ArticlePDF Available

Allogrooming as tension-reduction mechanism: A behavioural approach

Authors:

Abstract

The hypothesis that allogrooming functions as a tension-reduction mechanism was tested. Tension was measured by the frequency of displacement activities by an animal. Two adult male and 11 adult female Java (or long-tailed) monkeys (Macaca fascicularis) that were relatively unfamiliar with each other were paired 1 hour per day for five consecutive days during the periovulatory portion of the menstrual cycle. Female allogrooming was found to reduce the frequency of male displacement activities both during the course of interaction and outside it, and this decrease was proportional to the amount of allogrooming received. Female allogrooming did not, however, exert long-lasting effects on the frequency of female displacement activities. An increase in the frequency of male displacement activities was recorded during the 10-second interval immediately after the end of the female allogrooming bouts. Neither postinhibitory rebound nor frustration owing to the cessation of a pleasant situation, i.e., the two advanced explanatory hypotheses, accounted for this increase. The results of the present study concur with physiological findings that support the tension-reduction hypothesis. The social function of allogrooming appears quite important and is entirely compatible with the functional hypothesis that emphasizes hygiene.
... According to the primate experts at the park, if the monkeys perceived the UAV as a threat, they would have fled toward the wooded areas of the enclosure, ascended into the trees and mothers would have drawn juveniles close to them. Additionally, alarm calls would have been vocalized, individuals would have shown increased vigilance, and/ or the monkeys would have started to show stress behavior such as autogrooming, scratching, yawning, and/or shaking while repeatedly focusing on the stressor and after the stressor was gone (post-conflict reactions) (Kutsukake & Castles, 2001;Schino et al., 1988). A trained observer from the facility was situated within the park to assess whether the monkeys reacted to flights conducted at 120 m altitudes with a Leica Aibot AX20 hexacopter that emits a loud buzzing sound in-flight. ...
Article
Full-text available
An important component of wildlife management and conservation is monitoring the health and population size of wildlife species. Monitoring the population size of an animal group can inform researchers of habitat use, potential changes in habitat and resulting behavioral adaptations, individual health, and the effectiveness of conservation efforts. Arboreal monkeys are difficult to monitor as their habitat is often poorly accessible and most monkey species have some degree of camouflage, making them hard to observe in and below the tree canopy. Surveys conducted using uninhabited aerial vehicles (UAVs) equipped with thermal infrared (TIR) cameras can help overcome these limitations by flying above the canopy and using the contrast between the warm body temperature of the monkeys and the cooler background vegetation, reducing issues with impassable terrain and animal camouflage. We evaluated the technical and procedural elements associated with conducting UAV-TIR surveys for arboreal and terrestrial macaque species. Primary imaging missions and analyses were conducted over a monkey park housing approximately 160 semi-free-ranging Japanese macaques (Macaca fuscata). We demonstrate Repeat Station Imaging (RSI) procedures using co-registered TIR image pairs facilitate the use of image differencing to detect targets that were moving during rapid sequence imaging passes. We also show that 3D point clouds may be generated from highly overlapping UAV-TIR image sets in a forested setting using structure from motion (SfM) image processing techniques. A point cloud showing area-wide elevation values was generated from TIR imagery, but it lacked sufficient point density to reliably determine the 3D locations of monkeys.
... Receiving grooming likely has a calming effect as it reduces heart rate [9] and behavioral indicators of anxiety [10]. It also provides a pleasant sensation associated with beta endorphin release [11]. ...
Article
Recent findings have shown that the neurophysiological mechanisms involved in human massage and caress are similar to those involved in grooming of nonhuman primates. In contrast, little is known about the neurophysiological mechanisms of brief touch in both human and other primates. Here we review evidence for brief touch in nonhuman primates and contrast its patterns and potential functions with those better known of grooming. We show that brief touch is not an affiliative behavior as it functions to assess the competitive tendencies of unfamiliar individuals and former opponents, to test the state of a social relationship and to signal benign intent. Thus, brief touch plays an important role, complementary to that of grooming, in the regulation of social relationships.
