Abstract—Knowledge of grooming makes it possible to characterize the intragroup social connections of lemurs and accurately form groups in captivity. The results of this study showed that there are no significant differences in grooming between the black-and-white and red ruffed lemurs: in both subspecies, allogrooming is associated with a certain time of day to a lesser extent than autogrooming. In allogrooming, both subspecies of lemurs clean mainly those parts of the body that are difficult to reach for self-cleaning. An asymmetry in the distribution of allogrooming was revealed: a negative correlation between the age and frequency of the initiated mutual cleaning, predominance of grooming in male–female dyads and between related animals. Allogrooming in ruffed lemurs has three main contexts: the maintenance and establishment of social ties, pacification and buffer of aggression, and restoration of disturbed relations between social partners.
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REFERENCES
Afanas’ev, V.V., Teoriya veroyatnostei (Probability Theory), Moscow: Vlados, 2007.
Aureli, F., Preston, S.D., and de Waal, F.B.M., Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study, J. Comp. Psychol., 1999, vol. 113, no. 1, pp. 59–65.
Barton, R., Grooming site preferences in primates and their functional implications, Int. J. Primatol., 1985, vol. 5, no. 6, pp. 519–532.
Boccia, M.L., Reite, M., and Laudenslager, M., On the physiology of grooming in a pigtail macaque, Physiol. Behav., 1989, vol. 45, no. 3, pp. 667–670.
Cherevko, L.S. and Shapet’ko, E.V., Hierarchy and aggressive and affiliative behavior of ruffed lemurs (Varecia variegata variegata and Varecia variegata rubra) in captivity, Zool. Zh., 2014, vol. 93, no. 2, pp. 297–304.
Crawford, G.C., Andrews, G.A., Chavey, P.S., Dunker, F.H., Garner, M.M., and Sargent, E.L., Survey and clinical application of serum iron, total iron binding capacity, transferrin saturation, and serum ferritin in captive black and white ruffed lemurs (Varecia variegata variegata), J. Zoo Wildlife Med., 2005, vol. 36, no. 4, pp. 653–660.
Deryagina, M.A. and Butovskaya, M.L., Etologiya primatov (Primate Ethology), Moscow: Mosk. Gos. Univ., 1992.
Dunbar, R.M., Functional significance of social grooming in primates, Folia Primatologoca, 1991, vol. 57, no. 3, pp. 121–131.
Dunbar, R. and Lehmann, J., Grooming and social cohesion in primates: a comment on Grueter et al., Evol. Hum. Behav., 2013, vol. 34, no. 6, pp. 453–455.
Freeland, W.J., Functional aspects of primate grooming, Ohio J. Sci., 1981, vol. 81, no. 4, pp. 173–180.
Garrison, L. and White, F., Group formation and behavioral changes with release to free-ranging in red ruffed lemurs, Varecia variegata rubra, Anim. Welfare, 1993, vol. 2, pp. 219–233.
Gmurman, V.E., Teoriya veroyatnostei i matematicheskaya statistika (Theory of Probability and Mathematical Statistics), Moscow: Vysshaya Shkola, 2003.
Hick, U., Haltung, Zucht und kunstliche Aufzucht von Varis, Zeitschrift des Kolner Zoo, 1984, vol. 27, pp. 123–137.
Hosey, G.R. and Thompson, R.J., Grooming and touching behaviour in captive ring-tailed lemurs (Lemur catta L.), Primates, 1985, vol. 26, no. 1, pp. 95–98.
Hutchins, M. and Barash, D.P., Grooming in primates: implications for its utilitarian function, Primates, 1976, vol. 17, no. 2, pp. 145–150.
Iwano, T., Some observations of two kinds of lemuridae (Varecia variegata variegata and Lemur fulvus albifrons) in the reserve of Nosy Mangabe, Primates, 1989, vol. 30, no. 2, pp. 241–248.
Junge, R.E., Williams, C.V., and Campbell, J., Nutrition and behavior of lemurs, Vet. Clin. N. Am.: Exotic Anim. Pract., 2009, vol. 2, no. 12, pp. 339–348.
Kappeler, P.M., Agonistic and grooming behavior of captive crowned lemurs (Lemur coronatus) during the breeding season, Hum. Evol., 1989, vol. 4, no. 2, pp. 207–215.
Kaufman, R., Female dominance in semifree-ranging black-and-white ruffed lemurs, Varecia variegata variegata, Folia Primatologica, 1991, vol. 57, no. 1, pp. 39–41.
Keverne, E.B., Martensz, N.D., and Tuite, B., Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships, Psychoneuroendocrinology, 1989, vol. 14, nos. 1–2, pp. 155–161.
Kress, J.H., Conley, J.M., Eaglen, R.H., and Ibanez, E., The behavior of Lemur variegatus Kerr, 1792, Ethology, 1978, vol. 48, no. 1, pp. 87–99.
Lazaro-Perea, C., Arruda, M., and Snowdon, C., Grooming as a reward? Social function of grooming between females in cooperatively breeding marmosets, Anim. Behav., 2004, vol. 67, no. 1, pp. 627–636.
