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Individual and social behavioral responses to injury in wild toque macaques (Macaca Sinica)

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Abstract

Toque macaques (Macaca sinica),inhabiting natural forest at Polonnaruwa, Sri Lanka, are frequently injured in fights with conspecifics. The behavior of known individuals when they were injured was compared to that after they had recovered their health. Thus, injured animals rested and alloand autogroomed more, but they foraged less and initiated fewer aggressive episodes. They spent most time being sedentary in the safety of arboreal refuges and reduced acrobatic movements by locomoting more often terrestrially. Other group members showed no special tolerance (or altruism) toward injury victims during the costly and highly competitive activity of foraging for food. In fact, some injured animals received more aggression, or lost dominance rank, and thereby had their competitive abilities further impaired. Care for the injured was manifest mostly by grooming and wound cleaning. All hair in the area surrounding a wound, as well as dirt, scabs, and fly larvae, were removed, and saliva was applied by licking the wound (wounds so treated healed with no obvious signs of infection). (1) Injured macaques sought and received significantly more grooming (owing to wound care); (2) the amount so received increased with the severity of the injury; and (3) the initiative of other group members often compensated for a victim’s inability to solicit care. Juvenile males were especially attentive to injured adult males, suggesting that they were investing in a social bond with these adults, which might reciprocate altruism toward their juvenile caregivers in the future. Injured juvenile females received most care from their mothers.
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... Injury is common in free-living primates from conflict, falls, predator attacks and environmental hazards such as snares. Postinjury, effective adaptation to feeding and locomotion seems to be the norm, with some reduced activity and avoidance of conflict [80,81], but few interpretations of behaviour in terms of pain. Such adaptation is not incompatible with pain; in species where rank determines access to food and mating, showing vulnerability could be seriously disadvantageous. ...
... Among adult primates, there is very little evidence of directed care, other than social grooming, with release of oxytocin and endorphins associated with reward and with analgesia [103]. Wounded individuals, in particular their wounds, may receive extra grooming that reduces risk of infection [80,81], and in captive and free-living populations, adults sometimes comfort and protect dying individuals (e.g. [104,105]); the contribution of pain recognition is unknown. ...
Article
Evolutionary models of chronic pain are relatively undeveloped, but mainly concern dysregulation of an efficient acute defence, or false alarm. Here, a third possibility, mismatch with the modern environment, is examined. In ancestral human and free-living animal environments, survival needs urge a return to activity during recovery, despite pain, but modern environments allow humans and domesticated animals prolonged inactivity after injury. This review uses the research literature to compare humans and other mammals, who share pain neurophysiology, on risk factors for pain persistence, behaviours associated with pain, and responses of conspecifics to behaviours. The mammal populations studied are mainly laboratory rodents in pain research, and farm and companion animals in veterinary research, with observations of captive and free-living primates. Beyond farm animals and rodent models, there is virtually no evidence of chronic pain in other mammals. Since evidence is sparse, it is hard to conclude that it does not occur, but its apparent absence is compatible with the mismatch hypothesis. This article is part of the Theo Murphy meeting issue ‘Evolution of mechanisms and behaviour important for pain’.
... Chapman et al., 2009;Godfrey et al., 2006). Studies of house finches (Carpodacus mexicanus) and Toque macaques (Macaca sinica) have shown that healthy individuals can change their behaviour in the presence of sick or injured group members (Bouwman and Hawley, 2010;Dittus and Ratnayeke, 1989). Additionally, higher ranked individuals can afford to engage in sickness behaviours, while subordinates might be motivated to conceal their sickness in order to maintain their rank (Cohn and de Sá-Rocha, 2006;Fairbanks and Hawley, 2012;Lopes, 2014). ...
... Individual goats within this study were not able to defend their dominance status throughout non-FMD sicknesses and decreased in their rank, suggesting that other individuals took advantage of their weakness. Similarly, in wild Toque macaques injured individuals not only started less aggressive encounters during the recovery phase, but also often received more aggression and lost dominance rank (Dittus and Ratnayeke, 1989). In this study, the infection with FMDV did not influence the dominance rank of individual goats, and therefore this is not an adequate behavioural marker for an early detection of FMDV infections in goats. ...
