Ecogeographic variation of body size in the spectacled salamanders (Salamandrina): Influence of genetic structure and local factors

Journal of Biogeography

Volumn 37, Issue 12, 2010, Pages 2358-2370

  Romano, Antonio ^a   Ficetola, Gentile Francesco ^b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Amphibians; Bergmann's rule; Body size; Ecogeographical variation; Haplotype; Italy; Local factors; Mitochondrial DNA; Salamandridae; Salamandrina

Indexed keywords

ABANDONED LAND; AMPHIBIAN; BODY SIZE; CRYPSIS; ECTOTHERMY; ENDEMIC SPECIES; GENETIC STRUCTURE; GENETIC VARIATION; MITOCHONDRIAL DNA; SPAWNING;

ITALY;

AMPHIBIA; SALAMANDRIDAE; SALAMANDRINA; SALAMANDRINA PERSPICILLATA; SALAMANDRINA TERDIGITATA; SALAMANDROIDEA;

EID: 78649513720     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2010.02369.x     Document Type: Article

References (87)

1. Adams, D.C. & Church, J.O. (2008) Amphibians do not follow Bergmann's rule. Evolution, 62, 413-420.
2. Adolph, S.C. & Porter, W.P. (1996) Growth, seasonality, and lizard life histories: age and size at maturity. Oikos, 69, 267-278.
3. Angelini, C., Cari, B. & Utzeri, C. (2006) Records of Salamandrina perspicillata (Savi, 1821) in the Colli Albani (Latium, central Italy), with some ecological notes (Urodela, Salamandridae). Acta Herpetologica, 1, 53-60.
4. Angelini, C., Vanni, S. & Vignoli, L. (2007) Salamandrina terdigitata (Bonaterre, 1789), Salamandrina perspicillata (Savi, 1821). Fauna d'Italia, Vol. XLII: Amphibia (ed. by B. Lanza, F. Andreone, M.A. Bologna, C. Corti and E. Razzetti), pp. 228-237. Edizioni Calderini de Il Sole 24 ORE, Editoria Specializzata S.r.l., Bologna.
5. Angelini, C., Antonelli, D. & Utzeri, C. (2008) A multi-year and multi-site population study on the life history of Salamandrina perspicillata (Savi, 1821) (Amphibia, Urodela). Amphibia-Reptilia, 29, 161-170.
6. Angelini, C., Costa, C., Raimondi, S., Menesatti, P. & Utzeri, C. (2010) Image analysis of the ventral colour pattern discriminates between Spectacled salamanders, Salamandrina perspicillata and S. terdigitata (Amphibia, Salamandridae). Amphibia-Reptilia, 31, 273-282.
7. Angilletta, M.J., Jr, Steury, T.D. & Sears, M.W. (2004a) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integrative and Comparative Biology, 44, 498-509.
8. Angilletta, M.J., Jr, Niewiarowski, P.H., Dunham, A.E., Leache, A.D. & Porter, W.P. (2004b) Bergmann's clines in ectotherms: illustrating a life-history perspective with sceloporine lizards. The American Naturalist, 164, E168-E183.
9. Ashton, K.G. (2001) Body size variation among mainland populations of the western rattlesnake (Crotalus viridis). Evolution, 55, 2523-2533.
10. Ashton, K.G. (2002a) Do amphibians follow Bergmann's rule? Canadian Journal of Zoology, 80, 708-716.
11. Ashton, K.G. (2002b) Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule. Global Ecology and Biogeography, 11, 505-523.
12. Ashton, K.G. & Feldman, C.R. (2003) Bergmann's rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution, 57, 1151-1163.
13. Beale, C.M., Lennon, J.J., Yearsley, J.M., Brewer, M.J. & Elston, D.A. (2010) Regression analysis of spatial data. Ecology Letters, 13, 246-264.
14. Bergmann, C. (1847) Über die verhältnisse der warmeökonomie der thiere zuihrer grosse. Göttinger Studien, 1, 595-708.
15. Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution, 22, 148-155.
