from group to solitary living in the same direction (becoming more aggressive, etc.). Dyadic encounters were conducted on 42 group-living individuals and 13 individuals that were first group living and later became solitary. Striped mice that became solitary showed higher levels of aggression and social investigation than their conspecifics that remained group living, differences that were already present before individuals dispersed. Dispersing striped mice showed a negative correlation between amicability and aggression towards opposite-sex individuals, which could be linked to sexual motivation. A second behavioural syndrome in the form of a positive correlation between aggression and social investigation towards same-sex individuals might have indicated that dispersing striped mice were ready to defend their own territory. Our study provides evidence that within the same population and at the same time, individuals that disperse and become solitary differ behaviourally from their group-living conspecifics even before dispersal, and further change their behaviour after dispersal in an evolutionarily adaptive way.

On the evolutionary origins of the egalitarian syndrome

The evolutionary emergence of the egalitarian syndrome is one of the most intriguing unsolved puzzles related to the origins of modern humans. Standard explanations and models for cooperation and altruism--reciprocity, kin and group selection, and punishment--are not directly applicable to the emergence of egalitarian behavior in hierarchically organized groups that characterized the social life of our ancestors. Here I study an evolutionary model of group-living individuals competing for resources and reproductive success. In the model, the differences in fighting abilities lead to the emergence of hierarchies where stronger individuals take away resources from weaker individuals and, as a result, have higher reproductive success. First, I show that the logic of within-group competition implies under rather general conditions that each individual benefits if the transfer of the resource from a weaker group member to a stronger one is prevented. This effect is especially strong in small groups. Then I demonstrate that this effect can result in the evolution of a particular, genetically controlled psychology causing individuals to interfere in a bully-victim conflict on the side of the victim. A necessary condition is a high efficiency of coalitions in conflicts against the bullies. The egalitarian drive leads to a dramatic reduction in within-group inequality. Simultaneously it creates the conditions for the emergence of inequity aversion, empathy, compassion, and egalitarian moral values via the internalization of behavioral rules imposed by natural selection. It also promotes widespread cooperation via coalition formation.

Freshwater pearl mussels show plasticity of responses to different predation risks but also show consistent individual differences in responsiveness

Animals often show behavioural plasticity with respect to predation risk but also show behavioural syndromes in terms of consistency of responses to different stimuli. We examine these features in the freshwater pearl mussel. These bivalves often aggregate presumably to reduce predation risk to each individual. Predation risk, however, will be higher in the presence of predator cues. Here we use dimming light, vibration and touch as novel stimuli to examine the trade-off between motivation to feed and motivation to avoid predation. We present two experiments that each use three sequential novel stimuli to cause the mussels to close their valves and hence cease feeding. We find that mussels within a group showed shorter closure times than solitary mussels, consistent with decreased vulnerability to predation in group-living individuals. Mussels exposed to the odour of a predatory crayfish showed longer closures than control mussels, highlighting the predator assessment abilities of this species. However, individuals showed significant consistency in their closure responses across the trial series, in line with behavioural syndrome theory. Our results show that bivalves trade-off feeding and predator avoidance according to predation risk but the degree to which this is achieved is constrained by behavioural consistency.

Social flexibility and social evolution in mammals: a case study of the African striped mouse (Rhabdomys pumilio)

Environmental change poses challenges to many organisms. The resilience of a species to such change depends on its ability to respond adaptively. Social flexibility is such an adaptive response, whereby individuals of both sexes change their reproductive tactics facultatively in response to fluctuating environmental conditions, leading to changes in the social system. Social flexibility focuses on individual flexibility, and provides a unique opportunity to study both the ultimate and proximate causes of sociality by comparing between solitary and group-living individuals of the same population: why do animals form groups and how is group-living regulated by the environment and the neuro-endocrine system? These key questions have been studied for the past ten years in the striped mouse Rhabdomys pumilio. High population density favours philopatry and group-living, while reproductive competition favours dispersal and solitary-living. Studies of genetic parentage reveal that relative fitness of alternative reproductive tactics depends on the prevailing environment. Tactics have different fitness under constrained ecological conditions, when competitive ability is important. Under conditions with relaxed ecological constraints, alternative tactics can yield equal fitness. Both male and female striped mice display alternative reproductive tactics based on a single strategy, i.e. all individuals follow the same decision rules. These changes are regulated by endocrine mechanisms. Social flexibility is regarded as an adaptation to unpredictably changing environments, selecting for high phenotypic flexibility based on a broad reaction norm, not on genetic polymorphism for specific tactics.

