Abstract
Captive studies have shown that ruffed lemurs (Varecia) have an unusual suite of reproductive traits combined with extremely high maternal reproductive costs. These traits include the bearing of litters, nesting of altricial young, and absentee parenting. To characterize the breeding system of this enigmatic lemur, reproductive traits must be contextualized in the wild. Here, I provide a preliminary report of mating and infant care in one community of wild red ruffed lemurs (Varecia rubra). Observations span a 15-month period covering two birth seasons and one mating season on the Masoala Peninsula, Madagascar. Factors that are not possible to replicate in captivity are reported, such as mating pattern, natality and mortality rates, the location of nests within the home range, and the structuring of infant care within a natural community. V. rubra at Andranobe have a fission-fusion, multifemale-multimale grouping pattern and a polygamous mating system. They do not mate monogamously or live strictly in family-based groups as suggested by previous workers. During the first 2 months of life, nests and infant stashing localities are situated within each mother’s respective core area, and inhabitants of each core area within the communal home range provide care for young. As part of their absentee parenting system, infants are left in concealed, protected, and supportive spots high in the canopy, while mothers travel distantly. This practice is termed ‘infant stashing’. Alloparenting appears to be an integral part of V. rubra’s overall reproductive strategy in the wild, as it was performed by all age-sex classes. Among the alloparental behaviors observed were infant guarding, co-stashing, infant transport, and allonursing. Alloparenting and absentee parenting may mitigate high maternal reproductive costs. Furthermore, V. rubra may have a breeding system in which genetic partners (i.e., mating partners) do not always correspond to infant care-providers. Combined with recently available information on the behavioral ecology of wild ruffed lemurs, this preliminary report suggests directions for in-depth studies on Varecia’s breeding system.
Similar content being viewed by others
Notes
“Social organization” and related terms used in this paper (e.g., social group) are congruent with how these terms have been defined in the literature (e.g., Struhsaker 1969; Kummer 1971; Rowell 1972, 1979; Hinde 1976; Dolhinow 1993; Sussman 1999; cf. Kappeler and Van Schaik 2002). In a recent review Fuentes (2007) advocates retention of the commonly understood definitions, and in keeping with them, the term ‘social organization’ is defined as the network of behaviors and patterns that emerges from the conflux of mating and rearing patterns, grouping patterns, and intragroup and intergroup behavior.
References
Balko EA (1998) A behaviorally plastic response to forest composition and logging disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar. PhD thesis, College of Environmental Science and Forestry, State University of New York, Syracuse
Bogart MH, Cooper RW, Benirschke K (1977) Reproductive studies of black and ruffed lemurs. Int Zool Yearb 17:177–182
Boskoff KJ (1977) Aspects of reproduction in ruffed lemurs (Lemur variegatus). Folia Primatol 28:241–250
Brockman DK, Willis MS, Karesh WB (1987) Management and husbandry of ruffed lemurs, Varecia variegata, at the San Diego Zoo. II Reproduction, pregnancy, parturition, litter size, infant care, and reintroduction of hand-raised infants. Zool Biol 6:349–363
Charles-Dominique P (1977) Ecology and behavior of nocturnal primates. Columbia University Press, New York
Charles-Dominique P, Bearder SK (1979) Field studies of lorisid behavior: methodological aspects. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic, New York, pp 567–629
Charnov R (1981) Kin selection and helpers at the nest: effects of paternity and biparental care. Anim Behav 29:631–632
Clark A (1985) Sociality in a nocturnal ‘solitary’ prosimian, Galago crassicaudatus. Int J Primatol 6:581–600
Dolhinow P (1993) Social systems and the individual. Evol Anthropol 3:73–74
Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Oxford, pp 301–337
Fairbanks LA (1990) Reciprocal benefits of allomothering for female vervet monkeys. Anim Behav 9:425–441
Fietz J, Zischler H, Schwiegk C, Tomiuk J, Dausmann KH, Ganzhorn JU (2000) High rates of extra-pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behav Ecol Sociobiol 49:8–17
Foerg R (1982) Reproductive behavior in Varecia variegata. Folia Primatol 38:108–121
Fuentes A (2007) Social organization: social systems and the complexities in understanding the evolution of social behavior. In: Campbell CJ, Fuentes A, Mackinnon KC, Panger M, Bearder SK (eds) Primates in perspective. Oxford University Press, New York, pp 609–621
Glander KE, Fedigan LM, Fedigan L, Chapman C (1991) Field methods for capture and measurement of three monkey species in Costa Rica. Folia Primatol 57:70–82
Goldizen AW (1987) Tamarins and marmosets: cooperative care of offspring. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago, Chicago, pp 34–43
Goodall J (1986) The chimpanzees of gombe: patterns of behavior. Harvard University Press, Cambridge
Gould L (1990) The social development of free-ranging infant Lemur catta at Berenty Reserve, Madagascar. Int J Primatol 11:297–318
Gould L (1992) Alloparental care in free-ranging Lemur catta at Berenty Reserve, Madagascar. Folia Primatol 58:72–83
Grieser B (1992) Infant development and parental care in two species of sifakas. Primates 33:305–314
Groves C (2001) Primate taxonomy. Smithsonian Institution Press, Washington D.C.
