Primate Anti-Predator Strategies pp 222-240 | Cite as
Predator Defense by Slender Lorises and Pottos
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Abstract
Crypsis is argued to be the most widely used anti-predator strategy amongst nocturnal primates, wrought in its extreme form amongst the Asian lorises (Lorisinae: Loris and Nycticebus) and African pottos (Perodicticinae: Arctocebus and Perodicticus) (van Schaik & van Hoof, 1983; Terborgh & Janson, 1986; Cheney & Wrangham, 1987; Stanford, 2002; Wiens, 2002). Lorises and pottos are classically characterized by relatively slow, non-saltatory locomotion (Walker, 1969; Sellers, 1996). Silent movement, combined with cryptic coloration, small group size, discrete use of vocalizations, and increased olfactory communication are said to camouflage these primates (Petter & Hladik, 1970; Charles-Dominique, 1977). Much support for these notions has been offered by past studies of lorises and pottos.
Keywords
Potential Predator Alarm Pheromone Scent Mark Poison Frog Scent GlandPreview
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References
- Alberts, A.C. (1992). Constraints on the design of chemical communication systems in terrestrial vertebrates. The American Naturalist, 139: S62–S69.CrossRefGoogle Scholar
- Alterman, L. (1995). Toxins and toothcombs: Potential allospecific chemical defenses in Nycticebus and Perodicticus. In L. Alterman, G.A. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 413–424). New York: Plenum Press.Google Scholar
- Altman, J. (1974). Observational study of behavior: Sampling methods. Behavior, 49: 227–265.Google Scholar
- Ambrose, L. (1999). Species diversity in West and Central African galagos (Primates, Galagonidae): The use of acoustic analysis. Doctoral thesis. Oxford Brookes University, Oxford.Google Scholar
- Ambrose, L. (2003). Three acoustic forms of Allen’s galagos (Primates; Galagonidae) in the Central African region. Primates, 44: 25–39.PubMedGoogle Scholar
- Andersson, M. (1994). Sexual selection. Princeton, NJ: Princeton Univ. Press.Google Scholar
- Andrew, R.J., and Klopman, R.B. (1974). Urine-washing: Comparative notes. In R.D. Martin, G.A. Doyle, and A.C. Walker (Eds.), Prosimian biology (pp. 303–312). London: Duckworth.Google Scholar
- Banks, P.B., Norrdahl, K., and Korpimäki, E. (2000). Nonlinearity in the predation risk of prey mobility. Proceedings of the Royal Society Biological Sciences Series B, 267: 1621–1625.CrossRefGoogle Scholar
- Banks, P.B., Norrdahl, K., and Korpimäki, E. (2002). Mobility decisions and the predation risks of reintroduction. Biological Conservation, 103: 133–138.CrossRefGoogle Scholar
- Bearder, S.K., Honess, P.E., and Ambrose, L. (1995). Species diversity among galagos with special reference to mate recognition. In L. Alterman, G. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 331–352). New York: Plenum Press.Google Scholar
- Bearder, S.K., Nekaris, K.A.I., and Buzzell, C.A. (2002). Dangers of the night: Are some primates afraid of the dark? In L.E. Miller (Ed.), Eat or be eaten: Predator sensitive foraging in primates (pp. 21–43). Cambridge: Cambridge Univ. Press.Google Scholar
- Bearder, S.K., Nekaris, K.A.I., and Curtis, D.J. (2006). A re-evaluation of the role of vision in the activity and communication of nocturnal primates. Folia Primatologica, 77(1–2): 50–71.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). Behavioural Ecology and Sociobiology, 58(6): 587–596.CrossRefGoogle Scholar
- Caldwell, J. (1996). The evolution of myrmecophagy and its correlates in poison frogs (Family: Dendrobatidae). Journal of Zoology, 240: 75–100.Google Scholar
- Charles-Dominique, P. (1974). Vie sociale de Perodicticus potto (Primates: Lorisides). Étude de terrain en forêt equatorial de l’ouest africain au Gabon. Mammalia, 38: 355–379.Google Scholar
- Charles-Dominique, P. (1977). Ecology and behaviour of nocturnal primates. London: Duckworth.Google Scholar
- Charles-Dominique, P. (1978). Solitary and gregarious prosimians: Evolution of social structures in primates. In D.J. Chivers and K.A. Joysey (Eds.), Recent advances in primatology, Volume 3 (pp. 139–149). New York: Academic Press.Google Scholar
