Advances in Chemical Signals in Vertebrates pp 383-397 | Cite as
Musth, Sexual Selection, Testosterone, and Metabolites
Abstract
Musth is an annual, yet asynchronous, rut-like condition that is experienced by many adult African and Asian male elephants. Behaviorally, musth is characterized by heightened aggression, decreased feeding, urine dribbling, temporal gland secretion and enhanced sexual activity. Musth improves the access of a male to reproductively active females through increased mobility and a higher dominance ranking (intrasexual competition). Whether females prefer males in musth as mates is as yet uncertain (intersexual choice). Females can distinguish among the odors of males in musth and nonmusth. Although behavioral musth has been associated with greatly elevated plasma testosterone levels, a recent study in Sri Lanka shows that intensified aggressiveness follows maximal testosterone secretion and proposes that behavioral musth is a consequence of declining androgen levels. Our data from an Asian male elephant in North America suggest that either declining or rising serum testosterone may be related to “musth behaviors.” Our report demonstrates that certain aspects of body physiology are greatly altered during musth. Rather than a single state, our data suggest that musth is an ever-changing condition with some typical stages. Specific chemical compounds released at different stages of musth may serve individually or in combination as honest signals of male condition.
Keywords
Testosterone Level Sexual Selection Serum Testosterone Deviant Behavior Asian ElephantPreview
Unable to display preview. Download preview PDF.
References
- Andersson, M. 1982a. Female choice selects for extreme tail length in a widowbird. Nature, 299, 818–820.CrossRefGoogle Scholar
- Andersson, M. 1982b. Sexual selection, natural selection and quality advertisement. Biol. J. Linn. Soc., 77, 375–39CrossRefGoogle Scholar
- Andersson, M 1994. Sexual Selection. Princeton: Princeton University Press.Google Scholar
- Beehler, B.M. & Foster, M.S. 1988. Hotshots, hotspots and female preference in the organization of lek mating systems. Am. Nat., 131, 203–219.CrossRefGoogle Scholar
- Buss, I.O. 1991. Elephant Life: Fifteen Years of High Population Density. Ames: Iowa State University Press.Google Scholar
- Chandrasekharan K., Radhakrishnan K., Cheeran J., Nair, K.M. & Prabhakaran, T. 1992. Some observations on musth in captive elephants in Kerala (India). In: The Asian Elephant: Ecology, Biology, Disease, Conservation and Management (Ed. by E. Silas, M. Nair, & G. Nirmalan), pp. 71–74. India: Kerala Agricultural University.Google Scholar
- Cooper, K.A., Harder, J.D., Clawson, D.H., Fredrick, D.L., Lodge, G.A., Peachey, H.C., Spellmire, T.J. & Winstel, D.P. 1990. Serum testosterone and musth in captive male African and Asian elephants. Zoo Biol., 9, 297–306.CrossRefGoogle Scholar
- Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. London: Murray.CrossRefGoogle Scholar
- Dickerman, R.D., Pernikoff, D., Zachariah, N.Y., McConathy, W.J., Gracy, R.W. & Raven, P.V. 1994. Creatinine kinase and lactic dehydrogenase isozyme measurements in male Asian elephants (Elephas maximus) during musth and nonmusth. Clin. Chem., 40, 989.Google Scholar
- Doty, R. 1986. Odor-guided behavior in mammals. Experientia, 42, 251–211CrossRefGoogle Scholar
- Doty R. & Ferguson-Segal, M. 1989. Influence of castration on the odor detection performance of male rats. Behavior. Neurosci., 103, 691–693.CrossRefGoogle Scholar
- Dublin, H.T. 1983. Cooperation and reproductive competition among female African elephants. In:Social Behaviour of Female Vertebrates (Ed. by S.K. Wasser), pp. 291–313. New York: Academic Press.Google Scholar