Article
Infectious diseases and parasitic infestations can cause a set of non-specific clinical signs, such as increased body temperature and resting, and a decrease in food intake. These physiological and behavioural changes have an adaptive function facilitating defences against the pathogen and to support immune functions. These so-called' sickness behaviours' can also be used as an early detection tool for disease. Foot-and-mouth disease (FMD) still causes great economic losses in endemic countries, especially to smallholder farmers. The aim of this study was to determine if behavioural changes in goats can be used as an early indicator of FMD virus (FMDV) infection. The efficacy of a Southern African Territories (SAT) FMD vaccine was studied on forty South African indigenous goats. Changes in daily activities (resting, feeding, walking), as well as social behaviours (social resting, social feeding, dominance behaviours) were recorded and then compared over time and between clinically affected and unaffected goats. Pedometers were used to estimate average daily steps and to compare between groups of study animals. Eleven goats developed clinical signs of FMD, as well as non-FMD related sicknesses during the course of the study. Overall walking and resting behaviours were not significantly affected by the presence of FMD related clinical signs (p > 0.05). However, during the time of FMDV infection, social resting increased significantly (p < 0.001). Although goats developed FMD lesions on lips and tongues, percentage of time feeding was not affected (p = 0.762), suggesting that the study goats did not perceive the oral lesions as an important disturbance. Similarly, the number of steps did not consistently decrease in the presence of FMD-associated foot lesions. When affected by non-FMD related sicknesses, animals did not have an overall reduction in the time spent feeding (p = 0.867). However, goats affected with non-FMD conditions reduced the amount of social feeding (p = 0.002), potentially avoiding energetically costly competition at the feeding points. Overall, goats affected with FMD did not show more sickness behaviour, suggesting that FMDV infection in goats might not lead to obvious and therefore, easily detectable behavioural changes. This might have implications for farmers and animal health personnel, as individual goats infected with FMDV might be undetected within a flock due to the absence of obvious sickness behaviours, and the virus can therefore be spread more easily between herds through animal movements.
... Still, injuries occur in many species and often result from contests over valuable resources (Riechert 1998), such as mates (Clutton-Brock et al. 1979;Drews 1996), group membership (Crockett and Pope 1988;Soulsbury et al. 2008;MacCormick et al. 2012), or territory (Palombit 1993;Mosser and Packer 2009). Importantly, injuries are energetically expensive and can lead to reduced food intake, declines in rank position (Dittus and Ratnayeke 1989), trade-offs between healing and reproduction (French et al. 2009;Archie et al. 2014;Harris et al. 2018), fitness costs via hampered locomotion, and even death (Chilvers et al. 2005;Campbell 2006). Thus, when and why do escalations and injuries occur? ...
... Thus, further investigation of injuries in other species is necessary to associate the occurrence or severity of injury to measures of fitness, such as dispersal outcomes, mating success, or survival. Moreover, studying these phenomena in individualistic hierarchies, in which asymmetries may be less reliably assessed and injuries more prevalent, may be useful, particularly as injuries may influence future contests (primates: Franz et al. 2015;spiders: Taylor et al. 2003), rapidly precipitate rank changes (Dittus and Ratnayeke 1989;Marty et al. 2016), and generate long-term fitness deficits. ...
Article
Aggression rarely escalates to physical conflict because doing so puts individuals at risk of injury. Escalation only pays off when the potential benefits outweigh the potential costs, that is, when resources critical to fitness are at stake. Here, we investigated the occurrence of injury in 2 Asian colobine species: Nepal gray langurs (Semnopithecus schistaceus) and Phayre’s leaf monkeys (Trachypithecus phayrei crepusculus). In both species, younger individuals are higher-ranking and might have greater incentive to fight. However, Nepal gray langurs have a strict breeding season, which may magnify male mating competition, and Phayre’s leaf monkeys, unlike Nepal gray langurs, have female-biased dispersal, which may increase female injury risk during subadulthood. Using long-term data on observed injuries (Nepal gray langurs: n = 208; Phayre’s leaf monkeys: n = 225), we modeled the monthly occurrence of injury (Y/N) and found that males received more injuries than females in both species. Also, subadults generally experienced frequent injury, as young individuals likely face challenges when competing for group membership and/or establishing rank. In Nepal gray langurs, males received 3 times more injuries during the mating season, suggesting strong competition for mates during this period, and females experienced more injuries before conception, suggesting competition to meet the nutritional requirements for reproduction. Unexpectedly, females in smaller groups received more injuries in Nepal gray langurs. Overall, these results indicate that injuries are most likely when fighting may aid in establishing group membership, achieving high rank, and reproducing. Future research should investigate the influence of injuries on fitness outcomes.
