Grooming Partners Research Articles

Social tension after grooming in wild Japanese macaques (Macaca fuscata yakui) is sex specific and sensitive to social relationships.

Changes in the rate of self-directed behavior-a proxy for social tension-offer valuable insights into individuals' experiences of social interactions. Many studies have tested the tension-reduction hypothesis, whereby grooming is expected to reduce social tension in the grooming partners. However, it is still unclear whether responses to grooming are affected by social factors such as an individual's role or social relationship with their partner, and whether responses are similar for females and males. Focussing on same-sex grooming in Yakushima Japanese macaques (Macaca fuscata yakui), we analyzed the effects of two social factors on the change in the rate of self-scratching after receiving grooming: sitting in contact with their partner outside of grooming contexts (as a measure of relationship strength) and rank distance. We collected 10-min postgrooming and matched-control focal samples on recipients of grooming. After controlling for postinhibitory rebound effects, grooming reduced scratching in females (suggesting that grooming was relaxing for the receiver), but not in males. In females, this reduction was associated with increased sitting in contact and increased rank distance: being groomed was more tension-reducing if the grooming partners spent time together outside of grooming contexts, or if their difference in rank was greater and therefore more conspicuous. The reduction effect was mediated by sitting in contact only when females had a higher-ranking-that is, more dominant and potentially aggressive-groomer. Our findings suggest that not all grooming interactions are perceived as equal, which has implications for its use as an index of relationship quality. To our knowledge, this represents the first study of postgrooming social tension in male Japanese macaques and our results highlight the need for caution when generalizing findings from only one sex to the species level.

Behavioral responses of solicitors after failure to receive grooming in Macaca fuscata

Grooming is one of the most common cooperative behaviors among several animal species. However, the tactics used to cope with uncooperative partners in grooming interactions remain unclear. Japanese macaques (Macaca fuscata) solicit grooming from partners through postural behaviors, but may not necessarily receive grooming. This study investigated the behavior of female Japanese macaques after they solicited but did not receive grooming. We predicted that unsuccessful solicitors would engage in grooming interactions with uncooperative partners if they were affiliated. If they were not affiliated, the solicitors would not do so and may seek grooming interactions with other grooming partners. We used a focal-animal sampling method, targeting 17 females at Katsuyama, Okayama Prefecture, Japan. We recognized affiliative relationships by measuring close spatial association. After unsuccessful solicitation, females tended to scratch themselves, suggesting that solicitors may experience anxiety or distress when they do not receive grooming. They also tended to be proximate with affiliated partners after solicitation, regardless of whether the solicitors received grooming from their partners. In contrast, when solicitors failed to receive grooming from unaffiliated partners, their subsequent proximity was lower than when they were groomed. Moreover, unsuccessful solicitors were likely to engage in grooming interactions with affiliated partners who were uncooperative (receivers of unsuccessful solicitations). However, they were less likely to engage in grooming interactions with unaffiliated partners and instead engaged in grooming interactions with other nearby partners. These findings indicate that female Japanese macaques decide whether to engage in grooming interactions with uncooperative partners who have not groomed solicitors based on affiliative relationships and the availability of other grooming partners. It is probable that, when the cost of searching for a grooming partner is low, female Japanese macaques are likely to switch partners, potentially leading to an increase in the benefits obtained from grooming interactions.

Friends in high places: Interspecific grooming between chimpanzees and primate prey species in Budongo Forest

While cases of interspecies grooming have been reported in primates, no comprehensive cross-site review has been published about this behavior in great apes. Only a few recorded observations of interspecies grooming events between chimpanzees and other primate species have been reported in the wild, all of which have thus far been in Uganda. Here, we review all interspecies grooming events recorded for the Sonso community chimpanzees in Budongo Forest Reserve, Uganda, adding five new observations to the single, previously reported event from this community. A new case of interspecies play involving three juvenile male chimpanzees and a red-tailed monkey is also detailed. All events took place between 1993 and 2021. In all of the six interspecific grooming events from Budongo, the ‘groomer’ was a female chimpanzee between the ages of 4–6 years, and the ‘recipient’ was a member of the genus Cercopithecus. In five of these events, chimpanzee groomers played with the tail of their interspecific grooming partners, and except for one case, initiated the interaction. In three cases, chimpanzee groomers smelled their fingers after touching distinct parts of the receiver’s body. While a single function of chimpanzee interspecies grooming remains difficult to determine from these results, our review outlines and assesses some hypotheses for the general function of this behavior, as well as some of the costs and benefits for both the chimpanzee groomers and their sympatric interspecific receivers. As allogrooming is a universal behavior in chimpanzees, investigating the ultimate and proximate drivers of chimpanzee interspecies grooming may reveal further functions of allogrooming in our closest living relatives, and help us to better understand how chimpanzees distinguish between affiliative and agonistic species and contexts.

