Colonization of novel White Sands habitat is associated with changes in lizard anti-predator behaviour

Biological Journal of the Linnean Society

Volumn 103, Issue 3, 2011, Pages 657-667

  Robertson, Jeanne M ^a   Hoversten, Knut ^a   Gründler, Michael ^b   Poorten, Thomas J ^a   Hews, Diana K ^c   Rosenblum, Erica Bree ^a  

^a UNIVERSITY OF IDAHO   (United States)

^b Cornell University ^*  (United States)

^c INDIANA STATE UNIVERSITY   (United States)

Author keywords

Acute stress response; Corticosterone; ELISA; Predation; Sceloporus undulatus; Testosterone; White Sands

Indexed keywords

ABUNDANCE; ANTIPREDATOR DEFENSE; BASELINE CONDITIONS; COLONIZATION; DUNE; EVOLUTIONARY BIOLOGY; GYPSUM; HABITUATION; IMMUNOASSAY; LIZARD; REPRODUCTIVE COST; SEX HORMONE; STRESS CHANGE;

NEW MEXICO; UNITED STATES; WHITE SANDS;

ANIMALIA; SCELOPORUS UNDULATUS; SQUAMATA;

EID: 79959246375     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2011.01644.x     Document Type: Article

References (64)

1. Abramsky Z, Strauss E, Subach A, Kotler BP, Riechman A. 1996. The effect of barn owls (Tyto alba) on the activity and microhabitat selection of Gerbillus allenbyi and G. pyramidum. Oecologia 105: 313-319.
2. Adams JL, Camelio KW, Orique MJ, Blumstein DT. 2006. Does information of predators influence general wariness? Behavioral Ecology and Sociobiology 60: 742-747.
3. Adkins-Regan E. 2005. Hormones and animal social behavior. Princeton, NJ: Princeton University Press.
4. Baird TA, Hews DK. 2007. Hormone levels in territorial and non-territorial male collared lizards. Physiology & Behavior 92: 755-763.
5. Berger S, Wikelski M, Romero LM, Kalko EK, Roedl T. 2007. Behavioral and physiological adjustments to new predators in an endemic island species, the Galapagos marine iguana. Hormones and Behavior 52: 653-663.
6. Breuner CW, Orchinik M, Hahn TP, Meddle SL, Moore IT, Owen-Ashley NT, Sperry TS, Wingfield JC. 2003. Differential mechanisms for regulation of the stress response across latitudinal gradients. American Journal of Physiology-Regulatory Integrative and Comparative Physiology 285: R594-R600.
7. Burkett D, Black D. 2004. Final amphibian and reptile survey of White Sands Missile Range, New Mexico 1999-2002. In: Report # OMB No. 0704-0188. U. S. Army White Sands Missile Range Environmental Stewardship Division Environment and Safety Directorate White Sands Missile Range, New Mexico 88002-5048.
8. Charlier TD, Underhill C, Hammond GL, Soma KK. 2009. Effects of aggressive encounters on plasma corticosteroid-binding globulin and its ligands in white-crowned sparrows. Hormones and Behavior 56: 339-347.
9. Connell JH, Slatyer RO. 1977. Mechanisms of succession in natural communities and their role in community stability and organization. American Naturalist 111: 1119-1144.
10. Cooper WE. 1997. Factors affecting risk and cost of escape by the broad-headed skink (Eumeces laticeps): predator speed, directness of approach, and female presence. Herpetologica 53: 464-474.
11. Cooper WE, Steele LJ. 1997. Pheromonal discrimination of sex by male and female leopard geckos (Eublepharis macularius). Journal of Chemical Ecology 23: 2967-2977.
12. Cooper WE, Hawlena D, Perez-Mellado V. 2009. Islet tameness: escape behavior and refuge use in populations of the Balearic lizard (Podarcis lilfordi) exposed to differing predation pressure. Canadian Journal of Zoology-Revue Canadienne De Zoologie 87: 912-919.
13. Denardo DF, Licht P. 1993. Effects of corticosterone on social-behavior of male lizards. Hormones and Behavior 27: 184-199.
14. Diamond JM. 1970. Ecological consequences of island colonization by Southwest Pacific birds, I. Types of niche shifts. Proceedings of the National Academy of Sciences 67: 529-536.
15. Diego-Rasilla FJ. 2003. Influence of predation pressure on the escape behaviour of Podarcis muralis lizards. Behavioural Processes 63: 1-7.
16. Dunlap KD, Wingfield JC. 1995. External and internal influences on indexes of physiological stress. 1. Seasonal and population variation in adrenocortical secretion of free-living lizards, Sceloporus occidentalis. Journal of Experimental Zoology 271: 36-46.
