The Function of Howling in the Ring-Tailed Lemur (Lemur catta)

Abstract

Long calls are sex-specific vocalizations used for mate attraction or mate defense in many animal species. Ring-tailed lemurs (Lemur catta), female-dominant strepsirrhines, have a male-specific long call termed a howl, with proposed functions that have never been empirically tested. I aimed to investigate why ring-tailed lemur males howl and to test whether the mate defense and mate attraction hypotheses for long-calling were applicable to this species. From March to July 2010, I collected 600 h of focal data on 25 males aged ≥3 year at Beza Mahafaly Special Reserve, Madagascar. I observed each male continuously for 30 min at a time and noted all agonism using one–zero sampling at 2.5-min intervals. I calculated male dominance rank from these data. I recorded days when female estrus occurred and noted howling and intergroup encounters using all-occurrences sampling. Howling rate was not significantly related to female estrus or male dominance rank, providing no support for the mate attraction hypothesis or the intragroup mate defense hypothesis. In contrast, the intergroup mate defense hypothesis was strongly supported. During intergroup encounters, male howling rate significantly increased compared to howling rate at times without other groups present, and a greater number of males participated in multimale howling choruses when compared to times without nongroup members present. My results suggest that male ring-tailed lemurs howl to advertise their presence and location to other groups, but not to male or female members of their own group. Howling could discourage male immigration by advertising the number of males already present in a group. Long calls are used for similar mate defense purposes during intergroup encounters by other primates, including Thomas langurs (Presbytis thomasi) and chacma baboons (Papio ursinus).

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References

  1. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–265.

    PubMed  Article  CAS  Google Scholar 

  2. Andrew, R. (1963). The origins and evolution of calls and facial expressions of the primates. Behaviour, 20, 1–109.

    Article  Google Scholar 

  3. Beach, F. (1976). Sexual attractivity, proceptivity, and receptivity in female mammals. Hormones and Behavior, 7, 105–138.

    PubMed  Article  CAS  Google Scholar 

  4. Bradbury, J., & Vehrencamp, S. (1998). Principles of animal communication. Sunderland: Sinauer Associates.

    Google Scholar 

  5. Budnitz, N., & Dainis, K. (1975). Lemur catta: Ecology and behavior. In I. Tattersall & R. Sussman (Eds.), Lemur biology (pp. 219–235). New York: Plenum Press.

    Google Scholar 

  6. Cheney, D., & Seyfarth, R. (1977). Behavior of adult and immature male baboons during intergroup encounters. Nature, 269, 404–406.

    Article  Google Scholar 

  7. Cowlishaw, G. (1992). Song function in gibbons. Behaviour, 121, 131–153.

    Article  Google Scholar 

  8. Cowlishaw, G. (1995). Behavioural patterns in baboon group encounters: the role of resource competition and male reproductive tactics. Behaviour, 132, 75–86.

    Article  Google Scholar 

  9. Cuozzo, F., & Sauther, M. (2006). Severe wear and tooth loss in wild ring-tailed lemurs (Lemur catta): a function of feeding ecology, dental structure, and individual life history. Journal of Human Evolution, 51, 490–505.

    PubMed  Article  Google Scholar 

  10. Cuozzo, F., Sauther, M., Gould, L., Sussman, R., Villers, L., & Lent, C. (2010). Variation in dental wear and tooth loss in known-aged, older ring-tailed lemurs (Lemur catta): a comparison between wild and captive individuals. American Journal of Primatology, 72, 1026–1037.

    PubMed  Article  Google Scholar 

  11. Delgado, R. (2006). Sexual selection in the loud calls of male primates: signal content and function. International Journal of Primatology, 27, 5–25.

    Article  Google Scholar 

  12. Gould, L. (1994). Patterns of affiliative behavior in adult male ringtailed lemurs (Lemur catta) at the Beza-Mahafaly reserve, Madagascar. Ph.D. dissertation, Washington University, Missouri.