... SI did result in changes in social behavior. Similar to adults, rates of social grooming in the peer group significantly increased (i.e., the frequency tripled) during SI, potentially as a coping mechanism (Engh et al., 2006b;Schino et al., 1988;Wooddell et al., 2016), whereas rates of social play significantly decreased (e.g., the frequency nearly halved), possibly due in part to the risky nature of social play interactions (Paquette, 1994), which may be further escalated during a new group formation. However, individuals' social network positions (measured via EC) were rather stable across the study. ...
Article
Social instability (SI) occurs when there is competition over social status. Reduced certainty of social status can lead to heightened aggression, which can increase physiological stress responses as individuals prepare to fight for their social status. However, adults can use proactive coping mechanisms to reduce the physiological stress induced by SI, such as increasing affiliation. Very little is known, however, about the behavioral and hormonal effects of SI early in development. Filling these gaps in knowledge would add to the fields of primatology and developmental and comparative psychology. We conducted an opportunistic study of a peer group of 18 rhesus macaque (Macaca mulatta) yearlings before and during SI. We used social network analysis to measure individuals’ dominance certainty (DC; in their aggressive and submissive network) and their position in affiliative networks (grooming and play) and analyzed hair cortisol concentrations (HCCs). As predicted, during SI, we observed a decrease in DC, indicating that individuals had less stable dominance positions. As well, during SI, we observed increased rates of social grooming and decreased rates of social play, reflecting potential coping mechanisms. More socially connected individuals in social grooming and social play networks received higher levels of coalitionary support. Contrary to predictions, DC did not predict HCCs; rather, individuals that were more connected in the social play network exhibited smaller increases in HCCs during SI, revealing a potential buffering effect of social play. Our results underscore the need for further research on the effects of SI during ontogeny.
... We collected data using the Prim8 behavioural software (McDonald and Johnson 2014) on a handheld Lenovo tablet. During focal observations, we recorded all instances of self-directed behaviour, including self-scratch, self-groom, and self-touch behaviours (Schino et al. 1988;Castles, Whiten, and Aureli 1999). We calculated the number of bouts performed per focal observation and converted this to a frequency as in previous studies (Castles, Whiten, and Aureli 1999;Sclafani et al. 2012). ...
Article
Full-text available
The urban landscape is a complex mosaic of costs and benefits for urban wildlife. Although many species may adapt and thrive in the urban mosaic, the complexity of this landscape can be stressful and have health implications for urban wildlife, raising concerns for zoonosis and biodiversity. In this study, we assessed how human–primate interactions influenced parasite risk and anxiety-related behaviour of urban vervet monkeys in KwaZulu-Natal, South Africa. Over 1 year, we collected and analysed faecal samples, assessing eggs per gram, species richness, and Shannon’s diversity index. In addition, using behavioural sampling, we recorded self-directed scratching behaviour, as an indicator of anxiety, and human–primate interactions, both positive (human-food consumption) and negative (human–monkey aggression). To assess parasite risk in the urban mosaic, we ran three models with our parasite measures as dependent variables. Results showed that negative human interactions significantly increased with eggs per gram, species richness, and Shannon’s diversity index and positive human interactions increased with both eggs per gram and species richness. Furthermore, eggs per gram significantly increased with higher scratching rate. We also tested the relationship between scratching and human interactions, finding that scratching significantly increased under higher rates of negative human incidents. Overall, results suggest that there are costs to urban living that increase anxiety-related behaviour and parasite risk despite increased food availability. Our findings are important for developing effective management strategies that focus on cohabitation rather than conflict, for the benefit of human and wildlife health.
... In addition to its hygienic function, a vast body of work has shown that social grooming also serves numerous social functions, including close access to dominant individuals (Seyfarth, 1980), social bonding (Silk, 2002), tension reduction (Aureli et al., 1999;Schino et al., 1988;Terry, 1970) and reconciliation (Koyama, 2001;Palagi et al., 2008). As such, it is plausible to hypothesize that social characteristics may also play a role in influencing grooming site selection (Allanic et al., 2020a;Boccia et al., 1982). ...
