Abstract
Mate-guarding is a widespread and efficient male strategy for increasing paternity success. The inability to guard entire female receptive phases or complete lack of mate-guarding has been explained by energetic constraints posed on males. The energetic costs per unit time a male can afford to suffer are thought to be lowest in year-round breeding species in marginal habitats and highest in seasonally breeding species in rich habitats. Here we test the prediction that mate-guarding is energetically costly in seasonal breeders in marginal habitats. We observed all males in one group of wild Assamese macaques (Macaca assamensis) for two 4-mo mating seasons and recorded activity and travel paths via focal animal sampling, physical condition via visual inspection, and collected feces for analysis of glucocorticoid levels. Generalized linear mixed model (GLMM) analyses did not reveal an effect of mate-guarding on time spent feeding or moving or on distance traveled, travel speed, directedness of travel, or glucocorticoid levels. This lack of mate-guarding costs was consistent with the lack of a relationship between individual time spent mate-guarding and change in physical condition over the mating season. Within the limitations of our study the results do not support the idea that seasonally breeding males in marginal habitats face energetic costs of mate-guarding. With others we suggest instead that though these costs may be found in species where strength, size, and mass predict rank, mating, and reproductive success, males may not engage in costly mate-guarding in species such as Assamese macaques where also smaller, weaker males may attain high social status via political coalitions or other routes alternative to direct contest over guarded females.
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References
Alberts, S., Altmann, J., & Wilson, M. (1996). Mate guarding constrains foraging activity of male baboons. Animal Behaviour, 51, 1269–1277.
Alberts, S., Watts, H., & Altmann, J. (2003). Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons Papio cynocephalus. Animal Behaviour, 65(q), 821–840.
Alberts, S. C. (2012). Magnitude and sources of variation in male reproductive performance. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 412–431). Chicago: The University of Chicago Press.
Altmann, S. A. (1962). A field study of the sociobiology of the rhesus monkey, Macaca mulatta. Annals of the New York Academy of Sciences, 102, 338–435.
Ancona, S., Drummond, H., & Zaldívar-Rae, J. (2010). Male whiptail lizards adjust energetically costly mate guarding to male-male competition and female reproductive value. Animal Behaviour, 79(1), 75–82.
Berard, J., Nurnberg, P., Epplen, J., & Schmidtke, J. (1994). Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour, 129(3–4), 177–201.
Bercovitch, F., & Nürnberg, P. (1996). Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). Journal of Reproduction and Fertility, 107, 59–68.
Bercovitch, F. B. (1983). Time budgets and consortships in olive baboons (Papio anubis). Folia Primatologica, 41, 180–190.
Bergman, T., Beehner, J., Cheney, D., Seyfarth, R., & Whitten, P. (2005). Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Animal Behaviour, 70(3), 703–713.
Berman, C. M., & Schwartz, S. (1988). A nonintrusive method for determining relative body fat in freeranging monkeys. American Journal of Primatology, 14, 53–64.
Bertrand, M. (1969). The behavioral repertoire of the stumptail macaque. Basel: S. Karger.
Birkhead, T. (1987). Sperm competition in birds. TRENDS in Ecology and Evolution, 2(9), 268–272.
Borries, C., Larney, E., Kreetiyutanont, K., & Koenig, A. (2002). The diurnal primate community in a dry evergreen forest in Phu Khieo Wildlife Sanctuary, Northeast Thailand. Natural History Bulletin of the Siam Society, 50(1), 75–88.
Brotherton, P., & Komers, P. (2003). Mate guarding and the evolution of social monogamy in mammals. In U. Reichard & C. Boesch (Eds.), Monogamy: Mating strategies and partnerships in birds, humans and other mammals (pp. 42–58). Cambridge: Cambridge University Press.
Coelho, A. M., Bramblett, C. A., Quick, L. B., & Bramblett, S. S. (1976). Resource availability and population density in primates: a socio-bioenergetic analysis of the energy budgets of Guatemalan howler and spider monkeys. Primates, 17, 63–80.
Cooper, W. E., & Vitt, L. J. (2002). Increased predation risk while mate guarding as a cost of reproduction for male broad-headed skinks (Eumeces laticeps). Acta Ethologica, 5, 19–23.
De Waal, F. B. M., & Luttrell, L. M. (1989). Toward a comparative socioecology of the genus Macaca: different dominance styles in rhesus and stumptailed macaques. American Journal of Primatology, 19, 83–109.
Deschner, T., Kratzsch, J., & Hohmann, G. (2008). Urinary C-peptide as a method for monitoring body mass changes in captive bonobos (Pan paniscus). Hormones and Behavior, 4, 620–626.
Dubuc, C., Muniz, L., Heistermann, M., Widdig, A., & Engelhardt, A. (2012). Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques? Hormones and Behavior, 61(5), 696–705.
