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Developmental warming induces severe deformities and mortality in a thermally tolerant fish species


Abstract

Climate change poses an unprecedented global threat to wildlife, with projected environmental warming likely to push many species beyond optimum temperature ranges. Understanding thermal limits is therefore critical for risk predictions and conservation management, especially in the context of sensitive life stages such as early development. We investigated the effects of elevated developmental temperatures on the eastern mosquitofish, Gambusia holbrooki. This species is a highly successful invader across temperate to tropical regions, making it an ideal model for understanding potential outcomes for more tolerant species. Wild mosquitofish were collected from tropical waterways and bred under their thermal optimum of 27 °C. Offspring were reared from birth across three temperature treatments: 27 °C – control, 30 °C – a higher temperature within their thermal range, and 33 °C, a temperature designed to test their thermal boundaries. Alarmingly, 84% of the fish exposed to 33 °C developed severe spinal deformities and there was 100% mortality by 135 days old. While spinal deformation was less common at 30 °C, there was significantly reduced survival by 220 days. Our study demonstrates the importance of studying critical life stages, including early development, to understand the thermal sensitivity of wildlife, as even species that are known to have highly robust adults may face detrimental outcomes in climate change scenarios.

Data availability

The data that support the findings of this study are openly available in figshare at https://doi.org/10.6084/m9.figshare.31238707.

References

  1. IPCC. in Climate Change 2023: Synthesis Report. Contribution of Working Groups I, II and III To the Sixth Assessment Report of the Intergovernmental Panel on Climate Change [Core Writing Team. 35–115 (eds Lee, H. & Romero, J.) (IPCC, 2023). https://doi.org/10.59327/IPCC/AR6-9789291691647.

  2. Meehl, G. A., Tebaldi, C. M. & Intense More Frequent, and longer lasting heat waves in the 21st century. Science 305, 994–997 (2004).

    Google Scholar 

  3. Tewksbury, J. J., Huey, R. B. & Deutsch, C. A. Putting the heat on tropical animals. Science 320, 1296–1297 (2008).

    Google Scholar 

  4. Pinsky, M. L., Eikeset, A. M., McCauley, D. J., Payne, J. L. & Sunday, J. M. Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569, 108–111 (2019).

    Google Scholar 

  5. Fry, F. J. Responses of vertebrate poikilotherms to temperature. Thermobiology 375–409 (1967).

  6. Hayden Bofill, S. I. & Blom, M. P. K. Climate change from an ectotherm perspective: evolutionary consequences and demographic change in amphibian and reptilian populations. Biodivers. Conserv. 33, 905–927 (2024).

    Google Scholar 

  7. Angilletta, M. J., Niewiarowski, P. H. & Navas, C. A. The evolution of thermal physiology in ectotherms. J. Therm. Biol. 27, 249–268 (2002).

    Google Scholar 

  8. Laubenstein, T. D. et al. Correlated effects of ocean acidification and warming on behavioral and metabolic traits of a large pelagic fish. Diversity 10, 35 (2018).

    Google Scholar 

  9. Burraco, P., Orizaola, G., Monaghan, P. & Metcalfe N. B. Climate change and ageing in ectotherms. Glob. Change Biol. 26, 5371–5381 (2020).

    Google Scholar 

  10. Pimentel, M. S., Faleiro, F., Machado, J., Pousão-Ferreira, P. & Rosa, R. Seabream larval physiology under ocean warming and acidification. Fishes 5, 1 (2020).

    Google Scholar 

  11. Moore, B. et al. Clownfish larvae exhibit faster growth, higher metabolic rates and altered gene expression under future ocean warming. Sci. Total Environ. 873, 162296 (2023).

    Google Scholar 

  12. Reading, C. J. Linking global warming to amphibian declines through its effects on female body condition and survivorship. Oecologia 151, 125–131 (2007).

    Google Scholar 

  13. Cheung, W. W. L. et al. Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat. Clim. Change. 3, 254–258 (2013).

    Google Scholar 

  14. Nagelkerken, I. et al. The effects of climate change on the ecology of fishes. PLOS Clim. 2, e0000258 (2023).

    Google Scholar 

  15. Gibbons, J. W. et al. The global decline of reptiles, Déjà Vu amphibians: reptile species are declining on a global scale. Six significant threats to reptile populations are habitat loss and degradation, introduced invasive species, environmental pollution, disease, unsustainable use, and global climate change. BioScience 50, 653–666 (2000).

    Google Scholar 

  16. Stuart, S. N. et al. Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783–1786 (2004).

    Google Scholar 

  17. West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford University Press, 2003).

  18. Pörtner, H. O. & Knust, R. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 (2007).

    Google Scholar 

  19. Burton, T. & Metcalfe, N. B. Can environmental conditions experienced in early life influence future generations? Proc. R. Soc. B Biol. Sci. 281, 20140311 (2014).