Gursky SL (2000). Allocare in a nocturnal primate: data on the spectral tarsier, Tarsius spectrum. Folia Primatol 71:39–54
Harrington JE (1978) Development of behavior in Lemur macaco in the first nineteen week. Folia Primatol 29:107–128
Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17
Jennions MD, Macdonald DW (1994) Cooperative breeding in mammals. Trends Ecol Evol 9:89–93
Kappeler PM (1991) Patterns of sexual dimorphism in body weight among prosimian primates. Folia Primatol 57:132–146
Kappeler PM, van Schaik (2002) Evolution of primate social systems. Int J Primatol 23:707–740
Kerridge FJ (1999) Part-time fostering by a pair of black and white ruffed lemurs (Varecia variegata variegata). Anim Welf 8:35–42
Kleiman DG, Malcolm JR (1981) The evolution of male parental investment in mammals. In: Gubernick DJ, Klopfer PH (eds) Parental care in mammals. Plenum Press, New York, pp 347–387
Klopfer PH, Boskoff KJ (1979) Maternal behavior in prosimians. In: Doyle GA, Martin RD (eds) The study of prosimian behavior. Academic, New York, pp 123–156
Klopfer PH, Dugard J. (1976) Patterns of maternal care in lemurs III. Lemur variegatus. Z Tierpsychol 40:210–220
Klopfer PH, Klopfer MS (1970) Patterns of maternal care in three species of Lemur I. Normative description. Z Tierpsychol 27:984–996
Kress JH, Conley JM, Eaglen RH, Ibanez AE (1978) The behavior of Lemur variegatus KERR 1792. Z Tierpsychol 48:87–99
Kummer H (1971) Primate societies: group techniques of ecological adaptations. Aldine, Chicago
Lewis SE, Pusey AE (1997) Factors influencing the occurrence of communal care in plural breeding mammals. In: Solomon NG, French JA (eds) Cooperative breeding in mammals. Cambridge University Press, Cambridge, pp 335–363
Martin RD (1972) Adaptive radiation and behavior of the Malagasy lemurs. Philos T Roy Soc B 264:295–352
Martin RD (1990) Primate origins and evolution. Princeton University Press, Princeton
Maynard Smith J (1977) Parental investment: a prospective analysis. Anim Behav 25:1–9
Mitani J, Watts D (1997) The evolution of non-maternal caretaking among anthropoid primates: do helpers help? Behav Ecol Sociobiol 40:213–220
Morland HS (1990) Parental behavior and infant development in ruffed lemurs (Varecia variegata variegata). Am J Primatol 20:253–265
Morland HS (1991a) Social organization and ecology of black & white ruffed lemurs (Varecia variegata variegata) in lowland rain forest, Nosy Mangabe, eastern Madagascar. PhD thesis, Yale University, New Haven
Morland HS (1991b) Preliminary report on the social organization of ruffed lemurs (Varecia variegata variegata) in a northeast Madagascar rain forest. Folia Primatol 56:157–161
Morland HS (1993) Reproductive activity of ruffed lemurs (Varecia variegata variegata) in a Madagascar rain forest. Am J Phys Anthropol 91:71–82
Pereira ME, Klepper A, Simons EL (1987) Tactics of care for young infants by forest-living ruffed lemurs (Varecia variegata variegata): Ground nests, parking and biparental guarding. Am J Primatol 13:129–144
Petter JJ (1962) Recherches sur l’écologie et l’éthologie des lémuriens Malgaches. Mem Mus Nat Hist Nat Ser A Zool 27:1–146
Petter JJ, Albignac R, Rumpler Y (1977) Mammifères lémuriens (Primates, Prosimiens). Faune de Madagascar, vol. 44, pp 1–513. ORSTROM/CNRS, Paris
Petter-Rousseaux A (1962) Recherches sur la biologie de la reproduction des primates inférieurs. Mammalia 26[Suppl 1]:1–88
Porton I (1989) 1989 International studbook for the ruffed lemur Varecia variegata. St. Louis Zoological Park, St. Louis, Mo.
