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Environmental stress shapes life-history variation in the swelled-vented frog (Feirana quadranus)

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Abstract

Understanding how environmental stress modifies life-history traits of vertebrates is highly important for their conservation and management. Amphibians, in particular, have experienced rapid declines in abundance due to their relatively low mobility and strict physiological constraints. Therefore, it is important to understand how amphibians have evolved to cope with environmental stress, and to identify the relevant life-history traits that mediate these dynamics. In this study, we quantified the variation of life-history traits (i.e., body size and age) across the distributional range for a mountain frog species, Feirana quadranus, and identified potential impacts of environmental stress on these traits. Based on the similarity of environmental variables describing bioclimatic and ultraviolet-B radiation conditions from a hierarchical cluster analysis, all populations were assigned to three distinct groups: low, intermediate and high environmental harshness regimes. We found no significant difference in age structure among environmental regimes, with 68% of individuals being between four and six years old. The average age of individuals did not differ among regimes or between sexes, but snout-vent length (SVL) and hind limb length differed significantly among both. When environmental stress was represented along the principle component axes, we found a significant correlation between environmental stress and hind limb length, but not for age or SVL. Our results help us understand potential impacts of environmental stress on life-history variation in F. quadranus covering its whole distribution range. Specifically, our findings highlight the adaptive potential of amphibians to changing environmental conditions via life-history variation as a function of environmental stress.

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References

  • Adams DC, Church JO, Galis F (2008) Amphibians do not follow Bergmann’s rule. Evolution 62:413–420

    Article  PubMed  Google Scholar 

  • Angilletta JMJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  PubMed  Google Scholar 

  • Araújo MB, Rahbek C (2006) How does climate change affect biodiversity? Science 313:1396–1397

    Article  PubMed  Google Scholar 

  • Ashton KG (2002) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Glob Ecol Biogeogr 11:505–523

    Article  Google Scholar 

  • Ashton KG, Tracy MC, Queiroz Ad (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415

    Article  PubMed  Google Scholar 

  • Beattie RC (1987) The reproductive biology of Common frog (Rana temporaria) populations from different altitudes in northern England. J Zool 211:387–398

    Article  Google Scholar 

  • Beckmann M, Václavík T, Manceur AM et al (2014) gluv: a global UV-B radiation data set for macroecological studies. Methods Ecol Evol 5:372–383

    Article  Google Scholar 

  • Beebee TJ (2013) Effects of road mortality and mitigation measures on amphibian populations. Conserv Biol 27:657–668

    Article  PubMed  Google Scholar 

  • Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174

    Article  Google Scholar 

  • Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5:597–608

    Article  Google Scholar 

  • Chen IC, Hill JK, Ohlemüller R et al (2011) Rapid range shifts of species associated with high levels of climate warming. Sci 333:1024–1026

    Article  CAS  Google Scholar 

  • Citadini JM, Brandt R, Williams CR et al (2018) Evolution of morphology and locomotor performance in anurans: relationships with microhabitat diversification. J Evol Biol 31:371–381

    Article  CAS  PubMed  Google Scholar 

  • Eaton BR, Paszkowski CA, Kristensen K et al (2005) Life-history variation among populations of Canadian Toads in Alberta, Canada. Can J Zool 83:1421–1430

    Article  Google Scholar 

  • Elmberg J (1991) Ovarian cyclicity and fecundity in boreal common frogs Rana temporaria L. along a climatic gradient. Funct Ecol 5:340–350

    Article  Google Scholar 

  • Fei L, Hu S, Ye C et al (2009) Fauna Sinica Amphibia, vol 3. Anura Ranidae. Science Press, Beijing

    Google Scholar 

  • Feng X, Chen W, Hu J et al (2015) Variation and sexual dimorphism of body size in the plateau brown frog along an altitudinal gradient. Asian Herpetol Res 6:291–297

    Google Scholar 

  • Ficetola GF, Colleoni E, Renaud J et al (2016) Morphological variation in salamanders and their potential response to climate change. Glob Change Biol 22:2013–2024

    Article  Google Scholar 

  • Green DM (2015) Implications of female body-size variation for the reproductive ecology of an anuran amphibian. Ethol Ecol Evol 27:173–184

    Article  Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Article  Google Scholar 

  • Hjernquist MB, Söderman F, Jönsson KI et al (2012) Seasonality determines patterns of growth and age structure over a geographic gradient in an ectothermic vertebrate. Oecologia 170:641–649

    Article  PubMed  Google Scholar 

  • Hu J, Jiang J (2018) Inferring ecological explanations for biogeographic boundaries of parapatric Asian mountain frogs. BMC Ecol 18:3