All together now: behavioural synchrony in baboons

For group-living individuals to remain spatially coherent, coordinated behaviour across group members is essential. We investigated what factors can promote or constrain the achievement of such behavioural synchronization (measured as diversity in activities among group members) in a social primate. Two wild groups of chacma baboons, Papio ursinus, were studied in the field by instantaneous scan sampling during full-day follows to test the hypotheses that individual activity budgets, habitat constraints and group properties can all affect patterns of behavioural synchrony. Observed synchrony across individuals was variable, and analysed using a generalized linear mixed model. We found support for each of our three hypotheses. First, the probability of a group being synchronized increased with the number of pregnant females, but decreased with the number of sexually swollen females in a group. Synchrony also declined throughout the day. We interpret these two results in terms of variations in the activity budgets of both sexes related to their reproductive strategies, and changing levels of satiation among individual group members, respectively. Second, synchrony was highest in a ‘closed’ woodland habitat, and lowest in ‘open’ desert habitat. This is interpreted as a consequence of habitat differences in food patch configuration and/or predation risk. Third, we found a nonlinear relationship with increasing group cohesion, suggesting that where opportunities for information transfer are limited, behavioural synchrony may be constrained. Overall, our simple approach to quantifying behavioural synchrony highlights the role of both individual variation and the (social and ecological) environment in determining group-level patterns of behaviour.

Decision making in group departures of sheep is a continuous process

For coordinated movement, group-living individuals have to reach consensus decisions through recruitment processes. Success in recruitment can depend on the spatial distribution and behaviour of animals before and/or after departure, and on their affinitive relationships. We tested the effect of such factors on recruitment processes in a group of 19 ewe lambs, Ovis aries, at pasture. Two observers continuously videotaped the behaviours of animals from a platform located in the centre of the field. Results showed that group orientation, group vigilance and activities such as head movements, stillness and number of steps increased before departure. Using general linear modelling we found that changes in most of these variables predicted the number of participants in movements. Similarly, activity of the first mover was modified in the last 2 min preceding departure, and at departure time the location and number of close neighbours of the first mover were especially influential in recruiting conspecifics. Animals first recruited were those that were close to the first mover and also its preferential partners. The behaviours of the second and third moving individuals could further influence the recruitment process. Moreover, there were clues that individuals were able to recruit others intentionally. Our findings emphasize that decision making in a group of domestic sheep was a continuous and distributed process. Recruitment depended both on group state and on the behaviour of individuals and their social relationships.

Behavioural profile predicts dominance status in mountain chickadees, Poecile gambeli

Individual variation in stable behavioral traits may explain variation in ecologically-relevant behaviors such as foraging, dispersal, anti-predator behavior, and dominance. We investigated behavioral variation in mountain chickadees (Poecile gambeli), a North American parid that lives in dominance-structured winter flocks, using two common measures of behavioral profile: exploration of a novel room and novel object exploration. We related those behavioral traits to dominance status in male chickadees following brief, pair-wise encounters. Low-exploring birds (birds that visited less than four locations in the novel room) were significantly more likely to become dominant in brief, pairwise encounters with high-exploring birds (i.e., birds that visited all perching locations within a novel room). On the other hand, there was no relationship between novel object exploration and dominance. Interestingly, novel room exploration was also not correlated with novel object exploration. These results suggest that behavioral profile may predict the social status of group-living individuals. Moreover, our results contradict the idea that novel object exploration and novel room exploration are always interchangeable measures of individuals' sensitivity to environmental novelty.

The social function of tail up in the domestic cat (Felis silvestris catus)

We investigated the social function of tail up in order to verify its possible relationship with the hierarchical organization of a social group. Domestic cats live at higher densities than their ancestor which is a solitary species. Since the signals needed by solitary animals have different properties than those needed by group-living individuals, signalling pattern utilised by the domestic cat has inevitably changed. Kittens displayed the tail up when greeting their mother; this behaviour can also be observed in wild species. But, in domestic cat the tail up can be also observed when an adult individual meets another one and it signals the intention to interact amicably. Rank order affected the display of tail up posture: it was more frequently displayed by low-ranking cats, and high-ranking individuals received it more often than other members of the social group. Then, tail up seems to be a signal by means of which a cat shows the recognition of the higher social status of the individual to whom is directed. We confirmed the association between tail up and other affiliative behavioural patterns and the individual variability in displaying them. Considerations on the evolution of the tail up as a visual signal will be discussed.

