CoChat
Sign Up
Cited by 45Amphibian and Reptile BiologyPhysiological and biochemical adaptationsAnimal Behavior and Reproduction

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

Developmental plasticity in amphibian larvae across the world: Investigating the roles of temperature and latitude

Open access
Sinai, Noa, Glos, Julian, Mohan, Ashwini V., Lyra, Mariana L., Riepe, Maya, Thöle, Elena, Zummach, Cecile, Ruthsatz, Katharina·2022·Journal of Thermal Biology
DOI 10.1016/j.jtherbio.2022.103233
Open this paper in CoChat — free account

Abstract

Temperature-induced developmental plasticity could allow amphibian larvae to complete metamorphosis successfully despite new thermal challenges and increased desiccation risk due to climate change. Here we investigated how the capacity for temperature-induced developmental plasticity varies with latitude and whether population-specific biogeographic background accounts for the different degree of plastic responses to temperature. We carried out a combined analysis based on the data from 150 studies (93 articles) performed on 64 amphibian species. We collected empirical data for age and size at metamorphosis in amphibian larvae acclimated to different temperatures during development and found that all larvae from all populations in these studies revealed a change in metamorphic traits with a given change in temperature and thus, were able to exhibit temperature-induced developmental plasticity. Age at metamorphosis was more affected by temperature than size at metamorphosis. Age and size at the onset of metamorphosis were generally lowest at warmest temperatures during development. Furthermore, populations from tropical latitudes were less sensitive to a change in developmental temperature compared to populations from higher latitudes. Accordingly, we suggest tropical populations to be the most vulnerable to increasing temperatures during metamorphosis. Our analyses reveal biases with respect to taxonomy, biogeographic distribution of species, and study design. Data from tropical populations are underrepresented and thus, the capacity for developmental plasticity of the most threatened species probably remains poorly understood. Future studies should focus on under-represented regions, most threatened species, and include a broader range of temperatures during development in order to make robust projections on future sensitivity of populations to climate change.

