Primate Anti-Predator Strategies pp 100-126 | Cite as
Predation, Communication, and Cognition in Lemurs
- 26 Citations
- 1.5k Downloads
Abstract
Predation represents an important selective force shaping the evolution of primate behavior. Primates confronted with predators have evolved various strategies to minimize the probability of being eaten. Predation risk and hunting styles of predators should have selected for communicative and cognitive abilities linked to socioecology and life history. As studies on several socially cohesive mammals indicate, the study of anti-predator behavior represents an important tool for gaining insight into cognition, e.g., to understand how animals classify objects and events in the world around them (e.g., marmots: Blumstein, 1999; vervet monkeys: Seyfarth et al., 1980; Diana monkeys: Zuberbühler, 2000; suricates: Manser et al., 2002).
Keywords
Predation Risk Alarm Call Mouse Lemur Playback Experiment Gray Mouse LemurPreview
Unable to display preview. Download preview PDF.
References
- Alcock, J. (1997). Animal Behavior. Sunderland: Sinauer Assoc., Inc.Google Scholar
- Anderson, C.M. (1986). Primates and primate evolution. Primates, 27, 15–39.CrossRefGoogle Scholar
- Bearder, S.K., Nekaris, K.A.I., and Buzzell, C.A. (2002). Danger in the night: Are some nocturnal primates afraid of the dark? In L.E. Miller (Ed.), Eat or be eaten: Predator sensitive foraging among primates (pp. 21–40). Cambridge: Cambridge Univ. Press.Google Scholar
- Beck, B.B. (1994). Reintroduction of captive-born animals. In P.J.S. Olney, G.M. Mace, and A.T.C. Feistner (Eds.), Creative conservation: Interactive management of wild and captive animals (pp. 265–286). London: Chapman and Hall.Google Scholar
- Blumstein, D.T. (1999). Alarm calling in three species of marmots. Behav., 136: 731–757.CrossRefGoogle Scholar
- Braune, P., Schmidt, S., and Zimmermann, E. (2005). Spacing and group coordination in a nocturnal primate, the golden brown mouse lemur (Microcebus ravelobensis). Behav. Ecol. Sociobiol., 58: 587–596.CrossRefGoogle Scholar
- Brockman, D.K. (2003). Polyboroides radiatus predation attempts on Propithecus verreauxi. Folia Primatol., 74: 71–74.PubMedCrossRefGoogle Scholar
- Bunkus, E., Scheumann, M., and Zimmermann, E. (2005). Do captive-born grey mouse lemurs (Microcebus murinus) recognize their natural predators by acoustic cues? Primate Report, 72: 22.Google Scholar
- Bunte, S. (1998). Verhaltensbiologische und bioakustische Untersuchungen zum Wachsamkeitsverhalten und zur Räubervermeidung bei Mausmakis (Microcebus spp.) in Gefangenschaft. Unpublished thesis.Google Scholar
- Burney, D.A. (2002). Sifaka predation by a large boa. Folia Primatol., 73: 144–145.PubMedCrossRefGoogle Scholar
- Charles-Dominique, P., and Petter, J.J. (1980). Ecology and social life of Phaner furcifer. In P. Charles-Dominique, H.M. Cooper, A. Hladik, C.M. Hladik, E. Pages, G.F. Pariente., A. Petter-Rousseaux, A. Schilling, and J.J. Petter (Eds.), Nocturnal Malagasy primates: Ecology, physiology, and behavior (pp. 75–95). New York: Academic Press, New York.Google Scholar
- Clutton-Brock, T.H., and Harvey, P.H. (1980). Primates, brains and ecology. J. Zool. Lond., 190: 309–323.CrossRefGoogle Scholar
- Colquhoun, I.C. (1993). The socioecology of Eulemur macaco: A preliminary report. In P.M. Kappeler and J.U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 11–23). New York: Plenum Press.Google Scholar
- Curio, E. (1993). Proximate and developmental aspects of antipredator behavior. Adv. Study Behav., 22: 135–238.CrossRefGoogle Scholar
- Driver, P.M., and Humphries, D.A. (1969). The significance of the high-intensive alarm call in captured passerines. Ibis, 111: 243–244.Google Scholar
