mystery of yawning
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La parakinésie brachiale oscitante
Yawning: its cycle, its role
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Fetal yawning assessed by 3D and 4D sonography
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Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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mise à jour du
28 novembre 2011
Int J Primatol
2011;32:708&endash;720
Interactions Between Third Parties and Consortship Partners in Tonkean Macaques
(Macaca tonkeana)
 
Arianna De Marco Roberto Cozzolino
Francesco Dessi-Fulgheri Bernard Thierry

Chat-logomini

Abstract
 
Sexual competition is potentially disruptive for the cohesion of social groups because stress and conflicts can extend to other group members. The displays and interactions of sexual partners are liable to influence the behavior of groupmates, which may need to observe them to anticipate possible consequences. We studied 2 captive groups of Tonkean macaques (Macaca tonkeana) to test whether group-mates pay more attention to consort partners, modify their activities and social interactions, and exhibit signs of stress during periods of sexual consortships. We found that group-mates approached the top-ranking male more frequently and were more frequently oriented toward the consort pair at the time of consortship than at other times. Group-mates spent less time sleeping, and devoted less time to manipulating the environment and more time to monitoring during consortship. This indicates that consortships may incur costs in individuals not involved in sexual competition. However, Tonkean macaques did not exhibit any signs of increased stress during consortship periods, as their rates of scratching and yawning did not differ between consortship and nonconsortship periods. This study shows that not only direct competitors but also other individuals monitor the behavior of sexual partners. It is likely that group-mates obtain information this way about ongoing action, and take decisions accordingly.
 
Introduction
 
In group-living animals, sexual competition is potentially disruptive for the cohesion of social groups. With their large body size and large canines, males can compete overtly for access to females (Plavcan 2004). Not only can they fight and wound each other or attack the female (Clutton-Brock and Parker 1995; Huffman 1987; Manson 1994), but conflicts can also extend to other group members, increasing social tension and inducing energy loss (Smuts and Smuts 1993; van Schaik et al. 2004). The majority of researchers have focused on the behavior of sexual partners and competitors, and little is known about their influence on group-mates. Recent studies have shown that the outburst of conflicts influences the behavior not only of opponents but also of uninvolved individuals; in hamadryas baboons (Papio hamadryas hamadryas) and Tonkean macaques (Macaca tonkeana), bystanders are more likely to affiliate with one another to cope with social tension after fights (De Marco et al. 2010; Judge and Mullen 2005). In several species, individuals use social grooming to reduce the tension generated when group members anticipate the competition induced by a forthcoming food distribution (Macaca arctoides: Mayagoitia et al. 1993; Pan troglodytes: Koyama and Dunbar 1996; Cebus apella: Polizzi di Sorrentino et al. 2010).
 
Given the cognitive abilities of monkeys, it is expected that bystanders acquire information by following the interactions occurring between sexual partners. Not only do monkeys know their own affiliative bonds and dominance relationships with others, but they are also aware of the social relationships linking their group-mates (Bergman et al. 2003; Bovet and Washburn 2003; Cheney and Seyfarth 1990; Dasser 1988). They can take relative ranks between their opponents and potential allies into account when recruiting support (Silk 1999). They also track the gaze of others and predict their behavior from subtle gestures and vocal cues (Bergman et al. 2006; Tomasello et al. 1998; Wood et al. 2007). In Tonkean macaques, for instance, individuals orient their food search using visual and olfactory cues conveyed by group-mates (Drapier et al. 1999 2002).
 
In several Old World monkeys, the swelling of the perineal skin conspicuously signals female sexual receptivity (Dixson 1998; Higham et al. 2008). Males react to changes in genital swelling and are more likely to mate when it is particularly large and brightly colored (Dixson 1998; Domb and Pagel 2001). Females can utter specific vocalizations during the reproductive period (Maestripieri and Roney 2005; Pradhan et al. 2006). The finding that males inspect and smell the perineal area of estrous females suggests that they exploit olfactory signals to monitor a female's reproductive condition (Hausfater 1975; Hdry and Whitten 1987). There are hints that olfactory cues indicate fertility in macaques (Cerda-Molina et al. 2006; Michael and Keverne 1968), but their importance in catarrhines remains questionable (Dixson 1998; Snowdon 2004).
 
Whether sexual displays are reliable indicators of female fitness (Pagel 1994) or intracycle signals of the distribution of ovulation (Nunn 1999), it is certain that they convey information to competing males about the fertility of a potential mate (Deschner et al. 2003; Emery and Whitten 2003; Higham et al. 2008). The information provided by sexual displays is available not only to dominant males but also to other group members, albeit probably in different ways according to the distance between individuals (Higham et al. 2009). Signaling interactions represent an additional source of information about relative features that can be used by conspecifics to direct their behavior (McGregor 2005). In chacma baboons (Papio hamadryas ursinus), higherranking males monopolize mating by remaining close to sexually receptive females. Using playback experiments, Crockford et al. (2007) have demonstrated that lowerranking males specifically react when informed that dominant males and estrous females are temporarily apart, indicating that they can track changes in the status of consortship and quickly identify mating opportunities. In Barbary macaques (Macaca sylvanus), males respond more strongly to playbacks of copulatory calls uttered by females during ejaculatory copulations than after those recorded during nonejaculatory copulations, meaning that they eavesdrop on mating outcome (Pfefferle et al. 2008). Tonkean macaques originate from the island of Sulawesi, Indonesia, and form multimale, multifemale groups. Females show clear behavioral, morphological, and endocrine changes throughout the ovarian cycle (Aujard et al. 1998; Thierry et al. 1996). Around the ovulatory period they display brightly colored and voluminous genital swelling, and emit a specific estrus call (Masataka and Thierry 1993; Thierry et al. 1996). Reproduction occurs all year round. There is usually only one periovulatory female available at any one time, and the top-ranking male is able to monopolize sexual access to her over several days in a sexual consortship (Thierry 2010).
 
