Geographic body size variation in ectotherms: effects of seasonality on an anuran from the southern temperate forest

Frontiers in Zoology

Claudio Soto-Azat²  Andrew A. Cunningham³  Andrés Valenzuela-Sánchez¹ 

[1] ONG Ranita de Darwin, Nataniel Cox 152, Santiago, Chile;Centro de Investigación para la Sustentabilidad, Facultad de Ecología y Recursos Naturales, Universidad Andres Bello, República 440, Santiago, Chile;Institute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom

关键词: Starvation resistance;    Scaled mass index;    Rhinoderma darwinii;    Metabolic depression;    Hibernation hypothesis;   

Others  :  1235060
DOI  :  10.1186/s12983-015-0132-y

 received in 2015-10-29, accepted in 2015-12-18,  发布年份 2015

【 摘 要 】

Background

Body size variation has played a central role in biogeographical research, however, most studies have aimed to describe trends rather than search for underlying mechanisms. In order to provide a more comprehensive understanding of the causes of intra-specific body size variation in ectotherms, we evaluated eight hypotheses proposed in the literature to account for geographical body size variation using the Darwin’s frog (Rhinoderma darwinii), an anuran species widely distributed in the temperate forests of South America. Each of the evaluated hypotheses predicted a specific relationship between body size and environmental variables. The level of support for each of these hypotheses was assessed using an information-theoretic approach and based on data from 1015 adult frogs obtained from 14 sites across the entire distributional range of the species.

Results

There was strong evidence favouring a single model comprising temperature seasonality as the predictor variable. Larger body sizes were found in areas of greater seasonality, giving support to the “starvation resistance” hypothesis. Considering the known role of temperature on ectothermic metabolism, however, we formulated a new, non-exclusive hypothesis, termed “hibernation hypothesis”: greater seasonality is expected to drive larger body size, since metabolic rate is reduced further and longer during colder, longer winters, leading to decreased energy depletion during hibernation, improved survival and increased longevity (and hence growth). Supporting this, a higher post-hibernation body condition in animals from areas of greater seasonality was found.

Conclusions

Despite largely recognized effects of temperature on metabolic rate in ectotherms, its importance in determining body size in a gradient of seasonality has been largely overlooked so far. Based on our results, we present and discuss an alternative mechanism, the “hibernation hypothesis”, underlying geographical body size variation, which can be helpful to improve our understanding of biogeographical patterns in ectotherms.

