The ability to early detect a potential predator is essential for survival. The potential of Iberolacerta cyreni lizards to discriminate between chemical cues of their two predatory snakes Coronella austriaca (a non-venomous active-hunter saurophagous specialist) and Vipera latastei (a venomous sit-and-wait generalist) was evaluated herein. A third snake species, Natrix maura, which does not prey on lizards, was used as a pungent control. Thus, the behaviour of I. cyreni was studied regarding four treatments: (1) C. austriaca scent, (2) V. latastei scent, (3) N. maura scent and (4) odourless control. Lizards showed antipredator behaviour (such as slow-motion and tail waving) to C. austriaca and V. latastei chemicals. The antipredatory response was similar for both predators. This ability to react with an intensive behavioural pattern to the chemical cues of their predatory snakes may prevent lizards from being detected, and, if detected, dissuade the predator from beginning a pursuit.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Amo, L., López, P. & Martín, J. (2004). Chemosensory recognition and behavioral responses of wall lizards, Podarcis muralis, to scents of snakes that pose different risks of predation. — Copeia: 691-696.
Amo, L., López, P. & Martín, J. (2006). Can wall lizards combine chemical and visual cues to discriminate predatory from non-predatory snakes inside refuges? — Ethology 112: 478-484.
Amo, L., López, P. & Martín, J. (2007). Refuge use: a conflict between avoiding predation and losing mass in lizards. — Physiol. Behav. 90: 334-343.
Amo, L., Tomás, G. & López-García, A. (2017). Role of chemical and visual cues of mammalian predators in nest defense in birds. — Behav. Ecol. Sociobiol. 71: 49.
Apfelbach, R., Blanchard, C.D., Blanchard, R.I., Hayes, R.A. & McGregor, I.S. (2005). The effects of predator odors in mammalian prey species. A review of field and laboratory studies. — Neurosci. Biobehav. Rev. 29: 1123-1144.
Arnold, E.N. (1984). Evolutionary aspects of tail shedding in lizards and their relatives. — J. Nat. Hist. 18: 127-169.
Arnold, E.N. & Ovenden, D. (2002). A field guide to the reptiles and amphibians of Britain and Europe. — Harper Collins, London.
Arribas, O.J. (2014). Iberolacerta cyreni (Müller & Hellmich, 1937). — In: Reptiles, 2a edición revisada y aumentada. Fauna Ibérica, Vol. 10 (Salvador, A., ed.). Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, p. 383-398.
Baeckens, S., Herrel, A., Broeckhoven, C., Vasilopoulou-Kampitsi, M., Huyghe, K., Goyens, J. & Van Damme, R. (2017). Evolutionary morphology of the lizard chemosensory system. — Sci. Rep. 7: 10141.
Bateman, P.W. & Fleming, P.A. (2009). To cut a long tail short: a review of lizard caudal autotomy studies carried out over the last 20 years. — J. Zool. 277: 1-14.
Bea, A., Braña, F., Baron, J.P. & Saint-Girons, H. (1992). Régimes et cycles alimentaires des Vipères Européennes (Reptilia, Viperidae). — Ann. Biol. 31: 25-44.
Bohórquez-Alonso, M.L., Martínez-Cotrina, J., Aguilar-Pardo, D., Font, E. & Molina-Borja, M. (2010). Sex differences in antipredator tail-waving displays of the diurnal yellow-headed gecko Gonatodes albogularis from tropical forests of Colombia. — J. Ethol. 28: 305-311.
Cabido, C., Galán, P., López, P. & Martín, J. (2009). Conspicuousness-dependent antipredatory behavior may counteract coloration differences in Iberian rock lizards. — Behav. Ecol. 20: 362-370.
Cabido, C., Gonzalo, A., Galán, P., Martín, J. & López, P. (2004). Chemosensory predator recognition induces defensive behavior in the slow-worm (Anguis fragilis). — Can. J. Zool. 82: 510-515.
Caro, T.M. (2005). Antipredator defenses in birds and mammals. — University of Chicago Press, Chicago, IL.
Carrascal, L.M., López, P., Martín, J. & Salvador, A. (1992). Basking and antipredator behaviour in a high altitude lizard: implications of heat-exchange rate. — Ethology 92: 143-154.