  20. Jonsson, B. & Jonsson, N. Early environment influences later performance in fishes. J. Fish Biol. 85, 151–188 (2014).

    Google Scholar 

  21. Noble, D. W. A., Stenhouse, V. & Schwanz, L. E. Developmental temperatures and phenotypic plasticity in reptiles: a systematic review and meta-analysis. Biol. Rev. 93, 72–97 (2018).

    Google Scholar 

  22. O’Dea, R. E., Lagisz, M., Hendry, A. P. & Nakagawa, S. Developmental temperature affects phenotypic means and variability: A meta-analysis of fish data. Fish Fish. 20, 1005–1022 (2019).

    Google Scholar 

  23. Kourkouta, C. et al. Long lasting effects of early temperature exposure on the swimming performance and skeleton development of metamorphosing Gilthead seabream (Sparus aurata L.) larvae. Sci. Rep. 11, 8787 (2021).

    Google Scholar 

  24. Booth, D. T. Influence of incubation temperature on sea turtle hatchling quality. Integr. Zool. 12, 352–360 (2017).

    Google Scholar 

  25. De Jong, M. J. et al. Long-term effects of incubation temperature on growth and thermal physiology in a small ectotherm. Philosophical Trans. Royal Soc. B: Biol. Sci. 378, 20220137 (2023).

    Google Scholar 

  26. Pigliucci, M. Phenotypic Plasticity: Beyond Nature and Nurture (JHU, 2001).

  27. Scott, G. R. & Johnston, I. A. Temperature during embryonic development has persistent effects on thermal acclimation capacity in zebrafish. Proc. Natl. Acad. Sci. 109, 14247–14252 (2012).

    Google Scholar 

  28. Sunday, J. M., Bates, A. E. & Dulvy, N. K. Thermal tolerance and the global redistribution of animals. Nat. Clim. Change. 2, 686–690 (2012).

    Google Scholar 

  29. Seebacher, F., White, C. R. & Franklin, C. E. Physiological plasticity increases resilience of ectothermic animals to climate change. Nat. Clim. Change. 5, 61–66 (2015).

    Google Scholar 

  30. Rohr, J. R. & Palmer, B. D. Climate Change, multiple Stressors, and the decline of ectotherms. Conserv. Biol. 27, 741–751 (2013).

    Google Scholar 

  31. Wilson, R. S. Temperature influences the coercive mating and swimming performance of male Eastern mosquitofish. Anim. Behav. 70, 1387–1394 (2005).

    Google Scholar 

  32. Beaudouin, R., Ginot, V. & Monod, G. Growth characteristics of Eastern mosquitofish Gambusia holbrooki in a Northern habitat (Brittany, France). J. Fish Biol. 73, 2468–2484 (2008).

    Google Scholar 

  33. Meffe, G. K. Plasticity of Life-History Characters in Eastern Mosquitofish (Gambusia holbrooki: Poeciliidae) in Response to Thermal Stress. Copeia 94–102 (1992). (1992).

  34. Mulvey, M., Keller, G. P. & Meffe, G. K. Single- and Multiple-Locus genotypes and Life-History responses of Gambusia holbrooki reared at two temperatures. Evolution 48, 1810–1819 (1994).

    Google Scholar 

  35. Pyke, G. H. A review of the biology of Gambusia affinis and G. holbrooki. Rev. Fish. Biol. Fisheries. 15, 339–365 (2005).

    Google Scholar 

  36. Arthington, A. H. Ecological and genetic impacts of introduced and translocated freshwater fishes in Australia. Can. J. Fish. Aquat. Sci. 48, 33–43 (1991).

    Google Scholar 

  37. Pyke, G. H. Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu. Rev. Ecol. Evol. Syst. 39, 171–191 (2008).

    Google Scholar 

  38. Nekrasova, O. et al. A GIS modeling study of the distribution of viviparous invasive alien fish species in Eastern Europe in terms of global climate Change, as exemplified by poecilia reticulata Peters, 1859 and Gambusia holbrooki Girarg, 1859. Diversity 13, 385 (2021).

    Google Scholar 

  39. Taylor, W. R. & Van Dyke, G. Revised procedures for staining and clearing small fishes and other vertebrates for bone and cartilage study. (1985).

  40. Wang, L. H. & Tsai, C. L. Effects of temperature on the deformity and sex differentiation of tilapia, Oreochromis mossambicus. J. Exp. Zool. 286, 534–537 (2000).