Overview

Integrity signals

Registry

Crossref · 10.1016/j.jtherbio.2022.103233

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Show all 4 references

Research works printed but not linked: 93

  1. Addo-Bediako, 2000, Thermal tolerance, climatic variability and latitude, Proc. Roy. Soc. Lond. B Biol. Sci., 267, 739, 10.1098/rspb.2000.1065 · DOI
  2. Alroy, 2015, Current extinction rates of reptiles and amphibians, Proc. Natl. Acad. Sci. Unit. States Am., 112, 13003, 10.1073/pnas.1508681112 · DOI
  3. Alvarez, 2002, Effects of temperature and food quality on anuran larval growth and metamorphosis, Funct. Ecol., 16, 640, 10.1046/j.1365-2435.2002.00658.x · DOI
  4. Angilletta, 2002, The evolution of thermal physiology in ectotherms, J. Therm. Biol., 27, 249, 10.1016/S0306-4565(01)00094-8 · DOI
  5. Angilletta, 2003, The temperature-size rule in ectotherms: simple evolutionary explanations may not be general, Am. Nat., 162, 332, 10.1086/377187 · DOI
  6. Atkinson, 1994, Temperature and organism size: a biological law for ectotherms?, Adv. Ecol. Res., 25, 1, 10.1016/S0065-2504(08)60212-3 · DOI
  7. Barria, 2017, Intraspecific geographic variation in thermal limits and acclimatory capacity in a wide distributed endemic frog, J. Therm. Biol., 69, 254, 10.1016/j.jtherbio.2017.08.010 · DOI
  8. Bates, 2019, Captivity and infection by the fungal pathogen Batrachochytrium salamandrivorans perturb the amphibian skin microbiome, Front. Microbiol., 10, 1834, 10.3389/fmicb.2019.01834 · DOI
  9. Beck, 2000, Effects of age and size at metamorphosis on performance and metabolic rates of Southern Toad, Bufo terrestris, metamorphs, Funct. Ecol., 14, 32, 10.1046/j.1365-2435.2000.00386.x · DOI
  10. Bennett, 2018, GlobTherm, a global database on thermal tolerances for aquatic and terrestrial organisms, Sci. Data, 5, 1, 10.1038/sdata.2018.22 · DOI
  11. Berven, 1990, Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica), Ecology, 71, 1599, 10.2307/1938295 · DOI
  12. Boone, 2001, Growth and development of larval green frogs (Rana clamitans) exposed to multiple doses of an insecticide, Oecologia, 129, 518, 10.1007/s004420100749 · DOI
  13. Boorse, 2004, Expression and hypophysiotropic actions of corticotropin-releasing factor in Xenopus laevis, Gen. Comp. Endocrinol., 137, 272, 10.1016/j.ygcen.2004.04.001 · DOI
  14. Bozinovic, 2011, Physiological correlates of geographic range in animals, Annu. Rev. Ecol. Evol. Syst., 42, 155, 10.1146/annurev-ecolsys-102710-145055 · DOI
  15. Brattstrom, 1968, Thermal acclimation in anuran amphibians as a function of latitude and altitude, Comp. Biochem. Physiol., 24, 93, 10.1016/0010-406X(68)90961-4 · DOI
  16. Button, 2021, An integrative synthesis to global amphibian conservation priorities, Global Change Biol., 27, 4516, 10.1111/gcb.15734 · DOI
  17. Claussen, 1977, Thermal acclimation in ambystomatid salamanders, Comp. Biochem. Physiol. Physiol., 58, 333, 10.1016/0300-9629(77)90150-5 · DOI
  18. da Silva, 2020, Taxonomic bias in amphibian research: are researchers responding to conservation need?, J. Nat. Conserv., 56, 125829, 10.1016/j.jnc.2020.125829 · DOI
  19. Daufresne, 2009, Global warming benefits the small in aquatic ecosystems, Proc. Natl. Acad. Sci. Unit. States Am., 106, 12788, 10.1073/pnas.0902080106 · DOI
  20. Denver, 2021, Stress hormones mediate developmental plasticity in vertebrates with complex life cycles, Neurobiol. Stress, 14, 100301, 10.1016/j.ynstr.2021.100301 · DOI
  21. Denver, 2010, Lessons from evolution: developmental plasticity in vertebrates with complex life cycles, J. Dev. Orig. Health Dis., 1, 282, 10.1017/S2040174410000279 · DOI
  22. Deutsch, 2008, Impacts of climate warming on terrestrial ectotherms across latitude, Proc. Natl. Acad. Sci. Unit. States Am., 105, 6668, 10.1073/pnas.0709472105 · DOI · Paper page
  23. Duarte, 2012, Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities, Global Change Biol., 18, 412, 10.1111/j.1365-2486.2011.02518.x · DOI
  24. Earl, 2015, Are commonly used fitness predictors accurate? A meta-analysis of amphibian size and age at metamorphosis, Copeia, 103, 297, 10.1643/CH-14-128 · DOI
  25. Edge, 2016, The response of amphibian larvae to environmental change is both consistent and variable, Oikos, 125, 1700, 10.1111/oik.03166 · DOI
  26. Fick, 2017, WorldClim 2: new 1km spatial resolution climate surfaces for global land areas, Int. J. Climatol., 37, 4302, 10.1002/joc.5086 · DOI · Paper page
  27. Forster, 2012, The temperature‐size rule emerges from ontogenetic differences between growth and development rates, Funct. Ecol., 26, 483, 10.1111/j.1365-2435.2011.01958.x · DOI
  28. Ghalambor, 2006, Are mountain passes higher in the tropics? Janzen's hypothesis revisited, Integr. Comp. Biol., 46, 5, 10.1093/icb/icj003 · DOI
  29. Gienapp, 2008, Climate change and evolution: disentangling environmental and genetic responses, Mol. Ecol., 17, 167, 10.1111/j.1365-294X.2007.03413.x · DOI
