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Ranging Behavior and Possible Correlates of Pair-Living in Southeastern Avahis (Madagascar)

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Abstract

Researchers have proposed several hypotheses to explain pair-living in primates. In particular, when males are not involved in direct parental care, pair-living may be related to female dispersal, infanticide prevention, or male mate/resource defense. We aimed to evaluate, through a better understanding of the ranging patterns of avahis, which hypotheses may best account for pair-living in these nocturnal lemurs. We collected focal observations over 26 nights, June–September 2004, in a littoral forest (Sainte Luce, southeastern Madagascar) on 4 adult radiocollared avahis [Avahi laniger (Tattersall, I. (1982). The Primates of Madagascar. Columbia University Press, New York.) or Avahi meridionalis (Zaramody in Primate Reports 74:9–22, 2006)]. We followed 2 males and 2 females from 2 groups: B, a male-female couple, and A, comprising the parental pair and 1-yr-old female offspring. The adult females birthed in August. We recorded resting and feeding tree points (via global positioning system) for home range calculation through minimum convex polygon and kernel methods. We provide the first quantitative information on the ranging behavior of 2 male and 2 female avahis. Home range/daily path length values (means) are higher than the ones previously reported for the same and other folivorous pair-living lemur species. On average, the 2 females spent more time feeding and traveled shorter distances than the 2 males did. Male–female cohesion (mean values), possibly enhanced by offspring presence, was higher in A and after births than in B and before births, respectively. Although male avahis may be forced into pair-living owing to energy constraints related to size, locomotion, and diet, females might accept pair-living in exchange for indirect territory defense and mate guarding.

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References

  • Altmann, J. (1974). Observational study of behaviour: sampling methods. Behaviour, 49, 227–267.

    PubMed  CAS  Google Scholar 

  • Bollen, A., & Donati, D. (2005). Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar. Biotropica, 37, 32–43.

    Article  Google Scholar 

  • Brockman, D. K. (2003). Polyboroides radiatus predation attempts on Propithecus verreauxi. Folia Primatologica, 74, 71–74.

    Article  Google Scholar 

  • Brotherton, P. N. M., Pemberton, J. M., Komers, P. E., & Malarky, G. (1997). Genetic and behavioural evidence for monogamy in a mammal, Kirk’s dik-dik (Madoqua kirkii). Proceedings of the Royal Society of London Series B - Biological Sciences, 164, 675–681.

    Article  Google Scholar 

  • Charles-Dominique, P., & Petter, J. J. (1980). Ecology and social life of Phaner furcifer. In P. Charles-Dominique, H. M Cooper, A. Hladik, C. M. Hladik, E. Pages, G. F. Pariente et al. (Eds.), Nocturnal Malagasy Primates: Ecology, Physiology, and Behavior (pp. 75–95). New York: Academic Press.

    Google Scholar 

  • Clutton-Brock, T. H. (1989). Mammalian mating systems. Proceedings of the Royal Society of London Series B - Biological Sciences, 236, 339–372.

    CAS  Google Scholar 

  • Clutton-Brock, T. H., Guiness, F. E., & Albon, S. D. (1982). Red Deer-Behavior and Ecology of Two Sexes. Chicago: University of Chicago Press.

    Google Scholar 

  • Clutton-Brock, T. H., & Harvey, P. H. (1978). Mammals, resources, and reproductive strategies. Nature, 273, 191–195.

    Article  PubMed  CAS  Google Scholar 

  • Curtis, D. J., & Zaramody, A. (1999). Social structure and seasonal variation in the behaviour of Eulemur mongoz. Folia Primatologica, 70, 79–96.

    Article  CAS  Google Scholar 

  • Demes, B., Jungers, W. L., Fleagle, J. G., Wunderlich, R. E., Richmond, B. G., and Lemelin, P. (1996). Body size and leaping kinematics in Malagasy vertical clingers and leapers. Journal of Human Evolution, 31, 367–388.

    Article  Google Scholar 

  • Dunbar, R. (1995). The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Animal Behavior, 50, 1057–1070.

    Article  Google Scholar 

  • Emlen, S. T., & Oring, L. W. (1977). Ecology, sexual selection and the evolution of mating systems. Science, 197, 215–223.

