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

  • Xiaoyi Wang
  • Yan Huang
  • Maojun Zhong
  • Shengnan Yang
  • Xin Yang
  • Jianping Jiang
  • Junhua HuEmail author
Original Paper

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.

Keywords

Adaptive potential Environmental stress Life-history traits Qinling-Daba Mountains Skeletochronology 

Notes

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.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Human and animal rights

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.

Supplementary material

10682_2019_9980_MOESM1_ESM.docx (475 kb)
Supplementary material 1 (DOCX 475 kb)

References

  1. Adams DC, Church JO, Galis F (2008) Amphibians do not follow Bergmann’s rule. Evolution 62:413–420CrossRefPubMedGoogle Scholar
  2. 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 44:498–509CrossRefPubMedGoogle Scholar
  3. Araújo MB, Rahbek C (2006) How does climate change affect biodiversity? Science 313:1396–1397CrossRefPubMedGoogle Scholar
  4. Ashton KG (2002) Patterns of within-species body size variation of birds: strong evidence for Bergmann’s rule. Glob Ecol Biogeogr 11:505–523CrossRefGoogle Scholar
  5. Ashton KG, Tracy MC, Queiroz Ad (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415PubMedGoogle Scholar
  6. Beattie RC (1987) The reproductive biology of Common frog (Rana temporaria) populations from different altitudes in northern England. J Zool 211:387–398CrossRefGoogle Scholar
  7. Beckmann M, Václavík T, Manceur AM et al (2014) gluv: a global UV-B radiation data set for macroecological studies. Methods Ecol Evol 5:372–383CrossRefGoogle Scholar
  8. Beebee TJ (2013) Effects of road mortality and mitigation measures on amphibian populations. Conserv Biol 27:657–668CrossRefPubMedGoogle Scholar
  9. Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Divers Distrib 5:165–174CrossRefGoogle Scholar
  10. Blaustein AR, Kiesecker JM (2002) Complexity in conservation: lessons from the global decline of amphibian populations. Ecol Lett 5:597–608CrossRefGoogle Scholar
  11. Chen IC, Hill JK, Ohlemüller R et al (2011) Rapid range shifts of species associated with high levels of climate warming. Sci 333:1024–1026CrossRefGoogle Scholar
  12. Citadini JM, Brandt R, Williams CR et al (2018) Evolution of morphology and locomotor performance in anurans: relationships with microhabitat diversification. J Evol Biol 31:371–381CrossRefPubMedGoogle Scholar
  13. Eaton BR, Paszkowski CA, Kristensen K et al (2005) Life-history variation among populations of Canadian Toads in Alberta, Canada. Can J Zool 83:1421–1430CrossRefGoogle Scholar
  14. Elmberg J (1991) Ovarian cyclicity and fecundity in boreal common frogs Rana temporaria L. along a climatic gradient. Funct Ecol 5:340–350CrossRefGoogle Scholar
  15. Fei L, Hu S, Ye C et al (2009) Fauna Sinica Amphibia, vol 3. Anura Ranidae. Science Press, BeijingGoogle Scholar
  16. 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 6:291–297Google Scholar
  17. Ficetola GF, Colleoni E, Renaud J et al (2016) Morphological variation in salamanders and their potential response to climate change. Glob Change Biol 22:2013–2024CrossRefGoogle Scholar
  18. Green DM (2015) Implications of female body-size variation for the reproductive ecology of an anuran amphibian. Ethol Ecol Evol 27:173–184CrossRefGoogle Scholar
  19. Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  20. 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 170:641–649CrossRefPubMedGoogle Scholar
  21. Hu J, Jiang J (2018) Inferring ecological explanations for biogeographic boundaries of parapatric Asian mountain frogs. BMC Ecol 18:3CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hu J, Hu H, Jiang Z (2010) The impacts of climate change on the wintering distribution of an endangered migratory bird. Oecologia 164:555–565CrossRefPubMedGoogle Scholar
  23. Hu J, Xie F, Li C et al (2011) Elevational patterns of species richness, range and body size for spiny frogs. PLoS ONE 6:e19817CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hu J, Jiang Z, Mallon DP (2013) Metapopulation viability of a globally endangered gazelle on the Northeast Qinghai-Tibetan Plateau. Biol Conserv 166:23–32CrossRefGoogle Scholar
  25. Hu J, Broennimann O, Guisan A et al (2016) Niche conservatism in Gynandropaa frogs on the southeastern Qinghai-Tibetan Plateau. Sci Rep 6:32624CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hua F, Hu J, Liu Y et al (2016) Community-wide changes in intertaxonomic temporal co-occurrence resulting from phenological shifts. Glob Change Biol 22:1746–1754CrossRefGoogle Scholar
  27. Jiang J, Xie F, Zang C et al (2016a) Assessing the threat status of amphibians in China. Biodiver Sci 24:588–597CrossRefGoogle Scholar