Duffy, K., Wrangham, R., & Silk, J. (2007). Male chimpanzees exchange political support for mating opportunities. Current Biology, 17(15), R586–R587.
Emery Thompson, M., & Knott, C. (2008). Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Hormones and Behavior, 53, 526–535.
Emery Thompson, M., Muller, M. N., Wrangham, R. W., Lwanga, J. S., & Potts, K. B. (2009). Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Hormones and Behavior, 55(2), 299–305.
Fichtel, C., Kraus, C., Ganswindt, A., & Heistermann, M. (2007). Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux’s sifakas (Propithecus verreauxi). Hormones and Behavior, 51, 640–648.
Foster, M. W., Gilby, I. C., Murray, C. M., Johnson, A., Wroblewski, E. E., & Pusey, A. E. (2009). Alpha male chimpanzee grooming patterns: implications for dominance “style”. American Journal of Primatology, 71(2), 136–144.
Fürtbauer, I., Heistermann, M., Schülke, O., & Ostner, J. (2011). Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis). PLoS ONE, 6(8), e23105.
Fürtbauer, I., Schülke, O., Heistermann, M., & Ostner, J. (2010). Reproductive and life history parameters of wild female Assamese macaques (Macaca assamensis). International Journal of Primatology, 31, 501–517.
Ganswindt, A., Palme, R., Heistermann, M., Borragan, S., & Hodges, J. (2003). Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. General and Comparative Endocrinology, 134, 156–166.
Georgiev, A. V. (2012). Energetic costs of reproductive effort in male chimpanzees. Ph.D. dissertation, Harvard University.
Georgiev, A. V., Emery Thompson, M., Lotana, A. L., & Wrangham, R. W. (2011). Seed predation by bonobos (Pan paniscus) at Kokolopori, Democratic Republic of Congo. Primates, 52, 309–314.
Gilby, I. C., Brent, L. J. N., Wroblewski, E. E., Rudicell, R. S., Hahn, B. H., Goodall, J., et al. (2012). Fitness benefits of coalitionary aggression in male chimpanzees. Behavioral Ecology and Sociobiology, 1–9.
Girard-Buttoz, C. (2013). Costs of mate-guarding in male long-tailed macaques (Macaca fascicularis). PhD thesis. University of Göttingen, Göttingen, Germany.
Girard-Buttoz, C., Heistermann, M., Rahmi, E., Marzec, A., Agil, M., Fauzan, P. A., et al. (2014). Mate-guarding constrains feeding activity but not energetic status of wild male longtailed macaques (Macaca fascicularis). Behavioral Ecology and Sociobiology. doi:10.1007/s00265-013-1673-8.
Harris, T. R., Chapman, C. A., & Monfort, S. L. (2010). Small folivorous primate groups exhibit behavioral and physiological effects of food scarcity. Behavioral Ecology, 21(1), 46–56.
Hasselquist, D., & Bensch, S. (1991). Trade-off between mate guarding and mate attraction in the polygynous great reed warbler. Behavioral Ecology and Sociobiology, 28(3), 187–193.
Heesen, M., Rogahn, S., Ostner, J., & Schülke, O. (2013). Food abundance affects energy intake and reproduction in frugivorous female Assamese macaques. Behavioral Ecology and Sociobiology, 67, 1053–1066.
Heistermann, M., Finke, M., & Hodges, J. K. (1995). Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. American Journal of Primatology, 37, 275–284.
Heistermann, M., Palme, R., & Ganswindt, A. (2006). Comparison of different enzymeimmunoassays for assessment of adrenocortical activity in primates based on fecal analysis. American Journal of Primatology, 68, 257–273.
Henzi, S. P., Clarke, P. M. R., Van Schaik, C. P., Pradhan, G. R., & Barrett, L. (2010). Infanticide and reproductive restraint in a polygynous social mammal. Proceedings of the National Academy of Sciences of the USA, 107(5), 2130–2135.
Higham, J., Heistermann, M., & Maestripieri, D. (2013). The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behavioral Ecology and Sociobiology, 67, 19–30.
Higham, J. P., Heistermann, M., & Maestripieri, D. (2011). The energetics of male-male endurance rivalry in free-ranging rhesus macaques, Macaca mulatta. Animal Behaviour, 81(5), 1001–1007.
Hladik, C. M. (1977). A comparative study of the feeding startegies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys and apes (pp. 323–353). New York: Academic Press.
Hoffman, C. L., Higham, J. P., Heistermann, M., Prendergast, B., Coe, C., & Maestripieri, D. (2011). Immune function and HPA axis activity in free-ranging rhesus macaques. Physiology & Behavior, 104, 507–514.