- Charles-Dominique, P. (1990). Ecological adaptations related to locomotion in primates: An introduction. In F.K. Jouffroy, M.H. Stack, and C. Niemitz (Eds.), Gravity, posture and locomotion in primates (pp. 19–31). Sedicesimo: Editrice II.Google Scholar
- Cheney, D., and Wrangham, R.W. (1987). Predation. In B.B. Smuts, D.L. Cheney, R.M. Seyfarth, R.W. Wrangham, and T.T. Struhsaker (Eds.), Primate societies (pp. 227–239). Chicago: Univ. of Chicago Press.Google Scholar
- Chivers, D.P., Brown, G.E., and Smith, J.F. (1995). Chemical alarm signals: Predator deterrents or predator attractants? The American Naturalist, 145: 994–105.CrossRefGoogle Scholar
- Clark, A.B. (1982a). Scent marks as social signals in Galago crassicaudatus. I. Sex and reproductive status as factors in signals and responses. Journal of Chemical Ecology, 8(8): 1133–1151.CrossRefGoogle Scholar
- Clark, A.B. (1982b). Scent marks as social signals in Galago crassicaudatus. II. Discrimination between individuals by scent. Journal of Chemical Ecology, 8(8): 1153–1165.CrossRefGoogle Scholar
- Coultas, D.S. (2002). Bioacoustic analysis of the loud call of two species of slender loris (Loris tardigradus and L. lydekkerianus nordicus) from Sri Lanka. MSc thesis. Oxford Brookes University, Oxford.Google Scholar
- Darst, C.R., Menéndez-Guerrero, P.A., Coloma, L.A., and Cannatella, D.C. (2005). Evolution of dietary specialization and chemical defense in poison frogs (Dendrobatidae): A comparative analysis. The American Naturalist, 165: 56.PubMedCrossRefGoogle Scholar
- Daschbach, N.J., Schein, M.W., and Haines, D.E. (1981). Vocalizations of the slow loris, Nycticebus coucang (Primates, Lorisidae). Inter. Jour. of Primatol., 2, 71–80.Google Scholar
- Ehrlich, A., and Musicant, A. (1977). Social and individual behaviors in captive slow lorises (Nycticebus coucang). Behaviour, 60: 195–220.Google Scholar
- Epple, G. (1974). Primate pheromones. In M.C. Birch (Ed.) Pheromones (pp. 366–385). New York: Elsevier.Google Scholar
- Evans, C., and Schilling, A. (1995). The accessory (vomeronasal) chemoreceptor system in some prosimians. In L. Alterman, G.A. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 393–411). New York: Plenum Press.Google Scholar
- Fisher, H.S., Swaisgood, R.R., and Fitch-Snyder, H. (2003a). Odor familiarity and female preferences for males in a threatened primate, the pygmy loris Nycticebus pygmaeus: Applications for genetic management of small populations. Naturwissenschaften, 90(11): 509–512.PubMedCrossRefGoogle Scholar
- Fisher, H.S., Swaisgood, R.R., and Fitch-Snyder, H. (2003b). Countermarking by male pygmy lorises (Nycticebus pygmaeus): Do females use odor cues to select mates with high competitive ability? Behav. Ecol. and Sociobiol., 53(2): 123–130.Google Scholar
- Fitch-Snyder, H., and Schulze, H. (2001). Management of lorises in captivity: A husbandry manual for Asian lorisines. San Diego: Zoological Society of San Diego, Center for Reproduction of Endangered Species Press.Google Scholar
- Gosling, L.M. (1982). A reassessment of the function of scent marking in territories. Zeitschrift für Tierpsychologie, 60: 89–118.Google Scholar
- Gosling, L.M., and Roberts, S. (2001). Scent-marking by male mammals: Cheat-proof signals to competitors and mates. Advances in the Study of Behavior, 30: 169–217.CrossRefGoogle Scholar
- Gursky, S. (2002). Predation on a wild spectral tarsier (Tarsius spectrum) by a snake. Folia Primatol., 73: 60–62.PubMedCrossRefGoogle Scholar
- Gursky, S. (2003). Predation experiments on infant spectral tarsiers (Tarsius spectrum). Folia Primatol., 74(5–6): 272–284.PubMedCrossRefGoogle Scholar
- Gutzke, W.H.N. (2001). Field observations confirm laboratory reports of defense responses by snakes to the odors of predatory snakes. In A. Marchlewska-Koj, J. Lepri, and D. Muller-Schwarze (Eds.), Chemical signals in vertebrates (9th ed.). (pp. 285–288). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Hagey, L.R., Fry, B.G., and Snyder, H. (2006). Talking defensively: A dual use for the brachial gland exudate of slow and pygmy lorises. In S. Gursky (Ed.), this volume (pp. xx–yy). New York: Kluwer/Academic Press.Google Scholar