Chivers, D.P., Mirza, R.S., Bryer, P.J. & Kiesecker, J.M. (2001). Threat-sensitive predator avoidance by slimy sculpins: understanding the importance of visual versus chemical information. — Can. J. Zool. 79: 867-873.
Constanzo-Chávez, J., Penna, M. & Labra, A. (2018). Comparing the antipredator behaviour of two sympatric, but not syntopic, Liolaemus lizards. — Behav. Process. 148: 34-40.
Cooper, W.E. (1994). Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. — J. Chem. Ecol. 20: 439-487.
Cooper, W.E. (2010). Pursuit deterrence varies with predation risk affecting escape behaviour in the lizard Callisaurus draconoides. — Anim. Behav. 80: 249-256.
Cooper, W.E. & Burghardt, G.M. (1990). A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles. — J. Chem. Ecol. 16: 45-65.
Cooper, W.E., Pérez-Mellado, V., Baird, T.A., Caldwell, J.P. & Vitt, L.J. (2004). Pursuit deterrent signalling by the Bonaire whiptail lizard Cnemidophorus murinus. — Behaviour 141: 297-311.
Crawley, M.J. (2012). The R book. — Wiley, Chichester.
Dial, B.E. & Schwenk, K. (1996). Olfaction and predator detection in Coleonyx brevis (Squamata: Eublepharidae), with comments on the functional significance of buccal pulsing in geckos. — J. Exp. Zool. 276: 415-424.
Downes, S. (2002). Does responsiveness to predator scents affect lizard survivorship? — Behav. Ecol. Sociobiol. 52: 38-42.
Downes, S. & Shine, R. (1998). Sedentary snakes and gullible geckos: predator–prey coevolution in nocturnal rock-dwelling reptiles. — Anim. Behav. 55: 1373-1385.
Endler, J.A. (1986). Defense against predators. — In: Predator–prey relationships. Perspectives and approaches from the study of lower vertebrates (Feder, M.E. & Lauder, G.V., eds). The University of Chicago Press, Chicago, IL, p. 109-134.
Font, E., Carazo, P., Perez i de Lanuza, G. & Kramer, M. (2012). Predator-elicited foot shakes in wall lizards (Podarcis muralis): evidence for a pursuit-deterrent function. — J. Comp. Psychol. 126: 87-96.
Galán, P. (2014). Coronella austriaca Laurenti, 1768. — In: Reptiles, 2a edición revisada y aumentada. Fauna Ibérica, Vol. 10 (Salvador, A., ed.). Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, p. 681-706.
García-París, M., Martín, C., Dorda, J. & Esteban, M. (1989). Los anfibios y Reptiles de Madrid. — Ministerio de Agricultura, Pesca y Alimentación, Madrid.
Garvey, P.M., Glen, A.S. & Pech, R.P. (2016). Dominant predator odour triggers caution and eavesdropping behaviour in a mammalian mesopredator. — Behav. Ecol. Sociobiol. 70: 481-492.
Giraudoux, P. (2012). pgirmess: data analysis in ecology. — R package version 1.5.6.
Goddard, P. (1984). Morphology, growth, food habits and population characteristics of the smooth snake Coronella austriaca in southern Britain. — J. Zool. 204: 241-257.
Greene, H.W. (1988). Antipredator mechanisms in reptiles. — In: Biology of Reptilia, Vol. 16. Ecology B: defense and life history (Gans, C. & Huey, R.B., eds). Alan R. Liss, New York, NY, p. 1-152.
Hasson, O. (1991). Pursuit-deterrent signals: communication between prey and predator. — Trends Ecol. Evol. 6: 325-329.
Helfman, G.S. (1989). Threat-sensitive predator avoidance in damselfish–trumpetfish interactions. — Behav. Ecol. Sociobiol. 24: 47-58.
Hirvonen, H., Ranta, E., Piironen, J., Laurila, A. & Peuhkuri, N. (2000). Behavioral responses of naive Arctic charr to chemical cues from salmonid and non-salmonid fish. — Oikos 88: 191-199.
Kats, L.B. & Dill, L.M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. — EcoScience 5: 361-394.
Labra, A. & Hoare, M. (2015). Chemical recognition in a snake–lizard predator–prey system. — Acta Ethol. 18: 173-179.