- Ellis, D.H., Dobrott, S.J., and Goodwin, J.G. (1977). Reintroduction techniques for masked bobwhites. In S.A. Temple (Ed.), Endangered birds: Management techniques for preserving threatened species (pp. 345–354). Madison: Univ. of Wisconsin Press.Google Scholar
- Fay, R.R. (1988). Hearing in vertebrates: A psychophysics databook. Winnetka: Hill-Fay Associates.Google Scholar
- Fichtel, C. (2004). Reciprocal recognition of sifaka (Propithecus verreauxi verreauxi) and red-fronted lemur (Eulemur fulvus rufus) alarm calls. Anim. Cogn., 7: 45–52.PubMedCrossRefGoogle Scholar
- Fichtel, C., and Kappeler, P.M. (2002). Anti-predator behavior of group-living Malagasy primates: Mixed evidence of a referential alarm call system. Behav. Ecol. Sociobiol., 51: 262–275.CrossRefGoogle Scholar
- Fietz, J., and Dausmann, K.H. (2003). Costs and potential benefits of parental care in the nocturnal fat-tailed dwarf lemur (Cheirogaleus medius). Folia Primatol., 74: 246–258.PubMedCrossRefGoogle Scholar
- Gaffney, M.F., and Hodos, W. (2003). The visual acuity and refractive state of American kestrel (Falco sparverius). Vision Res., 43: 2053–2059.PubMedCrossRefGoogle Scholar
- Gilbert, M., and Tingay R.E. (2001). Predation of a fat tailed dwarf lemur Cheirogaleus medius by a Madagascar harrier-hawk Polyboroides radiatus: An incidental observation. Lemur News, 6: 6.Google Scholar
- Glaw, F., and Vences, M. (1996). A field guide to the amphibians and reptiles of Madagascar, (2nd ed.). Köln: Verlags GbR.Google Scholar
- Griffin, A.S., Blumstein, D.T., and Evans, C.S. (2000). Training captive bred and translocated animals to avoid predators. Conserv. Biol., 14: 1317–1326.CrossRefGoogle Scholar
- Griffin, A.S., Evans, C.S., and Blumstein, D.T. (2001). Learning specificity in acquired predator recognition. Anim. Behav., 62: 577–589.CrossRefGoogle Scholar
- Goodman, S.M. (2003). Predation on lemurs. In S.M. Goodman, and J.P. Benstead (Eds.), The natural history of Madagascar (pp. 1221–1228). Cambridge: Cambridge Univ. Press.Google Scholar
- Goodman, S.M., O’Connor, S., and Langrand, O. (1993). A review of predation on lemurs: Implications for the evolution of social behaviour in small, nocturnal primates. In P.M. Kappeler and J.U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 51–66). New York: Plenum Press.Google Scholar
- Goodman, S.M., Ganzhorn, J.U., and Rakotondravony, D. (2003). Introduction to mammals. In S.M. Goodman, and J.P. Benstead (Eds.), The natural history of Madagascar (pp. 1159–1186). Cambridge: Cambridge Univ. Press.Google Scholar
- Hill, R.A., and Dunbar, R.I.M. (1998). An evaluation of the roles of predation rate and predation risk as selective pressure on primate grouping behaviour. Behaviour, 135(4): 411–430.Google Scholar
- Hill, R.A., and Lee, P. (1998). Predation risk as an influence on group size in cercopithecoid primates: Implications for social structure. J. Zool., 245: 447–456.CrossRefGoogle Scholar
- Hogstedt, G. (1983). Adaptation unto death: Function of fear screams. Am. Nat., 121: 562–570.CrossRefGoogle Scholar
- Isbell, L.A. (1994). Predation on primates: Ecological patterns and evolutionary consequences. Evol. Anthropol., 3(2): 6171.CrossRefGoogle Scholar
- Janson, C.H. (2003). Puzzles, predation and primates: Using life history to understand selection pressures. In P.M. Kappeler and M.E. Pereira (Eds.), Primate life histories and socioecology (pp. 103–131). University of Chicago Press, Chicago.Google Scholar
- Janson, C.H. (1998). Testing the predation hypothesis for vertebrate sociality: Prospects and pitfalls. Behaviour, 135: 389–410.Google Scholar
