Experimental evidence for olfactory predator recognition in wild mouse lemurs

American Journal of Primatology

Volumn 73, Issue 9, 2011, Pages 928-938

  Kappel, Philipp ^a   Hohenbrink, Sarah ^a   Radespiel, Ute ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Antipredator behavior; Feces; Fossa; Microcebus; Olfaction; Primate

Indexed keywords

ANTIPREDATOR DEFENSE; AVOIDANCE REACTION; BONE; COGNITION; EXPERIMENTAL STUDY; FECES; HABITUATION; METABOLITE; ODOR; OLFACTORY CUE; PREDATOR; PRIMATE; RAPTOR; TIME ALLOCATION; WILD POPULATION;

ANIMAL; ARTICLE; CHEIROGALEIDAE; DECISION MAKING; EUPLERIDAE; FEMALE; HABITUATION; MADAGASCAR; MALE; NONPARAMETRIC TEST; ODOR; OWL; PHYSIOLOGY; PREDATION; PSYCHOLOGICAL ASPECT; RANDOMIZATION;

ANIMALS; CHEIROGALEIDAE; CHOICE BEHAVIOR; EUPLERIDAE; FEMALE; HABITUATION, PSYCHOPHYSIOLOGIC; MADAGASCAR; MALE; PREDATORY BEHAVIOR; RANDOM ALLOCATION; SMELL; STATISTICS, NONPARAMETRIC; STRIGIFORMES;

ANIMALIA; EULEMUR FULVUS; LEMUR; LEMURIDAE; MICROCEBUS; MICROCEBUS MURINUS; MICROCEBUS RAVELOBENSIS; MICROCEBUS RUFUS; PRIMATES; PROPITHECUS; STRIGIFORMES; TYTONIDAE;

EID: 79960555676     PISSN: 02752565     EISSN: 10982345     Source Type: Journal    
DOI: 10.1002/ajp.20963     Document Type: Article

References (49)

1. Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS. 2005. The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neuroscience and Biobehavioral Reviews 29:1123-1144.
2. Belton LE, Ball N, Waterman JM, Bateman PW. 2007. Do Cape ground squirrels (Xerus inauris) discriminate between olfactory cues in the faeces of predators versus non-predators? African Zoology 42:135-138.
3. Blanchard DC, Griebel G, Blanchard RJ. 2003. Conditioning and residual emotionality effects of predator stimuli: some reflections on stress and emotion. Progress in Neuro-Psychopharmacology and Biological Psychiatry 27:1177-1185.
4. Blumstein DT. 2010. Flush early and avoid the rush: a general rule of antipredator behavior? Behavioral Ecology 21:440-442.
5. Buchanan-Smith HM, Anderson DA, Ryan CW. 1993. Responses of cotton-top tamarins (Sanguinus oedipus) to faecal scents of predators and non-predators. Animal Welfare 2:17-32.
6. Caine NG, Weldon PJ. 1989. Responses by red-bellied tamarins (Saguinus labiatus) to fecal scents of predatory and non-predatory neotropical mammals. Biotropica 21:186-189.
7. Deppe AM, Randriamiarisoa M, Wright PC. 2007. Mammalian predator recognition via olfactory cues in wild brown mouse lemurs (Microcebus rufus). American Journal of Physical Anthropology 132:99.
8. Dickman CR, Doncaster CP. 1984. Responses of small mammals to red fox (Vulpes vulpes) odor. Journal of Zoology 204:521-531.
9. Dielenberg RA, McGregor IS. 2001. Defensive behavior in rats towards predatory odors: a review. Neuroscience and Biobehavioral Reviews 25:597-609.
10. Dollar L, Ganzhorn JU, Goodman SM. 2007. Primates and other prey in the seasonally variable diet of Cryptoprocta ferox in the dry deciduous forest of Western Madagascar. In: Gursky SL, Nekaris KAI, editors. Primate anti-predator strategies. New York: Springer. p 63-76.
11. Engelhart A, Müller-Schwarze D. 1995. Responses of beaver (Castor canadensis Kuhl) to predator chemicals. Journal of Chemical Ecology 21:1349-1364.
12. Fenn MGP, Macdonald DW. 1995. Use of middens by red foxes: risk reverses rhythms of rats. Journal of Mammalogy 76:130-136.
13. García LV. 2004. Escaping the Bonferroni iron claw in ecological studies. OIKOS 105:657-663.
14. Goodman SM, O'Connor S, Langrand O. 1993. A review of predation on lemurs: implications for the evolution of social behaviour in small, nocturnal primates. In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum. p 51-66.
15. Goodman SM, Ganzhorn JU, Rakotondravony D. 2003. Introduction to the mammals. In: Goodman SM, Benstead JP, editors. The natural history of Madagascar. Chicago: University of Chicago Press. p 1159-1186.
16. Hayes RA, Nahrung HF, Wilson JC. 2006. The response of native Australian rodents to predator odours varies seasonally: a by-product of life history variation? Animal Behaviour 71:1307-1314.
17. Hollén LI, Manser MB. 2007. Persistence of alarm-call behaviour in the absence of predators: a comparison between wild and captive-born meerkats (Suricata suricatta). Ethology 113:1038-1047.
18. Jedrzejewski W, Rychlik L, Jedrzejewska B. 1993. Responses of bank voles to odors of seven species of predators: experimental data and their relevance to natural predator-vole relationships. OIKOS 68:251-257.
19. Joly M, Zimmermann E. 2007. First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus). American Journal of Primatology 69:1045-1052.
20. Kats LB, Dill LM. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361-394.
21. Koenig A. 1998. Visual scanning by common marmosets (Callithrix jacchus): functional aspects and the special role of adult males. Primates 39:85-90.
22. Konishi M. 1973. Locatable and nonlocatable acoustic signals for barn owls. American Naturalist 107:775-785.
23. Koskela E, Ylonen H. 1995. Suppressed breeding in the field vole (Microtus agrestis): an adaptation to cyclically fluctuating predation risk. Behavioral Ecology 6:311-315.
24. Lima SL, Dill LM. 1990. Behavioral decisions made under the risk of predation-a review and prospectus. Canadian Journal of Zoology 68:619-640.
25. Martin RD. 1990. Primate origins and evolution: a phylogenetic reconstruction. London: Chapman and Hall.
26. Mittermeier RA, Konstant WR, Hawkins F, Louis EE, Langrand O, Ratsimbazafy J, Rasoloarison R, Ganzhorn JU, Rajaobelina S, Tattersall I, Meyers DM. 2006. Lemurs of Madagascar: Conservation International.
27. Müller S, Stanyon R, O'Brien PCM, Ferguson-Smith MA, Plesker R, Wienberg J. 1999. Defining the ancestral karyotype of all primates by multidirectional chromosome painting between tree shrews, lemurs and humans. Chromosoma 108:393-400.
28. Nolte DL, Mason JR, Epple G, Aronov E, Campbell DL. 1994. Why are predator urines aversive to prey? Journal of Chemical Ecology 20:1505-1516.
29. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, Radespiel U. 2007. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Molecular Phylogenetics and Evolution 43:309-327.
30. Ouattara K, Lemasson A, Zuberbuhler K. 2009. Anti-predator strategies of free-ranging Campbell's monkeys. Behaviour 146:1687-1708.
31. Pruitt JN, Riechert SE. 2009. Sex matters: sexually dimorphic fitness consequences of a behavioural syndrome. Animal Behaviour 78:175-181.
32. Radespiel U, Cepok S, Zietemann V, Zimmermann E. 1998. Sex-specific usage patterns of sleeping sites in gray mouse lemurs (Microcebus murinus) in northwestern Madagascar. American Journal of Primatology 46:77-84.
33. Radespiel U, Ehresmann P, Zimmermann E. 2003. Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in Northwestern Madagascar. American Journal of Primatology 59:139-151.
34. Radespiel U, Reimann W, Rahelinirina M, Zimmermann E. 2006. Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. International Journal of Primatology 27:311-321.
35. Rakotondravony R, Radespiel U. 2009. Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. American Journal of Primatology 71:928-938.
36. Rasoloarison RM, Rasolonandrasana BPN, Ganzhorn JU, Goodman SM. 1995. Predation on vertebrates in the Kirindy forest, Western Madagascar. Ecotropica 1:59-65.
37. Rendigs A, Radespiel U, Wrogemann D, Zimmermann E. 2003. Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. International Journal of Primatology 24:47-64.
38. Scheumann M, Rabesandratana A, Zimmermann E. 2007. Predation, communication, and cognition in lemurs. In: Gursky SL, Nekaris KAI, editors. Primate anti-predator strategies. New York: Springer. p 100-123.
39. Schmelting B, Ehresmann P, Lutermann H, Randrianambinina B, Zimmermann E. 2000. Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: first results of a long term study. In: Lourenco WR, Goodman SM, editors. Diversité et endémisme à Madagascar. Paris, France: Mémoires de la Sociéte de Biogeographie. p 1-12.
40. Sih A, Bell A, Johnson JC. 2004. Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology and Evolution 19:372-378.
41. Sike T, Rózsa L. 2006. Owl pellet avoidance in yellow-necked mice Apodemus fiavicollis and house mice Mus musculus. Acta Zoologica Academiae Scientiarum Hungaricae 52:77-80.
42. Sündermann D, Scheumann M, Zimmermann E. 2008. Olfactory predator recognition in predator-naive gray mouse lemurs (Microcebus murinus). Journal of Comparative Psychology 122:146-155.
43. Swihart RK, Pignatello JJ, Mattina MJI. 1991. Aversive responses of white-tailed deer, Odocoileus virginianus, to predator urines. Journal of Chemical Ecology 17:767-777.
44. Thorén S, Quietzsch F, Schwochow D, Sehen L, Meusel C, Meares K, Radespiel U. 2011. Seasonal changes in feeding ecology and activity patterns of two sympatric mouse lemur species, the gray mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (M. ravelobensis), in northwestern Madagascar. International Journal of Primatology 32:566-586.
45. Vasilieva NY, Cherepanova EV, von Holst D, Apfelbach R. 2000. Predator odour and its impact on male fertility and reproduction in Phodopus campbelli hamsters. Naturwissenschaften 87:312-314.
46. Ward JF, Macdonald DW, Doncaster CP. 1997. Responses of foraging hedgehogs to badger odour. Animal Behaviour 53:709-720.
47. Weidt A, Hagenah N, Randrianambinina B, Radespiel U, Zimmermann E. 2004. Social organization of the golden brown mouse lemur (Microcebus ravelobensis). American Journal of Physical Anthropology 123:40-51.
48. Wolf M, van Doorn GS, Leimar O, Weissing FJ. 2007. Life-history trade-offs favour the evolution of animal personalities. Nature 447:581-584.
49. Zimmermann E, Cepok S, Rakotoarison N, Zietemann V, Radespiel U. 1998. Sympatric mouse lemurs in north-west Madagascar: a new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatologica 69:106-114.