Effects of global warming on sensory ecology of rock lizards: Increased temperatures alter the efficacy of sexual chemical signals

Functional Ecology

Volumn 27, Issue 6, 2013, Pages 1332-1340

  Martín, José ^a   López, Pilar ^a  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

Author keywords

Chemoreception; Climate warming; Femoral secretions; Intraspecific communication; Pheromones; Sexual selection

Indexed keywords

CHEMORECEPTION; COMMUNICATION; ENVIRONMENTAL CONDITIONS; FEMALE; GLOBAL WARMING; LIZARD; PHEROMONE; SEXUAL SELECTION; SIGNAL; SPECIES CONSERVATION; TEMPERATURE EFFECT;

ANIMALIA; IBEROLACERTA CYRENI; PETROSAURUS; SQUAMATA;

EID: 84887821916     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12128     Document Type: Article

References (71)

1. Alberts, A.C. (1992) Constraints on the design of chemical communication systems in terrestrial vertebrates. American Naturalist, 139, 62-89.
2. Aragón, P., López, P. & Martín, J. (2004) The ontogeny of spatio-temporal tactics and social relationships of adult male Iberian rock lizards, Lacerta monticola. Ethology, 110, 1001-1019.
3. Araújo, M.B., Thuiller, W. & Pearson, R.G. (2006) Climate warming and the decline of amphibians and reptiles in Europe. Journal of Biogeography, 33, 1712-1728.
4. Aubret, F. & Shine, R. (2010) Thermal plasticity in young snakes: how will climate change affect the thermoregulatory tactics of ectotherms? Journal of Experimental Biology, 213, 242-248.
5. Boughman, J.W. (2002) How sensory drive can promote speciation. Trends in Ecology and Evolution, 17, 571-577.
6. Bradbury, J.W. & Vehrencamp, S.V. (2011) Principles of Animal Communication, 2nd edn. Sinauer Associates, Sunderland, MA.
7. Brennan, P.A. & Kendrick, K.M. (2006) Mammalian social odours: attraction and individual recognition. Philosophical Transactions of the Royal Society of London. Series B, 361, 2061-2078.
8. Candolin, U., Salesto, T. & Evers, M. (2007) Changed environmental conditions weaken sexual selection in sticklebacks. Journal of Evolutionary Biology, 20, 233-239.
9. Carazo, P., Font, E. & Desfilis, E. (2007) Chemosensory assessment of rival competitive ability and scent mark function in a lizard (Podarcis hispanica). Animal Behaviour, 74, 895-902.
10. Charmantier, A., McCleery, R.H., Cole, L.R., Perrins, C., Kruuk, L.E.B. & Sheldon, B.C. (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science, 320, 800-803.
11. Cooper, W.E. Jr (1994) Chemical discrimination by tongue-flicking in lizards: a review with hypotheses on its origin and its ecological and phylogenetic relationships. Journal of Chemical Ecology, 20, 439-487.
12. Cooper, W.E. Jr (1998) Evaluation of swab and related tests as a bioassay for assessing responses by squamate reptiles to chemical stimuli. Journal of Chemical Ecology, 24, 841-866.
13. Cooper, W.E. Jr & Burghardt, G.M. (1990) A comparative analysis of scoring methods for chemical discrimination of prey by squamate reptiles. Journal of Chemical Ecology, 16, 45-65.
14. Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak, D.C. & Martin, P.R. (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences of the United States of America, 105, 6668-6672.
15. Dubey, S. & Shine, R. (2011) Predicting the effects of climate change on an endangered montane lizard, Eulamprus leuraensis (Scincidae). Climatic Change, 107, 531-547.
16. Endler, J.A. & Basolo, A.L. (1998) Sensory ecology, receiver biases and sexual selection. Trends in Ecology and Evolution, 13, 416-420.
17. Epple, G., Alveario, M.C., Golob, N.F. & Smith, A.B. (1980) Stability and attractiveness related to age of scent marks of saddle back tamarins (Saguinus fuscicollis). Journal of Chemical Ecology, 6, 735-748.
18. Escobar, C.A., Labra, A. & Niemeyer, H.M. (2001) Chemical composition of precloacal secretions of Liolaemus lizards. Journal of Chemical Ecology, 27, 1677-1690.
19. Escobar, C.M., Escobar, C.A., Labra, A. & Niemeyer, H.M. (2003) Chemical composition of precloacal secretions of two Liolaemus fabiani populations: are they different? Journal of Chemical Ecology, 29, 629-638.
20. Ferrari, M.C.O., Dixson, D.L., Munday, P.L., McCormick, M.I., Meekan, M.G., Sih, A. & Chivers, D.P. (2011) Intrageneric variation in anti-predator responses of coral reef fishes to ocean acidification: implications of projecting climate change on marine communities. Global Change Biology, 17, 2980-2986.