- Harcourt, C.S. (1981). An examination of the function of urine washing in Galago senegalensis. Zeitschrift für Tierpsychologie, 55: 119–128.Google Scholar
- Hasson, O. (1991). Pursuit-deterrent signals: Communication between prey and predator. Trends in Ecology and Evolution, 6: 325–329.CrossRefGoogle Scholar
- Hersek, M.J, and Owings, D.H. (1993). Tail flagging by adult California ground squirrels: A tonic signal that serves different functions for males and females. Animal Behaviour, 46: 129–138.CrossRefGoogle Scholar
- Heymann, E.W. (2000). Spatial patterns of scent marking in wild moustached tamarins, Saguinus mystax: No evidence for a territorial function. Animal Behaviour, 2000: 723–730.CrossRefGoogle Scholar
- Heymann, E.W. (2001). Interspecific variation of scent-marking behaviour in wild tamarins, Saguinus mystax and Saguinus fuscicollis. Folia Primatol., 72: 253–267.PubMedCrossRefGoogle Scholar
- Hill, R.A., and Dunbar, R.I.M. (1998). An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour, 135(4): 411–430.Google Scholar
- Humphries, R.E., Robertson, D.H.L., Nevison, C.M., Beynon, R.J., and Hurst, J.L. (2001). The role of urinary proteins and volatiles in competitive scent marking among male house mice. In A. Marchlewskha-Koj, J. Lepri, and D. Muller-Schwarze (Eds.), Chemical signals in vertebrates (9th ed.). (pp. 353–360). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Ilse, D.R. (1955). Olfactory marking of territory in two young male lorises kept in captivity in Poona. British Jour. of Animal Behav., 3: 118–120.CrossRefGoogle Scholar
- Jackson, B.D., Morgan, E.D., and Billen, J.P.J. (1990). A note on pygidial glands of primitive Australian ants: A new source of odorous chemicals. In A.R. McCaffery and I.D. Wilson (Eds.), Chromatography and isolation of insect hormones and pheromones New York: Plenum Press. p. 335–341.Google Scholar
- Johnston, R.E. (1999). How do hamsters know whose scent is on top and why should it matter? In R. Johnston, D. Muller-Schwartz, and P. Sorenson (Eds.), Advances in chemical signals in vertebrates (pp. 227–238). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Koivula, M., Korpimaki, E. and Viitala, J. (1997). Do Tengmalm’s owls see vole scent marks visible in ultraviolet light? Animal Behaviour, 54: 873–877.PubMedCrossRefGoogle Scholar
- Kotenkova, E.V., and Naidenko, S.V. (1999). Discrimination of con-and heterospecific odors in different taxa of the Mus musculus species group. In R. Johnston, D. Muller-Schwartz, and P. Sorenson (Eds.), Advances in chemical signals in vertebrates (pp. 299–208). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Lewis, R.J. (2004). Sex differences in scent-marking in Sifaka: Mating conflict or male services? Unpublished doctoral dissertation. University of Texas at Austin, Texas.Google Scholar
- Lima, S. L. and Dill, L. M. (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology, 68: 619–640.Google Scholar
- Manley, G. (1974). Functions of the external genital glands of Perodicticus and Arctocebus. In R.D. Martin, G.A. Doyle, and A.C. Walker (Eds.), Prosimian biology (pp. 313–329). London: Duckworth.Google Scholar
- Mathis, A., Chivers, D.P., and Smith, J.F. (1995). Chemical alarm signals: Predator deterrents or predator attractants. The American Naturalist, 145(6): 994–1005.CrossRefGoogle Scholar
- Motulsky, H. (1995). Intuitive biostatistics. Oxford: Oxford Univ. Press.Google Scholar
- Nekaris, K.A.I. (2001). Activity budget and positional behavior of the Mysore slender loris (Loris tardigradus lydekkarianus): Implications for “slow climbing” locomotion. Folia Primatol., 72: 228–241.PubMedCrossRefGoogle Scholar
- Nekaris, K.A.I. (2002). Slender in the night. Natural History, 2(02): 54–59.Google Scholar