Huck, M., Löttker, P., & Heymann, E. W. (2004). Proximate mechanisms of reproductive monopolization in male moustached tamarins (Saguinus mystax). American Journal of Primatology, 64, 39–56.
Koenig, A., Borries, C., Chalise, M. K., & Winkler, P. (1997). Ecology, nutrition, and timing of reproductive events in an Asian primate, the Hanuman langur (Presbytis entellus). Journal of Zoology (London), 243, 215–235.
Koenig, A., Borries, C., Suarez, S., Kreetiyutanont, K., & Prabnasuk, J. (2004). Socio-ecology of Phayre’s leaf monkeys (Trachypithecus phayrei) at Phu Khieo Wildlife Sanctuary. Journal of Wildlife in Thailand, 12, 150–163.
Komdeur, J. (2001). Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proceedings of the Royal Society of London B: Biological Sciences, 268, 2103–2111.
Kraus, C., Heistermann, M., & Kappeler, P. M. (1999). Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiology & Behavior, 66, 855–861.
Maestripieri, D., Schino, G., Aureli, F., & Troisi, A. (1992). A modest proposal: displacement activities as an indicator of emotions in primates. Animal Behaviour, 44(967), 979.
Martin, P., & Bateson, P. (2007). Measuring behaviour (3rd ed.). Cambridge: Cambridge University Press.
Mass, V., Heistermann, M., & Kappeler, P. M. (2009). Mate-guarding as a male reproductive tactic in Propithecus verreauxi. International Journal of Primatology, 30(3), 389–409.
Matsubara, M. (2003). Costs of mate guarding and opportunistic mating among wild male Japanese macaques. International Journal of Primatology, 24(5), 1057–1075.
Mcewen, B. S., & Wingfield, J. C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2–15.
Møller, A. P., & Birkhead, T. R. (1991). Frequent copulations and mate guarding as alternative paternity guards. Behaviour, 118, 170–186.
Mougeot, F. (2004). Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis. Animal Behaviour, 67, 1067–1076.
Mysterud, A., Langvatn, R., & Stenseth, N. C. (2004). Patterns of reproductive effort in male ungulates. Journal of Zoology, 264, 209–215.
Nagy, K. A., & Milton, K. (1979). Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology, 60, 475–480.
Noë, R., & Sluijter, A. A. (1990). Reproductive tactics of male savanna baboons. Behaviour, 113(1–2), 117–169.
Oliveira, R. F., Taborsky, M., & Brockman, H. J. (Eds.). (2008). Alternative reproductive tactics: An integrative approach. Cambridge: Cambridge University Press.
Ostner, J., Heistermann, M., & Schülke, O. (2008a). Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Hormones and Behavior, 54, 613–619.
Ostner, J., Heistermann, M., & Schülke, O. (2011). Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis). Hormones and Behavior, 59(1), 105–113.
Ostner, J., Kappeler, P. M., & Heistermann, M. (2002). Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 52, 485–495.
Ostner, J., Kappeler, P., & Heistermann, M. (2008b). Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 62(4), 627–638.
Ostner, J., Vigilant, L., Bhagavatula, J., Franz, M., & Schülke, O. (2013). Stable heterosexual bonds in a promiscuous primate. Animal Behaviour, 86, 623–631.
Packer, C. (1979). Male dominance and reproductive activity in Papio anubis. Animal Behaviour, 27, 37–45.
Pirovino, M., Heistermann, M., Zimmermann, N., Zingg, R., Clauss, M., Codron, D., et al. (2011). Fecal glucocorticoid measurements and their relation to rearing, behaviour and environmental factors in the pileated gibbon population (Hylobates pileatus) held in European zoos. International Journal of Primatology, 32, 1161–1178.
Plavcan, J., Van Schaik, C., & Mcgraw, W. (2005). Seasonality, social organization, and sexual dimorphism in primates. In D. Brockman & C. Van Schaik (Eds.), Seasonality in primates (pp. 401–441). Cambridge: Cambridge University Press.
Plavcan, J. M., & Van Schaik, C. P. (1997). Intrasexual competition and body weight dimorphism in anthropoid primates. American Journal of Physical Anthropology, 103, 37–68.
Polo, P., & Colmenares, F. (2012). Behavioural processes in social context: female abductions, male herding and female grooming in hamadryas baboons. Behavioural Processes, 90(2), 238–245.
Port, M., & Kappeler, P. M. (2010). The utility of reproductive skew models in the study of male primates, a critical evaluation. Evolutionary Anthropology, 19(2), 46–56.
Rasmussen, K. L. R. (1985). Changes in the activity budgets of yellow baboons (Papio cynocephalus) during sexual consortships. Behavioral Ecology and Sociobiology, 17, 161–170.
