Honest signalling through chemicals by elephants with applications for care and conservation

Applied Animal Behaviour Science

Volumn 102, Issue 3-4, 2007, Pages 344-363

  Schulte, Bruce Alexander ^a   Freeman, Elizabeth Watson ^b   Goodwin, Thomas Elton ^c   Hollister Smith, Julie ^d   Rasmussen, L Elizabeth Little ^e  

^a GEORGIA SOUTHERN UNIVERSITY   (United States)

^b SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

^c HENDRIX COLLEGE   (United States)

^d DUKE UNIVERSITY   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Communication; Honesty; Management; Pheromone

Indexed keywords

CAPTIVE POPULATION; COMMUNICATION BEHAVIOR; ELEPHANT; EXPERIMENTAL STUDY; HONEST SIGNALING; INTRASPECIFIC INTERACTION; PHEROMONE; REPRODUCTIVE STATUS; SPECIES CONSERVATION; WILD POPULATION;

ANIMALIA; ELEPHANTIDAE; ELEPHAS MAXIMUS; LOXODONTA;

EID: 33845635173     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2006.05.035     Document Type: Article

References (111)

1. Alberts A.C. Constraints on the design of chemical communication systems in terrestrial vertebrates. Am. Nat. 139 (1992) S62-S89
2. Arthur C.L., and Pawliszyn J. Solid phase microextraction with thermal desorption using fused silica optical fibers. Anal. Chem. 62 (1990) 2145-2148
3. Bagley, K.R., 2004. Chemosensory behavior and development of African male elephants (Loxodonta africana). Master of Science Thesis. Georgia Southern University, Statesboro, GA, 83 pp.
4. Bagley K.R., Goodwin T.E., Rasmussen L.E.L., and Schulte B.A. Male African elephants (Loxodonta africana) can distinguish oestrous status via urinary signals. Anim. Behav. 71 (2006) 1439-1445
5. Baker S.E., Johnson P.J., David S., Watkins R.W., and Macdonald D.W. Learned food aversion with and without an odour cue for protecting untreated baits from wild mammal foraging. Appl. Anim. Behav. Sci. 102 (2007) 410-428
6. Barkawi L.S., Francke W., Blomquist G.J., and Seybold S.J. Frontalin: de novo biosynthesis of an aggregation pheromone component by Dendroctonus spp. bark beetles (Coleoptera: Scolytidae). Insect Biochem. Mol. Biol. 33 (2003) 773-788
7. Brown J.L. Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol. 19 (2000) 347-367
8. Brown J.L., Schmitt D.L., Bellem A., Graham L.H., and Lehnhardt J. Hormone secretion in the Asian elephant (Elephas maximus): characterization of ovulatory and anovulatory luteinizing hormone surges. Biol. Reprod. 61 (1999) 1294-1299
9. Brown R.E., and Macdonald D.W. Social Odours in Mammals (1985), Oxford University Press, Oxford
10. Carlstead K. Effects of captivity on the behavior of wild mammals. In: Kleinman D., Allen M., Thompson K., and Lumpkin S. (Eds). Wild Mammals in Captivity: Principles and Techniques (1996), University of Chicago Press, Chicago 317-333
11. Dawkins M.S. Unravelling Animal Behaviour. second ed. (1995), Longman Scientific and Technical, Singapore
12. Eisenberg J.F., McKay G.M., and Jainudeen M.R. Reproductive behavior of the Asiatic elephant (Elephas maximus maximus L.). Behaviour 38 (1971) 193-225
13. Elephant Pepper Development Trust, 2005. http://elephantpepper.org/downloads.html, accessed on June 20, 2006.
14. Endler J.A. Signals, signal conditions, and the direction of evolution. Am. Nat. 139 (1992) S125-S153
15. Estes R.D. The role of the vomeronasal organ in mammalian reproduction. Mammal 36 (1972) 315-341
16. In: Festa-Bianchet M., and Apollonio M. (Eds). Animal Behavior and Wildlife Conservation (2003), Island Press, Washington, DC
17. Freeman, E., 2005. Investigation of behavioral and socio-environmental factors associated with reproductive acyclicity in African elephants. Ph.D. Thesis. Department of Environmental Science and Policy. George Mason University, Fairfax, VA.
18. Ganswindt A., Rasmussen H.B., Heistermann M., and Hodges J.K. The sexually active states of free-ranging male African elephants (Loxodonta africana): defining musth and non-musth using endocrinology, physical signals, and behavior. Horm. Behav. 47 (2005) 83-91