17. Gillis JE. 1989. Selection for substrate reflectance-matching in 2 populations of red-chinned lizards (Sceloporus undulatus-erythrocheilus) from Colorado. American Midland Naturalist 121: 197-200.
18. Hager SB. 2001. Microhabitat use and activity patterns of Holbrookia maculata and Sceloporus undulatus at White Sands National Monument, New Mexico. Journal of Herpetology 35: 326-330.
19. Hasegawa M. 1994. Insular radiation in life-history of the lizard Eumeces okadae in the Izu Islands, Japan. Copeia 3: 732-747.
20. Hews DK, Moore MC. 1997. Hormones and sex-specific traits: critical questions. In: Beckage NE, ed. Parasites and pathogens: effects on host hormones and behavior. New York: Chapman and Hall, 277-292.
21. Huyghe K, Husak JF, Herrel A, Tadic Z, Moore IT, Van Damme R, Vanhooydonck B. 2009. Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Hormones and Behavior 55: 488-494.
22. Jennings DH, Moore MC, Knapp R, Matthews L, Orchinik M. 2000. Plasma steroid-binding globulin mediation of differences in stress reactivity in alternative male phenotypes in tree lizards, Urosaurus ornatus. General and Comparative Endocrinology 120: 289-299.
23. John-Alder HB, Cox RM, Haenel GJ, Smith LC. 2009. Hormones, performance and fitness: natural history and endocrine experiments on a lizard (Sceloporus undulatus). Integrative and Comparative Biology 49: 393-407.
24. Kabelik D, Weiss SL, Moore MC. 2008. Arginine Vasotocin (AVT) Immunoreactivity relates to testosterone but not territorial aggression in the tree lizard, Urosaurus ornatus. Brain Behavior and Evolution 72: 283-294.
25. Klukowski M, Nelson CE. 1998. The challenge hypothesis and seasonal changes in aggression and steroids in male northern fence lizards (Sceloporus undulatus hyacinthinus). Hormones and Behavior 33: 197-204.
26. Knapp R, Moore MC. 1996. Male morphs in tree lizards, Urosaurus ornatus, have different delayed hormonal responses to aggressive encounters. Animal Behaviour 52: 1045-1055.
27. Knapp R, Moore MC. 1997. Male morphs in tree lizards have different testosterone responses to elevated levels of corticosterone. General and Comparative Endocrinology 107: 273-279.
28. Knapp R, Hews DK, Thompson CW, Ray LE, Moore MC. 2003. Environmental and endocrine correlates of tactic switching by nonterritorial male tree lizards (Urosaurus ornatus). Hormones and Behavior 43: 83-92.
29. Leache AD. 2009. Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Systematic Biology 58: 547-559.
30. Lima SL. 2009. Predators and the breeding bird: behavioral and reproductive flexibility under the risk of predation. Biological Reviews 84: 485-513.
31. Lima SL, Dill LM. 1990. Behavioral decisions made under the risk of predation - a review and prospectus. Canadian Journal of Zoology-Revue Canadienne De Zoologie 68: 619-640.
32. Lister BC. 1976. Nature of niche expansion in West-Indian Anolis lizards. 1. Ecological consequences of reduced competition. Evolution 30: 659-676.
33. Luke CA. 1989. Color as a phenotypically plastic character in the side-blotched lizard, Uta stansburiana. Ph.D. dissertation. Thesis University of California, Berkeley.
34. McKeever B. 2009. Some notes on the herpetofauna of the White Sands National Monument.
35. McKinney RB, Marion KR. 1985. Plasma androgens and their association with the reproductive-cycle of the male fence lizard, Sceloporus undulatus. Comparative Biochemistry and Physiology a-Physiology 82: 515-519.
36. Martín J, López P. 1999. When to come out from a refuge: risk-sensitive and state-dependent decisions in an alpine lizard. Behavioral Ecology 10: 487-492.
37. Martín J, López P. 2000. Chemoreception, symmetry and mate choice in lizards. Proceedings of the Royal Society of London Series B-Biological Sciences 267: 1265-1269.
38. Mateo JM. 2007. Ecological and hormonal correlates of antipredator behavior in adult Belding's ground squirrels (Spermophilus beldingi). Behavioral Ecology and Sociobiology 62: 37-49.
39. Moore FL, Orchinik M. 1994. Membrane-receptors for corticosterone - a mechanism for rapid behavioral-responses in an amphibian. Hormones and Behavior 28: 512-519.
40. Moore IT, Jessop TS. 2003. Stress, reproduction, and adrenocortical modulation in amphibians and reptiles. Hormones and Behavior 43: 39-47.