    Article  PubMed  CAS  Google Scholar 

  • Emlen, S. T., & Wrege, P. H. (1986). Forced copulations and intraspecific parasitism: two costs of social living in the white bee-eater. Ethology, 71, 2–29.

    Article  Google Scholar 

  • Erhart, E. M., & Overdorff, D. J. (1998). Infanticide in Propithecus diadema edwardsi: An evaluation of the sexual selection hypothesis. International Journal of Primatology, 19, 73–81.

    Article  Google Scholar 

  • Fashing, P. J. (2001). Male and female strategies during intergroup encounters in guerezas (Colobus guereza): Evidence for resource defense mediated through males and a comparison with other primates. Behavioral Ecology and Sociobiology, 50, 219–230.

    Article  Google Scholar 

  • Fietz, J. (1999). Monogamy as a rule rather than exception in nocturnal lemurs: The case of the fat-tailed dwarf lemur, Cheirogaleus medius. Ethology, 105, 259–272.

    Article  Google Scholar 

  • Fietz, J. (2003). Primates: Cheirogaleus, Dwarf lemurs or fat tailed lemurs. In S. M. Goodman, & J. P. Benstead (eds.), The Natural History of Madagascar (pp. 1307–1309). Chicago: University of Chicago Press.

    Google Scholar 

  • Fietz., J., & Dausmann K. H. (2003). Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatologica, 74, 246–258.

    Article  Google Scholar 

  • Fietz, J., Zischler, H., Schwiegk, C., Tomiuk, J., Dausmann, K. H., & Ganzhorn, J. U. (2000). High rates of extra—. pair young in the pair-living fat-tailed dwarf lemur, Cheirogaleus medius. Behavioral Ecology and Sociobiology, 49, 8–17.

    Article  Google Scholar 

  • Fuentes, A. (1999). Re-evaluating primate monogamy. American Anthropologist, 100, 890–907.

    Article  Google Scholar 

  • Fuentes, A. (2002). Patterns and trends in primate pair bonds. International Journal of Primatology, 23, 953–978.

    Article  Google Scholar 

  • Ganzhorn, J. U., Abraham, J. P., & Razanahoera-Rakotomalala, M. (1985). Some aspects of the natural history and food selection of Avahi laniger. Primates, 26, 452–463.

    Article  Google Scholar 

  • Goodman, S. M. (2003). Predation on lemurs. In S. M. Goodman, & J. P. Benstead (eds), The Natural History of Madagascar (pp. 1221–1228). Chicago: University of Chicago Press.

    Google Scholar 

  • Gursky, S. (2000). Sociality in the spectral tarsier, Tarsius spectrum. American Journal of Primatology, 51, 89–101.

    Article  PubMed  CAS  Google Scholar 

  • Gursky, S. (2005). Associations between adul spectral tarsiers. American Journal of Physical Anthropology, 128, 74–83.

    Article  PubMed  Google Scholar 

  • Harcourt, C. (1991). Diet and behaviour of a nocturnal lemur, Avahi laniger, in the wild. Journal of Zoology London, 223, 667–674.

    Article  Google Scholar 

  • Hawkins, C. E. (2003). Cryptoprocta ferox, Fossa, Fosa. In S. M. Goodman, J. P. Benstead (eds.), The Natural History of Madagascar (pp. 1360–1363). Chicago: University of Chicago Press.

    Google Scholar 

  • Jolly, A. (1998). Pair bonding, female aggression and the evolution of lemur societies. Folia Primatologica, 69, 1–13.

    Article  Google Scholar 

  • Kappeler, P. M. (1998). Nests, tree holes and the evolution of primate life histories. American Journal of Primatology, 46, 7–33.

    Article  PubMed  CAS  Google Scholar 

  • Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23, 707–740.

    Article  Google Scholar 

  • Kleiman, D. G. (1977). Monogamy in mammals. Quarterly Review of Biology, 52, 39–69.

    Article  PubMed  CAS  Google Scholar 

  • Komers, P. E., & Brotherton, P. N. M. (1997). Female space use is the best predictor of monogamy in mammals. Proceedings of the Royal Society of London Series B - Biological Sciences, 264, 1261–1270.