16. Blackburn, T.M., Gaston, K.J. & Natasha, L. (1999) Geographic gradients in body size: a clarification of Bergmann's rule. Diversity and Distributions, 5, 165-174.
17. Blanckenhorn, W.U., Stillwell, R.C., Young, K.A., Fox, C.W. & Ashton, K.G. (2006) When Rensch meets Bergmann: does sexual size dimorphism change systematically with latitude? Evolution, 60, 2004-2011.
18. Bovero, S., Angelini, C. & Utzeri, C. (2006) Aging Salamandrina perpsicillata (Savi, 1821) by skeletrochronology. Acta Herpetologica, 1, 153-158.
19. Brattstrom, B.H. (1963) A preliminary review of the thermal requirements of amphibians. Ecology, 44, 238-255.
20. Bruce, R.C., Jaeger, R.G. & Houck, L.D. (2000) The biology of plethodontid salamanders. Kluwer Academic/Plenum Publishers, New York.
21. Burnham, K.P. & Anderson, D.R. (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Verlag, New York.
22. Butler, M.A. & King, A.A. (2004) Phylogenetic comparative analysis: a modelling approach for adaptive evolution. The American Naturalist, 164, 683-695.
23. Caetano, M.H. & Leclair, R., Jr (1996) Growth and population structure of red-spotted newts (Notophthalmus viridescens) in permanent lakes of the Laurentian Shield, Quebec. Copeia, 1996, 866-874.
24. Calder, W.A. (1984) Size, function and life history. Harvard University Press, Cambridge, MA.
25. Canestrelli, D., Zangari, F. & Nascetti, G. (2006) Genetic evidence for two distinct species within the Italian endemic Salamandrina terdigitata (Bonnaterre, 1789) (Amphibia: Urodela: Salamandridae). Herpetological Journal, 16, 221-227.
26. Cogalniceanu, D. & Miaud, C. (2003) Population age structure and growth in four syntopic amphibian species inhabiting a large river floodplain. Canadian Journal of Zoology, 81, 1096-1106.
27. Cooper, N., Bielby, J., Thomas, G.H. & Purvis, A. (2008) Macroecology and extinction risk correlates of frogs. Global Ecology and Biogeography, 17, 211-221.
28. Cushman, S.A. & McGarigal, K. (2002) Hierarchical, multi-scale decomposition of species-environment relationships. Landscape Ecology, 17, 637-646.
29. Cvetković, D., Tomašević, N., Ficetola, G.F., Crnobrnja-Isailović, J. & Miaud, C. (2009) Bergmann's rule in amphibians: combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo. Journal of Zoological Systematics and Evolutionary Research, 47, 171-180.
30. Dall'Alpi, A. & Sazzini, M. (2007) Status e conservazione di due popolazioni di Salamandrina perspicillata (Amphibia: Urodela: Salamandridae) nella provincia di Bologna. Atti del VI congresso nazionale Societas Hereptologica Italica (ed. by M.A. Bologna, M. Capula, G.M. Carpaneto, L. Luiselli, C. Marangoni and A. Venchi), pp. 13-20. Edizioni Belvedere, Latina.
31. Denoël, M., Ficetola, G.F., Cirovic, R., Radovic, D., Džukic, G., Kalezic, M.L. & Vukov, T.D. (2009) A multi-scale approach to facultative paedomorphosis of European newts (Salamandridae) in the Montenegrin karst: distribution pattern, environmental variables, and conservation. Biological Conservation, 142, 509-517.
32. Dubois, A., Crombie, R.I. & Glaw, F. (2005) Recent amphibians: generic and infrageneric taxonomic additions (1981-2002). Alytes, 23, 25-69.
33. Elmer, K.R., Davila, J.A. & Lougheed, S.C. (2007) Cryptic diversity and deep divergence in an upper Amazonian frog, Eleutherodactylus ockendeni. BMC Evolutionary Biology, 7, 247.