Riss, D., & Goodall, J. (1977). The recent rise to the alpha-rank in a population of free-living chimpanzees. Folia Primatologica, 27, 134–151.
Saeki, Y., Kruse, K. C., & Switzer, P. V. (2005). Physiological costs of mate guarding in the Japanese beetle (Popillia japonica Newman). Ethology, 111, 863–877.
Sapolsky, R., Romero, L., & Munk, A. (2000). How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews, 21(1), 55–89.
Schubert, M., Schradin, C., Roedel, H. G., Pillay, N., & Ribble, D. O. (2009). Male mate guarding in a socially monogamous mammal, the round-eared sengi: on costs and trade-offs. Behavioral Ecology and Sociobiology, 64(2), 257–264.
Schülke, O. (2001). Differential energy budget and monopolization potential of harem holders and bachelors in Hanuman langurs (Semnopithecus entellus): preliminary results. American Journal of Primatology, 55, 57–63.
Schülke, O., Bhagavatula, J., Vigilant, L., & Ostner, J. (2010). Social bonds enhance reproductive success in male macaques. Current Biology, 220, 2207–2210.
Schwagmeyer, P. L. (1988). Scramble-competition polygyny in an asocial mammal: male mobility and mating success. American Naturalist, 131, 885–892.
Setchell, J., Charpentier, M., & Wickings, E. (2005). Mate guarding and paternity in mandrills: factors influencing alpha male monopoly. Animal Behaviour, 70(5), 1105–1120.
Setchell, J. M., & Dixson, A. F. (2001). Circannual changes in the secondary sexual adornements of semifree-ranging male and female mandrills (Magrillus sphinx). American Journal of Primatology, 53, 109–121.
Shutt, C., Setchell, J., & Heistermann, M. (2012). Non-invasive monitoring of physiological stress in the western lowland gorilla (Gorilla gorilla gorilla): validation of a faecal glucocorticoid assay and methods for practical application in the field. General and Comparative Endocrinology, 179, 167–177.
Sparkes, T. C., Keough, D. P., & Parry, R. A. (1996). Energetic costs of mate guarding behavior in male stream-dwelling isopods. Oecologia, 106, 166–171.
Van Hooff, J. (1967). The facial displays of the catarrhine monkeys and apes. In D. Morris (Ed.), Primate ethology (pp. 7–68). London: Weidenfeld and Nicolson.
Van Noordwijk, M. A., & Van Schaik, C. P. (2004). Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In P. M. Kappeler & C. P. Van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 208–229). Cambridge: Cambridge University Press.
Weingrill, T., Lycett, J. E., Barrett, L., Hill, R. A., & Henzi, S. P. (2003). Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour, 140, 405–427.
Willisch, C. S., & Neuhaus, P. (2010). Social dominance and conflict reduction in rutting male Alpine ibex, Capra ibex. Behavioral Ecology, 21(2), 372–380.
Acknowledgments
We thank Melissa Emery Thompson and Alexander Georgiev for their invitation to contribute to this special issue. We thank the National Research Council of Thailand (NRCT) and the Department of National Parks, Wildlife and Plant Conservation Thailand (DNP) for permission to conduct this study and for all the support granted (Permit no. for this study 0004.3/3618, current permit 0002.3/2647). We thank J. Prabnasuk, K. Nitaya, Thanee Vongnak (current superintendent), and K. Kreetiyutanont (all Phu Khieo Wildlife Sanctuary) for their cooperation and permission to carry out this study. We thank A. Koenig and C. Borries (Stony Brook University), who developed the field site at Huai Mai Sot Yai. We thank D. Bootros, N. Bualeng, A. Chunchaen, I. Fürtbauer, M. Heesen, R. Intalo, N. Juntuch, S. Jumrudwong, M. Karlstetter, T. Kilawit, S. MacDonald, W. Nueorngshiyos, D. Pesek, N. Ponganan, S. Rogahn, P. Saaisawasthikul, B. Whitman and T. Wisate, and especially M. Swagemakers for their excellent help in the field. We also thank N. Bhumpakphan, W. Eiadthong (Kasetsart University), and W. Brockelman (Mahidol University) for their cooperation; A. Heistermann for her help in the laboratory work, and two anonymous reviewers and Alexander Georgiev for constructive comments. This research was supported by the Max-Planck Society, the National Geographic Society, and the German Initiative of Excellence through funds to University of Göttingen.
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Schülke, O., Heistermann, M. & Ostner, J. Lack of Evidence for Energetic Costs of Mate-Guarding in Wild Male Assamese Macaques (Macaca assamensis). Int J Primatol 35, 677–700 (2014). https://doi.org/10.1007/s10764-013-9748-y
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DOI: https://doi.org/10.1007/s10764-013-9748-y