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Contagious yawning in chimpanzees
James R. Anderson, Masako Myowa-Yamakoshi, Tetsuro Matsuzawa
The Royal Society
Biology letters
may 2004
 
Psychological influences on yawning
in children
JR Anderson, P Meno
Current Psychology Letters
Behaviour, brain, cognition
2003; 2; 11
 
Illustrations de la thèse de Wolter Seuntjens
 

 

 

 

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mise à jour du
4 décembre 2002
Ethology
1990;86:303-310
lexique
un gorille
The influence of age, sex, rank on yawning behavior in two species of macaques (Macaca fascicularis, Macaca fuscata)
Troisi A, Aureli F, Schino G, Rinaldi F, De Angeli N
Dipartimento di genetica e biologia moleculare Universita La Sapienza Roma et Rijksuniversiteit Utrecht
 
Inhibition of social behavior in chimpanzees under high-density conditions Aureli F, de Waal FB

Chat-logomini

Introduction : Current knowledge on yawning behavior in Old World monkeys can be summarized as follows. Three types of yawns have been distinguished: physiological yawn, emitted during periods of transition from waking to sleeping, or during the downward phases of cyclic arousal (Deputte 1978); stress yawn, occurring in conflict or anxiety-producing situations (Hinde & Rowell 1962); and threat yawn, involving canine display and characterized by direct orientation toward another animal (Hall & Devore1965). Yawning is displayed more frequently by males than females (e.g. Redican 1975). Its rate of occurrence is influenced by plasma levels of androgens; injection of testosterone propionate in adult rhesus females induced a 20-fold increase in yawning behavior (Goy & Resko 1972). Male yawning increases through adolescence and jumps dramatically as males enter early adulthood, whereas female yawning increases only slightly, if at all, after infancy (Hadidan 1980). The highest-ranking male in the dominance hierarchy tends to yawn at a much higher rate than other group members. Adult male macaques appear able to produce yawning voluntarily (Anderson & Wunderlich 1988). See photos in the bottom.

Most of the above information comes from either anecdotal reports or laboratory studies involving small numbers of subjects. Among published papers, only one naturalistic study has quantitatively investigated the spontaneous occurrence of yawning in a social group of nonhuman primates (Hadidan 1980). Surprisingly, the ethology of yawning bas been studied more systematically in humans than in nonhuman primates (e.g Baenninger 1987; Provine et al. 1987; Schino & Aureli 1989).

Adopting a naturalistic and quantitative approach, the present study aimed at documenting the occurrence of yawning behavior in two species of macaques: Macaca fascicularis and M. fuscata. In particular, the influence of age, sex, and dominance rank on yawning was investigated. Differences in the frequency of yawning by individuals from different age-sex classes within the group were analyzed with a view to elucidating proximate causation of yawning. Because of the methodological difficulties of distinguishing the various types of yawns according to their functional significance and context of occurrence, the present study deals only with the apparent structural pattern and not its functional types. [...]

 
Discussion : The two macaque groups of this study showed major differences in the overall frequency of yawning and in the influence that sex, age, and dominance rank exerted on yawning behavior. Japanese macaques yawned much more than long-tailed macaques. Although the long-tailed macaque data may underestimate the frequency of yawning, it seems unlikely that methodological differences could account for the 10-fold difference in yawning rates between the two species. In the long-tailed macaques, sex differences in frequency of yawning only emerged after sexual maturity; yawning rates increased significantly in both males and females as they reached sexual maturity; and, among males, rank was positively correlated with frequency of yawning. Differently, in the japanese macaques, males, both mature and immature, yawned more than same-aged females; sexual maturity was associated with an increase in yawning in males only; and male rank did not correlate with frequency of yawning.

Even though more than one group would need to be examined to advance hypotheses concerning interspecific distinctions, it may be interesting to discuss the differences between the two study groups in the light of comparative data on the social structure of macaque species. Caldecott (1986) has proposed a two group classification of macaque societies. Species in the first group (M. mulatta, M. fuscata, M. nemestrina, and M. silenus) are characterized by antagonistic inter-male relationships and a multiple-mount copulation pattern. Species in the second group (M. sylvanus, M. radiata, and, based on recent data by Thierry (1985) and DeWaal (1989), M. arctoïdes and M. tonkeana) show relaxed internale relationships and a single-mount copulation pattern. Based on the inconsistent copulatory pattern of M. fascicularis (both single- and multiple-mount copulations), considers this species as intermediate between the two groups. Comparative data on agonistic behavior support the view that the long-talled macaque occupies an intermediate position between the two groups of Caldecott's classification. Taken together, these data suggest that social relationships in M. fuscata are more tense than those found in M. fasciculars. It is possible that the interspecific difference in yawning rates that we found in this study reflects such a difference in the social structure of the two species.

Regardless of interspecific differences, the overall results of this study support only in part the finding that yawning is largely influenced by plasma concentrations of androgens (Phoenix & Chambers 1986). On the one hand, we found that mature males, the individuals with the highest concentrations of androgens, yawned much more than any other age-sex class, and that male yawning increased dramatically after sexual maturity, when the plasma levels of testosterone start to rise. Also the finding that, after the attainment of sexual maturity, long-tailed macaque females showed an increase in frequency of yawning may accord with an etiological explanation implicating an activational role of androgens: sexually-mature female monkeys secrete androgens from the ovary as well as from the adrenal gland (Hess & Resko 1973).