- Kappeler, P.M., and Pereira, M.E. (2003). Primate life histories and socioecology. Chicago: Univ. of Chicago Press.Google Scholar
- Karpanty, S.M., and Grella, R. (2001). Lemur response to diurnal raptor calls in Ranomafana National Park, Madagascar. Folia Primatol., 72: 100–103.PubMedCrossRefGoogle Scholar
- Konishi, M. (1973). Locatable and nonlocatable acoustic signals for barn owls. Am. Nat., 107: 775–785.CrossRefGoogle Scholar
- Langrand, O. (1990). Guide to the birds of Madagascar. New Haven: Yale Univ. Press.Google Scholar
- Macedonia, J.M. (1990). What is communicated in the antipredator calls of lemurs: Evidence from playback experiments with ring-tailed and ruffed lemurs. Ethology, 86: 177–190.CrossRefGoogle Scholar
- Macedonia, J.M. (1993). Adaption and phylogenetic in the antipredator behaviour of ringtails and ruffed lemurs. In P.M. Kappeler and J.U. Ganzhorn (Eds.), Lemur social systems and their ecological basis (pp. 67–84). New York: Plenum Press.Google Scholar
- Macedonia, J.M., and Evans, C.S. (1993). Variation among mammalian alarm call systems and the problem of meaning in animal signals. Ethology, 93: 177–197.CrossRefGoogle Scholar
- Macedonia, J.M., and Polak, J.F. (1989) Visual assessment of avian threat in semi-captive ringtailed lemurs (Lemur catta). Behaviour, 111: 291–304.Google Scholar
- Macedonia, J.M., and Yount, P.L. (1991) Auditory assessment of avian predator threat in semi-captive ring-tailed lemurs (Lemur catta). Primates, 32(2): 169–182.CrossRefGoogle Scholar
- MacMillon, B.W.H. (1990). Attempts to re-establish wekas, brown kiwis and red-crowned parakeets in the Waitakere Ranges. Notornis, 37: 45–51.Google Scholar
- Manser, M.B., Seyfarth, R.M., and Cheney, D.L. (2002). Suricate alarm calls signal predator class and urgency. Trends Cogn. Sci., 6(2): 55–57.PubMedCrossRefGoogle Scholar
- McLean, I.G., Schmitt, N.T., Jarman, P.J., Duncan, C., and Wynne, C.D.L. (2000). Learning for life: Training marsupials to recognise introduced predators. Behaviour, 137: 1361–1376.CrossRefGoogle Scholar
- Miller, D.B., Hicinbothom, G., and Blaich, C.F. (1990). Alarm call responsitivity of mallard ducklings: Multiple pathways in behavioural development. Anim. Behav., 39(6): 1207–1212.CrossRefGoogle Scholar
- Mittermeier, R.A., Konstant, W.R., and Rylands, A.B. (2003). Lemur conservation. In S.M. Goodman, and J.P. Benstead (Eds.), The natural history of Madagascar (pp. 1538–1543). Cambridge: Cambridge Univ. Press.Google Scholar
- Müller, A.E., Thalmann, U. ((2000). Origin and evolution of primate social organisation: A reconstruction Biol. Rev., 75: 405–435.PubMedCrossRefGoogle Scholar
- Neuweiler, G. (2003). Neuro-und Sinnesphysiologie. Berlin: Springer.Google Scholar
- Oda, R. (1998). The response of Verreaux’s sifakas to anti-predator alarm calls given by sympatric ring-tailed lemurs. Folia Primatol., 69: 357–360.PubMedCrossRefGoogle Scholar
- Oda, R., and Masataka, N. (1996). Interspecific responses of ring-tailed lemurs to playback of antipredator alarm calls given by Verreaux’s sifakas. Ethology, 102: 441–453.CrossRefGoogle Scholar
- Owings, D.H., and Hennessy, D.F. (1984). The importance of variation in sciurid visual and vocal communication. In J.O. Murie and G.R. Michener (Eds.), The biology of grounddwelling squirrels: Annual cycles, behavioural ecology, and sociality (pp. 169–200). Lincoln: Univ. of Nebraska Press.Google Scholar
- Owings, D.H., and Morton, E.S. (1998). Animal vocal communication: A new approach. Cambridge: Cambridge Univ. Press.Google Scholar