Article
When primates groom each other, they tend to concentrate on those parts of the body they cannot efficiently self-groom (i.e., not visually accessible), and prefer to intensify grooming in areas with high hair density, thus suggesting a hygienic function. However, preferences for some body sites over others during social grooming may also result from different degrees of social bonding and relative dominance. To assess the relative importance of physical (hygienic) and social factors, we examined grooming interactions in two groups of wild black capuchin monkeys (Sapajus nigritus) during 15 nonconsecutive months. We evaluated the distribution of social grooming across body sites according to their accessibility by self-grooming and hair density. At the same time, we assessed whether the degree of dyadic social bonding affects the relative body orientation between groomer and groomee and the access to vulnerable body sites (e.g., face, throat, groin) during grooming. As expected, capuchins preferentially groomed inaccessible body sites (e.g., back and head), with a disproportionate effort directed to the tufts of their partners. We found that dyadic social bond strength, together with rank distance, significantly affected the proportion of grooming in ventro-ventral body relative orientation only in dominant-subordinate groomer-groomee dyads. This may indicate that, when two individuals differ in rank but are strongly bonded, the level of uncertainty related to the social context is already resolved and thus grooming per se is no longer perceived by the subordinate as an uncertain/risky situation. We found no effect of social bonding on grooming vulnerable body sites for any type of dyad. Our findings suggest that grooming site preferences in black capuchin monkeys simultaneously reflect hygienic and social functions.
... more than groomed any other individual. Allogrooming rate is frequently positively correlated to dominance and kinship in primates and some ungulates (Schino et al., 1988;Dunbar, 1991;Mooring et al., 2004). Our results show that it may also be the case in T. setosus. ...
Article
Full-text available
Behavior is a useful trait for comparative studies that provide the comprehension of phylogenetic relationships among species. Here, we present a description of two spiny-rats species' behavioral repertoire, Clyomys laticeps and Trinomys setosus (Rodentia: Echimyidae). The affiliative and agonistic behavioral patterns were sampled during a three-year study of captive populations of wild animals. Observational data were collected in two phases under different arrangements of individuals in groups. We also compare the behavioral traits of T. setosus and C. laticeps with the known behavioral patterns of Trinomys yonenagae. We add categories to the previous descriptions of T. setosus and a standard ethogram for C. laticeps. Trinomys setosus showed a visual and vocal display we called foot-trembling, which was not described in this form and function for other species studied until now. We discuss the differences in their sociality levels and similarities and differences among behavior patterns and repertoires.
... That paired individuals continue to allopreen following their reunion at the beginning of the season and throughout breeding raises the prospect that allopreening may function to encourage or facilitate parental care. Whereas some evidence from other species points to mechanistic explanations for how this could operate, for example by stimulating the production of hormones such as oxytocin or prolactin (Keverne et al. 1989), or by reducing stress levels (Schino et al. 1988), functional hypotheses have been less well explored, particularly in birds. ...
Article
Full-text available
The functions of display between breeding pairs of animals have been given little attention outside of sexual selection. Yet evidence suggests that display between partners is in fact most commonly observed following mate choice, and is often just as elaborate. In many bird species, allopreening, when one member of a pair preens the other, is a major component of display both pre‐ and post‐pair formation. Despite this, there has been little investigation into its functions. Explanations that have been put forward tend to focus on its role in feather hygiene, which has limited phylogenetic support, or its function in the maintenance of the pair bond, though how this might occur or indeed what this actually represents has not been adequately explained. Phylogenetic evidence reveals that allopreening is most commonly observed in those species exhibiting high levels of partner retention and biparental care, and it appears to be functional in maintaining cooperation in parental behaviour in at least one species. In our observational study, we explored the patterns and putative functions of allopreening during the nest‐relief displays of breeding pairs of Black‐browed Albatrosses Thalassarche melanophris during incubation and chick‐provisioning. Allopreening was an important feature of displays, constituting 30% of display time. We found that the bird returning from its foraging trip usually initiated allopreening, and preened more than its partner prior to change‐over of nesting duties. We further found a positive relationship between the amount of time the pair spent in display and the duration of the subsequent foraging trip, providing tentative support for a function in maintaining cooperative parental behaviour between the parents. Although we cannot be conclusive as to its exact functions, we add to a limited literature the first exploration of functions for this conspicuous behaviour in albatrosses.