Labra, A. & Niemeyer, H.M. (2004). Variability in the assessment of snake predation risk by Liolaemus lizards. — Ethology 110: 649-662.
Landová, E., Musilová, V., Polák, J., Sedláčková, K. & Frynta, D. (2016). Antipredatory reaction of the leopard gecko Eublepharis macularius to snake predators. — Curr. Zool. 62: 439-450.
Lima, S.L. (1993). Ecological and evolutionary perspectives on escape from predatory attack. — Wilson Bull. 105: 1-47.
Lima, S.L. (1998). Stress and decision making under the risk of predation: recent developments from behavioral, reproductive, and ecological perspectives. — Adv. Stud. Behav. 27: 215-290.
Lima, S.L. & Dill, L.M. (1990). Behavioural decisions made under the risk of predation: a review and prospectus. — Can. J. Zool. 68: 619-640.
Lloyd, R., Alford, R.A. & Schwarzkopf, L. (2009). Chemical discrimination among predators by lizards: responses of three skink species to the odours of high- and low-threat varanid predators. — Austr. Ecol. 34: 50-54.
López, P., Hawlena, D., Polo, V., Amo, L. & Martín, J. (2005). Sources of interindividual shy-bold variations in antipredatory behaviour of male Iberian rock-lizards. — Anim. Behav. 69: 1-9.
Magnusson, W.E. (1996). Tail and hand waves: a come-on for predators? — Herpetol. Rev. 27: 60.
Martín, J. (2001). When hiding from predators is costly: optimization of refuge use in lizards. — Etologia 9: 9-13.
Martín, J. & López, P. (2003). Ontogenetic variation in antipredatory behavior of Iberian-rock lizards (Lacerta monticola): effects of body-size-dependent thermal-exchange rates and costs of refuge use. — Can. J. Zool. 81: 1131-1137.
Martín, J. & López, P. (2004). Iberian rock lizards (Lacerta monticola) assess short-term changes in predation risk level when deciding refuge use. — J. Comp. Psychol. 118: 280-286.
Martín, J. & López, P. (2013). Responses of female rock lizards to multiple scent marks of males: effects of male age, male density and scent over-marking. — Behav. Process. 94: 109-114.
Martín, J. & Salvador, A. (1992). Tail loss consequences on habitat use by the Iberian rock lizard Lacerta monticola. — Oikos 65: 328-333.
Martín, J. & Salvador, A. (1993a). Thermoregulatory behaviour of rock-lizards in response to tail loss. — Behaviour 124: 123-136.
Martín, J. & Salvador, A. (1993b). Tail loss reduces mating success in the Iberian rock-lizard. — Behav. Ecol. Sociobiol. 32: 185-189.
Martín, J. & Salvador, A. (1995). Effects of tail loss on activity patterns of rock-lizards, Lacerta monticola. — Copeia: 984-988.
Martín, J. & Salvador, A. (1997a). Microhabitat selection by the Iberian rock lizard Lacerta monticola: effects on density and spatial distribution of individuals. — Biol. Conserv. 79: 303-307.
Martín, J. & Salvador, A. (1997b). Effects of tail loss on the time budgets, movements, and spacing patterns of Iberian rock lizards, Lacerta monticola. — Herpetologica 53: 117-125.
Martín, J., López, P. & Polo, V. (2009a). Temporal patterns of predation risk affect antipredator behaviour allocation by Iberian rock lizards. — Anim. Behav. 77: 1261-1266.
Martín, J., Luque-Larena, J.J. & Lopez, P. (2009b). When to run from an ambush predator: balancing crypsis benefits with costs of fleeing in lizards. — Anim. Behav. 78: 1011-1018.
Martínez-Freiría, F., Brito, J.C., Pleguezuelos, J.M. & Santos, X. (2014). Vipera latastei Boscá, 1878. — In: Reptiles, 2a edición revisada y aumentada. Fauna Ibérica, Vol. 10 (Salvador, A., ed.). Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, p. 920-941.
Martins, E.P. (1993). Contextual use of the push-up display by the sagebrush lizard, Sceloporus graciosus. — Anim. Behav. 45: 25-36.
Martins, E.P., Labra, A., Halloy, M. & Thompson, J.T. (2004). Large-scale patterns of signal evolution: an interspecific study of Liolaemus lizard headbob displays. — Anim. Behav. 68: 453-463.