- Dublin, H. T. 1996. Elephants of the Masai Mara, Kenya: seasonal habitat selection and group size patterns. Pachyderm, 22, 25–35.Google Scholar
- Eberhard, W.G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton: Princeton University Press.Google Scholar
- Eisenberg, J.F. 1980. Recent research on the biology of the Asiatic elephant (Elephas m. maximus) on Sri Lanka. Spolia Zeglavica, 35, 213–218.Google Scholar
- Eisenberg, J.F. & Lockhart, M.C. 1972. An ecological reconnaissance of Wilpattu National Park, Ceylon. Smithson. Contrib. Zool., 101, 1–118.CrossRefGoogle Scholar
- Eisenberg, J.F., McKay, G.M. & Jainudeen, M.R. 1971. Reproductive behavior of the Asiatic elephant (Elephas maximus maximus L.). Behaviour, 38, 193–2PubMedCrossRefGoogle Scholar
- Gaal T., Mezes M., Miskucza O. & Ribiczey-Szabo, P. 1993. Effect of fasting on blood lipid peroxidation parameters of sheep. Res. Vet. Sci., 55, 104–107.PubMedCrossRefGoogle Scholar
- Gadgil M. & Nair, P.V. 1984. Observations on the social behaviour of free ranging groups of tame Asiatic elephant (Elephas maximus Linn.). Proceedings of the Indian Academy of Science (Animal Science), 93, 225–233.CrossRefGoogle Scholar
- Hall-Martin, A.J. 1987. The role of musth in the reproductive strategy of the African elephant (Loxondonta africana). S. Afr. J. Sci., 83, 616–620.Google Scholar
- Hall-Martin, A.J. & Van der Walt, L.A. 1984. Plasma testosterone levels in relation to musth in the male African elephant. Koedoe, 27, 147–149.Google Scholar
- Harlow, H.J. & Braun, E.J. 1995. Kidney structure and function of obligate and facultative hibernators: the white-tailed prairie dog (Cynomys leucurus) and the black-tailed prairie dog (Cynomys ludovicianus). J. Comp. Physiol. B. Biochem. Sys. & Environ. Physiol., 165, 320–328.CrossRefGoogle Scholar
- Hellgren, E.C., Rogers, L.L. & Seal, U.S. 1993. Serum chemistry and hematology of black bears: physiological indices of habitat quality or seasonal preferences? J. Mamm., 74, 304–315.CrossRefGoogle Scholar
- Hess, D.L., Schmidt, A.M. & Schmidt, M.J. 1983. Reproductive cycle of the Asian elephant (Elephas maximus) in captivity. Biol. Reprod., 28, 161–113.CrossRefGoogle Scholar
- Hess, D.L., Spies, H.G. & Hendrickx, A.G. 1981. Diurnal steroid patterns during gestation in the rhesus macaque: onset, daily variation and the effects of dexamethasone treatment. Biol. Reprod., 24, 609–616.PubMedCrossRefGoogle Scholar
- Hochachka, P. 1973. Comparative intermediary metabolism. In: Comparative Animal Physiology (Ed. C. Prosser), pp. 212–278. Philadelphia: Saunders.Google Scholar
- Jainudeen, M.R., Katongole, C.B. & Short, R.V. 1972a. Plasma testosterone levels in relation to musth and sexual activity in the male Asiatic elephant, Elephas maximus. J. Reprod. Fertil., 29, 99–103.CrossRefGoogle Scholar
- Jainudeen, M.R., McKay, G.M. & Eisenberg, J.F. 1972b. Observations on musth in the domesticated Asiatic elephant. Mammalia, 36, 247–261.CrossRefGoogle Scholar
- Kurt, F. 1974. Remarks on the social structure and ecology of the Ceylon elephant in the Yala National Park. In: Behavior of Ungulates and Its Relation to Management (Ed. by V. Geist & F. Walther), pp. 618–634. International Union for Conservation of Nature and Natural Resources, Publication 24.Google Scholar
- Langbauer, W.R., Jr., Payne, K.B., Charif, R.A., Rapaport, L. & Osborn, F. 1991. African elephants respond to distant playbacks of low-frequency conspecific calls. J. exp. Biol., 157, 35–46.Google Scholar
- Laws, R.M. 1969. Aspects of reproduction in the African elephant, Loxodonta africana. J. Reprod. Fertil. Suppl., 6, 193–217.Google Scholar
- Lincoln, G.A. & Ratnasooriya, W.D. 1996. Testosterone secretion, musth behaviour and social dominance in captive male Asian elephants living near the equator. J. Reprod. Fert., 108, 107–113.CrossRefGoogle Scholar