On the other hand, the increase in female yawning after sexual maturity was recorded only in the long-tailed macaque group. In addition, in the Japanese macaque group, sex differences in frequency of yawning were clearly evident prior to the attainment of sexual maturity, indicating that the higher rate of male yawning was not simply due to plasma concentrations of androgens. Although this latter finding can be explained by hypothesizing an organizational role for androgens (ie, in the prenatal period, the male hormone would organize and differentiate the neural tissues that mediate the display of yawning), these results suggest that social factors are also important in influencing the age-sex class distribution of yawning behavior. For example, it is possible that, among immature Japanese macaques, yawns were emitted more often by males than by females because the males were generally more tense, a possible result of their more frequent involvement in agonistic behavior.

The role of social factors clearly emerges from the data on the relationship between male dominance rank and yawning. The finding that higher-ranking long-tailed macaque males yawned more than subordinate males fits well with the notion that yawning is a mild form of threat. Yet, this was not true for the Japanese macaque males. This result brings to attention the hypothesized dual function of emotional yawning in Old World monkeys (Redican 1982). It is possible that most of the yawns emitted by low-ranking males were a result of conflict or stress, whereas yawns by high-ranking males were made as intimidating displays. If this was the case, the same rate of yawning by males of different rank shoul d be viewed as the final outcome of two different motivational processes: intention of eliciting submission from another animal (threat yawn) and response to stressful circumstances (stress yawn). The difficulty of testing this hypothesis relates to the general problem of distinguishing between primate displacement activities (e.g. scratching, self-grooming, yawning, and shaking) and the same behavior patterns carried out in a "normal" context, ie. as comfort behaviors (Diezinger & Anderson 1986).

In conclusion, the present study shows that macaque yawning has a complex causation which is likely to result from an interaction between hormonal and social factors. However, the heterogeneity of the few available data, including those in the present study, indicates that there is a need for further naturalistic studies of yawning behavior in different primate groups and species.

 
Literature Cited
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  2. BAENNINGER, R. 1987: Some comparative aspects of yawning in Betta splendens, Homo sapiens, Panthera leo, and Papio sphinx. J. Comp. Psychol. 101, 349-354
  3. CALDECOTT, J. 0. 1986: Mating patterns, societies, and the ecogeography of macaques. Anim. Behav. 34, 208-220.
  4. DEPUTTE, B. 1978; Etude du bâillement chez deux espèces de Cercopithecidae, Cercocebus albigena Gray et Macaca fascicularis Raffles: Recherche des facteurs de causalité et de fonction. Mise en évidence des facteurs socio-bioénergétiques. Thesis, Université de Rennes
  5. DE WAAL, F. B. M. & LUTTRELL, L. M. 1989: Toward a comparative socioecology of the genus Macaca: different dominance styles in rhesus and stumptail monkeys. Am. J. Primatol. 19, 93-109
  6. DIEZINGER, F. & ANDERSON, J. R. 1986: Starting from scratch: a first look at a "displacement activity" in group-living rhesus monkeys. Am. J. Primatol. 11, 117-124.
  7. Goy, R. W. & RESKO, G. A. 1972: Gonadal hormones and behavior of normal and pseudohermaphroditic nonhuman female primates. Rec. Progr. Horm. Res. 28, 707-733
  8. HADIDIAN, J. 1980: Yawning in an Old World monkey, Macaca nigra (Primates: Cercopithecidae) Behaviour 75, 133-147
  9. HALL, K. R. L. & DEVORE, 1. 1965: Baboon social behavior. In: Primate Behavior: Field Studies of Monkeys and Apes. (DEVORE, I., ed.) Holt, Rinehart & Winston, New York, pp. 53-110.
  10. HESS, D. L. & RESKO, G. A. 1973: The effects of progesterone on the patterns of the testosterone and estradiol concentrations in the systemic plasma of the fernale rhesus monkey during the intermenstrual period. Endocrinology 92, 446-453
  11. HINDE, R. A. & ROWELL, T. E. 1962: Communication by posture and facial expression in the rhesus monkey. Proc. Zool. Soc. Lond. 138, 1-21.
  12. MARTIN, P. & BATESON, P. 1986: Measuring Behaviour. Cambridge Univ. Press, Cambridge.
  13. NAPIER, P. H. 1967: A Handbook of Living Primates. Acad. Press, London.
  14. PHOENIX, C. H. & CHAMBERS, K. C., 1986: Threshold for behavioral responses to testosterone in old castrated male rhesus macaques. Biol. Reprod. 35, 918-926.
  15. PROVINE, R. R., HAMERINK, H. B. & CURCHACK, B. C. 1987: Yawning: relation to sleeping and stretching in humans. Ethology 76, 152-160.
  16. REDICAN, W. K. 1975: Facial expressions in nonhuman primates. In: Primate Behavior: Developments in Field and Laboratory Research, Vol. 4. (RoSENBLum, L. A., ed.) Acad. Press, New York, pp. 103-194.
  17. 1982: An evolutionary perspective on human facial displays. In: Emotion in the Human Face, 2nd ed. (EKMAN, P., ed.) Cambridge Univ. Press, Cambridge, pp. 212-280.
  18. SCHINO, G. & AURELI, F. 1989: Do men yawn more than women? Ethol. Sociobiol. 10, 375-378.
  19. THIERRY, B. 1985: Patterns of agonistic interactions in three species of macaques (M. mulatta, M. fascicularis, M. tonkeana). Aggress. Behav. 11, 223-33

« It is ironic that testosterone "the male sex hormone," is more closely associated with the yawning rate than with the mounting or intromitting rates » Charles Phoenix
 
 
Sexual steroids exert several effects on both central dopaminergic and oxytocinergic systems by acting either at the genomic or membrane level  
 
yawns-canines
credit photo : "Asif A. Ghazanfar and Aristides Arrenberg"
Max Planck Institute for Biological Cybernetics
Tuebingen; Germany.
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