We investigated changes in the behaviors of group-mates at the time of sexual consortship in 2 groups of Tonkean macaques. Because periods of sexual competition correspond to heightened levels of conflicts between males (Thierry, unpubl. data), group-mates may need to follow the interactions occurring around sexual partners to anticipate better their potential consequences even if this imposes a load on their activity budget. On the other side, the top-ranking male has to maintain his monopoly over the estrous female by keeping other individuals at a distance. We predicted that during consortship 1) group-mates should pay more attention to sexual partners and possibly approach them; 2) the top-ranking male should prevent the approaches of group members, increasing his rate of conflicts with other males; 3) group-mates should spend more time monitoring at the expense of other activities; and 4) group-mates should exhibit signs of stress in relation to the context of sexual competition.
 
Discussion
 
This is the first study demonstrating that the behavior of group members is modified at the time of sexual consortship in primates. The close association between sexual partners influenced the social interactions, activities, and interindividual distances of group-mates significantly. As found in a previous study (Aujard et al. 1998), topranking males also spent more time in contact-sitting with receptive females and more frequently copulated with them.
 
Our first prediction was supported, i.e., that group-mates would pay special attention to sexual partners. Not only was the proportion of affiliative interferences in mating between the top-ranking male and the estrous female higher during consortship than in control periods, but also the consort pair attracted the attention of other group members. In general, group-mates were more frequently oriented toward the top-ranking male and the female at the time of consortship and they approached the top-ranking male more often. Different individuals could have different motivations for paying attention to sexual partners. For instance, adult males could be waiting for mating opportunities if the female escapes the attention of the topranking male. On the other hand, group-members interfered in mounts more often at the time of consortship than at other times. It is known that immature individuals interfere more often than older group members, especially when their mother is involved (Thierry 1986). Here they watched and followed the behaviors of sexual partners, being in a position to learn about mate guarding and mating. The previous results are particularly interesting in view of the fact that the topranking male performed mate guarding by spending more time positioned between the female and group-mates during consortship, and by actively interposing himself between her and approaching group-mates, especially when the latter were males. Rates of conflicts between him and other males remained relatively low at the time of consortship, but they increased in 1 of the 2 groups, consistent with our second prediction.
 
It is a general finding that females increase their locomotory activity and reduce foraging during the periovulatory period (Aujard et al. 1998; Bercovitch 1983; Dixson 1998). Mate guarding and aggression are also associated with costs for dominant males in terms of time and energy expenditure, as reported in savannah baboons (Papio sp.: Alberts et al. 1996; Bercovitch 1983). Although the amount of sexual effort in lower-raking males is weaker than those of the top-ranking one in Japanese macaques (Macaca fuscata: Matsubara, 2003), our results in captive Tonkean macaques show that the daily activities of other group members&emdash;adults and subadults&emdash;can be significantly affected regardless of their sex. In accordance with our third prediction, group-mates spent less time sleeping or manipulating the environment, and they devoted more time to monitoring during consortship. Thus, the consort period could incur costs for other group members, even those not directly involved in sexual competition.
 
Contrary to our fourth prediction, group-mates did not exhibit signs of stress during sexual consortship. Because the rates of conflict remained relatively low, and thus the likelihood of injuries, it may be that mate guarding did not make groupmates more anxious than usual. In a previous study in Tonkean macaques, we found higher rates of affiliation between group-mates having observed a conflict, although they display low levels of scratching and yawning (De Marco et al. 2010). Compared to other macaque species, Tonkean macaques are characterized by relaxed dominance (Thierry 2010; Thierry et al. 1994). Agonistic interactions usually remain at low levels of intensity, third parties can stop aggression by addressing appeasement signals to opponents, and a majority of conflicts are followed by reconciliation (Demaria and Thierry 2001; Petit and Thierry 1994; Thierry 1985). An alternative explanation would be that scratching and yawning are not reliable indices of anxiety in Tonkean macaques. Different measures of anxiety will be necessary to know whether Tonkean macaque group-mates are particularly able to cope with the stressful situation induced by sexual competition.
 
In chacma baboons and Barbary macaques, listening to vocalizations emitted by sexual partners provides adult males with information about their interactions (Crockford et al. 2007; Pfefferle et al. 2008). Our study in Tonkean macaques adds that not only direct competitors but also other conspecifics closely monitor the behaviors of sexual partners. Given the cognitive abilities of monkeys, it is likely that bystanders can pick up on multiple cues through observation and take decisions accordingly (McGregor 2005; Valone 2007). The present results are drawn from 2 small groups, and further sampling will be needed to increase statistical power. Future research should investigate whether the present conclusions are applicable to wild animals, and determine which behavioral cues are informative for bystanders.