- Mason, R.T. & Crews, D. 1985. Female mimicry in garter snakes. Nature, 316, 59–60.PubMedCrossRefGoogle Scholar
- Maynard Smith J. & Price, G.R. 1973. The logic of animal conflict. Nature, 246, 15–18.CrossRefGoogle Scholar
- Meltzer, H. 1968. Creatine kinase and aldolase in serum: abnormality common to acute psychoses. Science, 159, 1368–1370.PubMedCrossRefGoogle Scholar
- Moss, C.J. 1983. Oestrous behavior and female choice in the African elephant. Behaviour, 86, 167–196.CrossRefGoogle Scholar
- Moss, C.J. & Poole, J.H. 1983. Relationships and social structure of African elephants. In: Primate Social Relationships: An Integrated Approach (Ed. by R.A. Hinde), pp. 315–325. Oxford: Blackwell Scientific Publications.Google Scholar
- Niemuller C. & Liptrap, R.M. 1991. Altered androstenedione to testosterone ratios and LH concentrations during musth in the captive male Asian elephant (Elephas maximus). J. Reprod. Fertil 91, 139–146.PubMedCrossRefGoogle Scholar
- Nirmalan G. & Nair, S.G. 1971. Plasma proteins and certain non-protein nitrogenous constituents in the blood of Indian elephants Elephas maximus. British vet. J., 127, 207–213.Google Scholar
- Perrin, T.E. & Rasmussen, L.E.L. 1994. Chemosensory responses of female Asian elephants (Elephas maximus) to cyclohexanone. J. Chem. Ecol., 20, 2577–2586.CrossRefGoogle Scholar
- Perrin, T.E., Rasmussen, L.E.L., Gunawardena, R. and Rasmussen, R.A. 1996. A method for collection, long-term storage, and bioassay of labile volatile chemosignals. J. Chem. Ecol., 22, 207–221.CrossRefGoogle Scholar
- Plotka, E.D., Seal, U.S., Zarembka, F.R., Simmons, L.G., Teare, A., Phillips, L.G., Hinshaw, K.C. & Wood, D.G. 1988. Ovarian function in the elephant luteinizing hormone and progesterone cycles in African and Asian elephants. Biol. Reprod., 38, 309–314.PubMedCrossRefGoogle Scholar
- Poole, J. H. 1987. Rutting behavior in African elephants: the phenomenon of musth. Behaviour, 102, 283–316.CrossRefGoogle Scholar
- Poole, J. H. 1989a. Announcing intent: the aggressive state of musth in African elephants. Anim. Behav., 37, 140–152.CrossRefGoogle Scholar
- Poole, J.H. 1989b. Mate guarding, reproductive success and female choice in African elephants. Anim. Behav., 37, 842–849.CrossRefGoogle Scholar
- Poole, J. 1994. Sex differences in the behaviour of African elephants. In: The Differences between the Sexes (Ed. by R.V. Short & E. Balaban), pp. 331–346. New York: Cambridge University Press.Google Scholar
- Poole, J.H. & Moss, C.J. 1981. Musth in the African elephant, Loxodonta africana. Nature, 292, 830–831.PubMedCrossRefGoogle Scholar
- Poole, J.H. & Moss, C.J. 1989. Elephant mate searching: group dynamics and vocal and olfactory communication. Symp. zool. Soc. Lond., 61, 111–125.Google Scholar
- Poole, J.H., Kasman, L.H., Ramsay, E.C. & Lasley, B.L. 1984. Musth and urinary testosterone concentrations in the African elephant (Loxodonta africana). J. Reprod. Fertil., 70, 255–260.PubMedCrossRefGoogle Scholar
- Poole, J.H., Payne, K.B., Langbauer, W.R., Jr., & Moss, C.J. 1988. The social contexts of some very low frequency calls of African elephants. Behav. Ecol. Sociobiol., 22, 385–392.CrossRefGoogle Scholar
- Poole, T. 1985. Social Behaviour in Mammals. New York: Blackie.CrossRefGoogle Scholar
- Querengaesser A., Iben C. & Leibetseder, J. 1994. Blood changes during training and racing in sled dogs. J. Nutr., 124, 2760S–2764S.PubMedGoogle Scholar
- Rapaport L. & Haight, J. 1987. Some observations regarding allomaternal caretaking among captive Asian elephants (Elephas maximus). J. Mamm., 68, 438–442.CrossRefGoogle Scholar
- Rasmussen, L.E.L. 1988. Chemosensory responses in two species of elephants to constituents of temporal gland secretion and musth urine. J. Chem. Ecol., 14, 1687–1711.CrossRefGoogle Scholar