McAdam, A.G. & Kramer, D.L. (1998). Vigilance as a benefit of intermittent locomotion in small mammals. — Anim. Behav. 55: 109-117.
Mencía, A., Ortega, Z. & Pérez-Mellado, V. (2016). Chemical discrimination of sympatric snakes by the mountain lizard Iberolacerta galani (Squamata: Lacertidae). — Herpetol. J. 26: 149-155.
Mencía, A., Ortega, Z. & Pérez-Mellado, V. (2017). From tameness to wariness: chemical recognition of snake predators by lizards in a Mediterranean island. — PeerJ 5: e2828.
Mitchell, M.D., Chivers, D.P., McCormick, M.I. & Ferrari, M.C. (2015). Learning to distinguish between predators and non-predators: understanding the critical role of diet cues and predator odours in generalisation. — Sci. Rep. 5: 13918.
Monasterio, C., Salvador, A. & Díaz, J.A. (2010a). Altitude and rock cover explain the distribution and abundance of a Mediterranean alpine lizard. — J. Herpetol. 44: 158-163.
Monasterio, C., Salvador, A. & Díaz, J.A. (2010b). Competition with wall lizards does not explain the alpine confinement of Iberian rock lizards: an experimental approach. — Zoology 113: 275-282.
Mori, A. & Hasegawa, M. (1999). Geographic differences in behavioral responses of hatchling lizards (Eumeces okadae) to snake-predator chemicals. — Jpn. J. Herpetol. 18: 45-56.
Murphy, T.G. (2006). Predator-elicited visual signal: why the turquoise-browed motmot wag-displays its racketed tail. — Behav. Ecol. 17: 547-553.
Ortega, Z., Mencía, A. & Pérez-Mellado, V. (2016). Behavioral buffering of global warming in a cold-adapted lizard. — Ecol. Evol. 6: 4582-4590.
Ortega, Z., Mencía, A. & Pérez-Mellado, V. (2017). Rapid acquisition of antipredatory responses to new predators by an insular lizard. — Behav. Ecol. Sociobiol. 71: 1-9.
Pérez-Mellado, V. (1982). Datos sobre Lacerta monticola Boulenger, 1905 (Sauria: Lacertidae) en el oeste del Sistema Central. — Doñana Acta Vertebrata 9: 107-129.
Polo, V., López, P. & Martín, J. (2005). Balancing thermal costs and benefits of refuge use to cope with persistent attacks from predators: a model and an experiment with an alpine lizard. — Evol. Ecol. Res. 7: 23-35.
Polo, V., López, P. & Martín, J. (2011). Uncertainty about future predation risk modulates monitoring behavior from refuges in lizards. — Behav. Ecol. 22: 218-223.
R Development Core Team (2015). A language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna.
Roth, T.C., Cox, J.C. & Lima, S.L. (2008). Can foraging birds assess predation risk by scent? — Anim. Behav. 76: 2021-2027.
Rugiero, L., Capula, M., Filippi, E. & Luiselli, L. (1995). Food habits of Mediterranean populations of the smooth snake (Coronella austriaca). — Herpetol. J. 5: 316-318.
Santos, X. (2014). Natrix maura (Linnaeus, 1758). — In: Reptiles, 2a edición revisada y aumentada. Fauna Ibérica, Vol. 10 (Salvador, A., ed.). Museo Nacional de Ciencias Naturales, Consejo Superior de Investigaciones Científicas, Madrid, p. 820-842.
Santos, X., Llorente, G.A., Pleguezuelos, J.M., Brito, J.C., Fahd, S. & Parellada, X. (2007). Variation in the diet of the Lataste’s viper Vipera latastei in the Iberian Peninsula: seasonal, sexual and size-related effects. — Anim. Biol. 57: 49-61.
Schätti, B. (1982). Bemerkungen zur ökologie, verbreitung und intraspezifischen variation der vipernatter, Natrix maura (Linné, 1758) (Reptilia, Serpentes). — Revue Suisse de Zoologie 89: 521-542.
Schleich, H.H., Kastle, W. & Kabisch, K. (1996). Amphibians and reptiles of north Africa. — Koeltz Scientific Publishers, Koenigstein.