Reactions to a dead adult female in Japanese macaques at Arashiyama: Why did a non-affiliated female groom the corpse?

Reporting reactions to death in nonhuman primates can provide valuable information for understanding the evolutionary origin of human ways of dealing with death. Although many studies have reported nonhuman primates' reactions to infant corpses, less is known about their reactions toward dead adults or adolescents. The deaths of adult primates, who usually form complex social relationships, may have social impacts. Here, we described in detail the reactions of Japanese macaques (Macaca fuscata) to the corpse of an adult female in a free-ranging multi-male multi-female group. We analyzed quantitative data on the whole group to determine how death-related behaviors were related to social relationships. Most group members in this case, including social partners of the deceased, exhibited no notable interest in the corpse. Only one adult female, who was not a grooming partner of the female before she died, touched and groomed the corpse. We examined four possible reasons why this female groomed the corpse: unawareness of death, learning about death, desire to consume insects, and reputation-building with other group members. This study highlights the potential value of closer examination of associations between reactions to dead adults or adolescents and social relationships before and after death in primate groups.

The effects of allogrooming and social network position on behavioural indicators of stress in female lion-tailed macaques (Macaca silenus)

Allogrooming serves an important social function in primates and confers short term benefits such as parasite removal and stress-relief. There is currently mixed evidence as to the immediate impact of allogrooming on an individual’s stress levels, which may be influenced by their role in the grooming dyad, position in their social network, or their relationship with their grooming partner. In this study of seven captive adult female lion-tailed macaques (Macaca silenus) in a mixed sex group at Chester Zoo, UK, we found evidence to support a tension-reduction function of allogrooming. Focal animal sampling showed that the duration of self-directed behaviour (SDB), which indicates moderate to high levels of stress, was significantly lower in the five-minute period following allogrooming than the five-minute period preceding it for both recipients and groomers. However, when compared to match-control periods, both SDB rates and durations were significantly lower across all individuals in the five-minute period both before and after allogrooming, indicating that although allogrooming reduces stress, it is also more likely to occur when individuals are already in a relatively relaxed state. The rate and duration of SDB post-grooming did not correlate with the strength of a dyad’s bond (based on proximity). This suggests that it is the act of allogrooming itself, rather than the identity of the partner, that reduces stress for both parties. Analysis of the proximity network highlighted a clear cost to social integration; node strength, a measure of the number and strength of an individual’s direct relationships, positively correlated with the duration of self-directed behaviour, suggesting that more gregarious individuals may experience higher levels of stress. These findings add to the growing body of literature that examines the effect of the individual social environment on primate stress levels, and also highlight the need to further investigate the link between social integration and the stress experienced by group-living animals.

Eyeblink rate as an indicator of concentration on grooming in Japanese macaques (Macaca fuscata).

In primates, social relationships with a high frequency of social grooming are referred to as "affiliate relationships," "friendship," "bonding," and are described as involving positive emotion. However, the psychological state during social grooming has not been fully understood. In this study, I focused on blinking as a behavior that reflects psychological state during grooming in Macaca fuscata, a nonhuman wild primate, and examined for the first time whether the blink rate reflects concentration on social grooming. To test this hypothesis, I focused on ectoparasite removals during social grooming with the following three predictions: (1) blinks are synchronized with breakpoints (when monkeys can release visual attention) of mouthing ectoparasites during grooming, (2) the blink rate is lower during grooming (when requiring visual concentration) than during resting (when no visual concentration is required), and (3) the lower the blink rate during grooming (supposedly in high concentration), the higher the frequency of ectoparasites removals (outputs of the task). I recorded the faces of 10 wild female Japanese macaques on Kinkazan Island, Miyagi Prefecture, with video, while they were resting and grooming, and recorded the timing and frequency of eyeblink and ectoparasite removals. All three predictions were supported, suggesting that the blink rate during grooming can be an indicator of concentration on grooming in nonhuman primates. Whether grooming concentration is associated with an affiliative relationship with the grooming partner is an issue that should be carefully examined in future studies, but eyeblink studies may provide new perspectives for understanding the psychological state of individuals during grooming in a noninvasive manner.