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu J, Hu H, Jiang Z (2010) The impacts of climate change on the wintering distribution of an endangered migratory bird. Oecologia 164:555–565

    Article  PubMed  Google Scholar 

  • Hu J, Xie F, Li C et al (2011) Elevational patterns of species richness, range and body size for spiny frogs. PLoS ONE 6:e19817

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu J, Jiang Z, Mallon DP (2013) Metapopulation viability of a globally endangered gazelle on the Northeast Qinghai-Tibetan Plateau. Biol Conserv 166:23–32

    Article  Google Scholar 

  • Hu J, Broennimann O, Guisan A et al (2016) Niche conservatism in Gynandropaa frogs on the southeastern Qinghai-Tibetan Plateau. Sci Rep 6:32624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua F, Hu J, Liu Y et al (2016) Community-wide changes in intertaxonomic temporal co-occurrence resulting from phenological shifts. Glob Change Biol 22:1746–1754

    Article  Google Scholar 

  • Jiang J, Xie F, Zang C et al (2016a) Assessing the threat status of amphibians in China. Biodiver Sci 24:588–597

    Article  Google Scholar 

  • Jiang Z, Jiang J, Wang Y et al (2016b) Red list of China’s vertebrates. Biodiver Sci 24:500–551

    Article  Google Scholar 

  • Klaus SP, Lougheed SC (2013) Changes in breeding phenology of eastern Ontario frogs over four decades. Ecol Evol 3:835–845

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai YC, Lee TH, Kam YC (2005) A skeletochronological study on a subtropical, riparian ranid (Rana swinhoana) from different elevations in Taiwan. Zool Sci 22:653–658

    Article  Google Scholar 

  • Laugen AT, Laurila A, Jönsson KI et al (2005) Do common frogs (Rana temporaria) follow Bermann’s rule? Evol Ecol Res 7:717–731

    Google Scholar 

  • Li P, Zhao W (2004) Nanorana quadranus. The IUCN Red List of Threatened Species 2004: e.T58245A11756909. http://www.iucnredlist.org/. Accessed 31 Jan 2018

  • Liao WB, Lu X (2012) Adult body size = f (initial size + growth rate × age): explaining the proximate cause of Bergman’s cline in a toad along altitudinal gradients. Evol Ecol 26:579–590

    Article  Google Scholar 

  • Liao WB, Lu X, Jehle R (2014) Altitudinal variation in maternal investment and trade-offs between egg size and clutch size in the Andrew’s toad. J Zool 293:84–91

    Article  Google Scholar 

  • Liao WB, Luo Y, Lou SL et al (2016) Geographic variation in life-history traits: growth season affects age structure, egg size and clutch size in Andrew’s toad (Bufo andrewsi). Front Zool 13:6

    Article  PubMed  PubMed Central  Google Scholar 

  • MacNally R, Horrocks GFB, Lada H (2017) Anuran responses to pressures from high-amplitude drought-flood-drought sequences under climate change. Clim Change 141:243–257

    Article  Google Scholar 

  • Miaud C, Guyétant R, Elmberg J (1999) Variations in life-history traits in the common frog Rana temporaria (Amphibia: Anura): a literature review and new data from the French Alps. J Zool 249:61–73

    Article  Google Scholar 

  • Mitchell A, Bergmann PJ (2016) Thermal and moisture habitat preferences do not maximize jumping performance in frogs. Funct Ecol 30:733–742

    Article  Google Scholar 

  • Moritz C, Agudo R (2013) The future of species under climate change: resilience or decline? Science 341:504–508

    Article  CAS  PubMed  Google Scholar 

  • Morrison C, Hero JM (2003) Geographic variation in life-history characteristics of amphibians: a review. J Anim Ecol 72:270–279

    Article  Google Scholar 

  • Muñoz MM, Wegener JE, Algar AC (2014) Untangling intra- and interspecific effects on body size clines reveals divergent processes structuring convergent patterns in Anolis lizards. Am Nat 184:636–646

    Article  PubMed  Google Scholar 

  • Olalla-Tárraga MÁ, Rodríguez MÁ (2007) Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann’s rule, urodeles its converse. Glob Ecol Biogeogr 16:606–617

    Article  Google Scholar 

  • Özdemir N, Altunışık A, Ergül T et al (2012) Variation in body size and age structure among three Turkish populations of the treefrog Hyla arborea. Amphibia-Reptilia 33:25–35

    Article  Google Scholar 

  • Qiao H, Peterson AT, Ji L et al (2017) Using data from related species to overcome spatial sampling bias and associated limitations in ecological niche modelling. Methods Ecol Evol 8:1804–1812