Schoeppner, N.M. & Relyea, R.A. (2009). Interpreting the smells of predation: how alarm cues and kairomones induce different prey defences. — Funct. Ecol. 23: 1114-1121.
Schwenk, K. (1995). Of tongues and noses: chemoreception in lizards and snakes. — Trends Ecol. Evol. 10: 7-12.
Semlitsch, R.D. & Gavasso, S. (1992). Behavioural responses of Bufo bufo and Bufo calamita tadpoles to chemical cues of vertebrate and invertebrate predators. — Ethol. Ecol. Evol. 4: 165-173.
Shaffery, H.M. & Relyea, R.A. (2016). Dissecting the smell of fear from conspecific and heterospecific prey: investigating the processes that induce anti-predator defenses. — Oecologia 180: 55-65.
Sherbrooke, W.C. (2008). Antipredator responses by Texas horned lizards to two snake taxa with different foraging and subjugation strategies. — J. Herpetol. 42: 145-152.
Sih, A. (1987). Predators and prey lifestyles: an evolutionary and ecological overview. — In: Predation: direct and indirect impacts on aquatic communities (Kerfoot, W.C. & Sih, A., eds). University Press of New England, Hanover, p. 203-204.
Stapley, J. (2003). Differential avoidance of snake odours by a lizard: evidence for prioritised avoidance based on risk. — Ethology 109: 785-796.
Thoen, C., Bauwens, D. & Verheyen, R.F. (1986). Chemoreceptive and behavioural responses of the common lizard Lacerta vivipara to snake chemical deposits. — Anim. Behav. 34: 1805-1813.
Van Damme, R. & Quick, K. (2001). Use of predator chemical cues by three species of lacertid lizards (Lacerta bedriagae, Podarcis tiliguerta, Podarcis sicula). — J. Herpetol. 35: 27-36.
Van Damme, R., Bauwens, D., Thoen, C., Vanderstighelen, D. & Verheyen, R.F. (1995). Responses of naive lizards to predator chemical cues. — J. Herpetol. 2: 38-43.
Vermeij, G.J. (1994). The evolutionary interaction among species: selection, escalation, and coevolution. — Annu. Rev. Ecol. Syst. 25: 219-236.
Vicente, N.S. (2018). Headbob displays signal sex, social context and species identity in a Liolaemus lizard. — Amphibia-Reptilia 39: 203-218.
Webb, J.K., Du, W.G., Pike, D.A. & Shine, R. (2009). Chemical cues from both dangerous and nondangerous snakes elicit antipredator behaviours from a nocturnal lizard. — Anim. Behav. 77: 1471-1478.
Woodland, D.J., Jaafar, Z. & Knight, M.L. (1980). The ‘pursuit deterrent’ function of alarm signals. — Am. Nat. 115: 748-753.
Ydenberg, R.C. & Dill, L.M. (1986). The economics of fleeing from predators. — Adv. Stud. Behav. 16: 229-249.
Zahavi, A. (1977). Reliability of communication systems and the evolution of altruism. — In: Evolutionary ecology (Stonehouse, B. & Perrins, C.M., eds). MacMillan, London, p. 253-259.
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 952 | 189 | 23 |
Full Text Views | 143 | 9 | 1 |
PDF Views & Downloads | 74 | 11 | 0 |
The ability to early detect a potential predator is essential for survival. The potential of Iberolacerta cyreni lizards to discriminate between chemical cues of their two predatory snakes Coronella austriaca (a non-venomous active-hunter saurophagous specialist) and Vipera latastei (a venomous sit-and-wait generalist) was evaluated herein. A third snake species, Natrix maura, which does not prey on lizards, was used as a pungent control. Thus, the behaviour of I. cyreni was studied regarding four treatments: (1) C. austriaca scent, (2) V. latastei scent, (3) N. maura scent and (4) odourless control. Lizards showed antipredator behaviour (such as slow-motion and tail waving) to C. austriaca and V. latastei chemicals. The antipredatory response was similar for both predators. This ability to react with an intensive behavioural pattern to the chemical cues of their predatory snakes may prevent lizards from being detected, and, if detected, dissuade the predator from beginning a pursuit.
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 952 | 189 | 23 |
Full Text Views | 143 | 9 | 1 |
PDF Views & Downloads | 74 | 11 | 0 |