19. Goodwin T.E., Brown F.D., Counts R.W., Dowdy N.C., Fraley P.L., Hughes R.A., Liu D.Z., Mashburn C.D., Rankin J.D., Roberson R.S., Wooley K.D., Rasmussen L.E.L., Riddle S.W., Riddle H.S., and Schulz S. African elephant sesquiterpenes. II. Identification and synthesis of new derivatives of 2,3-dihydrofarnesol. J. Nat. Prod. 65 (2002) 1319-1322
20. Goodwin T.E., Rasmussen L.E.L., Schulte B.A., Brown P.A., Davis B.L., Dill W.M., Dowdy N.C., Hicks A.R., Morshedi R.G., Mwanza D., and Loizi H. Chemical analysis of preovulatory female African elephant urine: a search for putative pheromones. In: Mason R.T., LeMaster M.P., and Müller-Schwarze D. (Eds). Chemical Signals in Vertebrates, vol. 10 (2005), Springer Press, New York 128-139
21. Gosling L.M., and Roberts S.C. Scent-marking by male mammals: cheat-proof signals to competitors and mates. In: Slater P.J.B., Rosenblatt J.S., Snowdon C.T., and Roper T.J. (Eds). Advances in the Study of Behavior (2001), Academic Press, New York 169-217
22. Grafen A. Biological signals as handicaps. J. Theor. Biol. 144 (1990) 517-546
23. Guilford T., and Dawkins M.S. Receiver psychology and the evolution of animal signals. Anim. Behav. 42 (1991) 1-14
24. Hakeem A.Y., Hof P.R., Sherwood C.C., Switzer R.C., Rasmussen L.E.L., and Allman J.M. The brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images. Anat. Rec. 287A (2005) 1117-1127
25. Hall-Martin A.J., and Van der Walt L.A. Plasma testosterone levels in relation to musth in the male African elephant. Koedoe 27 (1984) 147-149
26. Halpin Z.T. Individual odors among mammals: origins and functions. Adv. Study Behav. 16 (1986) 39-70
27. Hasson O. Cheating signals. J. Theor. Biol. 167 (1994) 223-238
28. Hebets E.A., and Papaj D.R. Complex signal function: developing a framework of testable hypotheses. Behav. Ecol. Sociobiol. 57 (2005) 197-214
29. Hinshaw K.C., Amand W.B., and Tinkelman C.L. Preventive medicine. In: Kleinman D., Allen M., Thompson K., and Lumpkin S. (Eds). Wild Mammals in Captivity: Principles and Techniques (1996), University of Chicago Press, Chicago 16-24
30. Hollister-Smith, J., 2005. Reproductive behavior in male African elephants (Loxodonta africana) and the role of musth: a genetic and experimental analysis. Ph.D. Thesis. Department of Biology, Duke University, Durham, NC.
31. Johnston R.E. Chemical signals and reproductive behavior. In: Vandenbergh J.G. (Ed). Pheromones and Reproduction in Mammals (1983), Academic Press, New York 3-37
32. Kapustin N., Critser J.K., Olson D., and Malven P.V. Nonluteal estrous cycles of 3-week duration are initiated by anovulatory luteinizing hormone peaks in African elephants. Biol. Reprod. 55 (1996) 1147-1154
33. Kelly D.R. When is a butterfly like an elephant?. Chem. Biol. 3 (1996) 595-602
34. Krebs J.R., and Dawkins R. Animal signals: mind-reading and manipulation. In: Krebs J.R., and Davies N.B. (Eds). Behavioural Ecology: An Evolutionary Approach. second ed. (1984), Blackwell Scientific Publications, Boston, MA 380-402
35. Lamps L.W., Smoller B.R., Rasmussen L.E.L., Slade B.E., Fritsch G., and Goodwin T.E. Characterization of interdigital glands in the Asian elephant (Elephas maximus). Res. Vet. Sci. 71 (2001) 1-4
36. Lamps L.W., Smoller B.R., Goodwin T.E., and Rasmussen L.E.L. Hormone receptor expression in interdigital glands of the Asian elephant (Elephas maximus). Zoo Biol. 23 (2004) 463-469
37. Langbauer Jr. W.R. Elephant communication. Zoo Biol. 19 (2000) 425-446
38. Langbauer W.R., Payne K.B., Charif R.A., Rapaport L., and Osborn F. African elephants respond to distant playbacks of low-frequency conspecific calls. J. Exp. Biol. 15 (1991) 35-46
39. Lazar J., Greenwood D.R., Rasmussen L.E.L., and Prestwich G.D. Molecular and functional characterization of an odorant binding protein of the Asian elephant, Elephas maximus: implications for the role of lipocalins in mammalian olfaction. Biochemistry 41 (2002) 11786-11794