- Nekaris, K.A.I. (2003). Observations on mating, birthing and parental care in three taxa of slender loris in India and Sri Lanka (Loris tardigradus and Loris lydekkerianus). Folia Primatol., 74: 312–336.PubMedCrossRefGoogle Scholar
- Nekaris, K.A.I., and Jayewardene, J. (2003). Pilot study and conservation status of the slender loris (Loris tardigradus and Loris lydekkerianus) in Sri Lanka. Primate Conservation, 19: 83–90.Google Scholar
- Nekaris, K.A.I., and Jayewardene, J. (2004). Distribution of slender lorises in four ecological zones in Sri Lanka. Journal of Zoology, 262: 1–12.CrossRefGoogle Scholar
- Nekaris, K.A.I., and Rasmussen, D.T. (2003). Diet of the slender loris. Inter. Jour. of Primatol., 24(1): 33–46.CrossRefGoogle Scholar
- Osman Hill, W.C. (1938). A curious habit common to lorisoid and platyrrhine monkeys. Ceylon Journal of Science B, 21(1): 65.Google Scholar
- Palagi, E., Gregorace, A., and Borgognini Tarli, S.M. (2002). Development of olfactory behavior in captive ring-railed lemurs (Lemur catta). Inter. Jour. of Primatol., 23(3): 587–599.CrossRefGoogle Scholar
- Perret, M. (1995). Chemocommunication in the reproduction function of mouse lemurs. In L. Alterman, G.A. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 372–392). New York: Plenum Press.Google Scholar
- Perrot-Sinal, T., Kavaliers, M., and Ossenkopp, P. (1999). Changes in locomotor activity following predator odor exposure are dependent on sex and reproductive status in the meadow vole. In R. Johnston, D. Muller-Schwartz, and P. Sorenson (Eds.), Advances in chemical signals in vertebrates (pp. 497–504). New York: Kluwer Academic/Plenum Press.Google Scholar
- Petrulis, A., Peng, M., and Johnston, R.E. (2000). The role of the hippocampal system in social odor discrimination and scent-marking in female golden hamsters (Mesocricetus auratus). Behavioural Neuroscience, 114(1): 184–195.CrossRefGoogle Scholar
- Petter, J.J., and Hladik C.M. (1970). Observations sur le domaine vital et la densité de population de Loris tardigradus dans les forêts de Ceylon. Mammalia, 34: 394–409.CrossRefGoogle Scholar
- Pimley, E.R. (2002). The behavioural ecology and genetics of the potto (Perodicticus potto edwardsi) and Allen’s bushbaby (Galago alleni cameronensis). Doctoral thesis. University of Cambridge, Cambridge.Google Scholar
- Pimley, E.R., and Bearder, S.K. (In press). Potto (Perodicticus). In J. Kingdon, D. Happold, and T. Butysnki (Eds.), Mammals of Africa, Vol. 1. (pp. xx–yy). Cambridge: Cambridge Univ. Press.Google Scholar
- Pimley, E.R., Bearder, S.K., and Dixson, A.F. (2005a) Examining the social organization of the Milne-Edwards’ potto Perodicticus potto edwardsi. Amer. Jour. of Primatol., 66(4): 317–330.CrossRefGoogle Scholar
- Pimley, E.R., Bearder, S.K., and Dixson, A.F. (2005b). Home range analysis of Perodicticus potto edwardsi and Sciurocheirus cameronensis. Inter. Jour. of Primatol., 26(1): 191–206.CrossRefGoogle Scholar
- Rasmussen, D.T. (1986). Life history and behavior of slow lorises and slender lorises. Doctoral thesis. Duke University, Durham, NC.Google Scholar
- Rasmussen, D.T., and Nekaris, K.A.I. (1998). Evolutionary history of the lorisiform primates. Folia Primatol., 69: 250–285.PubMedCrossRefGoogle Scholar
- Roberts, S.C., and Gosling, L.M. (2001). The economic consequences of advertising scent mark location on territories. In A. Marchlewsha-Koj, J. Lepri, and D. Schwarze (Eds.), Chemical signals in vertebrates (9th ed.). (pp. 11–17). New York: Kluwer Academic/Plenum Press, New York.Google Scholar
- Rohr, J.R., and Madison, D.M. (2001). A chemically mediated trade-off between predation risk and mate search in newts. Animal Behaviour, 62: 863–869.CrossRefGoogle Scholar
- Schilling, A. (1979). Olfactory communication in prosimians. In G.A. Doyle and R.D. Martin (Eds.), The study of prosimian behaviour (pp. 461–542). London: Academic Press, Inc.Google Scholar
- Schülke, O.(2001). Social anti-predator behaviour in a nocturnal lemur. Folia Primatologica, 72(6): 332–334.Google Scholar