- Rasmussen, L.E.L. 1998. Chemical communication: an integral part of functional Asian elephant (Elephas maximus) society. Ecoscience, in press.Google Scholar
- Rasmussen, L.E.L., Buss, I.O., Hess, D.L., & Schmidt, M.J. 1984. Testosterone and dihydrotestosterone concentrations in elephant serum and temporal gland secretions. Biol. Reprod., 30, 352–362.PubMedCrossRefGoogle Scholar
- Rasmussen, L.E.L., Hess, D.L., & Haight, J.D. 1990. Chemical analysis of temporal gland secretions collected from an Asian bull elephant during a four-month musth period. J. Chem. Ecol., 16, 2167–2181.CrossRefGoogle Scholar
- Rasmussen, L.E.L., Lee, T.D., Daves, G.D., Jr, & Schmidt, M.J. 1993. Female-to-male sex pheromones of low volatility in the Asian elephant, Elephas maximus. J. Chem. Ecol., 19, 2115–2128.CrossRefGoogle Scholar
- Rasmussen, L.E.L., Hall-Martin, A.J. & Hess, D.L. 1996a. Chemical profiles of male African elephant, Loxodonta africana: physiological and ecological implications. J. Mamm., 77, 422–439.CrossRefGoogle Scholar
- Rasmussen, L.E.L., Lee, T.D., Roelofs, W.L., Zhang, A. & Daves, G.D. Jr. 1996b. Insect pheromone in elephants. Nature, 379, 684.Google Scholar
- Rasmussen, L.E.L., Lee, T.D., Zhang A., Roelofs, W.L. & Daves, G.D., Jr. 1997a. Purification, identification, concentration and bioactivity of (Z)-7-dodecen-l-yl acetate: sex pheromone of the female Asian elephant, Elephas maximus. Chemical Senses, 22, 417–437.CrossRefGoogle Scholar
- Rasmussen, L.E.L., Gunawardena R. & Rasmussen, R.A. 1997b. Do Asian elephants, especially males in musth, chemically signal via volatiles in breath? Chemical Senses, in press.Google Scholar
- Resko J. A., Malley A., Begley D. & Hess, D.L. 1973. Radioimmunoassay of testosterone during fetal development of the rhesus monkey. Endocrinology, 93, 156–171.PubMedCrossRefGoogle Scholar
- Resko, J.A., Ellinwood, W.E., Pasztor, L.M. & Buhl, A.E. 1980. Sex steroids in the umbilical circulation of fetal rhesus monkey from the time of gonadal differentiation. J. Clin. Endocrinol. Metab., 50, 900–905.PubMedCrossRefGoogle Scholar
- Santiapillai C. & Suprahman, H. 1986. The ecology of the elephant (Elephas maximus L.) in the Way Kambas Game Reserve, Sumatra. World Wildlife Fund/International Union for Conservation of Nature and Natural Resources, 3133, 1–96.Google Scholar
- Shieh, S.D., Lin, Y.F., Lin, S.H. & Lu, K.C. 1995. A prospective study of calcium metabolism in exertional heat stroke with rhabdomyolysis and acute renal failure. Nephron, 71, 428–432.PubMedCrossRefGoogle Scholar
- Short, R.V. 1966. Oestrous behavior, ovulation and the function of the corpus luteum in the African elephant, Loxodonta africana. E. Afr. Wildl. J., 4, 56–68.CrossRefGoogle Scholar
- Sikes, S.K. 1971. The Natural History of the African Elephant. London: Weidenfield & Nicholson.Google Scholar
- Silva I. & Kuruwita, V.Y. 1993. Hematology, plasma and serum biochemistry values in free-ranging elephants (Elephas maximus Ceylonicus) in Sri Lanka. J. Zoo Wildl. Med., 24, 434–439.Google Scholar
- Sukumar, R. 1989. The Asian Elephant: Ecology and Management. Cambridge: Cambridge University Press.Google Scholar
- Trivers, R.I. 1972. Parental investment and sexual selection. In: Sexual selection and the Descent of Man, 1871-1971 (Ed. by B. Campbell), pp. 136–179. London: Heinemann.Google Scholar
- Wiley, R.H. & J. Poston. 1996. Indirect mate choice, competition for males, and coevolution of the sexes. Evolution, 50, 1371–81.CrossRefGoogle Scholar
- Zahavi, A. 1975. Mate selection-a selection for a handicap. J. Theor. Biol., 53, 205–214.PubMedCrossRefGoogle Scholar
- Zahavi, A. 1977. Reliability in communication systems and the evolution of altruism. In: Evolutionary Ecology (Ed. by B. Stonehouse & CM. Perrins), pp. 253–259. London: Macmillan Press.Google Scholar