No evidence that grooming is exchanged for coalitionary support in the short- or long-term via direct or generalized reciprocity in unrelated rhesus macaques

Reciprocity is a prominent explanation for cooperation between non-kin. Studies designed to demonstrate reciprocity often focus on direct reciprocity in the timescale of minutes to hours, whereas alternative mechanisms like generalized reciprocity and the possibility of reciprocation over longer timescales of months and years are less often explored. Using a playback experiment, we tested for evidence of direct and generalized reciprocity across short and longer timescales. We examined the exchange of grooming for coalitionary support between unrelated female rhesus macaques in a population with a complete genetic pedigree. Females that received grooming were not more responsive to calls for coalitionary support from unrelated female group mates compared to control females that received agonism or no interaction — even when the call belonged to a females’ most recent grooming partner. Similarly, females were not more responsive to calls for support from their most frequent unrelated grooming partner of the last two years, nor if they received large amounts of grooming from all other females in their group. We interpret these results as an absence of evidence for direct or generalized reciprocity on any timescale in the exchange of grooming for coalitionary support in rhesus macaques. If grooming is exchanged for support in this population, it is with an intensity below our ability to detect it or over a longer timescale than we examined. We propose by-product explanations may also be at play and highlight the importance of investigating multiple mechanisms when testing apparently cooperative behaviors.Significance statementThe receipt of help can make some animals more likely to provide help in return, whether it be a singular act, or many acts accumulated over months. Similarly, the receipt of help, be it one act of aid, or a group’s worth of help over time, can make some animals more likely to pay help forward to others. Studies on Old World monkeys suggest females may give grooming and in return receive aid in future physical conflicts. Using a playback experiment, we found female rhesus macaques were not more responsive to calls for intervention in a simulated conflict after being groomed by unrelated females, even if the calling combatant was her most recent, or a long-time grooming partner. Our results suggest females in our study population may be receiving benefits other than support in conflicts for the grooming they provide.

Sociality predicts individual variation in the immunity of free-ranging rhesus macaques

Social integration and social status can substantially affect an individual's health and survival. One route through which this occurs is by altering immune function, which can be highly sensitive to changes in the social environment. However, we currently have limited understanding of how sociality influences markers of immunity in naturalistic populations where social dynamics can be fully realized. To address this gap, we asked if social integration and social status in free-ranging rhesus macaques (Macaca mulatta) predict anatomical and physiological markers of immunity. We used data on agonistic interactions to determine social status, and social network analysis of grooming interactions to generate measures of individual variation in social integration. As measures of immunity, we included the size of two of the major organs involved in the immune response, the spleen and liver, and counts of three types of blood cells (red blood cells, platelets, and white blood cells). Controlling for body mass and age, we found that neither social status nor social integration predicted the size of anatomical markers of immunity. However, individuals that were more socially connected, i.e., with more grooming partners, had lower numbers of white blood cells than their socially isolated counterparts, indicating lower levels of inflammation with increasing levels of integration. These results build upon and extend our knowledge of the relationship between sociality and the immune system in humans and captive animals to free-ranging primates, demonstrating generalizability of the beneficial role of social integration on health.

Social network changes during the development of immature capuchin monkeys (Sapajus spp.).

Immatureindivuduals influence the formation and maintenance of social relationships within groups in diverse ways. Because of the increased interest of group members toward newborns, lactating females may use infants as social tools to temporally gain rank positions in matrilineal societies, and differential support received by the mothers may bias the network of immatures born to females of different ranks. In this study, we investigated the changes in proximity, grooming, play, and agonism networks of lactating females and immatures of different developmental periods, sex, and mothers' dominance rank. A semi-free-ranging group of 22 capuchin monkeys (Sapajus spp) was monitored for 12months, totaling over 300 hours of observation. During this period, the age changes of 13 immatures were monitored and recorded. Best regression models showed that an increased number of grooming partners while lactating did not translate into changes in the proximity or agonistic network positions for females. Age was the main predictor of social network changes, while sex had a minor influence on the play network and no influence on the grooming or agonistic networks. Finally, mothers' rank predicted differences in the affiliative but not the agonistic social network. This pattern points to a more affiliative and individual-based rather than agonistic and nepotism-based strategy for social network insertion, which can be explained by the decreased competition faced by the focal group and by the behavioral flexibility of the clade.