40. Lazar J., Rasmussen L.E.L., Greenwood D.R., Bang I., and Prestwich G.D. Elephant albumin: a multipurpose pheromone shuttle. Chem. Biol. 11 (2004) 1093-1100
41. Leong K.M., Ortolani A., Graham L.H., and Savage A. The use of low-frequency vocalizations in African elephant (Loxodonta africana) reproductive strategies. Horm. Behav. 43 (2003) 433-443
42. Leong K.M., Burks K., Rizkalla C.E., and Savage A. Effects of reproductive and social context on vocal communication in captive female African elephants (Loxodonta africana). Zoo Biol. 24 (2005) 331-347
43. Loizi, H., 2004. The development of chemosensory behaviors in African elephants (Loxodonta africana) and male responses to female urinary compounds. Master of Science Thesis. Georgia Southern University, Statesboro, GA, 78 pp.
44. Maguire L.A., and Servheen C. Intergrating biological and sociological concerns in endangered species management: augmentation of grizzly bear populations. Conserv. Biol. 6 (1992) 426-434
45. Martin P., and Bateson P. Measuring Behaviour: An Introductory Guide. second ed. (1993), Cambridge University Press, NY
46. Mason G., Clubb R., Latham N., and Vickery S. Why and how should we use environmental enrichment to tackle stereotypic behaviour?. Appl. Anim. Behav. Sci. 102 (2007) 163-188
47. Maynard-Smith J., and Harper D. Animal Signals (2003), Oxford University Press, NY
48. Maynard-Smith J., and Price G.R. The logic of animal conflict. Nature 246 (1973) 15-18
49. Meehan C., and Mench J. The challenge of challenge: Can problem solving opportunities enhance animal welfare?. Appl. Anim. Behav. Sci. 102 (2007) 246-261
50. Mills G.A., and Walker V. Headspace solid phase microextraction of volatile compounds in urine: application to metabolic investigations. J. Chromatogr. B 753 (2001) 259-268
51. Moodie E.M., and Chamove A.S. Brief threatening events beneficial for captive tamarins?. Zoo Biol. 9 (1990) 275-286
52. Moss C.J. Oestrous behavior and female choice in the African elephant. Behaviour 86 (1983) 167-196
53. O'Connell R.J., and Meredith M. Effects of volatile and nonvolatile chemical signals on male sex behaviors mediated by the main and accessory olfactory systems. Behav. Neurosci. 98 (1984) 1083-1093
54. O'Connell-Rodwell C.E., Arnason B.T., and Hart L.A. Seismic properties of Asian elephant (Elephas maximus) vocalizations and locomotion. J. Acoust. Soc. Am. 108 (2000) 3066-3072
55. Osborn F.V. Capsicum oleoresin as an elephant repellent: field trials in the communal lands of Zimbabwe. J. Wildl. Manage. 66 (2002) 674-677
56. Osborn F.V., and Parker G.E. Toward an integrated approach for reducing the conflict between elephants and people: a review of current research. Oryx 37 (2003) 80-84
57. Osborn F.V., and Rasmussen L.E.L. Evidence for the effectiveness of an oleo-resin capsicum against wild elephants in Zimbabwe. Pachyderm 20 (1995) 15-22
58. Parker G.A. Assessment strategy and the evolution of fighting behaviour. J. Theor. Biol. 47 (1974) 223-243
59. Payne K.B., Langbauer Jr. W.R., and Thomas E.M. Infrasonic calls of the Asian elephant (Elephas maximus). Behav. Ecol. Sociobiol. 18 (1986) 297-301
60. Perrin T., and Rasmussen L.E.L. Chemosensory responses of female Asian elephants (Elephas maximus) to cyclohexanone. J. Chem. Ecol. 20 (1994) 2857-2866
61. Perrin T.E., Rasmussen L.E.L., Gunawardena R., and Rasmussen R.A. A method for collection, long-term storage, and bioassay of labile volatile chemosignals. J. Chem. Ecol. 22 (1996) 207-221
62. Polisar J., Maxit I., Scognamillo D., Farrell L., Sunquist M.E., and Eisenberg J.F. Jaguars, pumas, their prey base, and cattle ranching: ecological interpretations of a management problem. Biol. Conserv. 109 (2003) 297-310
63. Poole J.H. Rutting behavior in African elephants: the phenomenon of musth. Behaviour 102 (1987) 283-316
64. Poole J.H. Announcing intent: the aggressive state of musth in African elephants. Anim. Behav. 37 (1989) 140-152