- Schulze, H., and Meier, B. (1995). Behaviour of captive Loris tardigradus nordicus: A qualitative description including some information about morphological bases of behavior. In L. Alterman, M. Doyle, and M.K. Izard (Eds.), Creatures of the dark: The nocturnal prosimians (pp. 221–250). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Seitz, E. (1969). Die Bedeutung gerüchlicher Orientierung beim Plumplori Nycticebus coucang Boddaert 1785 (Prosimii, Lorisidae). Zeitschrift für Tierpsychologie, 26: 73–103.PubMedCrossRefGoogle Scholar
- Sellers, W. (1996). A biomechanical investigation into the absence of leaping in the locomotor repertoire of the slender loris (Loris tardigradus). Folia Primatol., 67: 1–14.PubMedGoogle Scholar
- Shivik, J.A., and Clark, L. (1999). The development of chemosensory attractants for brown tree snakes. In R. Johnston, D. Muller-Schwartz, and P. Sorsenson (Eds.), Advances in chemical signals in vertebrates (pp. 649–654). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Smith, E.T., and Gordon, J.S. (2002). Sex differences in olfactory communication in Saguinus labiatus. Inter. Jour. of Primatol., 23(2): 429–441.CrossRefGoogle Scholar
- Solomon, N.G. (1999). The functional significance of olfactory cues in the pine vole (Microtus pinetorum). In R. Johnston, D. Muller-Schwartz, and P. Sorsenson (Eds.), Advances in chemical signals in vertebrates (pp. 407–419). New York: Kluwer Academic/Plenum Publishers.Google Scholar
- Stanford, C. (2002). Avoiding predators: Expectations and evidence in primate antipredator behavior. Inter. Jour. of Primatol., 23(4): 741–757.CrossRefGoogle Scholar
- Still, J. (1905). On the loris in captivity. Spolia Zeylanica, 3: 155–157.Google Scholar
- Terborgh, J., and Janson, C. (1986). Socioecology of primate groups. Annual Review of Ecological Systematics, 17: 111–135.CrossRefGoogle Scholar
- van Schaik, C., and van Hoof, J. (1983). On the ultimate causes of primate social systems. Behaviour, 5: 91–117.Google Scholar
- Walker, A.C. (1969). The locomotion of the lorises, with special reference to the potto. East African Wildlife Journal, 7: 1–5.Google Scholar
- Watson, S.L., Ward, J.P., David, K.B., and Stavisky, R.C. (1999). Scent-marking and cortisol response in the small-eared bushbaby (Otolemur garnettii). Physiology & Behavior, 66(4): 695–699.CrossRefGoogle Scholar
- Welker, C. (1973). Ethological significance of the urine washing by Galago crassicaudatus E. Geoffroy, 1812 (Lorisiformes: Galagidae). Folia Primatol., 20: 429–452.PubMedCrossRefGoogle Scholar
- Wiens, F. and Zitzmann, A. (1999). Predation on a wild slow loris (Nycticebus coucang) by a reticulated python (Python reticulatus). Folia Primatol., 70: 362–364.PubMedCrossRefGoogle Scholar
- Wiens, F. (2002). Behavior and ecology of wild slow lorises (Nycticebus coucang): Social organisation, infant care system and diet. Doctoral thesis. Bayreuth University, Bayreuth (Germany).Google Scholar
- Wiens, F., and Zitzmann, A. (2003). Social structure of the solitary slow loris Nycticebus coucang (Lorisidae). Journal of Zoology, 261(1): 35–46.CrossRefGoogle Scholar
- Wiley, R.H., and Richards, D.G. (1978). Physical constraints on acoustic communication in the atmosphere: Implications for the evolution of animal vocalizations. Behav. Ecol. and Sociobiol., 3: 69–94.CrossRefGoogle Scholar
- Wolff, J.O., Mech, S.G., and Thomas, S.A. (2002). Scent marking in female prairie voles: A test of alternative hypotheses. Ethology, 108: 483–494.CrossRefGoogle Scholar
- Woodland, D.J., Jaafar, Z., and Knight, M.-L. (1980). The “pursuit deterrent” function of alarm signals. American Naturalist, 115: 748–753.CrossRefGoogle Scholar
- Wyatt, T.D. (2003). Pheromones and animal behavior: Communication by smell and taste. Cambridge: Cambridge Univ. Press.Google Scholar
- Zimmerman, E. (1985). Vocalisations and associated behaviours in adult slow loris (Nycticebus coucang). Folia Primatol., 44: 52–64.Google Scholar
- Zimmermann, E. (1995). Acoustic communication in nocturnal prosimians. In: Alterman, L., Doyle, G. A. and Izard, M. K. (eds.), Creatures of the Dark: The nocturnal prosimians (pp. 311–330). New York: Plenum Press.Google Scholar