34. Ficetola, G.F., Thuiller, W. & Miaud, C. (2007) Prediction and validation of the potential global distribution of a problematic alien invasive species - the American bullfrog. Diversity and Distributions, 13, 476-485.
35. Ficetola, G.F., Scali, S., Denoël, M., Montinaro, G., Tanja, D., Vukov, T.D., Zuffi, M.A.L. & Padoa-Schioppa, E. (2010) Ecogeographical variation of body size in the newt Triturus carnifex: comparing the hypotheses using an information-theoretic approach. Global Ecology and Biogeography, 19, 485-495.
36. Gaston, K.J., Chown, S.L. & Evans, K.L. (2008) Ecogeographical rules: elements of a synthesis. Journal of Biogeography, 35, 483-500.
37. Hauswaldt, J.S., Angelini, C., Utzeri, C. & Steinfartz, S. (2008) Phylogeography and fine-scale population structure of the Spectacled Salamander (Salamandrina perspicillata and S. terdigitata). Herpetologia Sardiniae (ed. by C. Corti), pp. 291-294. Edizioni Belvedere, Latina, Italy.
38. Heyer, W.R., Donelly, M.A., McDiamid, R.W., Hayek, L.A.C. & Foster, M.S. (1994) Measuring and monitoring biological diversity. Standard methods for amphibians. Smithsonian Institution Press, Washington, DC.
39. Highton, R. (2000) Detecting cryptic species using allozyme data. The biology of plethodontid salamanders (ed. by R.C. Bruce, R.G. Jaeger and L.D. Houck), pp. 215-241. Kluwer Academic/Plenum Publishers, New York.
40. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G. & Jarvis, A. (2005) High resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
41. Hutchinson, V.H. & Dupré, R.K. (1992) Thermoregulation. Environmental physiology of the amphibians (ed. by M.E. Feeder and W.W. Burggren), pp. 206-249. University of Chicago Press, Chicago, IL.
42. IUCN (2001) IUCN Red List categories and criteria: Version 3.1. IUCN Species Survival Commission. IUCN, Gland, Switzerland/Cambridge, UK.
43. James, F.C. (1970) Geographic size variation in birds and its relationship to climate. Ecology, 51, 365-390.
44. Kissling, W.D. & Carl, G. (2008) Spatial autocorrelation and the selection of simultaneous autoregressive models. Global Ecology and Biogeography, 17, 59-71.
45. Lanza, B. (1983) Anfibi, rettili (Amphibia, Reptilia). AQ/1/205. Collana del Progetto Finalizzato 'Promozione della Qualità dell' Ambiente'. Guide per il riconoscimento delle specie animali delle acque interne italiane, 27. Consiglio Nazionale delle Ricerche, Rome.
46. Lindsey, C.C. (1966) Body sizes of poikilotherm vertebrates at different latitudes. Evolution, 20, 456-465.
47. Litzgus, J.D., DuRant, S.E. & Mousseau, T.A. (2004) Clinal variation in body and cell size in a widely distributed vertebrate ectotherm. Oecologia, 140, 551-558.
48. Maletzky, A., Mikulíĉek, P., Franzen, M., Goldschmid, A., Gruber, H.-J., Horák, A. & Kyek, M. (2008) Hybridization and introgression between two species of crested newts (Triturus cristatus and T. carnifex) along contact zones in Germany and Austria: morphological and molecular data. Herpetological Journal, 18, 1-15.
49. Mattoccia, M., Romano, A. & Sbordoni, V. (2005) Mitochondrial DNA sequence analysis of the spectacled salamander, Salamandrina terdigitata (Urodela: Salamandridae), supports the existence of two distinct species. Zootaxa, 995, 1-19.
50. Mayr, E. (1942) Systematics and the origin of species. Columbia University Press, New York.