65. Poole J.H. Mate guarding, reproductive success and female choice in African elephants. Anim. Behav. 37 (1989) 842-849
66. Poole J. Sex differences in the behaviour of African elephants. In: Short R.V., and Balaban E. (Eds). The Differences between the Sexes (1994), Cambridge University Press, New York 331-346
67. Poole J.H., and Moss C.J. Musth in the African elephant, Loxodonta africana. Nature 292 (1981) 830-831
68. Poole J.H., and Moss C.J. Elephant mate searching: group dynamics and vocal and olfactory communication. In: Jewell P.A., and Maloiy G.M.O. (Eds). The Biology of Large African Mammals in their Environment vol. 61 (1989), Symp. Zool. Soc. Lond. 111-125
69. Poole J.H., Payne K., Langbauer Jr. W.R., and Moss C.J. The social contexts of some very low frequency calls of African elephants. Behav. Ecol. Sociobiol. 22 (1988) 385-392
70. Powell D.M. Preliminary evaluation of environmental enrichment techniques for African lions (Panthera leo). Anim. Welfare 4 (1995) 361-370
71. Rabin L.A. Maintaining behavioral diversity in captivity for conservation: natural behaviour management. Anim. Welfare 12 (2003) 85-94
72. Rabin L.A., and Greene C.M. Changes to acoustic communication systems in human-altered environments. J. Comp. Psychol. 116 (2002) 137-141
73. Rasmussen L.E.L. Chemical communication: an integral part of functional Asian elephant (Elephas maximus) society. Ecosciences 5 (1998) 410-426
74. Rasmussen L.E.L. Evolution of chemical signals in the Asian elephant, Elephas maximus: behavioural and ecological influences. J. Biosci. 24 (1999) 241-251
75. Rasmussen L.E.L. Source and cyclic release pattern of (Z)-7-dodecenyl acetate, the pre-ovulatory pheromone of the female Asian elephant. Chem. Senses 26 (2001) 611-623
76. Rasmussen, L.E.L., 2006. Olfactory systems and pheromones: taste, touch and trigeminal systems. In: Fowler, M.E., Mikota, S.K. (Eds.), The Biology, Medicine and Surgery of Elephants. Blackwell Publishing, Ames, Iowa, pp. 409-414 (chapter 32).
77. Rasmussen L.E.L., and Greenwood D.R. Frontalin: a chemical message of musth in Asian elephants, Elephas maximus. Chem. Senses 28 (2003) 433-446
78. Rasmussen L.E.L., and Perrin T.E. Physiological correlates of musth: lipid metabolites and chemical composition of exudates. Phys. Behav. 67 (1999) 539-549
79. Rasmussen L.E.L., and Riddle S.W. Development and initial testing of pheromone-enhanced mechanical devices for deterring crop raiding elephants: a positive conservation step. J. Eleph. Manage. Assoc. 15 (2004) 30-37
80. Rasmussen L.E.L., and Wittemyer G. Chemosignaling of musth by individual wild African elephants (Loxodonta africana): implications for conservation and management. Proc. R. Soc. Lond. 269 (2002) 853-860
81. Rasmussen L.E.L., Riddle H.S., and Krishnamurthy V. Mellifluous matures to malodorous in musth. Nature 415 (2002) 975-976
82. Rasmussen L.E.L., Schmidt M.J., Henneous R., Groves D., and Daves G.D. Asian bull elephants: flehmen-like responses to extractable components in female elephant estrous urine. Science 217 (1982) 159-162
83. Rasmussen L.E.L., Lee T.D., Roelofs W.L., Zhang A., and Daves Jr. G.D. Asian elephants and Lepidoptera have a common sex pheromone. Nature 379 (1996) 684
84. Rasmussen L.E.L., Lee T.D., Zhang A., Roelofs W.L., and Daves Jr. G.D. Purification, identification, concentration and bioactivity of (Z)-7-dodecen-1-yl acetate: sex pheromone of the female Asian elephant, Elephas maximus. Chem. Senses 22 (1997) 417-437
85. Rasmussen L.E.L., Krishnamurthy V., and Sukumar R. Behavioural and chemical confirmation of the preovulatory pheromone, (Z)-7-dodecenyl acetate, in wild Asian elephants: its relationship to musth. Behaviour 142 (2005) 351-396
86. Reby D., and McComb K. Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim. Behav. 65 (2003) 317-329
87. Riddle H.S., Rasmussen B., and Schmitt D.L. Are captive elephants important to conservation?. Gajah 22 (2003) 57-60