21. Fox, S.F. & Shipman, P.A. (2003) Social behavior at high and low elevations: Environmental release and phylogenetic effects in Liolaemus. Lizard Social Behavior (eds F. Fox, J.K. McCoy & T.A. Baird ), pp. 310-355. John Hopkins University Press, New York.
22. Green, P.J. & Silverman, B.W. (1994) Nonparametric Regression and Generalized Linear Models: A Roughness Penalty Approach. Chapman & Hall, London.
23. Guilford, T. & Dawkins, M.S. (1991) Receiver psychology and the evolution of animal signals. Animal Behaviour, 42, 1-14.
24. Gunderson, A.R. & Leal, M. (2012) Geographic variation in vulnerability to climate warming in a tropical Caribbean lizard. Functional Ecology, 26, 783-793.
25. Herbert-Read, J.E., Logendran, D. & Ward, A.J.W. (2010) Sensory ecology in a changing world: salinity alters conspecific recognition in an amphidromous fish, Pseudomugil signifer. Behavioral Ecology and Sociobiology, 64, 1107-1115.
26. Hoffman, A.A. & Sgrò, C.M. (2011) Climate change and evolutionary adaptation. Nature, 470, 479-485.
27. Hosmer, D.W. Jr & Lemeshow, S. (1989) Applied Logistic Regression. Wiley, New York.
28. Huey, R.B. (1982) Temperature, physiology and the ecology of reptiles. Biology of the Reptilia. Physiology C. Physiological Ecology (eds C. Gans & F.H. Pough ), pp. 25-67. Academic Press, London.
29. Huey, R.B., Deutsch, C.A., Tewksbury, J.J., Vitt, L.J., Hertz, P.E., Álvarez-Pérez, H.J. & Garland, T. Jr (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society of London. Series B, 276, 1939-1948.
30. IPCC (2007) Climate Change 2007. The Physical Science Basis. Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge.
31. Iraeta, P., Monasterio, C., Salvador, A. & Díaz, J.A. (2011) Sexual dimorphism and interpopulation differences in lizard hind limb length: locomotor performance or chemical signalling? Biological Journal of the Linnean Society, 104, 318-329.
32. Kearney, M.R., Porter, W. & Shine, R. (2009) The potential for behavioral thermoregulation to buffer 'cold-blooded' animals against climate warming. Proceedings of the National Academy of Sciences of the United States of America, 106, 3835-3840.
33. López, P., Amo, L. & Martín, J. (2006) Reliable signaling by chemical cues of male traits and health state in male lizards, Lacerta monticola. Journal of Chemical Ecology, 32, 473-488.
34. López, P., Aragón, P. & Martín, J. (1998) Iberian rock lizards (Lacerta monticola cyreni) assess conspecific information using composite signals from faecal pellets. Ethology, 104, 809-820.
35. López, P., Gabirot, M. & Martín, J. (2009) Immune activation affects chemical sexual ornaments of male Iberian wall lizards. Naturwissenschaften, 96, 65-69.
36. López, P. & Martín, J. (2002) Chemical rival recognition decreases aggression levels in male Iberian wall lizards, Podarcis hispanica. Behavioral Ecology and Sociobiology, 51, 461-465.
37. López, P. & Martín, J. (2005) Chemical compounds from femoral gland secretions of male Iberian rock lizards, Lacerta monticola cyreni. Zeitschrift für Naturforschung C, 60, 632-636.
38. López, P. & Martín, J. (2011) Male Iberian rock lizards may reduce the costs of fighting by scent-matching of the resource holders. Behavioral Ecology and Sociobiology, 65, 1891-1898.
39. Lurling, M. & Scheffer, M. (2007) Info-disruption: pollution and the transfer of chemical information between organisms. Trends in Ecology and Evolution, 22, 374-379.
40. Martín, J. & López, P. (2000) Chemoreception, symmetry and mate choice in lizards. Proceedings of the Royal Society of London. Series B, 267, 1265-1269.
41. Martín, J. & López, P. (2006a) Links between male quality, male chemical signals, and female mate choice in Iberian rock lizards. Functional Ecology, 20, 1087-1096.
42. Martín, J. & López, P. (2006b) Vitamin D supplementation increases the attractiveness of males' scent for female Iberian rock lizards. Proceedings of the Royal Society of London. Series B, 273, 2619-2624.
43. Martín, J. & López, P. (2006c) Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex. Chemoecology, 16, 31-38.
44. Martín, J. & López, P. (2007) Scent may signal fighting ability in male Iberian rock lizards. Biology Letters, 3, 125-127.
45. Martín, J. & López, P. (2008) Intersexual differences in chemosensory responses to selected lipids reveal different messages conveyed by femoral secretions of male Iberian rock lizards. Amphibia-Reptilia, 29, 572-578.
46. Martín, J. & López, P. (2011) Pheromones and reproduction in Reptiles. Hormones and Reproduction in Vertebrates. Vol. 3. Reptiles (eds D.O. Norris & K.H. Lopez ), pp. 141-167. Academic Press, San Diego, CA.