41. Moore MC. 1987. Castration affects territorial and sexual-behavior of free-living male lizards, Sceloporus jarrovi. Animal Behaviour 35: 1193-1199.
42. Moore MC, Lindzey JA. 1992. Physiological basis of sexual behavior in male reptiles. In: Gans C, Crews D, eds. Biology of the reptilia; volume 18; physiology E; hormones, brain and behavior. Chicago, IL: University of Chicago Press, 70-113.
43. Moore MC, Thompson CW, Marler CA. 1991. Reciprocal changes in corticosterone and testosterone levels following acute and chronic handling stress in the tree lizard, Urosaurus ornatus. General and Comparative Endocrinology 81: 217-226.
44. Nava SS. 2009. Sex-specific visual performance and receiver divergence in lizard communication. Unpublished Ph.D., Indiana University.
45. Oswald M. 2010. Behavioral evolution in zebrafish, Danio rerio. Unpublished Ph.D., University of Idaho.
46. Robertson JM, Rosenblum EB. 2009. Rapid divergence of social signal coloration across the White Sands ecotone for three lizard species under strong natural selection. Biological Journal of the Linnean Society 98: 243-255.
47. Robertson JM, Rosenblum EB. 2010. Male territoriality and 'sex confusion' in recently adapted lizards at White Sands. Journal of Evolutionary Biology 23: 1928-1936.
48. Romero LM, Wikelski M. 2002. Exposure to tourism reduces stress-induced corticosterone levels in Galapagos marine iguanas. Biological Conservation 108: 371-374.
49. Rosenblum EB. 2006. Convergent evolution and divergent selection: lizards at the White Sands ecotone. American Naturalist 167: 1-15.
50. Rosenblum EB, Harmon LJ. 2010. 'Same same but different': replicated ecological speciation at White Sands. Evolution DOI: 10.1111/j.1558-5646.2010.01190.
51. Rosenblum EB, Rompler H, Schoneberg T, Hoekstra HE. 2010. Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proceedings of the National Academy of Sciences of the United States of America 107: 2113-2117.
52. Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21: 55-89.
53. SAS. 2007. JMP Version 7. Cary, NC: SAS Institute Inc.
54. Schluter D. 2000. The ecology of adaptive radiation. Oxford: Oxford University Press.
55. Smith LC, John-Alder HB. 1999. Seasonal specificity of hormonal, behavioral, and coloration responses to within- and between-sex encounters in male lizards (Sceloporus undulatus). Hormones and Behavior 36: 39-52.
56. Stone PA, Snell HL, Snell HM. 2003. Island biogeography of morphology and social behavior in the lava lizards of the Galapagos Islands. In: Fox SF, McCoy JK, Baird TA, eds. Lizard social behavior. Baltimore, MD: John Hopkins University Press, 172-189.
57. Thaker M, Lima SL, Hews DK. 2009a. Acute corticosterone elevation enhances antipredator behaviors in male tree lizard morphs. Hormones and Behavior 56: 51-57.
58. Thaker M, Lima SL, Hews DK. 2009b. Alternative antipredator tactics in tree lizard morphs: hormonal and behavioural responses to a predator encounter. Animal Behaviour 77: 395-401.
59. Thaker M, Vanak AT, Lima SL, Hews DK. 2010. Stress and aversive learning in a wild vertebrate: the role of corticosterone in mediating escape from a novel stressor. American Naturalist 175: 50-60.
60. Tokarz RR, McMann S, Smith LC, John-Alder H. 2002. Effects of testosterone treatment and season on the frequency of dewlap extensions during male-male interactions in the lizard Anolis sagrei. Hormones and Behavior 41: 70-79.
61. Wada H, Hahn TP, Breuner CW. 2007. Development of stress reactivity in white-crowned sparrow nestlings: total corticosterone response increases with age, while free corticosterone response remains low. General and Comparative Endocrinology 150: 405-413.
62. Wilson BS, Wingfield JC. 1994. Seasonal and interpopulational variation in plasma-levels of corticosterone in the side-blotched lizard (Uta stansburiana). Physiological Zoology 67: 1025-1049.
63. Wilson EO. 1961. The nature of the taxon cycle in the melanesian ant fauna. American Naturalist 95: 169-193.
64. Wingfield JC, Smith JP, Farner DS. 1982. Endocrine responses of white-crowned sparrows to environmental-stress. Condor 84: 399-409.