- Pages, E. (1980). Ethoecology of Microcebus coquereli during the dry season. In P. Charles-Dominique, H.M. Cooper, A. Hladik, C.M. Hladik, E. Pages, G.F. Pariente., A. Petter-Rousseaux, A. Schilling, and J.J. Petter (Eds.), Nocturnal Malagasy primates: Ecology, physiology, and behavior (pp. 97–116). New York: Academic Press, New York.Google Scholar
- Paillette, M., and Petter, J.J. (1978). Vocal repertoire of Lemur fulvus albifrons. In D.J. Chivers and J. Herbert (Eds.), Recent advances in primatology, Vol. 1. (pp. 831–834). London: Academic Press.Google Scholar
- Pereira, M.E., and Macedonia, J.M. (1991). Ring-tailed lemur anti-predator calls denote predator class, not response urgency. Anim. Behav., 41: 543–544.CrossRefGoogle Scholar
- Pereira, M.E., Seeligson, M.L., and Macedonia, J.M. (1988). The behavioral repertoire of the black-and-white ruffed lemur, Varecia variegata variegata (Primates: Lemuridae). Folia Primatol., 51: 1–32.PubMedCrossRefGoogle Scholar
- Petter, J.J., and Charles-Dominique, P.C. (1979). Vocal communication in prosimians. In G.A. Doyle and R.D. Martin (Eds.), The study of prosimian behavior (pp. 247–305). London: Academic Press, Inc.Google Scholar
- Pollock, J.I. (1975). Field observations on Indri indri: A preliminary report. In I. Tattersall and R.W. Sussman (Eds.), Lemur biology (pp. 287–311). New York: Plenum Press.Google Scholar
- Rabesandratana, Z.A., Raminosoa, N., and Zimmermann, E. (2005). How the Milne Edwards’ sportive lemur (Lepilemur edwardsi) reacts to a fossa encounter. Primate Report, 72: 79.Google Scholar
- Radespiel, U., Cepok, S., Zietemann, V., and Zimmermann, E. (1998). Sex-specific usage patterns of sleeping sites in grey mouse lemurs (Microcebus murinus) in northwestern Madagascar. Am. J. Primatol., 46: 77–84.PubMedCrossRefGoogle Scholar
- Radespiel, U., Ehresmann, P., and Zimmermann, E. (2003). Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. Am. J. Primatol., 59: 139–151.PubMedCrossRefGoogle Scholar
- Rainey, H.J., Zuberbühler, K., and Slater, P.J.B. ((2004). Hornbills can distinguish between primate alarm calls. Proc. R. Soc. Lond. B, 271: 755–759.CrossRefGoogle Scholar
- Rakotoarison, N., Zimmermann, H., and Zimmermann, E. (1996). Hairy-eared dwarf lemur (Allocebus trichotis) discovered in a highland rain forest of eastern Madagascar. In W.R. Lourenço (Ed.), Biogéographie de Madagascar (pp. 275–282). OSTROM, Paris.Google Scholar
- Rakotondravony, D., Goodman, S. M., and Soarimalala, V. (1998). Predation on Hapalemur griseus griseus by Boa manditra (Boidae) in the Littoral Forest of Eastern Madagascar. Folia Primatol., 69: 405–408.PubMedCrossRefGoogle Scholar
- Rasoloharijaona, S. (2001). Contribution à l’étude comparative de la communication vocale et de la vie sociale de deux formes de Lepilemur (Geoffroy, 1858) (Lepilemuridae, Petter et al. 1977) provenant de la forêt sèche de l’ouest et de la forêt humide de l’est de Madagascar. Doctorat de troisième cycle, Université d’Antananarivo, Antananarivo, Madagascar.Google Scholar
- Richard, A.F. (1978). Behavioral variation: Case study of a Malagasy lemur. Lewisburg, PA: Bucknell Univ. Press.Google Scholar
- Richards, J. (1998). Return of the natives. Aust. Geographic, special edition: 91–105.Google Scholar
- Safer, A.B., and Grace, M.S. (2004). Infrared imaging in vipers: Differential response of crotaline and viperine snakes to paired thermal targets. Behav. Brain Res., 154: 55–61.PubMedCrossRefGoogle Scholar
- Sauther M.L. (1989). Antipredator behavior in troops of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Int. J. Primatol., 10: 595–606.Google Scholar
- Schmelting, B. (2000). Saisonale Aktivität und Reproduktionsbiologie von Grauen Mausmaki-Männchen (Microcebus murinus, J.F. Miller 1777) in Nordwest-Madagaskar. Dissertation, Tierärztliche Hochschule Hannover, Hannover.Google Scholar