... Indeed, one female received two near-fatal early-life injuries, exhibited permanent locomotor impairments, and did not mature until 88.4 months-the oldest age at maturation observed in this population by over one year. Repairing such wounds likely shunts resources away from growth and reproduction, and these deficits could be exacerbated if associated locomotor difficulties hamper foraging or alter dominance trajectories (Dittus and Ratnayeke 1989). ...
Article
Female reproductive maturation is a critical life-history milestone, initiating an individual's reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more "classic" socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas-a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to "faster" development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.
... Indeed, one female received two near-fatal early-life injuries, exhibited permanent locomotor impairments, and did not mature until 88.4 months-the oldest age at maturation observed in this population by over one year. Repairing such wounds likely shunts resources away from growth and reproduction, and these deficits could be exacerbated if associated locomotor difficulties hamper foraging or alter dominance trajectories (Dittus and Ratnayeke 1989). ...
Article
Female reproductive maturation is a critical life-history milestone, initiating an individual's reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more "classic" socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas-a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to "faster" development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.
... In addition, macaques are also listed in Appendix II of CITES (Convention on International Trade in Endangered Species) that includes species not necessarily threatened with extinction (CITES, 2005). Even though there are reports on the health, behaviour, and ecology of toque macaques (Dittus, 1984(Dittus, , 1986Dittus and Ratnayeke, 1989;Keane et al., 1997;Weerasekara et al., 2021), parasite diversity of these animals is not well studied. A single study was reported on the macaque populations across the country, representing the three subspecies while others were mainly focused on macaques inhabiting specific regions, i.e Polonnaruwa (M. ...
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Full-text available
Understanding variations in host-parasite relationships with urbanization is vital for both, public health management and conservation of endemic animals with high anthropogenic interactions. Toque macaques (Macaca sinica) are such endemic old-world monkeys in Sri Lanka. Three macaque sub species inhabit the main climatic zones of the island; M. s. sinica, M. s. aurifrons and M. s. opisthomelas inhabit the dry zone, wet zone, and montane regions of the island, respectively. This study aimed to examine parasite prevalence in this host in association with urbanization. A total of 180 fecal samples were collected from the three sub species of toque macaques inhabiting the main climatic zones (dry, wet, and montane) in Sri Lanka; 20 samples each were collected from urban, suburban, and wild populations representing each climatic zone. Twenty gastrointestinal (GI) parasite genera types i.e. five types of protozoan cysts, two types of trematode ova, four types of cestode ova, eight types of nematode ova, and a single type of acanthocephalan ova were identified. The overall prevalence of parasites was 62% (112/180) with the highest prevalence of Strongyloides infection. In all three sub species, toque macaque populations with proximity to human settlements, including urban and suburban populations, manifested a greater GI parasitic prevalence, mean ova/cyst counts and species richness, compared to their wild counterparts. Importantly, records of five parasite types in toques in Sri Lanka are reported for the first time, while Moniliformis type was reported as a first record in free ranging macaques, globally. This study clearly demonstrated that human contact and habitat modification may influence patterns of parasitic infections in macaques. As most of the parasite types identified manifest zoonotic potential, with public health implications, close associations of macaques may cause a threat to human well-being.
... We would generally expect infected individuals to be avoided by conspecifics (Müller-Klein et al. 2019b), and it remains unclear if this relationship is due to juveniles seeking out these males as grooming partners or if their immaturity makes them lower value grooming partners who are more likely to respond positively to grooming invitations from males with activated immune systems. Increased investment by groupmates toward immune activated individuals has been observed in the context of injury (Simonds 1965;Dittus and Ratnayeke 1989); however, this is the first study to our knowledge demonstrating a relationship between non-injury-related immune activation and increased grooming in a non-human primate. Additionally, the proportion of time spent engaged in any direction of grooming (total grooming) had a marginal positive effect on uNEO concentrations. ...