  13. Gould, L., & Zeigler, T. (2007). Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta). American Journal of Primatology, 69, 1325–1339.

    PubMed  Article  CAS  Google Scholar 

  14. Gould, L., Sussman, R., & Sauther, M. (2003). Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve, Madagascar: a 15-year perspective. American Journal of Physical Anthropology, 120, 182–194.

    PubMed  Article  Google Scholar 

  15. Grinnell, J., Packer, C., & Pusey, A. (1995). Cooperation in male lions: kinship, reciprocity or mutualism? Animal Behavior, 49, 95–105.

    Article  Google Scholar 

  16. Jolly, A. (1966). Lemur behavior: A Madagascar field study. London: University of Chicago Press.

    Google Scholar 

  17. Jones, K. (1983). Inter-troop transfer of Lemur catta males at Berenty, Madagascar. Folia Primatologica, 40, 145–160.

    Article  CAS  Google Scholar 

  18. Kitchen, D. (2004). Alpha male black howler monkey responses to loud calls: effect of numeric odds, male companion behaviour and reproductive investment. Animal Behavior, 67, 125–139.

    Article  Google Scholar 

  19. Kitchen, D. (2006). Experimental test of female black howler monkey (Alouatta pigra) responses to loud calls from potentially infanticidal males: effects of numeric odds, vulnerable offspring and companion behavior. American Journal of Physical Anthropology, 131, 73–83.

    PubMed  Article  Google Scholar 

  20. Kitchen, D., Seyfarth, R., Fischer, J., & Cheney, D. (2003). Loud calls as indicators of dominance in male baboons (Papio cynocephalus ursinus). Behavioral Ecology and Sociobiology, 53, 374–384.

    Google Scholar 

  21. Kitchen, D., Cheney, D., & Seyfarth, R. (2004). Factors mediating inter-group encounters in chacma baboons (Papio cynocephalus ursinus). Behaviour, 141, 197–218.

    Article  Google Scholar 

  22. Kitchen, D., Horwich, R., & James, R. (2004). Subordinate male black howler monkey (Alouatta pigra) responses to loud calls: experimental evidence for the effects of intra-group male relationships and age. Behaviour, 141, 703–723.

    Article  Google Scholar 

  23. Koyama, N. (1988). Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty, Madagascar. Primates, 29, 163–175.

    Article  Google Scholar 

  24. Lewis, R., & van Schaik, C. (2007). Bimorphism in male Verreaux’s sifaka in the Kirindy forest of Madagascar. International Journal of Primatology, 28, 159–182.

    Article  Google Scholar 

  25. Macedonia, J. (1986). Individuality in a contact call of the ringtailed lemur. American Journal of Primatology, 11, 163–179.

    Article  Google Scholar 

  26. Macedonia, J. (1990). Vocal communication and antipredator behavior in the ringtailed lemur (Lemur catta). Ph.D. dissertation, Duke University, Durham, North Carolina.

  27. Macedonia, J. (1993). The vocal repertoire of the ringtailed lemur (Lemur catta). Folia Primatologica, 61, 186–217.

    Article  CAS  Google Scholar 

  28. Martin, P., & Bateson, P. (2007). Measuring behavior: An introductory guide (3rd ed.). Cambridge: Cambridge University Press.

    Google Scholar 

  29. Maynard Smith, J. (1982). Evolution and the theory of games. Oxford: Oxford University Press.

    Google Scholar 

  30. McComb, K., Packer, C., & Pusey, A. (1994). Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Animal Behavior, 47, 379–387.

    Article  Google Scholar 

  31. Mertl-Milhollen, A., Gustafson, H., Budnitz, N., Dainis, K., & Jolly, A. (1979). Population and territory stability of the Lemur catta at Berenty, Madagascar. Folia Primatologica, 31, 106–122.

    Article  Google Scholar 

  32. Mertl-Millhollen, A. (2006). Scent marking as resource defense by female Lemur catta. American Journal of Primatology, 68, 605–621.