Social strategies used by dispersing males to integrate into a new group in Tibetan macaques (Macaca thibetana).

In group-living mammals, an individual's fitness depends, in part, on the quality of social relationships it has with others. Among species of nonhuman primates in which one sex is philopatric, individuals of that sex often develop strong social bonds and alliances with closely related kin. Less is known regarding the social processes used by dispersing adults to form stable bonds with nonkin in their new group. From May to December 2009, April to August 2010, September to December 2011, and February to May 2012, we collected data on grooming interactions in wild Tibetan macaques (Macaca thibetana), a female philopatric species, at Mt. Huangshan, China. Our goal was to compare social interactions and bond formation between resident males, recent immigrant males, and resident females. Our results indicate that recent immigrant males formed stable partner relationships with a small number of resident females and groomed these females more frequently or for longer than they received grooming. In contrast, resident males switched female grooming partners more frequently, received more grooming than they gave, and formed relationships with a greater number of female partners. We argue that the ability of recent immigrant male Tibetan macaques to maintain strong and persistent social bonds with a small set of resident adult females is a primary factor that enables them to establish residence in a new multimale-multifemale group. The present study provides new and important insights into the integrated social strategies used by dispersing males and resident females to maintain group stability.

Factors affecting tolerance persistence after grooming interactions in wild female vervet monkeys, Chlorocebus pygerythrus

Grooming is the most common cooperative behaviour in primates. It has helped advance our understanding of how animals achieve reciprocal cooperation without using precise counting strategies. For example, attitudinal reciprocity refers to recipients making short-term adjustments like reciprocated grooming or tolerance at food sources based on a change in emotional states. Here, we used an experimental set-up to investigate in unprecedented detail the building blocks of attitudinal reciprocity that govern wild dominant females' tolerance around food after a grooming interaction with a subordinate female partner in vervet monkeys. We measured the tolerance of dominant females towards the previous grooming partner within 4 h after a grooming interaction. Tolerance levels remained elevated compared to baseline for the entire period, decreasing with time and predicted to fall to baseline levels after approximately 6 h. The decline in tolerance was not affected by the relationship quality between females, further grooming received from other group members or the surplus grooming that the dominant received relative to what she gave. However, the duration of grooming by the subordinate influenced the dominant's tolerance positively. These results suggest that the temporal dynamics of tolerance are best described as grooming triggering the start of a partner-specific ‘hourglass’, where the amount of remaining ‘sand’ equates to the dominant's current tolerance level above baseline. The results challenge the notion that dominants use scorekeeping regarding their grooming debts towards subordinates to make decisions about reciprocating with tolerance.

Strongly bonded individuals prefer to forage together in cooperatively breeding dwarf mongoose groups

In many social species, group members form strong social bonds. Such strong bonds are well-known to generate long-term fitness benefits, but they are also expected to influence short-term behavioural decisions. Here, we use field observations and an experimental manipulation to investigate whether variation in social-bond strength (as determined from grooming interactions) influences nearest-neighbour choices while foraging in wild dwarf mongooses (Helogale parvula). Preferred grooming partnerships (PGPs), representing particularly strong bonds, were found predominately between male–female dyads but among a range of dominance-status dyads. When searching for food, dwarf mongooses with PGPs were more likely than expected by chance to forage close to a preferred grooming partner. Foraging near a strongly bonded groupmate might reduce the predation risk or increase foraging opportunities and the transfer of social information. In addition, there could be stress-reducing benefits, although our field experiment provided no evidence that nearest-neighbour preferences for strongly bonded groupmates were additionally favoured, or indeed disrupted, in the aftermath of a short-term stressful event. Investigating the potential influence of strong social bonds on short-term behavioural decisions with potential fitness consequences is important for our understanding of social interactions and cooperation. Enduring, close social bonds between individuals provide considerable long-term health and fitness benefits, but are also expected to influence short-term behavioural decisions. We investigated whether social-bond strength (as determined from grooming interactions) influenced foraging decisions in cooperatively breeding dwarf mongoose groups. We found particularly strong social bonds in the form of preferred grooming partnerships in a subset of male–female dyads. Dwarf mongoose foraging decisions were affected by the strength of their social relationships with groupmates: individuals with preferred grooming partners preferred to have these individuals as their nearest neighbours when searching for food. We used a field-based experimental manipulation to investigate whether stressful events impact nearest-neighbour choices, but found no evidence that preferences to forage near strongly bonded groupmates were disrupted or more additionally favoured in the aftermath of a stressful event. Our current work extends understanding of how social bonds can potentially influence within-group behaviour.