Article
Full-text available
Social interactions are well known to influence fitness in social animals, but the physiological processes that connect the two remain largely unknown. This study aimed to explore how variation in sociality influences the adrenocortical and/or immune system in the rhesus macaque, a seasonally breeding species engaging in indirect male-male mating competition. We collected data on 18 adult male rhesus macaques living on Cayo Santiago over 4 months during the mating season. We assessed fecal glucocorticoids (fGCs), a marker of the physiological stress response, and urinary neopterin (uNEO), a marker of immune system activation. We predicted that males who spent more time affiliated with groupmates would have decreased fGCs due to the physiological buffering potential of positive social interaction and increased uNEO associated with increased exposure to disease. Additionally, we predicted that uNEO would increase in response to copulation, consortship, and as the mating season progressed due to infection associated with sexual behavior. Although none of our sociosexual behaviors of interest predicted fGCs, the proportion of time males spent grooming, and specifically the proportion of time males spent receiving grooming from juveniles, was positively associated with concurrent uNEO concentrations. Copulation was negatively correlated with concurrent uNEO, and uNEO, but not fGCs, increased as the mating season progressed. These results indicate that certain social behaviors are associated with immune system activation and provide a putative physiological link between the physical demands of endurance rivalry and mortality commonly observed in males of this species. Significance statement Social interactions can strongly influence health in social animals, possibly mediated through the endocrine and/or immune system. We investigated how affiliative social and sexual interactions influence these systems in male rhesus macaques by non-invasively measuring hormones associated with energy allocation and responses to stressors (glucocorticoids) and a marker of immune system activation (neopterin). The sociosexual behaviors measured here did not appear to covary with glucocorticoid concentrations; however, higher neopterin concentrations were observed when males spent more time grooming. We also found that males spent less time copulating when their neopterin concentrations were high and that there is a general increase in neopterin concentrations as the mating season progresses. Our results show that variation in social and sexual behavior is associated with neopterin production in the rhesus macaque, suggesting that social investment by groupmates and disease transmission may be important factors mediating the relationship between sociality and fitness in social species.
... Empathetic responses to others in distress can either be based on the sufferer's behavioral expressions, such as screaming or distressed facial expressions, or contextual cues, such as injury or inability to escape from a trap (Goubert et al. 2005(Goubert et al. , 2009. A variety of species have been reported to show affiliation to injured conspecifics after fights or accidents (e.g., monkeys: Campbell et al. 2016;Clyvia et al. 2014;Dittus and Ratnayeke 1989;dolphins: Warren-Smith and Dunn 2006;elephants: Douglas-Hamilton et al. 2006). Chimpanzees are one of the species in which this behavior has been most frequently documented. ...
Article
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Previous studies have shown that humans experience negative emotions when seeing contextual cues of others’ pain, such as injury (i.e., empathic pain), even without observing behavioral expressions of distress. However, this phenomenon has not been examined in nonhuman primates. We tested six chimpanzees (Pan troglodytes) to experimentally examine their reactions to others’ injury. First, we measured viewing responses using eye-tracking. Chimpanzees spontaneously attended to injured conspecifics more than non-injured conspecifics, but did not do so in a control condition in which images of injuries were scrambled while maintaining color information. Chimpanzees did not avoid viewing injuries at any point during stimulus presentation. Second, we used thermal imaging to investigate chimpanzees’ physiological responses to others’ injury. Previous studies reported that reduced nasal temperature is a characteristic of arousal, particularly arousal associated with negative valence. We presented chimpanzees with a realistic injury: a familiar human experimenter with a prosthetic wound and artificial running blood. Chimpanzees exhibited a greater nasal temperature reduction in response to injury compared with the control stimulus. Finally, chimpanzees were presented with a familiar experimenter who stabbed their (fake) thumb with a needle, with no running blood, a situation that may be more challenging in terms of understanding the cause of distress. Chimpanzees did not physiologically distinguish this condition from the control condition. These results suggest that chimpanzees inspect others’ injuries and become aroused by seeing injuries even without observing behavioral cues, but have difficulty doing so without explicit (or familiar) cues (i.e., open wound and blood).
... When cutaneous wounds fail to heal, animals can experience high risk of infection [2,3]. Moreover, injuries can affect reproductive activities, increase predation risk, and decrease feeding opportunities in wild vertebrates such as lizards [6], bats [7], red deer [8,9], and primates [10][11][12]. a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 ...