    PubMed  Article  Google Scholar 

  33. Mitani, J. (1988). Male gibbon (Hylobates agilis) singing behavior: natural history, song variations and function. Ethology, 79, 177–194.

    Article  Google Scholar 

  34. Parga, J. (2006). Male mate choice in Lemur catta. International Journal of Primatology, 27, 107–131.

    Article  Google Scholar 

  35. Parga, J. (2010). Evaluation of male inter-troop transfer as a mating strategy in ring-tailed lemurs on St. Catherines Island, USA. Folia Primatologica, 81, 146–162.

    Article  Google Scholar 

  36. Parga, J., & Lessnau, R. (2008). Dispersal among male ring-tailed lemurs (Lemur catta) on St. Catherines Island. American Journal of Primatology, 70, 650–660.

    PubMed  Article  CAS  Google Scholar 

  37. Pereira, M., & Kappeler, P. (1997). Divergent systems of agonistic behaviour in lemurid primates. Behaviour, 134, 225–274.

    Article  Google Scholar 

  38. Petter, J., & Charles-Dominique, P. (1979). Vocal communication in prosimians. In G. Doyle & R. Martin (Eds.), The study of prosimian behavior (pp. 247–305). New York: Academic.

    Google Scholar 

  39. Pride, R. (2005). Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta). Behavioral Ecology, 16, 550–560.

    Article  Google Scholar 

  40. Raemaekers, J., Raemaekers, P., & Haimoff, E. (1984). Loud calls of the gibbon (Hylobates lar): repertoire, organisation and context. Behaviour, 91, 146–189.

    Article  Google Scholar 

  41. Sauther, M. (1991). Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. American Journal of Physical Anthropology, 84, 463–477.

    Article  Google Scholar 

  42. Sauther, M., & Cuozzo, F. (2008). Somatic variation in living, wild ring-tailed lemurs (Lemur catta). Folia Primatologica, 79, 55–78.

    Article  Google Scholar 

  43. Sauther, M., & Cuozzo, F. (2009). The impact of fallback foods on wild ring-tailed lemur biology: a comparison of intact and anthropogenically disturbed habitat. American Journal of Physical Anthropology, 140, 671–686.

    PubMed  Article  Google Scholar 

  44. Sauther, M., Sussman, R., & Cuozzo, F. (2002). Dental and general health in a population of wild ring-tailed lemurs: a life history approach. American Journal of Physical Anthropology, 117, 122–132.

    PubMed  Article  Google Scholar 

  45. Sekulic, R. (1982). The function of howling in red howler monkeys (Alouatta seniculus). Behaviour, 81, 38–54.

    Article  Google Scholar 

  46. Sussman, R. (1991). Demography and social organization of freeranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. American Journal of Physical Anthropology, 84, 43–58.

    Article  Google Scholar 

  47. Sussman, R. (1992). Male life history and intergroup mobility among ringtailed lemurs (Lemur catta). International Journal of Primatology, 13, 395–413.

    Article  Google Scholar 

  48. Sussman, R., & Ratsirarson, J. (2006). Beza Mahafaly special reserve: A research site in southwestern Madagascar. In A. Jolly, R. Sussman, N. Koyama, & H. Rasamimanana (Eds.), Ringtailed lemur biology: Lemur catta in Madagascar (pp. 43–51). New York: Springer.

    Google Scholar 

  49. Sussman, R., Richard, A., Ratsirarson, J., Sauther, M., Brockman, D., Gould, L., Lawler, R., & Cuozzo, F. (2012). Beza Mahafaly Special Reserve: A research site in southwestern Madagascar. In P. Kappeler & D. Watts (Eds.), Long term field studies of primates (pp. 45–66). New York: Springer.

    Google Scholar 

  50. Taylor, L. (1986). Kinship, dominance, and social organization in a semi-free ranging group of ringtailed lemurs (Lemur catta). Ph.D. dissertation, Washington University, St. Louis, Missouri.