47. Martín, J. & López, P. (2012) Supplementation of male pheromone on rock substrates attracts female rock lizards to the territories of males: a field experiment. PLoS ONE, 7, e30108.
48. Martín, J. & Salvador, A. (1993) Thermoregulatory behaviour of rock-lizards in response to tail loss. Behaviour, 124, 123-136.
49. Martín, J. & Salvador, A. (1997a) Microhabitat selection by the Iberian rock-lizard Lacerta monticola: effects on density and spatial distribution of individuals. Biological Conservation, 79, 303-307.
50. 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.
51. Martín, J., Civantos, E., Amo, L. & López, P. (2007) Chemical ornaments of male lizards Psammodromus algirus may reveal their parasite load and health state to females. Behavioral Ecology and Sociobiology, 62, 173-179.
52. Martins, E.P., Ord, T.J., Slaven, J., Wright, J.L. & Housworth, E.A. (2006) Individual, sexual, seasonal, and temporal variation in the amount of sagebrush lizard scent marks. Journal of Chemical Ecology, 32, 881-893.
53. Mason, R.T. (1992) Reptilian pheromones. Biology of Reptilia. Vol. 18. Hormones, Brain, and Behavior (ed C. Gans ), pp. 114-228. University of Chicago Press, Chicago, IL.
54. Mason, R.T. & Parker, M.R. (2010) Social behavior and pheromonal communication in reptiles. Journal of Comparative Physiology A, 196, 729-749.
55. McDonough, L.M., Brown, D.F. & Aller, W.C. (1989) Insect sex pheromones: effect of temperature on evaporation rates of acetates from rubber septa. Journal of Chemical Ecology, 15, 779-790.
56. Möller, A.P. (2011) When climate change affects where birds sing. Behavioral Ecology, 22, 212-217.
57. Monasterio, C., Salvador, A., Iraeta, P. & Diaz, J.A. (2009) The effects of thermal biology and refuge availability on the restricted distribution of an alpine lizard. Journal of Biogeography, 36, 1673-1684.
58. Moyes, K., Nussey, D.H., Clements, M.N., Guiness, F.E., Morris, A., Morris, S., Pemberton, J.M., Kruuk, L. & Clutton-Brock, T.H. (2011) Advancing breeding phenology in response to environmental change in a wild red deer population. Global Change Biology, 17, 2455-2469.
59. Müller-Schwarze, D. (2006) Chemical Ecology of Vertebrates. Cambridge University Press, Cambridge.
60. Nogués-Bravo, D., Araújo, M.B., Lasanta, T. & López Moreno, J.Y. (2008) Climate change in Mediterranean mountains during the 21st Century. Ambio, 37, 280-285.
61. Olsson, M., Madsen, T., Nordby, J., Wapstra, E., Ujvari, B. & Wittsell, H. (2003) Major histocompatibility complex and mate choice in sand lizards. Proceedings of the Royal Society of London. Series B, 270, S254-S256.
62. Parmesan, C. (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology, Evolution and Systematics, 37, 637-669.
63. Regnier, F.E. & Goodwin, M. (1977) On the chemical and environmental modulation of pheromone release from vertebrate scent marks. Chemical Signals in Vertebrates (eds D. Müller-Schwarze & M.M. Mozell ), pp. 115-133. Plenum Press, New York.
64. Salvador, A., Díaz, J.A., Veiga, J.P., Bloor, P. & Brown, R.P. (2008) Correlates of reproductive success in male lizards of the alpine species Iberolacerta cyreni. Behavioral Ecology, 19, 169-176.
65. Sih, A., Ferrari, M.C.O. & Harris, D.J. (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evolutionary Applications, 4, 367-387.
66. Sinervo, B., Méndez-de-la-Cruz, F., Miles, D.B., Heulin, B., Bastiaans, E., Villagrán-Santa Cruz, M., Lara-Resendiz, R., Martínez-Méndez, N., Calderón-Espinosa, M.L., Meza-Lázaro, R.N., Gadsden, H., Avila, L.J., Morando, M., de la Riva, I.J., Sepulveda, P.V., Rocha, C.F.D., Ibarguéngoytía, N., Puntriano, C.A., Massot, M., Lepetz, V., Oksanen, T.A., Chapple, D.G., Bauer, A.M., Branch, W.R., Clobert, J. & Sites, J.W. Jr (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science, 328, 894-899.
67. Sokal, R.R. & Rohlf, F.J. (1995) Biometry 3rd edn. W.H, Freeman, New York.
68. Telemeco, R.S., Elphick, M.J. & Shine, R. (2009) Nesting lizards (Bassiana duperreyi) compensate partly, but not completely, for climate change. Ecology, 90, 17-22.
69. Tuomainen, U. & Candolin, U. (2011) Behavioural responses to human-induced environmental change. Biological Reviews, 86, 640-657.
70. Visser, M.E. (2008) Keeping up with a warming world; assessing the rate of adaptation to climate change. Proceedings of the Royal Society of London, Series B, 275, 649-659.
71. Wyatt, T.D. (2003) Pheromones and Animal Behaviour. Cambridge University Press, Cambridge.