Grooming interventions in female rhesus macaques as social niche construction

Social animals invest time and resources into adapting their social environment, which emerges not only from their own but also from the decisions of other group members. Thus, individuals have to monitor interactions between others and potentially decide when and how to interfere to prevent damage to their own investment. These interventions can be subtle, as in the case of affiliative interactions such as grooming, but they can inform us about how animals structure their world and influence other group members. Here, we used interventions into grooming bouts in female rhesus macaques, Macaca mulatta, to determine who intervened in which grooming bouts, and what determined intervention outcomes, based on kinship, dominance rank and affiliative relationships between groomers and (potential) interveners. We show that high dominance rank of groomers reduced the risk of intervention. Bystanders, particularly when high ranking, intervened in grooming of their kin, close affiliates and close-ranked competitors. Interveners gained access to their close affiliates for subsequent grooming. Reduced aggression risk facilitated grooming involving three individuals, which was more common when a strong affiliative relationship existed and when interveners were lower in rank than the groomers. Thus, interventions in this species involved the monitoring of grooming interactions, decision making based on several individual and dyadic characteristics, and potentially allowed individuals to broaden their access to grooming partners, protect their own relationships and influence their social niche.

Familiarity influences social networks in dairy cows after regrouping

Regrouping is common practice when managing dairy cow groups, and it is known to have disruptive effects on behavior and production. The presence of a small group of familiar cows upon regrouping may provide social support and mitigate some of the negative effects. In this study we investigated (1) how regrouping affects social relationships among familiar cows and (2) if cows prefer familiar individuals over unfamiliar ones as social partners after regrouping. We used 3 established groups of cows to create 2 new groups, each containing 14 cows, using subgroups of familiar animals (i.e., 4, 6, and 4 cows) from the original groups. The new groups were similar in respect to the age, parity, and sire of cows. The frequencies of grooming and displacements were determined in the walking alley, lying stalls, and feed bunk by observing 48 h of continuous video before regrouping, directly after regrouping, and 1 wk later. First, social network analysis was applied to investigate the effects of regrouping on the relationships within the subgroups of familiar cows. Second, we determined if familiar cows were more or less connected than would be expected by chance (i.e., assortment), considering displacement, grooming, and feed bunk neighbor networks (derived from electronic feeder data) after regrouping. Regrouping increased the number of displacements, especially in the walking alley. Within the subgroups of familiar cows, regrouping resulted in slightly more displacements, but the network structure did not change. The frequency of grooming among familiar cows remained stable across all observation periods, and the network structure was not affected by regrouping. We found positive assortment in grooming and feed bunk neighbor networks, thereby suggesting that cows preferred familiar individuals as grooming partners and feeding neighbors directly after regrouping and, to a smaller extent, 1 wk later. The effect of familiarity on displacements depended on the pen area. The weak assortment directly after regrouping at the feed bunk indicated that familiar cows displaced each other more than unfamiliar ones, possibly because they were neighbors more often. Our results indicated that a small group of familiar cows may provide ongoing social buffering after regrouping. Further research with multiple groups and larger group sizes is needed to determine whether similar effects are consistently present when groups of familiar cows are subjected to regrouping.