51. Mayr, E. (1956) Geographical character gradients and climatic adaptation. Evolution, 10, 105-108.
52. Measey, G.J. & Van Dongen, S. (2006) Bergmann's rule and the terrestrial caecilian Schistometopum thomense (Amphibia: Gymnophiona: Caeciliidae). Evolutionary Ecology Research, 8, 1049-1059.
53. Meiri, S., Yom-Tov, Y. & Geffen, E. (2007) What determines conformity to Bergmann's rule? Global Ecology and Biogeography, 16, 788-794.
54. Millien, V., Lyons, S.K., Olson, L., Smith, F.A., Wilson, A.B. & Yom-Tov, Y. (2006) Ecotypic variation in the context of global climate change: revisiting the rules. Ecology Letters, 9, 853-869.
55. Nascetti, G., Zangari, F. & Canestrelli, D. (2005) The spectacled salamanders, Salamandrina terdigitata (Lacépède, 1788) and S. perspicillata (Savi, 1821): genetic differentiation and evolutionary history. Rendiconti Lincei, 16, 159-169.
56. Ogielska, M., Kazana, K., Palczynsky, M. & Tomaszewska, A. (1999) An influence of the great flood 1997 on amphibian and reptilian populations in the Odra River valley near Wroclaw (Lower Silesia, Poland). Current studies in herpetology (ed. by C. Miaud and R. Guyetant), pp. 345-349. SEH, Le Bourget du Lac, France.
57. Olalla-Tárraga, M.A. & Rodríguez, M.A. (2007) Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann's rule, urodeles its converse. Global Ecology and Biogeography, 16, 606-617.
58. Olalla-Tárraga, M.A., Rodríguez, M.A. & Hawkins, B.A. (2006) Broad-scale patterns of body size in squamate reptiles of Europe and North America. Journal of Biogeography, 33, 781-793.
59. Olson, V.A., Davies, R.G., Orme, C.D.L., Thomas, G.H., Meiri, S., Blackburn, T.M., Gaston, K.J., Owens, I.P.F. & Bennett, P.M. (2009) Global biogeography and ecology of body size in birds. Ecology Letters, 12, 249-259.
60. Pfenninger, M. & Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology, 7, 121.
61. Pincheira-Donoso, D., Hodgson, D.J. & Tregenza, T. (2008) The evolution of body size under environmental gradients in ectotherms: why should Bergmann's rule apply to lizards? BMC Evolutionary Biology, 8, 68.
62. De Queiroz, A. & Ashton, K.G. (2004) The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann's rule in tetrapods. Evolution, 58, 1674-1684.
63. R Development Core Team (2007) R: A language and environment for statistical computing, reference index version 2.5.1. R Foundation for Statistical Computing, Vienna, Austria. Available at.
64. Raffalovich, L.E., Deane, G.D., Armstrong, D. & Tsao, H.S. (2008) Model selection procedures in social research: Monte-Carlo simulation results. Journal of Applied Statistics, 35, 1093-1114.
65. Rangel, T.F.L.V.B., Diniz-Filho, J.A.F. & Bini, L.M. (2010) SAM: a comprehensive application for Spatial Analysis in Macroecology. Ecography, 33, 46-50.
66. Ray, C. (1960) The application of Bergmann's rule and Allen's rule to the poikilotherms. Journal of Morphology, 106, 85-109.
67. Rensch, B. (1938) Some problems of geographical variation and species-formation. Proceedings of the Linnean Society, 150, 275-285.
68. Richards, S.A. (2005) Testing ecological theory using the information-theoretic approach: examples and cautionary results. Ecology, 86, 2805-2814.
69. Richards, S.A. (2008) Dealing with overdispersed count data in applied ecology. Journal of Applied Ecology, 45, 218-227.