Article
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Wound healing in animals is important to minimize the fitness costs of infection. Logically, a longer healing time is associated with higher risk of infection and higher energy loss. In wild mammals, wounds caused by aggressive intraspecific interactions can potentially have lethal repercussions. Clarifying wounding rate and healing time is therefore important for measuring the severity of the attacks. In addition, impact of secondary damage of wounds (e.g., accidental peeling off of scabs) on heeling time is unknown despite the risk of infection in wild mammals. In baboons, most male injuries have been reported to result from male to male fights. Here, we investigated the relationship between wound size and healing time in wild anubis baboons to clarify the healing cost of physical attacks including secondary damage of wounds. Observations were conducted daily between August 2016 and July 2017 in Kenya for seven adult male anubis baboons. The individual wound rate was one per month on average. In 16 cases, we were able to assess the number of days required for wound healing, and the median healing time was 13 d. Wound healing time was longer for larger wounds. When the scab was peeled off accidentally because of external factors, healing time became longer. One of the causes of scabs’ peeling off was baboons’ scab-picking behavior, and the behaviour was considered self-injurious behavior. However, its predicted healing cost might not be high. We concluded that wounds less than 800 mm² (the largest observed in this study) in baboon males have little effect on survival. Our results suggest that lethal wounds by physical attacks rarely occur in male baboons, and that healing time and delay caused by secondary damages can be estimated by measuring wound area.
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Caring for others is a key feature of human behavior. Mothers, fathers, siblings, grandparents, and other group members provide care in the form of provisioning, protection, and first aid. To what extent is other-regarding behavior present in our primate relatives? Here we describe an unusual incident of other-regarding behavior toward an injured juvenile female chimpanzee (Pan troglodytes schweinfurthii) at Ngogo in Kibale National Park, Uganda. After the juvenile received a mild head wound from an adult female, several adolescent and juvenile chimpanzees gathered to touch, lick, and peer at the wound. One adolescent male wiped a leaf across the cut. Another adolescent male later groomed the injured female and briefly carried her. Across a 5-year period, we observed only three other instances of other-directed wound care in chimpanzees, occurring in 4% (4/100) of cases in which we observed individuals with fresh wounds, and 57 other instances of allomaternal carrying. Despite the infrequency of such behaviors, our study adds another chimpanzee field site to the list of those where other-directed wound care has been observed. Observations from wild chimpanzees provide insight into empathy and may inform our understanding of the evolution of other-regarding behavior in humans.
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Semi-evergreen forests cover the dry zone plains of Sri Lanka and constitute four-fifths of the island's vegetation. In a sample area of 3 km2, in the Polonnaruwa Sanctuary, 63 tree species were found; 46 were characteristic of other dry zone forests, and 17 occurred only under special edaphic and biotic conditions. As in other dry zone forests, Drypetes sepiara (Euphorbiaceae) prevailed with a relative density of 21.3 percent. The Shannon index of diversity was 4.23 bits per individual, of which 79.4 percent was attributable to evenness; most species had few individuals. Dominance was shared between species typical of the subcanopy and canopy. Measures of diversity and of dominance between species placed the semi-evergreen community in Polonnaruwa as a type intermediate between tropical rainforest and deciduous monsoon forest. Measures of diameters (DBH) and estimates of the height of trees indicated that all species with typically very large trees had few individuals that were distributed more or less evenly through all the size classes. Typically smaller species had large numerical representation. These facts are discussed in light of dominance relationships and regenerative patterns in the community, and are related to possible evolutionary trends. The distribution of most species was clumped, but that of certain rare species was random. Clumping at 2,500 m2 plot size usually meant clumping at smaller-sized plots. Clumping on a large scale reflected local differences in species dominance. Five shrub associations were distinguished by density and constitute dominant and co-dominant species. Differences were related to the amount of light penetrating through the tree canopy and to edaphic factors. Glycosmis pentaphylla (Rutaceae) was the dominant shrub species in the climax association which flourished under a fairly closed tree canopy and lacked an herbaceous layer.
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1. Two independent groups of toque macaques (Macaca sinica) fused into one larger cohesive group. The groups were part of a population of 18 to 22 groups that inhabit natural forest at Polonnaruwa, Sri Lanka, and that had been observed more or less continuously from 1968 to 1985. 2. The group fusion generally supports WRANGHAM'S (1980) model of the evolution of group living and female residence patterns in