88. Riddle H.S., Riddle S.W., Rasmussen L.E.L., and Goodwin T.E. The first disclosure and preliminary investigation of a liquid released from the ears of African elephants. Zoo Biol. 19 (2000) 475-480
89. Schetini de Azevedo C., Cipreste C.F., and Young R.J. Environmental enrichment: a GAP analysis. Appl. Anim. Behav. Sci. 102 (2007) 329-343
90. Schneider K.M. Das Flehmen. Zool. Gart. 43 (1930) 183-198
91. Schulte B.A. Social structure and helping behavior in captive elephants. Zoo Biol. 19 (2000) 447-459
92. Schulte B.A. Scientific writing and the scientific method: parallel structure in form and content. Am. Biol. Teach. 65 (2003) 582-585
93. Schulte, B.A., 2006. Elephant behavior and social life. In: Fowler, M.E., Mikota, S.K. (Eds.), The Biology, Medicine and Surgery of Elephants. Blackwell Publishing, Ames, Iowa, pp. 35-43 (chapter 4).
94. Schulte B.A., and Rasmussen L.E.L. Signal-receiver interplay in the communication of male condition by Asian elephants. Anim. Behav. 57 (1999) 1265-1274
95. Schulte B.A., Loizi H., Bagley K., Gray A., Stanley L., Correll M., Goodwin T.E., Brown P.A., Davis B.L., Dill W.M., Dowdy N.C., Hicks A.R., Morshedi R.G., Mwanza D., and Rasmussen L.E.L. Elephant chemotactile communication and conservation. J. Eleph. Manage. Assoc. 15 (2004) 16-23
96. Schulte B.A., Bagley K., Correll M., Gray A., Heineman S.M., Loizi H., Malament M., Scott N.L., Slade B.E., Stanley L., Goodwin T.E., and Rasmussen L.E.L. Assessing chemical communication in elephants. In: Mason R.T., LeMaster M.P., and Müller-Schwarze D. (Eds). Chemical Signals in Vertebrates, vol. 10 (2005), Springer Press, New York 140-151
97. Shepherdson D.J., Carlstead K., Mellen J.D., and Seidensticker J. The influences of food presentation on the behavior of small cats in confined environments. Zoo Biol. 12 (1993) 203-216
98. Shepherdson D.J., Mellen J.D., and Hutchins M. Second Nature: Environmental Enrichment for Captive Animals (1998), Smithsonian Institution, Washington, DC
99. Shoshani J., and Eisenberg J.F. Elephas maximus. Mammalian Species 182 (1982) 108
100. Sikes S.K. The Natural History of the African Elephant (1971), American Elsevier Publ. Co. Inc., New York
101. Slade B.E., Schulte B.A., and Rasmussen L.E.L. Oestrous state dynamics in chemical communication by captive female Asian elephants. Anim. Behav. 65 (2003) 813-819
102. Stevens B., LeBlanc D., Gutman R., and Kirkpatrick N. Olfactory enrichment with Rodrigues's flying foxes (Pteropus rodricensis): just nosing around. AZA Regional Conference Proceedings (1995)
103. Sukumar R. The Asian Elephant: Ecology and Management (1989), Cambridge Univ. Press, Cambridge
104. Sukumar R., and Gadgil M. Male-female differences in foraging for crops by Asian elephants. Anim. Behav. 36 (1988) 1233-1235
105. Swaisgood R.R., White A.M., Zhou X., Zhang H., Zhang G., Wei R., Hare V.J., Tepper E.M., and Lindburg D.G. A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas. Anim. Behav. 61 (2001) 447-457
106. Treves A., and Karanth K.U. Human-carnivore conflict and perspectives on carnivore management worldwide. Conserv. Biol. 17 (2003) 1491-1499
107. Wells D.L., and Egli J.M. The influence of olfactory enrichment on the behaviour of captive black-footed cats, Felis nigripes. Appl. Anim. Behav. Sci. 85 (2004) 107-119
108. Wemelsfelder F. The scientific validity of subjective concepts in models of animal welfare. Appl. Anim. Behav. Sci. 53 (1997) 75-88
109. Wyatt T.D. Pheromones and Animal Behaviour: Communication by Smell and Taste (2003), Cambridge University Press, Oxford
110. Zahavi A., and Zahavi A. The Handicap Principle: A Missing Piece of Darwin's Puzzle (1997), Oxford University Press, NY
111. Ziegler T.E., Schultz-Darken N.J., Scott J.J., Snowdon C.T., and Ferris C.F. Neuroendocrine response to female ovulatory odors depends upon social condition in male common marmosets, Callithrix jacchus. Horm. Behav. 47 (2005) 56-64