  30. Glennemeier, 2002, Developmental changes in interrenal responsiveness in anuran amphibians, Integr. Comp. Biol., 42, 565, 10.1093/icb/42.3.565 · DOI
  31. Glennemeier, 2002, Small changes in whole-body corticosterone content affect larval Rana pipiens fitness components, Gen. Comp. Endocrinol., 127, 16, 10.1016/S0016-6480(02)00015-1 · DOI
  32. Glennemeier, 2002, Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition, J. Exp. Zool., 292, 32, 10.1002/jez.1140 · DOI
  33. Gomez-Mestre, 2010, The shape of things to come: linking developmental plasticity to post‐metamorphic morphology in anurans, J. Evol. Biol., 23, 1364, 10.1111/j.1420-9101.2010.02016.x · DOI
  34. Gosner, 1960, A simplified table for staging anuran embryos and larvae with notes on identification, Herpetologica, 16, 183
  35. Green, 2020, Amphibian population declines: 30 years of progress in confronting a complex problem, Herpetologica, 76, 97, 10.1655/0018-0831-76.2.97 · DOI
  36. Hadfield, 2010, MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package, J. Stat. Software, 33, 1, 10.18637/jss.v033.i02 · DOI
  37. Huey, 1979, Integrating thermal physiology and ecology of ectotherms: a discussion of approaches, Am. Zool., 19, 357, 10.1093/icb/19.1.357 · DOI
  38. Huey, 2012, Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation, Phil. Trans. Biol. Sci., 367, 1665, 10.1098/rstb.2012.0005 · DOI
  39. Janzen, 1967, Why mountain passes are higher in the tropics, Am. Nat., 101, 233, 10.1086/282487 · DOI · Paper page
  40. Johansson, 2020, Temperate insects with narrow seasonal activity periods can be as vulnerable to climate change as tropical insect species, Sci. Rep., 10, 1, 10.1038/s41598-020-65608-7 · DOI
  41. Kearney, 2009, Mechanistic niche modelling: combining physiological and spatial data to predict species' ranges, Ecol. Lett., 12, 334, 10.1111/j.1461-0248.2008.01277.x · DOI
  42. King, 2004, The scientific impact of nations, Nature, 430, 311, 10.1038/430311a · DOI · Paper page
  43. Kingsolver, 2008, Size, temperature, and fitness: three rules, Evol. Ecol. Res., 10, 251
  44. Kulkarni, 2012, Beyond synergy: corticosterone and thyroid hormone have numerous interaction effects on gene regulation in Xenopus tropicalis tadpoles, Endocrinology, 153, 5309, 10.1210/en.2012-1432 · DOI
  45. Laudet, 2011, The origins and evolution of vertebrate metamorphosis, Curr. Biol., 21, R726, 10.1016/j.cub.2011.07.030 · DOI
  46. Laurila, 1999, Habitat duration, predation risk and phenotypic plasticity in common frog (Rana temporaria) tadpoles, J. Anim. Ecol., 68, 1123, 10.1046/j.1365-2656.1999.00354.x · DOI
  47. Lesbarrères, 2007, Genetic variability predicts common frog (Rana temporaria) size at metamorphosis in the wild, Heredity, 99, 41, 10.1038/sj.hdy.6800961 · DOI
  48. Loman, 2002, Temperature, genetic and hydroperiod effects on metamorphosis of brown frogs Rana arvalis and R. temporaria in the field, J. Zool., 258, 115, 10.1017/S0952836902001255 · DOI
  49. Lowe, 2021, Metamorphosis in an era of increasing climate variability, Trends Ecol. Evol., 36, 360, 10.1016/j.tree.2020.11.012 · DOI
  50. Mahlstein, 2013, Pace of shifts in climate regions increases with global temperature, Nat. Clim. Change, 3, 739, 10.1038/nclimate1876 · DOI
  51. Merilä, 2000, Plasticity in age and size at metamorphosis in Rana temporaria‐comparison of high and low latitude populations, Ecography, 23, 457, 10.1111/j.1600-0587.2000.tb00302.x · DOI
  52. Molina-Venegas, 2017, Revisiting phylogenetic signal; strong or negligible impacts of polytomies and branch length information?, BMC Evol. Biol., 17, 1
  53. Morley, 2019, Physiological acclimation and persistence of ectothermic species under extreme heat events, Global Ecol. Biogeogr., 28, 1018, 10.1111/geb.12911 · DOI
  54. Münkemüller, 2012, How to measure and test phylogenetic signal, Meth. Ecol. Evol., 3, 743, 10.1111/j.2041-210X.2012.00196.x · DOI
  55. Navas, 2008, Thermal relationships and exercise physiology in anuran amphibians: integration and evolutionary implications, Comp. Biochem. Physiol. Mol. Integr. Physiol., 151, 344, 10.1016/j.cbpa.2007.07.003 · DOI
  56. Naya, 2011, Exploring the functional association between physiological plasticity, climatic variability, and geographical latitude: lessons from land snails, Evol. Ecol. Res., 13, 647
  57. Newman, 1992, Adaptive plasticity in amphibian metamorphosis, Bioscience, 42, 671, 10.2307/1312173 · DOI
  58. Ohlberger, 2013, Climate warming and ectotherm body size–from individual physiology to community ecology, Funct. Ecol., 27, 991, 10.1111/1365-2435.12098 · DOI
  59. Oyamaguchi, 2018, Thermal sensitivity of a Neotropical amphibian (Engystomops pustulosus) and its vulnerability to climate change, Biotropica, 50, 326, 10.1111/btp.12519 · DOI
  60. Pacifici, 2015, Assessing species vulnerability to climate change, Nat. Clim. Change, 5, 215, 10.1038/nclimate2448 · DOI
  61. Paradis, 2019, Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R, Bioinformatics, 35, 526, 10.1093/bioinformatics/bty633 · DOI