Variable use of polyadic grooming and its effect on access to social partners in wild chimpanzees and bonobos

In mammals, allogrooming is prominent in forming and maintaining social and cooperative relationships. Yet an animal's social time is constrained, which may limit its access to a large number of partners. Dunbar (1993, Behavioral and Brain Sciences, 16 (4), 681–694) proposed that human polyadic conversations, which allow access to several social partners simultaneously, evolved as a form of social grooming to circumvent this time constraint. In nonhuman primates, polyadic grooming (PG), in contrast to dyadic grooming, may similarly be a time-efficient way to maintain weak social relationships with many partners which can be important for group level cooperation. It remains unknown whether PG is used to fulfil specific cooperative needs by accessing numerous weakly bonded partners and increasing the number of partners accessed per unit of time. We compared the use and effect of PG between chimpanzees, Pan troglodytes, which are highly territorial and collaborative (especially males), and bonobos, Pan paniscus, which are less territorial and collaborative and in which females are the main co-operators. We carried out focal grooming observations in one bonobo and two chimpanzee communities in the wild. As predicted, chimpanzees engaged in more PG than bonobos. Surprisingly, males engaged in PG more than females in both species. While chimpanzees accessed more partners per minute of grooming than bonobos via dyadic grooming, PG increased the number of partners accessed per minute only in bonobos. Finally, chimpanzees primarily used PG with individuals who were close in rank and frequent grooming partners, whereas bonobos used PG with individuals who were distant in rank, close party associates and frequent grooming partners. We suggest that bonobo males use PG to enhance conspecific social tolerance and mate choice. The overall higher rate of PG in chimpanzees suggests that between-group competition may promote polyadic affiliation, which possibly reinforces group cohesion and coordination. © 2020 The Authors

Sickness effects on social interactions depend on the type of behaviour and relationship.

Infections can change social behaviour in multiple ways, with profound impacts on pathogen transmission. However, these impacts might depend on the type of behaviour, how sociality as a biological trait is defined (e.g. network degree vs. mean edge strength) and the type of social relationship between the interacting individuals. We used the highly social common vampire bat Desmodus rotundus to test how an immune challenge by lipopolysaccharide (LPS) injections affects two different social behaviours and three alternate measures of sociality, and whether the LPS effect differs by kinship relationship. Effects of sickness should be lower for social behaviours that bestow greater benefits to inclusive fitness, such as food sharing. As predicted, immune-challenged bats experienced a greater reduction in allogrooming received than food sharing received. Sickness effects might also depend on how a social interaction is defined (e.g. the number of grooming partners vs. the duration of grooming events). We predicted that sickness would impact both the number and duration of social encounters, but we only detected a decrease in the number of grooming partners. Finally, sickness effects might vary with social relationship type. We predicted that sickness effects should be smaller for interactions among close kin. As expected, the immune challenge had smaller effects on mother-offspring interactions. In conclusion, our results highlight the need to explicitly consider how the effects of sickness on social network structure can differ depending on the 'who, what, and how' of social interactions, because these factors are likely to influence how sickness behaviour alters pathogen transmission.

Individual behavioral differences and health of golden-headed lion tamarins (Leontopithecus chrysomelas).

Individual behavioral differences may influence how animals cope with altered environments. Depending on their behavioral traits, individuals may thus vary in how their health is affected by environmental conditions. We investigated the relationship between individual behavior of free-living golden-headed lion tamarins (Leontopithecus chrysomelas) responding to a novel object (to assess exploration-avoidance), and their habitat use and health status (endoparasitism; clinical measures: biometric data, heart rate, respiratory frequency, and temperature; fecal glucocorticoid metabolites). As parasite transmission can be affected by individual variation in social contact and social grooming, we also evaluated whether more sociable individuals show higher endoparasite loads compared with less sociable animals. Four groups living in landscapes with different levels of human disturbance were investigated: two in degraded forest fragments in an agricultural matrix (DFAM-higher disturbance), and two in a cocoa agroforestry system (cabruca-lower disturbance) in the Atlantic forest of South Bahia, Brazil. Using a subjective ratings approach, highly correlated adjective descriptors were combined to produce z-score ratings of one derived variable ("confidence"), which was selected to characterize the tamarins' exploration/avoidance responses during a novel object test. The higher the confidence score, the longer female tamarins spent foraging for prey independent of landscape, and the greater their body mass independent of sex and landscape. Only DFAM individuals showed intestinal parasite infection. Endoparasite loads were positively correlated with the number of grooming partners, suggesting an association between social grooming and transmission (more groomers = more endoparasites). Individual behavior, including in a test situation, may thus have some predictive value for behavior in a free-living context, and for its health consequences.