    Article  CAS  Google Scholar 

  • Lawes, M. J., & Henzi, S. P. (1995). Inter-group encounters in blue monkeys: How territorial must a territorial species be? Animal Behavior, 49, 240–243.

    Article  Google Scholar 

  • Lewis, R. J. (2002). Beyond dominance: The importance of leverage. Quarterly Review of Biology, 77, 149–164.

    Article  PubMed  Google Scholar 

  • Lewis, R. J. (2005). Sex differences in scent—marking in Sifaka: Mating conflict or mate guarding. American Journal of Physical Anthropology, 128, 389–398.

    Article  PubMed  Google Scholar 

  • Lewis, R. J., Razafindrasamba, S. M., & Tolojanahary, J. P. (2003). Observed infanticide in a seasonal breeding prosimian (Propithecus verreauxi verreauxi) in Kirindy Forest, Madagascar. Folia Primatologica, 74, 101–103.

    Article  Google Scholar 

  • Martin, R. D. (1990). Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Mesnik, S. L. (1997). Sexual alliances: Evidence and evolutionary implications. In P. A. Gowaty (ed.), Feminism and Evolutionary Biology: Boundaries, Intersections, and Frontiers (pp. 207–260). Georgia: University of Georgia Press.

    Google Scholar 

  • Mitani, J. C., & Rodman, P. (1979). Territoriality: The relation of ranging pattern and home range size to defendability, with an analysis of territoriality among primate species. Behavioral Ecology and Sociobiology, 5, 241–251.

    Article  Google Scholar 

  • Müller, A. E. (1998). A prelimianry report on the social organization of Cheirogaleus medius (Cheirogaleide: Primates) in north-west Madagascar. Folia Primatologica, 69, 160–166.

    Article  Google Scholar 

  • Müller, A. E., & Thalmann, U. (2000). Origin and evolution of primate social organization: A reconstruction. Biological Reviews, 75, 405–435.

    Article  PubMed  Google Scholar 

  • Nievergelt, C. M., Mutschler, T., Feistner, A. T. C., & Woodruff, D. S. (2002). Social system and the Aloatran Gentle Lemur (Hapalemur griseus alaotrensis): Genetic characterization of group composition and mating system. American Journal of Primatology, 57:157–176.

    Article  PubMed  Google Scholar 

  • Norscia, I. (2006). Adaptation Strategies of a Nocturnal Lemur (Avahi laniger) in a Pluvial Littoral Forest of Southeastern Madagascar; Implications for Conservation. Italy: Ph.D. dissertation, University of Pisa.

    Google Scholar 

  • Norscia, I. (2007). Pilot survey of avahi population (woolly lemurs) in the littoral forest fragments of southeast Madagascar. Primates doi:10.1007/s10329-007-0061-2.

  • Norscia, I., Carrai, V., & Borgognini-Tarli, S. M. (2006). Influence of dry season, food quality and quantity on behavior and feeding strategy of Propithecus verreauxi in Kirindy, Madagascar. International Journal of Primatology, 27, 1001–1022.

    Google Scholar 

  • Norscia, I., Jolly, A., Rahanitriniaina, O. G., & Donati, G. (2006). Preliminary survey of lemur density in the semimontane rainforest of Anka, Fort-Dauphin region. Lemur News, 10.

  • Overdorff, D. J., Strait, S. G., & Telo, A. (1997). Seasonal variation in activity and diet in a small-bodied folivorous primate, Hapalemur griseus, in southeastern Madagascar. American Journal of Primatology, 43, 211–223.

    Article  PubMed  CAS  Google Scholar 

  • Palagi, E., Telara, S., & Borgognini-Tarli, S. M. (2004). Reproductive strategies in Lemur catta: Balance among sending, receiving, and countermarking scent signals. International Journal of Primatology, 25, 1019–1039.

    Article  Google Scholar 

  • Palombit, R. A. (1999). Infanticide and the evolution of pair bonds in nonhuman primates. Evolutionary Anthropology, 7, 117–129.

    Article  Google Scholar 

  • Pereira, M. E., & Weiss, M. L. (1991). Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behavioral Ecology and Sociobiology, 28, 141–152.

    Article  Google Scholar 

  • Pimley, E. R., Bearder, S. K., & Dixson, A. F. (2005a). Home range analysis of Perodicticus potto and Sciurocheirus cameronensis. International Journal of Primatology, 26, 191–206.