  62. Pawar, 2003, Taxonomic chauvinism and the methodologically challenged, Bioscience, 53, 861, 10.1641/0006-3568(2003)053[0861:TCATMC]2.0.CO;2 · DOI
  63. Pennell, 2014, Geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees, Bioinformatics, 30, 2216, 10.1093/bioinformatics/btu181 · DOI
  64. Pullin, 2006, Guidelines for systematic review in conservation and environmental management, Conserv. Biol., 20, 1647, 10.1111/j.1523-1739.2006.00485.x · DOI · Paper page
  65. Pyron, 2011, A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians, Mol. Phylogenet. Evol., 61, 543, 10.1016/j.ympev.2011.06.012 · DOI
  66. Rohr, 2018, The complex drivers of thermal acclimation and breadth in ectotherms, Ecol. Lett., 21, 1425, 10.1111/ele.13107 · DOI
  67. Rollins, 2020, Challenges in predicting the outcome of competition based on climate change-induced phenological and body size shifts, Oecologia, 193, 749, 10.1007/s00442-020-04705-w · DOI
  68. Rudolf, 2007, Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints, Evol. Ecol., 21, 121, 10.1007/s10682-006-0017-9 · DOI
  69. Ruthsatz, 2020, Altered thyroid hormone levels affect the capacity for temperature-induced developmental plasticity in larvae of Rana temporaria and Xenopus laevis, J. Therm. Biol., 90, 102599, 10.1016/j.jtherbio.2020.102599 · DOI
  70. Ruthsatz, 2018, Thyroid hormone levels and temperature during development alter thermal tolerance and energetics of Xenopus laevis larvae, Conserv. Physiol., 6, coy059, 10.1093/conphys/coy059 · DOI
  71. Ruthsatz, 2019, Endocrine disruption alters developmental energy allocation and performance in Rana temporaria, Integr. Comp. Biol., 59, 70, 10.1093/icb/icz041 · DOI
  72. Ruthsatz, 2018, Patterns of temperature induced developmental plasticity in anuran larvae, J. Therm. Biol., 74, 123, 10.1016/j.jtherbio.2018.03.005 · DOI
  73. Ryan, 2009, Global multi‐resolution topography synthesis, G-cubed, 10
  74. Schiesari, 2007, Biogeographic biases in research and their consequences for linking amphibian declines to pollution, Conserv. Biol., 21, 465, 10.1111/j.1523-1739.2006.00616.x · DOI
  75. Semlitsch, 1988, Time and size at metamorphosis related to adult fitness in Ambystoma talpoideum, Ecology, 69, 184, 10.2307/1943173 · DOI
  76. Smith, 1987, Adult recruitment in chorus frogs: effects of size and date at metamorphosis, Ecology, 68, 344, 10.2307/1939265 · DOI
  77. Smith-Gill, 1979, Predicting amphibian metamorphosis, Am. Nat., 113, 563, 10.1086/283413 · DOI
  78. Somero, 2005, Linking biogeography to physiology: evolutionary and acclimatory adjustments of thermal limits, Front. Zool., 2, 1, 10.1186/1742-9994-2-1 · DOI
  79. Stevens, 1989, The latitudinal gradient in geographical range: how so many species coexist in the tropics, Am. Nat., 133, 240, 10.1086/284913 · DOI
  80. Stuart, 2004, Status and trends of amphibian declines and extinctions worldwide, Science, 306, 1783, 10.1126/science.1103538 · DOI · Paper page
  81. Sunday, 2014, Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation, Proc. Natl. Acad. Sci. Unit. States Am., 111, 5610, 10.1073/pnas.1316145111 · DOI
  82. Tewksbury, 2008, Putting the heat on tropical animals, Science, 320, 1296, 10.1126/science.1159328 · DOI · Paper page
  83. Tejedo, 2010, Contrasting effects of environmental factors during larval stage on morphological plasticity in post-metamorphic frogs, Clim. Res., 43, 31, 10.3354/cr00878 · DOI
  84. Van Buskirk, 2017, Is bigger really better? Relative and absolute body size influence individual growth rate under competition, Ecol. Evol., 7, 3745, 10.1002/ece3.2978 · DOI
  85. Verberk, 2021, Shrinking body sizes in response to warming: explanations for the temperature–size rule with special emphasis on the role of oxygen, Biol. Rev., 96, 247, 10.1111/brv.12653 · DOI
  86. Wickham, 2009, Elegant graphics for data analysis, Media, 35, 10
  87. Wickham, 2016, 10.1007/978-3-319-24277-4 · DOI
  88. Wilbur, 1980, Complex life cycles, Annu. Rev. Ecol. Systemat., 11, 67, 10.1146/annurev.es.11.110180.000435 · DOI
  89. Wilbur, 1973, Ecological aspects of amphibian metamorphosis: nonnormal distributions of competitive ability reflect selection for facultative metamorphosis, Science, 182, 1305, 10.1126/science.182.4119.1305 · DOI
  90. Winter, 2016, Patterns and biases in climate change research on amphibians and reptiles: a systematic review, R. Soc. Open Sci., 3, 160158, 10.1098/rsos.160158 · DOI
  91. Woods, 2015, The roles of microclimatic diversity and of behavior in mediating the responses of ectotherms to climate change, J. Therm. Biol., 54, 86, 10.1016/j.jtherbio.2014.10.002 · DOI
  92. Yu, 2015, Joint effects of pesticides and ultraviolet-B radiation on amphibian larvae, Environ. Pollut., 207, 248, 10.1016/j.envpol.2015.09.029 · DOI
  93. Yu, 2017, ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data, Meth. Ecol. Evol., 8, 28, 10.1111/2041-210X.12628 · DOI