Article
Background: The aim of this work was to identify gram-positive bacteria and their respective resistance profiles of free-living capuchin monkeys. Methods: For this, 15 Sapajus nigritus were captured in a municipal urban park in the northern region of the state of Paraná, Brazil, and under pharmacological restraint, samples were collected with sterile swabs from the oral, rectal, ocular, nasal, and auricular regions. After isolation of the 22 gram-positive bacteria, each isolate was subjected to the catalase and coagulase tests for presumptive identification. Subsequently, phenotypic tests for bacterial resistance were performed using the agar diffusion disc method. The samples resistant to oxacillin were submitted to the PCR technique to search for the mecA gene. Results: Of the 22 gram-positive cocci of these two (9.09%) are Streptococcus spp. and twenty (90.91%) Staphylococcus spp. Among Staphylococcus spp. three (13.64%) were coagulate-negative (CoNS) and seventeen (86.36%) coagulate-positive (CoPS). Of the antimicrobials tested, enrofloxacin had the best performance, with only one (04.54%) isolate resistant to it, on the other hand, the antimicrobials with the lowest performance were cefotaxime and penicillin with 19 (82.36%) and 18 (81.81%) resistant isolates, respectively. Only five isolates had MAR less than 0.2, being one ocular, one oral, and three nasal, they had multiple resistance index varied between 0.07 and 0.92, with an average of 0.45 and a mode of 0.3. Among the samples with the highest resistance index, a positive coagulase Staphylococcus stood out, being intermediate to gentamicin and resistant to other antibiotics and an intermediate streptococcus to gentamicin, enrofloxacin, and resistant to other antibiotics. No sample was positive to mecA gene. Conclusions: Future studies should be conducted to identify the Staphylococcus species, the high rate of antimicrobial resistance of the monkeys in this study suggests that Grooming's behavior may be contributing to the sharing of the resistant microorganism among the members of this group of primates.
Article
Emotional contagion refers to the mechanism of aligning with conspecifics' emotional states and is thought to be highly beneficial in social group living. While emotional contagion is well studied in humans, most studies in nonhuman animals fail to clearly distinguish between behavioural and emotional contagion. Furthermore, evidence for positive emotional contagion in nonhuman animals is almost entirely restricted to the context of play. In the present study, we aimed at adding observational evidence of contagion in a positive context, while separating aspects of behavioural and emotional contagion. In a group of nonbreeder common ravens, Corvus corax, we investigated whether witnessing conspecifics in positive social interaction, namely allopreening, would influence a bystander's behavioural and, possibly, emotional state. We recorded behavioural expressions of bystanders in postpreening observation phases and compared them to those in matched-control observation phases. We found effects of witnessing others' allopreening on the bystanders' subsequent affiliative interactions but not on their self-directed behaviours (e.g. autopreening) or agonistic interactions. Specifically, bystanders were more likely to engage in allopreening themselves in the postpreening observation phase than in the matched-control observation phase, which could be explained via behavioural and emotional contagion; however, bystanders also showed elevated levels of nonpreening affiliative interactions and spent more time close to conspecifics after observing others allopreening, which hints towards a more general effect on the bystanders' emotional states. Whether these nonpreening affiliative interactions are indeed an indication of emotional contagion needs to be tested in further studies that measure, and manipulate, emotional states.
Article
In human and nonhuman primates eye-to-eye contact (EEC), a face-to-face communication component, can promote emotional/attentional engagement and prolong affiliative interactions. Owing to its direct impact on fitness, the reproductive context is perhaps the most critical context for investigating EEC's importance. However, the presence of this phenomenon around mating and its functions in primates is still understudied. In this work, we investigated whether EEC was present during copulations and influenced the copula duration and postcopulation grooming occurrence in the wild gelada, Theropithecus gelada, an Old World monkey species. We found that the previous presence of the male ‘look-at’ triggered the female ‘look-at’. Moreover, copulations were most likely to last longer in the presence of EEC. In addition, the occurrence of postcopulation grooming between partners, most frequently initiated by females, increased when copulations included EEC. Females' engagement in EEC with the male may be a form of continuation of female precopulatory proceptivity and facilitate males' copulatory activity. By prolonging sexual contacts, EEC may also increase the chances of ejaculation. By grooming their partners after mating, female geladas may attempt to reduce male arousal and prolong the social interaction with them, possibly strengthening their social bond. These results provide the first quantitative evidence that EEC is an effective mechanism for prolonging mating interactions and enhancing postmating affiliation in a Papionini species. On a broader perspective, the presence of EEC in an Old World monkey species suggests that EEC may have been favoured by natural selection to promote reproductive advantages during human evolution.