【 授权许可】

   
2015 Valenzuela-Sánchez et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

【 参考文献 】

• [1]Watts C, Mitchell S, Salewski V. Bergmann’ s rule; a concept cluster? Oikos. 2010; 119:89-100.
• [2]Blackburn TM, Gaston KJ, Loder N. Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib. 1999; 5:165-174.
• [3]Ashton KG. Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Global Ecol Biogeogr. 2002; 11:505-523.
• [4]Ashton KG. Do amphibians follow Bergmann’s rule? Can J Zoolog. 2002; 80:708-716.
• [5]Ashton KG, Feldmann CR. Bergmann’s rule in nonavian reptiles: turtles follow it, lizards and snakes reverse it. Evolution. 2003; 57:1151-1163.
• [6]Pincheira-Donoso D, Hodgson DJ, Tregenza T. The evolution of body size under environmental gradients in ectotherms: why should Bergmann’s rule apply to lizards? BMC Evol Biol. 2008; 8:68. BioMed Central Full Text
• [7]Ashton KG. Body size variation among mainland populations of the Western Rattlesnake (Crotalus viridis). Evolution. 2001; 55:2523-2533.
• [8]Blanckenhorn WU, Demont M. Bergmann and converse Bergmann latitudinal clines in arthropods: two ends of a continuum? Integr Comp Biol. 2004; 44:413-424.
• [9]Ficetola GF, Scali S, Denoël M, Montinaro G, Vukov TD, Zuffi MAL et al.. Ecogeographical variation of body size in the newt Triturus carnifex: comparing the hypotheses using an information-theoretic approach. Global Ecol Biogeogr. 2010; 19:485-495.
• [10]Bidau CD, Martí DA. Dichroplus vittatus (Orthoptera: Acrididae) follows the converse to Bergmann’s rule although male morphological variability increases with latitude. B Entomol Res. 2007; 97:69-79.
• [11]Cvetkovic D, Tomaševic N, Ficetola GF, Crnobrnja-Isailovic J, Miaud C. Bergmann’s rule in amphibians: combining demographic and ecological parameters to explain body size variation among populations in the common toad Bufo bufo. J Zool Syst Evol Res. 2009; 47:171-180.
• [12]Lindsey CC. Body sizes of poikilotherm vertebrates at different latitudes. Evolution. 1996; 20:283-291.
• [13]Cushman JH, Lawton JH, Manly BFJ. Latitudinal patterns in European ant assemblages: variation in species richness and body size. Oecologia. 1993; 95:30-37.
• [14]Arnett AE, Gotelli NJ. Bergmann’s rule in larval ant lions: testing the starvation resistance hypothesis. Ecol Entomol. 2003; 28:645-650.
• [15]Olalla-Tárraga MÁ, Rodríguez MÁ, Hawkins BA. Broad-scale patterns of body size in squamate reptiles of Europe and North America. J Biogeogr. 2006; 33:781-793.
• [16]Olalla-Tárraga MÁ, Rodríguez MÁ. Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann’s rule, urodeles its converse. Global Ecol Biogeogr. 2007; 16:606-617.
• [17]Atkinson D. Temperature and organism size — a biological law for ectotherms? Adv Ecol Res. 1994; 25:1-58.
• [18]Newman RA, Dunham AE. Size at metamorphosis and water loss in a desert anuran (Scaphiopus couchii). Copeia. 1994; 1994:372-381.
• [19]Donnelly MA, Crump ML. Potential effects of climate change on two neotropical amphibian assemblages. Clim Chang. 1998; 39:541-561.
• [20]Soto-Azat C, Valenzuela-Sánchez A, Collen B, Rowcliffe MC, Veloso A, Cunningham AA. The population decline and extinction of Darwin’s frogs. PLoS ONE. 2013; 8: Article ID e66957
• [21]Valenzuela-Sánchez A, Harding G, Cunningham AA, Chirgwin C, Soto-Azat C. Home range and social analyses in a mouth brooding frog: testing the coexistence of paternal care and male territoriality. J Zool. 2014; 294:215-223.
• [22]Jorquera B, Pugin E, Garrido O, Goicoechea O, Formas R. Procedimiento de desarrollo en dos especies del género Rhinoderma. Medio Ambiente. 1981; 5:58-71.
• [23]Burnham KP, Anderson DR. Model selection and multimodel inference. 2nd ed. Springer, New York; 2002.
• [24]Lukacs PM, Thompson WL, Kendall WL, Gould WR, Doherty PF, Burnham KP. Concerns regarding a call for pluralism of information theory and hypothesis testing. J Appl Ecol. 2007; 44:456-460.
• [25]Crump ML. Natural history of Darwin’s, Rhinoderma darwinii. Herpetol Nat Hist. 2002; 9:21-30.
• [26]Bourke JE. Darwin’s frogs: Ecology and conservation in Chile (Anura: Rhinodermatidae), Population characteristics and microhabitat use in Rhinoderma darwinii. PhD Thesis. Germany: University of Bonn; 2012.
• [27]Peig J, Green AJ. New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos. 2009; 118:1883-1891.
• [28]Peig J, Green AJ. The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Funct Ecol. 2010; 24:1323-1332.