  51. Taylor, L., & Sussman, R. (1985). A preliminary study of kinship and social organization in a semi-free-ranging group of Lemur catta. International Journal of Primatology, 6, 601–614.

    Article  Google Scholar 

  52. van Horn, R., & Resko, J. (1977). Reproductive cycle of the ringtailed lemur (Lemur catta): sex steroid levels and sexual receptivity under controlled photoperiods. Endocrinology, 101, 1579.

    PubMed  Article  Google Scholar 

  53. van Schaik, C., Assink, P., & Salafsky, N. (1992). Territorial behavior in southeast Asianlangurs: resource defense or mate defense? American Journal of Primatology, 26, 233–242.

    Article  Google Scholar 

  54. Waser, P. (1975). Experimental playbacks show vocal mediation of intergroup avoidance in a forest monkey. Nature, 255, 56–58.

    Article  Google Scholar 

  55. Wich, S., & Nunn, C. (2002). Do male “long-distance calls” function in mate defense? A comparative study of long-distance calls in primates. Behavioral Ecology and Sociobiology, 52, 474–484.

    Article  Google Scholar 

  56. Wilson, M., Hauser, M., & Wrangham, R. (2001). Does participation in intergroup conflict depend on numerical assessment, range location or rank for wild chimpanzees? Animal Behavior, 61, 1203–1216.

    Article  Google Scholar 

  57. Zimmermann, E. (1995). Loud calls in nocturnal prosimians: Structure, evolution, and ontogeny. In E. Zimmermann, J. Newman, & U. Jürgens (Eds.), Current topics in primate vocal communication (pp. 47–72). New York: Plenum Press.

    Google Scholar 

  58. Zimmermann, E., & Lerch, C. (1993). The complex acoustic design of an advertisement call in male mouse lemurs (Microcebus murinus, Prosimii, Primates) and sources of its variation. Ethology, 93, 211–224.

    Article  Google Scholar 

  59. Zumpe, D., & Michael, R. (1986). Dominance index: a simple measure of relative dominance status in primates. American Journal of Primatology, 10, 291–300.

    Article  Google Scholar 

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Acknowledgments

All data were collected in Madagascar with the approval of Madagascar National Parks (MNP), formerly known as Association Nationale pour la Gestion des Aires Protégées (ANGAP). I thank Jacky Ibrahim Antho Youssouf and Andry Randrianandrasana at the Beza Mahafaly Special Reserve for their facilitation of my project. My appreciation goes to Jeannin Rainavanosy and Joel Ratsirarson of the Département des Eaux et Forêts de l’Ecole Supérieure des Sciences Agronomiques (ESSA) and MNP/ANGAP for permission to work at Beza Mahafaly, and to Madagascar Institut pour la Conservation des Ecosystèmes Tropicaux (MICET) and Benjamin Andriamihaja for their help with logistics. I thank Elahavelo, Efitiria, Enafa, Edouard, Ralaevo, and Monja of the Beza Mahafaly Ecological Monitoring team for field assistance, and Teague O’Mara and his assistants for their help with orientation at Beza.

I sincerely thank Michelle Sauther and Frank Cuozzo for sharing ring-tailed lemur age data. I also thank Joyce Parga and Shawn Lehman for their excellent comments on this manuscript, Drew Rendall and Shannon Digweed for introducing me to acoustic research, and Ryan Janzen for technological aid. Finally, I am grateful to Joanna Setchell and two anonymous reviewers for their helpful suggestions. For funding, I acknowledge an Alexander Graham Bell Canada Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada, the American Museum of Natural History, the Edward. J. Noble Foundation, St. Catherines Island Foundation, Ontario Graduate Scholarships, and the University of Toronto.

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Correspondence to Laura M. Bolt.

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Bolt, L.M. The Function of Howling in the Ring-Tailed Lemur (Lemur catta). Int J Primatol 34, 157–169 (2013). https://doi.org/10.1007/s10764-012-9654-8

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Keywords

  • Long call
  • Loud call
  • Mate attraction hypothesis
  • Mate defense hypothesis