    Article  Google Scholar 

  • Reniers J, Brendonck L, Roberts JD et al (2015) Environmental harshness shapes life-history variation in an Australian temporary pool breeding frog: a skeletochronological approach. Oecologia 178:931–941

    Article  PubMed  Google Scholar 

  • Rodrigues JFM, Olalla-Tárraga MÁ, Iverson JB et al (2018) Temperature is the main correlate of the global biogeography of turtle body size. Glob Ecol Biogeogr 27:429–438

    Article  Google Scholar 

  • Root TL, Price JT, Hall KR et al (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig C, Karoly D, Vicarelli M et al (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353

    Article  CAS  PubMed  Google Scholar 

  • Rozenblut B, Ogielska M (2005) Development and growth of long bones in European water frogs (Amphibia: Anura: Ranidae), with remarks on age determination. J Morphol 265:304–317

    Article  PubMed  Google Scholar 

  • Ruland F, Jeschke JM (2017) Threat-dependent traits of endangered frogs. Biol Conserv 206:310–313

    Article  Google Scholar 

  • Ryan MJ, Keddy-Hector A (1992) Directional patterns of female mate choice and the role of sensory biases. Am Nat 139:S4–S35

    Article  Google Scholar 

  • Tracy CR, Christian KA, Tracy CR (2010) Not just small, wet, and cold: effects of body size and skin resistance on thermoregulation and arboreality of frogs. Ecology 91:1477–1484

    Article  PubMed  Google Scholar 

  • Trenham PC, Bradley Shaffer H, Koenig WD et al (2000) Life history and demographic variation in the California tiger salamander (Ambystoma californiense). Copeia 2000:365–377

    Article  Google Scholar 

  • Tuljapurkar S (1990) Delayed reproduction and fitness in variable environments. Proc Natl Acad Sci USA 87:1139–1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vincze O, Kosztolányi A, Barta Z et al (2017) Parental cooperation in a changing climate: fluctuating environments predict shifts in care division. Glob Ecol Biogeogr 26:347–358

    Article  Google Scholar 

  • Wake DB, Vredenburg VT (2008) Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc Natl Acad Sci USA 105:11466–11473

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang B, Jiang J, Xie F et al (2009) Molecular phylogeny and genetic identification of populations of two species of Feirana frogs (Amphibia: Anura, Ranidae, Dicroglossinae, Paini) endemic to China. Zool Sci 26:500–509

    Article  CAS  Google Scholar 

  • Wang B, Jiang J, Xie F et al (2012) Postglacial colonization of the Qinling Mountains: phylogeography of the swelled vent frog (Feirana quadranus). PLoS ONE 7:e41579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Woodward G, Ebenman B, Emmerson M et al (2005) Body size in ecological networks. Trends Ecol Evol 20:402–409

    Article  PubMed  Google Scholar 

  • Yang X (2011) Speciation and geographic distribution pattern of the genus Feirana. MSc Dissertation, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu

  • Yang S, Jiang J, Luo Z et al (2019) Microhabitat segregation of parapatric frogs in the Qinling Mountains. Asian Herpetol Res. https://doi.org/10.16373/j.cnki.ahr.180078

    Article  Google Scholar 

  • Yu X, Zhong M, Li D et al (2018) Large-brained frogs mature later and live longer. Evolution 72:1174–1183

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported by the National Natural Science Foundation of China (31572290, 31770568, 31270568), National Key Research and Development Plan (2016YFC0503303), Science and Technology Service Network Initiative CAS (KFJ-STS-ZDTP-013), and Youth Innovation Promotion Association CAS (2015304). We thank Huijie Qiao and Yang Liu for their help in data analysis and revision; Bin Wang, Jie Wang, Cheng Li, Shangling Lou, Jianping Yu and Qiang Wu for their help in the data collections. Many thanks to the Herpetological Museum of Chengdu Institute of Biology, Chinese Academy of Sciences for providing access to the specimens. We also thank Dr. Murphy Stephen at the Yale University for his assistance with language and grammatical editing of the manuscript.

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Correspondence to Junhua Hu.

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The collection of specimens for this paper was part of a long-term series of studies of Feirana frogs carried out by the research team (e.g., Wang et al. 2009, 2012; Yang 2011; Yang et al. 2019). All animal handling and processing were in accordance with the Law of the People’s Republic of China on the Protection of Wildlife and approved by the Animal Care Committee of CIB, CAS.

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Wang, X., Huang, Y., Zhong, M. et al. Environmental stress shapes life-history variation in the swelled-vented frog (Feirana quadranus). Evol Ecol 33, 435–448 (2019). https://doi.org/10.1007/s10682-019-09980-5

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