Article
Full-text available
This study was aimed at evaluating the influence of environmental and social factors on autogrooming behaviour of captive Java monkeys. The subjects were one male and five female adult monkeys housed in an outdoor cage measuring 3.3 x 2.2 x 3.3(H) m. Data on autogrooming were collected during one-hour observation sessions by combining focal behaviour and complete record sampling techniques. A total of 150 hr of observation were made with each daylight hour between 0800 hours and 1600 hours sampled 16 to 20 times. 1) Autogrooming by each of the study subjects showed marked variations throughout the day. The major amount of autogrooming was recorded between 0800 hours and 1100 hours with a second minor peak occurring between 1200 hours and 1400 hours. The lowest mean levels were recorded in the late morning and in the late afternoon. 2) Although there was evidence that the influence of climatic factors was less than that exerted by the time of day, the results indicated that temperature and/or relative humidity were instrumental in influencing the amount of autogrooming that the monkeys performed. More autogrooming was done under conditions of high temperature and low relative humidity. 3) Interindividual proximity was shown to influence autogrooming. Female autogrooming proved to be positively correlated with proximity (within 1 m) to the male. By contrast, there was no significant correlation between autogrooming by the females and their contact score with the male. We interpreted these results as evidence that a relevant portion of the autogrooming recorded in the study group was done as a displacement activity and/or as a redirected activity. Our interpretation is based on the assumption that, for the females, being close to the male can result in a conflict situation whereas being in contact with him is a goal situation which thus corresponds, by definition, to the absence of conflict.
Article
An analysis of the results of 1,259 limited-duration matings was conducted on colonies of Macaco arctoides and M. fascicularis. Maximum conception occurred at a day of breeding/cycle length (DB/CL) ratio of 0.40-0.41 with a range of DB/CL ratios for successful matings from 0.39 to 0.44. These values are compared with published values for various endocrine parameters equated to cycle length.
Chapter
Grooming behavior is a very common type of social interaction between adults of many species of Old-World monkeys. In this interaction, one individual appears to closely examine the coat or skin of his partner (allogrooming), while parting or plucking at hairs. This paper briefly considers various current hypotheses; a more extensive discussion is given elsewhere (Goosen 1980b). Hypotheses concerning the survival function can be divided into two groups: clean and eat hypotheses and social bonding and tension reduction ones. As discussed below, both types of hypotheses are incomplete; those in the first group are incomplete because removal or recovery of debris or vermin from the pelage being groomed is of only minor significance. Hypotheses of the second group are incomplete because they are too broad; the concepts of social bond or low tension are defined such that they cannot explain why grooming varies with the type of situation in which animals meet. An alternative hypothesis which combines several elements included in the others and which is in good agreement with the literature data is later presented here.
Article
Data on scratching behavior were collected from a group of rhesus monkeys living in spacious surroundings. Juveniles scratched more often than adults. Adults scratched most often in social contexts and in close temporal association with a change of behavior. Subjects of intermediate dominance rank, in particular, scratched around the time of a behavioral change, and these subjects were the only ones to show increased scratching during tests involving restricted access to food (thwarting or frustration). The outer thighs, lower back, and sides were the sites scratched most frequently, not necessarily matching sites reported to be preferred for self-grooming. Scratching in monkeys has certain characteristics in common with some well-studied displacement activities in other species, and it possibly also serves as a signal that the individual is preparing to change behavior.
Article
Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
Article
The yawn of the black ape appears to be structurally homologous to the behavior pattern widely described for other vertebrates, even in its finer details. The pattern is highly stereotypic, showing only minor structural variants and not exhibiting any tendency to grade continuously into other expressive or communicative behavior patterns. The yawn occurs in many different contexts, in association with a variety of social and nonsocial situations. Yawns tend to be occur in contexts which elicit some level of stress in the performer. Yawns commonly follw "demonstrations" in which a performer vigorously manipulates an environmental object, with the result of producing a loud noise which draws the attention of others. Adult males yawn significantly more frequently than any other age-sex class. The highest ranking or alpha male tends to yawn at a higher rate than other group members, and in at least one case this was found to be true even following a dominance reversal involving alphas. An ontogenetic trend appears in males: yawning rates increase with age. The most dramatic change occurs during adolescence preceding the eruption of permanent canine dentition. Typical adult male rates are probably reached prior to the completed eruption of the canine teeth.