- Schülke, O. ((2001). Social anti-predator behaviour in a nocturnal lemur. Folia Primatol., 72: 332–334.PubMedCrossRefGoogle Scholar
- Schülke, O., and Ostner J. (2001). Predation on Lepilemur by a harrier hawk and implications for sleeping site quality. Lemur News, 6:5.Google Scholar
- Seyfarth, R. M., and Cheney, D. L. (2003). Signalers and receivers in animal communication. Annu. Rev. Psychol., 54: 145–173.PubMedCrossRefGoogle Scholar
- Seyfarth, R.M., Cheney, D.L., and Marler, P. (1980). Monkey responses to three different alarm calls: Evidence of predator classification and semantic communication. Science, 210: 801–803.PubMedCrossRefGoogle Scholar
- Stanford, C.B (2002). Predation in primates. Inter. Jour. of Primatol., 23: 741–757.CrossRefGoogle Scholar
- Stanger, K.F. (1995). Vocalizations of some cheirogaleid prosimians evaluated in a phylogenetic context. In L. Alterman, G.A. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 353–376.). New York: Plenum Press.Google Scholar
- Stanger, K.F., and Macedonia, J.M. (1994). Vocalizations of aye-ayes (Daubentonia madagascariensis) in captivity. Folia Primatol., 62: 160–169.PubMedCrossRefGoogle Scholar
- Sündermann, D.; Scheumann, M. and Zimmermann, E. ((2005). Olfactory predator recognition in predator-naive grey mouse lemurs (Microcebus murinus). Primate Report, 72: 94.Google Scholar
- Sussman, R.W. (1975) A preliminary study of the behavior and ecology of Lemur fulvus rufus Audebert 1800. In I. Tattersall and R.W. Sussman (Eds.), Lemur biology (pp. 237–258). New York: Plenum Press.Google Scholar
- Terborgh, J., and Janson, C.H. (1986). The socioecology of primate groups. Annu. Rev. Ecol. Syst., 17: 111–136.CrossRefGoogle Scholar
- van Schaik, C.P., and van Hooff, J.A.R.A.M. (1983). On ultimate causes of primate social systems. Behaviour, 85: 91–117.Google Scholar
- Wolf, C.M., Griffith, B., Reed, C., and Temple, S.A. (1996). Avian and mammalian translocations: An update and reanalyses of 1987 survey data. Conserv. Biol., 10: 1142–1154.CrossRefGoogle Scholar
- Yoder, A. D. (2003). Phylogeny of the lemurs. In S.M. Goodman, and J.P. Benstead (Eds.), The natural history of Madagascar (pp. 1242–1247). Cambridge: Cambridge Univ. Press.Google Scholar
- Zietemann, V. (2000). Artendiversität bei Mausmakis: die Bedeutung der akustischen Kommunikation. Dissertation, Universität Hannover, Hannover.Google Scholar
- Zimmermann, E. (1995). Acoustic communication in nocturnal primates. In L. Alterman, G.A. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 311–330). New York: Plenum Press.Google Scholar
- Zimmermann, E., and Radespiel, U. (in press). Primate life histories. In W. Henke, H. Rothe, and I. Tattersall (Eds.), Handbook of palaeoanthropology, Vol. 2. Heidelberg: Springer-Verlag.Google Scholar
- Zimmermann, E., Newman, J.D., and Jürgens, U. (Eds.). (1995). Current topics in primate vocal communication. New York: Plenum Press.Google Scholar
- Zimmermann, E., Vorobieva, E., Wrogemann, D., and Hafen, T. (2000). Use of vocal fingerprinting for specific discrimination of gray (Microcebus murinus) and rufous mouse lemurs (Microcebus rufus). Int. J. Primatol., 21(5): 837–852.CrossRefGoogle Scholar
- Zuberbühler, K. (2000). Referential labelling in Diana monkeys. Anim. Behav., 59: 917–927.PubMedCrossRefGoogle Scholar
- Zuberbühler, K. (2003). Referential signalling in non-human primates: Cognitive precursors and limitations for the evolution of language. Adv. Study Behav., 33: 265–307.Google Scholar
- Zuberbühler, K., and Jenny, D. ((2002). Leopard predation and primate evolution. J. Hum. Evol., 43: 873–886.PubMedCrossRefGoogle Scholar