Impact of anthropogenic factors on affiliative behaviors among bonnet macaques

In primates, allogrooming and other affiliative behaviors confer many benefits and may be influenced by many socioecological factors. Of these, the impact of anthropogenic factors remain relatively understudied. Here we ask whether interactions with humans decreased macaques' affiliative behaviors by imposing time-constraints, or increased these behaviors on account of more free-/available-time due to macaques' consumption of high-energy human foods. In Southern India, we collected data on human-macaque and macaque-macaque interactions using focal-animal sampling on two groups of semi-urban bonnet macaques for 11 months. For each macaque within each climatic season, we calculated frequencies of human-macaque interactions, rates of monitoring human activity and foraging on anthropogenic food, dominance ranks, grooming duration, number of unique grooming partners, and frequencies of other affiliative interactions. We found strong evidence for time-constraints on grooming. Macaques that monitored humans more groomed for shorter durations and groomed fewer partners, independent of their group membership, sex, dominance rank, and season. However, monitoring humans had no impact on other affiliative interactions. We found no evidence for the free-time hypothesis: foraging on anthropogenic food was unrelated to grooming and other affiliation. Our results are consistent with recent findings on other urban-dwelling species/populations. Macaques in such environments may be especially reliant on other forms of affiliation that are of short duration (e.g., coalitionary support, lip-smacking) and unaffected by time-constraints. We stress on the importance of evaluating human impact on inter-individual differences in primate/wildlife behavior for conservation efforts.

Sulawesi Crested Macaque (Macaca nigra) Grooming Networks Are Robust to Perturbation While Individual Associations Are More Labile

Social and environmental disturbance occurs naturally, and species in bonded social groups should be resilient to it. Empirical evidence of social responses to disturbance in primates, however, remains limited. We constructed social networks using group-level scan samples (N = 299) to test the robustness of grooming networks in a captive group of 20 Sulawesi crested macaques (Macaca nigra) to two management interventions involving environmental and social disturbance. During the first, the institution removed six castrated males and one female, contracepted six of the nine remaining females, and moved the group to a new enclosure. The second involved the introduction of a novel, reproductive male five weeks later. Networks remained stable following the first intervention. However, after introduction of the male, the number of grooming partners and the frequency of grooming with non-maternal kin increased in female-only networks. We observed less marked increases in the grooming frequency and number of grooming partners in whole group networks. Ten weeks later, network structure was more similar to that of pre-intervention networks than post-intervention networks. Our results suggest that reproductive males play a more important role in structuring Sulawesi crested macaque social networks than castrated males, as networks expanded and relationships between non-maternal kin occurred more frequently after introduction of the reproductive male. However, network responses to interventions appeared to be temporary as networks following a period of acclimation more closely resembled pre-intervention networks than post-intervention networks. Our study demonstrates the utility of social network analysis for understanding the impact of disturbance on stable social groups.

Early life experience and alterations of group composition shape the social grooming networks of former pet and entertainment chimpanzees (Pan troglodytes).

The long-term effects of early life adversities on social capacities have been documented in humans and wild-caught former laboratory chimpanzees (Pan troglodytes). However, former pet and entertainment chimpanzees have received little attention to date. This study aimed to investigate the long-term effects of early life experience on 18 former pet and entertainment chimpanzees, based on social grooming data collected at a primate rescue centre over a 12-year period. Moreover, we also focused on the possible short-term effects that alterations to group composition might have on grooming patterns. For this purpose, we compared stable and unstable periods (i.e. where alterations to group composition occurred). We used two individual social network measures to analyse the grooming activity and the distribution of grooming among group mates for each individual. We could show that wild-caught chimpanzees were significantly more selective regarding their grooming partners and spent less time grooming when compared to their captive born companions. We also found that individuals who were predominantly housed without conspecifics during infancy spent less time grooming compared to those who were predominantly housed with conspecifics during infancy. Furthermore, we found that alterations to the group composition had short-term effects on the distribution of social grooming from a more equal distribution during periods with a stable group composition towards a more unequal and selective distribution during unstable periods. Thus, we conclude that the social grooming networks of former pet and entertainment chimpanzees are shaped not only by long-term effects such as early life experience, but also by short-term effects such as alterations to group composition. Remarkably, we found not only captive born chimpanzees but also wild-caught individuals to adjust their grooming to socially challenging situations by modifying their grooming distribution in a similar way.