• [29]MacCracken JG, Stebbings JL. Test of a body condition index with amphibians. J Herpetol. 2012; 46:346-350.
• [30]Lleonart J, Salat J, Torres GJ. Removing allometric effects of body size in morphological analysis. J Theor Biol. 2000; 205:85-93.
• [31]Pliscoff P, Luebert F, Hilger HH, Guisan A. Effects of alternative sets of climatic predictors on species distribution models and associated estimates of extinction risk: A test with plantsin an arid environment. Ecol Model. 2014; 288:166-177.
• [32]Pettorelli N, Vik JO, Mysterud A, Gaillard J, Tucker CJ, Stenseth NC. Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol Evol. 2005; 20:503-510.
• [33]Sugiura N. Further analysis of the data by Akaike’s information criterion and the finite corrections. Commun Stat Theory. 1978; A7:13-26.
• [34]Chevan A, Sutherland M. Hierarchical Partitioning. Am Stat. 1991; 45:90-96.
• [35]Graham MH. Confronting multicollinearity in ecological multiple regression. Ecology. 2003; 84:2809-2815.
• [36]Mac Nally R, Walsh CP. Hierarchical partitioning public-domain software. Biodivers Conserv. 2004; 13:659-660.
• [37]Rangel TF, Diniz-Filho JAF, Bini LM. SAM: a comprehensive application for spatial analysis in macroecology. Ecography. 2010; 33:46-50.
• [38]Reim C. Size-dependent effects of temperature and food stress on energy reserves and starvation resistance in yellow dung flies. Evol Ecol Res. 2006; 8:1215-1234.
• [39]Blanckenhorn WU, Fanti J, Reim C. Size-dependent energy reserves, energy utilization and longevity in the yellow dung fly. Physiol Entomol. 2007; 32:372-381.
• [40]Wikelski M, Carrillo V, Trillmich F. Energy limits to body size in a grazing reptile, the Galapagos marine iguana. Ecology. 1997; 78:2204-2217.
• [41]Schultz ET, Conover DO. The allometry of energy reserve depletion: test of a mechanism for size-dependent winter mortality. Oecologia. 1999; 119:474-483.
• [42]Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL. Effects of size and temperature on metabolic rate. Science. 2001; 294:1463.
• [43]Brown JH, Gillooly JF, Allen AP, Savage VM, West GB. Toward a metabolic theory of ecology. Ecology. 2004; 85:1771-1789.
• [44]Hillman SS, Withers PC, Drewes RC, Hillyard SD. Ecological and environmental physiology of amphibians. Oxford Univ Press, New York; 2009.
• [45]White CR. The scaling and temperature dependence of vertebrate metabolism. Biol letters. 2006; 2:125-127.
• [46]Busse K. Biología de la reproducción del Sapito de Darwin (Rhinoderma darwinii) y su cría en cautividad. In: Cría en Cautividad de Fauna Chilena. Iriarte A, Tala C, González B, Zapata B, González G, Maino M, editors. Servicio Agrícola y Ganadero, Santiago de Chile; 2004: p.139-146.
• [47]Hjernquist MB, Söderman F, Jönsson KI, Herczeg G, Laurila A, Merilä J. Seasonality determines patterns of growth and age structure over a geographic gradient in an ectothermic vertebrate. Oecologia. 2012; 170:641-649.
• [48]Pullin AS, Bale JS. Effects of low temperature on diapausing Aglais urticae and Inachis io (Lepidoptera: Nymphalidae): Cold hardiness and overwintering survival. J Insect Physiol. 1989; 35:277-281.
• [49]Irwin JT, Lee RE. Mild winter temperatures reduce survival and potential fecundity of the goldenrod gall fly, Eurosta solidaginis (Diptera: Tephritidae). J Insect Physiol. 2000; 46:655-661.
• [50]Reading CJ. Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia. 2007; 151:125-131.
• [51]Liao W, Lu X. Adult body size = f (initial size + growth rate x age): explaining the proximate cause of Bergman’s cline in a toad along altitudinal gradients. Evol Ecol. 2012; 26:579-590.
• [52]Jørgensen CB. External and internal control of patterns of feeding, growth and gonadal function in a temperate zone anuran, the toad Bufo bufo. J Zool. 1986; 210:211-241.
• [53]Jönsson KI, Herczeg G, O’Hara RB, Söderman F, ter Schure AFH, Larsson P et al.. Sexual patterns of prebreeding energy reserves in the common frog Rana temporaria along a latitudinal gradient. Ecography. 2009; 32:831-839.
• [54]Culler LE, McPeek MA, Ayres MP. Predation risk shapes thermal physiology of a predaceous damselfly. Oecologia. 2014; 176:653-660.
• [55]Tejedo M, Marangoni F, Pertoldi C, Richter-Boix A, Laurila A, Orizaola G et al.. Contrasting effects of environmental factors during larval stage on morphological plasticity in post-metamorphic frogs. Clim Res. 2010; 43:31-39.
• [56]Clarke A. Is there a universal temperature dependence of metabolism? Funct Ecol. 2004; 18:252-256.