    Article  Google Scholar 

  • Pimley, E. R., Bearder, S. K., & Dixson, A. F. (2005b). Social organization of the Milne-Edward’s Potto. American Journal of Primatology, 66, 317–330.

    Article  PubMed  Google Scholar 

  • Powzyk, J. A. (1997). The Socio-ecology of Two Sympatric Indriids: Propithecus diadema diadema and Indir indri: A Comparison of Feeding Strategies and Their possible repercussion on species-specific behaviors. Durham, NC: Ph.D. Dissertation, Duke University.

    Google Scholar 

  • Rasoloharijaona, S., Rakotosamimanana, R., Randrianambinina B., & Zimmermann, E. (2003). Pair-specific usage of sleeping sites and their implications for social organization in a nocturnal Malagasy primate, the Milne Edwards’ sportive lemur Lepilemur edwardsi. American Journal of Physical Anthropology, 122, 252–258.

    Article  Google Scholar 

  • Reichard, U. (1995). Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology, 100, 99–112.

    Google Scholar 

  • Ross, C. (2001). Park or ride? Evolution of infant carrying in primates. International Journal of Primatology, 22, 749–771.

    Article  Google Scholar 

  • Rutberg, A. T. (1983). The evolution of monogamy in primates. Journal of Theoretical Biology, 104, 93–112.

    Article  PubMed  CAS  Google Scholar 

  • Schuiling, G. A. (2003). The benefit and the doubt: Why monogamy? Journal of Psychosomatic Obstetrics and Gynecology, 24, 55–61.

    Article  PubMed  CAS  Google Scholar 

  • Schülke, O. (2001). Social anti-predator behaviour in a nocturnal lemur. Folia Primatologica, 72, 332–334.

    Article  Google Scholar 

  • Schülke, O. (2003a). To breed or not to breed — food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behavioral Ecology and Sociobiology, 55, 11–21.

    Article  Google Scholar 

  • Schülke, O. (2003b). Phaner furcifer, Fork-marked lemur, Vakihandry, Tanta. In S. M. Goodman, & J. P. Benstead (eds.), The Natural History of Madagascar (pp. 1318–1320). Chicago: University of Chicago Press.

    Google Scholar 

  • Schülke, O. (2005). Evolution of pair-living in Phaner furcifer. International Journal of Primatology, 26, 903–919.

    Article  Google Scholar 

  • Schülke, O., & Kappeler, P. M. (2003). So near and yet so far. Territorial pairs, but low cohesion between pair partners in a nocturnal lemur, Phaner furcifer. Animal Behavior, 65, 331–343.

    Article  Google Scholar 

  • Seaman, D. E., Griffith, B., & Powell, R. A. (1998). KERNELHR: A program for estimating animal home ranges. Wildlife Society Bulletin, 26, 95–100.

    Google Scholar 

  • Southwood, T. R. E. (1996) Ecological Methods: With Particular to the Study of Insect Populations. London: Chapman & Hall.

    Google Scholar 

  • Tattersall, I. (1982). The Primates of Madagascar. New York: Columbia University Press.

    Google Scholar 

  • Thalmann, U. (2001). Food resources in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology, 22, 287–324.

    Article  Google Scholar 

  • Thalmann, U. (2003). Avahi, wolly lemurs, avahy, fotsy-fe, ampongy, tsarafangitra, dadintsifaky. In S. M. Goodman, & J. P. Benstead (eds.), The Natural History of Madagascar (pp. 1340–1342). Chicago: University of Chicago Press.

    Google Scholar 

  • Thalmann, U., & Ganzhorn, J. U. (2003). Lepilemur, Sportive lemur. In S. M. Goodman, & J. P. Benstead (eds.), The Natural History of Madagascar (pp. 1336–1340). Chicago: University of Chicago Press.

    Google Scholar 

  • van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen, & R. A. Foley (eds.), Comparative Socioecology. The Behavioural Ecology of Humans and Other Mammals (pp. 195–218). Oxford: Blackwell.