Cited by

Sorted by citations

See all 45

Metadata

Authors
Sinai, N., Glos, J., Mohan, A. V., Lyra, M. L., Riepe, M., Thöle, E., Zummach, C., & Ruthsatz, K.
Affiliations
  • Universität Hamburg (DE)
  • Natural History Museum (GB)
  • Universidade Estadual Paulista (Unesp) (BR)
  • Technische Universität Braunschweig (DE)
Corresponding author
Ruthsatz, Katharina
ORCID
Venue
Journal of Thermal Biology
Publisher
Elsevier BV
Published
2022-05
Volume
106
Pages
103233
ISSN
0306-4565 (ISSN-L)
DOI
10.1016/j.jtherbio.2022.103233
OpenAlex
W4226017637
Cited by
45
References
4
Citations by year
2026: 9 · 2025: 11 · 2024: 16 · 2023: 6 · 2022: 3
FWCI
3.58
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Thermal Biology (publishedVersion)
  • PubMed (publishedVersion)
  • LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (publishedVersion, other-oa)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Amphibian and Reptile Biology
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
developmental plasticity, amphibian larvae, metamorphic ages, size at metamorphosis, latitude, climate change vulnerability, thermal sensitivity, tropical populations, desiccation risk, metamorphosis
MeSH terms
Acclimatization, Amphibians, Animals, Larva, Metamorphosis, Biological, Temperature

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Developmental plasticity in amphibian larvae across the world: Investigating the roles of temperature and latitude. https://app.cochat.ai/papers/10.1016/j.jtherbio.2022.103233
The paper
Sinai, N., Glos, J., Mohan, A. V., Lyra, M. L., Riepe, M., Thöle, E., Zummach, C., & Ruthsatz, K. (2022). Developmental plasticity in amphibian larvae across the world: Investigating the roles of temperature and latitude. Journal of Thermal Biology. https://doi.org/10.1016/j.jtherbio.2022.103233