Lewis, R., Grooming patterns in Verreaux’s sifaka, Am. J. Primatol., 2010, vol. 72, no. 3, pp. 254–261.
Meller, R.E., Keverne, E.B., and Herbert, J., Behavioural and endocrine effects of naltrexone in male talapoin monkeys, Pharmacol. Biochem. Behav., 1980, vol. 13, no. 5, pp. 663–672.
Meyer, C., Gallo, T., and Schultz, S.T., Female dominance in captive red ruffed lemurs, Varecia variegata rubra (Primates, Lemuridae), Folia Primatologica, 1999, vol. 70, no. 6, pp. 358–361.
Morland, H.S., Preliminary report on the social organization of ruffed lemurs (Varecia variegata variegata) in a northeast Madagascar rain forest, Folia Primatologica, 1991, vol. 56, no. 3, pp. 157–161.
Muroyama, Y., Mutual reciprocity of grooming in female Japanese macaques (Macaca fuscata), Behaviour, 1991, vol. 119, nos. 3–4, pp. 161–170.
Overdorff, D. and Erhart, E., Does female dominance facilitate feeding priority in black and white ruffed lemurs (Varecia variegata) in south-eastern Madagascar?, Am. J. Primatol., 2005, vol. 66, no. 1, pp. 7–22.
Overdorff, D.J. and Tecot, S.R., Social pair-bonding and resource defense in wild red-bellied lemurs (Eulemur rubriventer), in Lemurs: Ecology and Adaptation, New York: Springer, 2007, pp. 235–254.
Pereira, M.E., Seeligson, M.L., and Macedonia, J.M., The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae), Folia Primatologica, 1988, vol. 51, no. 1, pp. 1–32.
Popov, S.V. and Il’chenko, O.G., Guidelines on ethological observations of mammals in captivity, in Rukovodstvo po nauchnym issledovaniyam v zooparkakh (A Guide for Research in Zoos), Moscow: Moskovskii zoopark, 2008, pp. 3–65.
Port, M., Clough, D., and Kappeler, P.M., Market effects offset the reciprocation of grooming in free-ranging red-fronted lemurs, Eulemur fulvus rufus, Anim. Behav., 2009, vol. 77, no. 1, pp. 29–36.
Porton, I., International Studbook for the Ruffed Lemur (Varecia variegata variegata and Varecia variegata rubra), Saint-Louis, Missouri: Saint Louis Zoo, 2000.
Raps, S. and White, F.J., Female social dominance in semifree-ranging ruffed lemurs (Varecia variegata), Folia Primatologica, 1995, vol. 65, no. 3, pp. 163–168.
Rigamonti, M.M., Home range and diet in red ruffed lemurs (Varecia variegata rubra) on the Masoala Peninsula, Madagascar, in Lemur Social Systems and Their Ecological Basis, New York: Springer, 1993, pp. 25–39.
Schino, G., Grooming and agonistic support: a meta-analysis of primate reciprocal altruism, Behav. Ecol., 2007, vol. 18, no. 1, pp. 115–120.
Schino, G. and Aureli, F., Trade-offs in primate grooming reciprocation: testing behavioural flexibility and correlated evolution, Biol. J. Linn. Soc., 2008, vol. 95, no. 3, pp. 439–446.
Sueur, C., Deneubourg, J.L., Petit, O., and Couzin, D., Group size, grooming and fission in primates: a modeling approach based on group structure, J. Theor. Biol., 2011, vol. 273, no. 1, pp. 156–166.
Tattersal, I., The Primates of Madagascar, New York: Columbia: Univ. Press, 1982.
Thierry, B., Gauthier, C., and Peignot, P., Social grooming in tonkean macaques (Macaca tonkeana), Int. J. Primatol., 1990, vol. 11, no. 4, pp. 357–375.
Vasey, N., Impact of seasonality and reproduction on social structure, ranging patterns, and fission-fusion social organization in red ruffed lemurs, in Lemurs: Ecology and Adaptation, New York: Springer, 2007, pp. 275–304.
Vasey, N., The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report, Primates, 2007a, vol. 48, no. 1, pp. 41–54.
Ventura, R., Majolo, B., Koyama, N.F., Hardie, S., and Schino, G., Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support, Am. J. Primatol., 2006, vol. 68, no. 12, pp. 1138–1149.
Weigler, B.J., Feeser, P.L., Grant, S.M., and Norris, C.A., Epidemiologic assessment of reproductive success and infant mortality in ruffed lemurs (Varecia variegata), Zoo Biol., 1994, vol. 13, no. 6, pp. 527–536.
Wolfe, L., Social networks in ring-tailed lemurs, Am. J. Phys. Anthropol., 2000, vol. 12, no. 4, pp. 325–329.
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The author thanks the anonymous reviewer and N.A. Formozov for valuable advice and comments during the preparation of the manuscript for publication.
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Cherevko, L.S. Comfort Behavior of Black-and-White (Varecia variegata variegata) and Red (Varecia variegata rubra) Ruffed Lemurs (Primates, Lemuridae). Biol Bull Russ Acad Sci 45, 973–982 (2018). https://doi.org/10.1134/S1062359018090042
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DOI: https://doi.org/10.1134/S1062359018090042