70. Romano, A. (2007) Genetic characterisation of the Italian endemic genus Salamandrina (Fitzinger, 1826) (Amphibia: Salamandridae). PhD Thesis, University of Tor Vergata, Rome, Italy.
71. Romano, A. & Mattoccia, M. (2005) Maximum size of the spectacled salamander, Salamandrina perspicillata (Savi, 1821) (Urodela; Salamandridae). Herpetozoa, 18, 186-187.
72. Romano, A., Mattoccia, M., Marta, S., Bogaerts, S., Pasmans, F. & Sbordoni, V. (2009a) Distribution and morphological characterisation of the endemic Italian salamanders Salamandrina perspicillata (Savi, 1821) and S. terdigitata (Bonnaterre, 1789) (Caudata: Salamandridae). Italian Journal of Zoology, 76, 422-432.
73. Romano, A., Bruni, G. & Paoletti, C. (2009b) Sexual dimorphism in the Italian endemic species Salamandrina perspicillata (Savi, 1821) and testing of a field method for sexing salamanders. Amphibia-Reptilia, 30, 425-434.
74. Sáez, A.G. & Lozano, E. (2005) Body doubles. Nature, 433, 111.
75. Spilinga, C., Chierchia, S. & Ragni, B. (2006) Caratterizzazione biometrica di una popolazione di salamandrina dagli occhiali dell'Umbria centro-occidentale. Atti del V congresso nazionale Societas Hereptologica Italica (ed. by M. Zuffi), pp. 245-250. Firenze University Press, Firenze.
76. Tucker, J.K., Paukstis, G.L. & Theiling, C.H. (2001) Anuran response to catastrophic flooding. Herpetological Natural History, 8, 83-86.
77. Utzeri, C., Antonelli, D. & Angelini, C. (2004) A note on terrestrial activity and feeding in the spectacled salamander, Salamandrina terdigitata (Urodela, Salamandridae). Herpetological Bulletin, 90, 27-31.
78. Vences, M. & Köhler, J. (2006) The current status of genetic exploration in amphibians: taxonomic and geographical disparities. Herpetologia Bonnensis II (ed. by M. Vences, J. Köhler, T. Ziegler and W. Böhme), pp. 193-195. Societas Europaea Herpetologica, Bonn.
79. Vieites, D.R., Wollenberg, K.C., Andreone, F., Köhler, J., Glaw, F. & Vences, M. (2009) Vast underestimation of Madagascar's biodiversity evidenced by an integrative amphibian inventory. Proceedings of the National Academy of Sciences USA, 106, 8267-8272.
80. Wake, D.B., Maxson, L.R. & Wurst, G.Z. (1978) Genetic differentiation, albumin evolution, and their biogeographic implications in plethodontid salamanders of California and southern Europe. Evolution, 32, 529-539.
81. Watt, C., Mitchell, S. & Salewski, V. (2010) Bergmann's rule; a concept cluster? Oikos, 119, 89-100.
82. Wheeler, C.A. & Welsh, H.H., Jr (2008) Mating strategy and breeding patterns of the foothill yellow-legged frog (Rana boylii). Herpetological Conservation and Biology, 3, 128-142.
83. Wilson, A.B. (2009) Fecundity selection predicts Bergmann's rule in syngnathid fishes. Molecular Ecology, 18, 1263-1272.
84. Winker, K. (2009) Reuniting phenotype and genotype in biodiversity research. BioScience, 59, 657-665.
85. Yom-Tov, Y. & Geffen, E. (2006) Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia, 148, 213-218.
86. Zuffi, M.A.L. (1999) Salamandrina terdigitata (Lacépède, 1788) - Brillensalamander. Handbuch der Reptilien und Amphibien Europas (ed. by K. Grossenbacher and B. Thiesmeir), pp. 229-246. Aula-Verlag, Wiebelsheim, Germany.
87. Zug, G.R., Vitt, L.J. & Caldwell, J.P. (2001) Herpetology. An introductory biology of amphibians and reptiles, 2nd edn. Academic Press, San Diego.