    Google Scholar 

  • van Schaik, C. P. (2000). Vulnerability to infanticide by males: Patterns among mammals. In C. P. van Schaik, & C. H. Janson (eds.), Infanticide by Males and Its Implications (pp. 61–71). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • van Schaik, C. P., & Dunbar, R. I. M. (1990). The evolution of monogamy in large primates: A new hypothesis and some crucial tests. Behaviour, 115, 241–261.

    Google Scholar 

  • van Schaik, C. P., & Kappeler, P. M. (1993). Life history, activity pattern and lemur social systems. In P. M. Kappeler, & J. U. Ganzhorn (eds.), Lemur Social Systems and Their Ecological Basis (pp. 241–260). New York: Plenum Press.

    Google Scholar 

  • van Schaik, C. P., & van Hoof, J. (1983). On the ultimate causes of primates social systems. Behaviour, 85, 91–117.

    Google Scholar 

  • Warren, R. D., & Crompton, R. H. (1997). Locomotor ecology of Lepilemur edwardsi and Avahi occidentalis. American Journal of Physical Anthropology, 104, 471–486.

    Article  PubMed  CAS  Google Scholar 

  • Warren, R. D., & Crompton, R. H. (1998). Diet, body size and the energy costs of locomotion in salutatory primates. Folia Primatologica, 69, 86–100.

    Article  Google Scholar 

  • Wittenberger, J. F., & Tilson, R. L. (1980). The evolution of monogamy: Hypothesis and evidence. Annual Review of Ecology and Systematics, 11, 197–232.

    Article  Google Scholar 

  • Wrangham, R. W., & Rubenstein, D. I. (1986). Social evolution in birds and mammals. In D. I. Rubenstein, & R. W. Wrangham (eds.), Ecology and Social Evolution: Birds and Mammals (pp. 452–470). Princeton, NJ: Princeton University Press.

    Google Scholar 

  • Wright, P. C. (1986). Ecological correlates of monogamy in Aotus and Callicebus. In J. Else, & P. Leein (eds.), Primate Ecology and Conservation (pp. 159–167). Cambridge, U.K.: Cambridge University Press.

    Google Scholar 

  • Wright, P. C. (1990). Patterns of parental care in primates. International Journal of Primatology, 11, 89–102.

    Article  Google Scholar 

  • Wright, P. C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. Yearbook of Physical Anthropology, 42, 31–72.

    Article  Google Scholar 

  • Wronski, T., & Apio, A. (2005). Home range overlap, social vicinity and agonistic interactions denoting matrilineal organization in bushbuck, Tragelaphus scriptus. Behavioral Ecology and Sociobiology doi:10.1007/s00265-005-0128-2.

  • Zaramody, A., Fausser, J. L., Roos, C., Zinner, D., Andriaholinirina, N., Rabarivola, C. et al. (2006). Molecular phylogeny and taxonomic revision of the eastern woolly lemurs (Avahi laniger). Primate Reports, 74, 9–22.

    Google Scholar 

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Acknowledgments

We thank the Commission Tripartite du Département des Eaux et Forêt, the Parque Botanique et Zoologique de Tsimbasasa, and the Université d’Antananarivo for research permits; Jean-Baptiste Ramanamanjato, Manon Vincelette, and the staff of the conservation section of QMM for providing support for our research; Givet, Kadoff , Roline, and Josette, for their invaluable help in the field; and the people of the villages of Ambandriky and S. Luce for providing assistance when needed.

We also thank Joerg Ganzhorn for the possibility of doing this research in the field (part of the Ph.D. program of I. Norscia), Giuseppe Donati for opening the door of Sainte Luce, Stacey Schmidt for the first linguistic revision, Barbara Leporini for data elaboration support, and Elisabetta Palagi for providing useful discussion on the manuscript. Finally, we thank the 2 anonymous reviewers who improved the manuscript with their comments and suggestions. This research was partly funded by MIUR.

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  1. Dipartimento di Biologia and Centro Interdipartimentale, Museo di Storia Naturale e del Territorio, Università di Pisa, 56011, Calci, Pisa, Italy

    Ivan Norscia & Silvana M. Borgognini-Tarli

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Norscia, I., Borgognini-Tarli, S.M. Ranging Behavior and Possible Correlates of Pair-Living in Southeastern Avahis (Madagascar). Int J Primatol 29, 153–171 (2008). https://doi.org/10.1007/s10764-007-9219-4

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