  28. Jiang Z, Jiang J, Wang Y et al (2016b) Red list of China’s vertebrates. Biodiver Sci 24:500–551CrossRefGoogle Scholar
  29. Klaus SP, Lougheed SC (2013) Changes in breeding phenology of eastern Ontario frogs over four decades. Ecol Evol 3:835–845CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lai YC, Lee TH, Kam YC (2005) A skeletochronological study on a subtropical, riparian ranid (Rana swinhoana) from different elevations in Taiwan. Zool Sci 22:653–658CrossRefPubMedGoogle Scholar
  31. Laugen AT, Laurila A, Jönsson KI et al (2005) Do common frogs (Rana temporaria) follow Bermann’s rule? Evol Ecol Res 7:717–731Google Scholar
  32. 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
  33. 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 26:579–590CrossRefGoogle Scholar
  34. 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 293:84–91CrossRefGoogle Scholar
  35. 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 13:6CrossRefPubMedPubMedCentralGoogle Scholar
  36. MacNally R, Horrocks GFB, Lada H (2017) Anuran responses to pressures from high-amplitude drought-flood-drought sequences under climate change. Clim Change 141:243–257CrossRefGoogle Scholar
  37. 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 249:61–73CrossRefGoogle Scholar
  38. Mitchell A, Bergmann PJ (2016) Thermal and moisture habitat preferences do not maximize jumping performance in frogs. Funct Ecol 30:733–742CrossRefGoogle Scholar
  39. Moritz C, Agudo R (2013) The future of species under climate change: resilience or decline? Science 341:504–508CrossRefPubMedGoogle Scholar
  40. Morrison C, Hero JM (2003) Geographic variation in life-history characteristics of amphibians: a review. J Anim Ecol 72:270–279CrossRefGoogle Scholar
  41. 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 184:636–646CrossRefPubMedGoogle Scholar
  42. 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 16:606–617CrossRefGoogle Scholar
  43. 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 33:25–35CrossRefGoogle Scholar
  44. 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 8:1804–1812CrossRefGoogle Scholar
  45. 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 178:931–941CrossRefPubMedGoogle Scholar
  46. 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 27:429–438CrossRefGoogle Scholar
  47. Root TL, Price JT, Hall KR et al (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57CrossRefPubMedGoogle Scholar
  48. Rosenzweig C, Karoly D, Vicarelli M et al (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453:353CrossRefPubMedGoogle Scholar
  49. 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 265:304–317CrossRefPubMedGoogle Scholar
  50. Ruland F, Jeschke JM (2017) Threat-dependent traits of endangered frogs. Biol Conserv 206:310–313CrossRefGoogle Scholar
  51. Ryan MJ, Keddy-Hector A (1992) Directional patterns of female mate choice and the role of sensory biases. Am Nat 139:S4–S35CrossRefGoogle Scholar
  52. 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 91:1477–1484CrossRefPubMedGoogle Scholar
  53. Trenham PC, Bradley Shaffer H, Koenig WD et al (2000) Life history and demographic variation in the California tiger salamander (Ambystoma californiense). Copeia 2000:365–377CrossRefGoogle Scholar
  54. Tuljapurkar S (1990) Delayed reproduction and fitness in variable environments. Proc Natl Acad Sci USA 87:1139–1143CrossRefPubMedGoogle Scholar
  55. 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 26:347–358CrossRefGoogle Scholar
  56. 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 105:11466–11473CrossRefPubMedGoogle Scholar
  57. 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 26:500–509CrossRefPubMedGoogle Scholar
  58. 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:e41579CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wells KD (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  60. Woodward G, Ebenman B, Emmerson M et al (2005) Body size in ecological networks. Trends Ecol Evol 20:402–409CrossRefPubMedGoogle Scholar
  61. Yang X (2011) Speciation and geographic distribution pattern of the genus Feirana. MSc Dissertation, Chengdu Institute of Biology, Chinese Academy of Sciences, ChengduGoogle Scholar
  62. 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 Google Scholar
  63. Yu X, Zhong M, Li D et al (2018) Large-brained frogs mature later and live longer. Evolution 72:1174–1183CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Xiaoyi Wang
    • 1
    • 2
  • Yan Huang
    • 1
    • 3
  • Maojun Zhong
    • 3
  • Shengnan Yang
    • 1
    • 3
  • Xin Yang
    • 1
  • Jianping Jiang
    • 1
  • Junhua Hu
    • 1
    Email author
  1. 1.Chengdu Institute of BiologyChinese Academy of SciencesChengduChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education)China West Normal UniversityNanchongChina

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