Kin selection and the distribution of altruism in relation to degree of kinship in Japanese macaques ( Macaca fuscata )

Using kin selection theory and Hamilton's equation (B/C > 1/r) to determine how group-living individuals should allocate altruism among their various categories of kin has proven extremely difficult. Among the factors responsible are: (1) the unclear altruistic status of many behavioral categories, (2) the difficulty of assessing the values of B and C, and hence their impact on the distribution of altruism according to relatedness, (3) the potentially confounding effect of reciprocal altruism on kin selection, and (4) the various time constraints limiting the ability of individuals to favor distant kin. We report experiments on Japanese macaques (Macaca fuscata) which made it possible to assess or control the effect of these factors on the distribution of altruism in relation to degree of kinship. We concentrated on a clearly altruistic behavioral category with a particularly large B/C ratio to maximize the distribution of altruism according to relatedness. The behavior was unilaterally distributed between kin, hence minimizing the confounding effect of reciprocal altruism on its distribution. Time constraints were eliminated by giving potential donors equal opportunities to behave altruistically with every kin tested. In each experiment, an adult female was given an opportunity to help at low cost one of her juvenile kin outrank its dominant peers. In previous experiments of this sort carried out on juveniles females, we had tested the impact of four categories of adult female kin. In the present experiments carried out on juvenile males, we tested new categories of adult female kin and increased our sample of kin dyads considerably. Altruism toward young males extended to r=0.125 among direct kin (great-grandmother/great-grandson dyads), and to r=0.25 among collateral kin (siblings), or inconsistently to r=0.125 (aunt-nephew dyads). These relatedness limits of nepotism may reflect the limit of the profitability of altruism as defined by the terms of Hamilton's equation and/or the limit of kin discrimination in our group.

Solitude versus Gregariousness: Do Physical Benefits Drive the Choice in Overwintering Meadow Voles?

Winter group formation has been described for many small rodent species living in temperate environments. Physical benefits (e.g. energy and water conservation) of huddling are generally considered to be the ultimate cause of these aggregations. We manipulated group size of meadow voles (1 versus 4 individuals) in a field experiment involving 40 individuals (5 replicates, each including 4 solitary-living and 4 group-living individuals) to test the validity of the physical benefits hypothesis. Energy expenditures and water flux were measured using the doubly labelled water method. Group size had no effect on field metabolic rate, water turnover, body mass changes, body composition, and survival. The role of physical benefits as the driving force behind winter aggregations should thus be reevaluated. Future studies should concentrate on specific time periods characterized by extreme climatic conditions. Alternative benefits of aggregations, such as decreased predation risk or social transmission of information, should also be considered.

Some neo-Darwinian decision rules for altruism: Weighing cues for inclusive fitness as a function of the biological importance of the decision.

A neo-Darwinian heuristic for decisions involving altruism is'hypothesized in this article. Following W. Hamilton's (1964) analysis of inclusive fitness, the assumption of this study is that tendencies to help another person are selected against, except when the donor and recipient are related and share genes underlying these tendencies. An important social psychological implication of Hamilton's formulation is that in group-living individuals (a) natural selection favors those who are prone to help others as a function of the latters' relatedness, potential fecundity, or other features indicating a recipient's capacity to enhance the donors' inclusive fitness, and (b) this effect is especially strong when help is biologically significant (e.g., the recipient will not survive otherwise). Such a heuristic is demonstrated in several studies involving hypothetical decisions to help: In life-or-death situations, people chose to aid close kin over distant kin, the young over the old, the healthy over the sick, the wealthy over the poor, and the premenopausal woman over the postmenopausal woman; whereas when it is a matter of an everyday favor, they gave less weight to kinship and opted to help either the very young or the very old over those of intermediate age, the sick over the healthy, and the poor over the wealthy.

Variation among juvenile capuchins in social influences on exploration.

The exploratory or feeding activities of others might influence the timing, the place, or both, of exploratory activities among young group-living individuals, and this influence might affect the information gained by individuals during exploration. This study examined the temporal and spatial aspects of adults' influence on the exploratory behavior of juvenile capuchins, and on the juveniles' acquisition of a novel behavior. Two experimental apparatus, which were initially novel to the juvenile subjects but familiar to the adults, and which provided food when a tool was used properly, were presented to group-housed capuchin monkeys. The apparatus were presented (a) in a central area, in which all animals could interact with the apparatus and in which several older group members regularly solved the tasks (group site), and (b) in a protected site within the home cage (crèche) that only juveniles could enter, but from which the rest of the cage, including the group site, could be viewed. Juveniles contacted the apparatus at the crèche more often when there was no apparatus at the group site, but only half the individuals made greater use of the apparatus at the group site than at the crèche when an apparatus was present at both sites. Seven of nine used an apparatus more often when adults also had an apparatus, than when adults did not have an apparatus. These results indicate that juveniles' exploratory activity is only weakly related to adults' activity. The linkage appears closer for younger juveniles (20 months or less) than for older juveniles. Moreover, as only older juveniles learned to solve the tasks, coordination of exploration with adults was evidently not related to learning a new skill. © Wiley-Liss, Inc.