Rasmussen DT (1985) A comparative study of breeding seasonality and litter size in eleven taxa of captive lemurs (Lemur and Varecia). Int J Primatol 6:501–517
Reynolds JD (1996) Animal breeding systems. Trends Ecol Evol 2:68–72
Richard A (1985) Primates in nature. Freeman, New York
Rigamonti MM (1993) Home range and diet in red ruffed lemurs (Varecia variegata rubra) on the Masoala Peninsula, Madagascar. In: Kappeler PM, Ganzhorn JU (eds) Lemur social systems and their ecological basis. Plenum Press, New York, pp 25–39
Ross C, MacLarnon A. (1995) Ecological and social correlates of maternal expenditure on infant growth in haplorhine primates. In: Pryce C, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 37–46
Rowell TE (1972) Social behavior of monkeys. Penguin Press, Middlesex
Rowell TE (1979) How would we know if social organization were not adaptive. In: Bernstein IS, Smith EO (eds) Primate ecology and human origins. Garland, New York, pp 1–22
Shideler SE, Lindburg DG (1982) Selected aspects of Lemur variegatus reproductive biology. Zool Biol 1:127–134
Shideler SE, Lindburg DG, Lasley BL (1983) Estrogen-behavior correlates in the reproductive physiology and behavior of the ruffed lemur (Lemur variegatus). Hormones Behav 17:249–263
Skutch AF (1961) Helpers among birds. Condor 63:198–226
Stacey PB (1982) Female promiscuity and male reproductive success in social birds and mammals. Am Nat 120:51–64
Stacey PB, Koenig WD (1990) Introduction. In: Stacey PB, Koenig WD (eds) Cooperative breeding in birds. Cambridge University Press, Cambridge, pp 9–18
Stanford CB (1992) The costs and benefits of allomothering in wild capped langurs (Presbytis pileata). Behav Ecol Sociobiol 30:29–34
Struhsaker TT (1969) Correlates of ecology and social organization among African cercopithecines. Folia Primatol 11:80–118
Sussman RW (1977) Socialization, social structure, and ecology of two sympatric species of Lemur. In: Chevalier-Skolnikoff S, Poirier FE (eds) Primate bio-social development. Garland, New York and London, pp 515–528
Sussman RW (1999) Primate ecology and social structure, vol 1: Lorises, lemurs and tarsiers. Pearson Education Custom Publ, Upper Saddle River, N.J.
Sussman RW, Garber PA (1987) A new interpretation of the social organization and mating system of the Callitrichidae. Int J Primatol 8:73–92
Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: a review. Am J Phys Anthropol 84:43–58
Tattersall I (1982) Primates of Madagascar. Columbia University Press, New York
Tilden CT, Oftedal OT (1995) Bioenergetics of reproduction in prosimian primates: Is it related to female dominance. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark. Plenum Press, New York, pp 119–128
Tilden CT, Oftedal OT (1997) Milk composition reflects pattern of maternal care in prosimian primates. Am J Primatol 41:195–211
Vasey N (1997a) Community ecology and behavior of Varecia variegata rubra and Lemur fulvus albifrons on the Masoala Peninsula, Madagascar. PhD thesis, Washington University, St. Louis, Mo.
Vasey N (1997b) The cooperative breeding system of Varecia variegata. Am J Phys Anthropol Suppl 24:232
Vasey N (2000) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I Interspecific patterns. Am J Phys Anthropol 112:411–431
Vasey N (2002) Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns. Am J Phys Anthropol 118:169–183
Vasey N (2003) Varecia, ruffed lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. University of Chicago Press, Chicago, pp 1332–1336
Vasey N (2005) Activity budgets and activity rhythms in red ruffed lemurs (Varecia rubra) on the Masoala Peninsula, Madagascar: seasonality and reproductive energetics. Am J Primatol 66:23–44
Vasey N (2006) Impact of seasonality and reproduction on social structure, ranging patterns and fission-fusion social organization in red ruffed lemurs. In: Gould L, Sauther ML (eds) Lemurs: ecology and adaptation. Springer/Kluwer, New York (in press)
Vasey N, Tattersall I (2002) Do ruffed lemurs form a hybrid zone? Distribution and discovery of Varecia, with systematic and conservation implications. Am Mus Novitates 3376:1–26
White FJ (1991) Social Organization, feeding ecology, and reproductive strategy of ruffed lemurs, Varecia variegata variegata. In: Kimuya T, Takenaka O, Iwamoto M (eds) Primatology today: XII congress of the international primatological society. Elsevier, Amsterdam, pp 81–84
Wilson EO (1975) Sociobiology: the new synthesis. Harvard University Press, Cambridge
Woodroffe R, Vincent A (1994) Mother’s little helpers: patterns of male care in mammals. Trends Ecol Evol 9:294–297
Young AL, Richard AF, Aiello LC (1990) Female dominance and maternal investment in strepsirrhine primates. Am Nat 135:473–488
Acknowledgments
I thank Bob Sussman, Steve Goodman, and two anonymous reviewers for comments on earlier versions of this article. I thank the Tripartite Committee of the Malagasy government for permission to complete this research under an accord between the Department of Paleontology and Biological Anthropology, University of Antananarivo and the Department of Anthropology, Washington University. Grant sponsors include: The Wenner-Gren Foundation, the Leakey Foundation, the National Science Foundation, Primate Conservation, Inc., the Boise Fund; Sigma Xi provided funding for fieldwork.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Vasey, N. The breeding system of wild red ruffed lemurs (Varecia rubra): a preliminary report. Primates 48, 41–54 (2007). https://doi.org/10.1007/s10329-006-0010-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-006-0010-5