    Google Scholar 

  41. Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear Mixed-Effects Models using ‘Eigen’ and S4. 1.1–37. https://doi.org/10.32614/CRAN.package.lme4 (2003).

  42. Lenth, R. Package ‘lsmeans’. Am. Stat. 34, 216–221 (2018).

    Google Scholar 

  43. Kassambara, A. Rstatix: Pipe-Friendly framework for basic statistical tests. CRAN: Contributed Packages. https://doi.org/10.32614/cran.package.rstatix (2019). doi:10.32614/cran.package.rstatix.

    Google Scholar 

  44. Therneau, T. M. & coxme Mixed Effects Cox Models. 2.2–22 (2009). https://doi.org/10.32614/CRAN.package.coxme.

  45. Wickham, H. Ggplot2 (Springer International Publishing, 2016). https://doi.org/10.1007/978-3-319-24277-4.

  46. Alboukadel, K., Marcin, K. & Przemyslaw, B. Drawing Survival Curves using ‘ggplot2’. CRAN: Contributed Packages https://doi.org/10.32614/cran.package.survminer (2016). https://doi.org/10.32614/cran.package.survminer.

  47. Wilson, R. S. & Johnston, I. A. Combining studies of comparative physiology and behavioural ecology to test the adaptive benefits of thermal acclimation. Int. Congr. Ser. 1275, 201–208 (2004).

    Google Scholar 

  48. Wilson, R. S., Condon, C. H. L. & Johnston, I. A. Consequences of thermal acclimation for the mating behaviour and swimming performance of female mosquito fish. Philosophical Trans. Royal Soc. B: Biol. Sci. 362, 2131–2139 (2007).

    Google Scholar 

  49. Seebacher, F. & Kazerouni-Ghanizadeh, E. Water flow and temperature interact to determine oxidative status, swimming performance, and dispersal of mosquitofish (Gambusia holbrooki). Freshw. Biol. 66, 1366–1374 (2021).

    Google Scholar 

  50. Arthington, A. H. & Lloyd, L. N. Introduced poeciliids in Australia and New Zealand. (1989). https://www.cabidigitallibrary.org/doi/full/10.5555/19900502748.

  51. Hubbs, C. High incidence of vertebral deformities in two natural populations of fishes inhabiting warm springs. Ecology 40, 154–155 (1959).

    Google Scholar 

  52. Sassi, A. et al. Influence of high temperature on cadmium-induced skeletal deformities in juvenile mosquitofish (Gambusia affinis). Fish. Physiol. Biochem. 36, 403–409 (2010).

    Google Scholar 

  53. Yang, Q. et al. Effect of temperature on growth, survival and occurrence of skeletal deformity in the golden Pompano Trachinotus ovatus larvae. Indian J. Fisheries. 63, 74–82 (2016).

    Google Scholar 

  54. Han, M., Luo, M., Yang, R., Qin, J. G. & Ma, Z. Impact of temperature on survival and spinal development of golden Pompano Trachinotus ovatus (Linnaeus 1758). Aquaculture Rep. 18, 100556 (2020).

    Google Scholar 

  55. Rodríguez-Ibarra, L. E., Abdo-de La Parra, M. I., Velasco-Blanco, G., Aguilar-Zárate, G. & Martínez-Brown, J. M. Effect of temperature on the incubation, growth, survival, and presence of skeletal deformities in larvae of the clownfish amphiprion ocellaris (Pomacentridae) under rearing conditions. Lat Am. J. Aquat. Res. 52, 501–507 (2024).

    Google Scholar 

  56. Sfakianakis, D. G. et al. Environmental determinants of haemal lordosis in European sea bass, dicentrarchus labrax (Linnaeus, 1758). Aquaculture 254, 54–64 (2006).

    Google Scholar 

  57. Balbuena-Pecino, S. et al. Temperature affects musculoskeletal development and muscle lipid metabolism of Gilthead sea Bream (Sparus aurata). Front. Endocrinol. 10, (2019).

  58. Stickland, N. C., White, R. N., Mescall, P. E., Crook, A. R. & Thorpe, J. E. The effect of temperature on myogenesis in embryonic development of the Atlantic salmon (Salmo Salar L). Anat. Embryol. 178, 253–257 (1988).

    Google Scholar 

  59. Usher, M. L., Stickland, N. C. & Thorpe, J. E. Muscle development in Atlantic salmon (Salmo salar) embryos and the effect of temperature on muscle cellularity. J. Fish Biol. 44, 953–964 (1994).

    Google Scholar 

  60. López-Albors, O. et al. Early temperature effects on muscle growth dynamics and histochemical profile of muscle fibres of sea bass dicentrarchus labrax L., during larval and juvenile stages. Aquaculture 220, 385–406 (2003).

    Google Scholar 

  61. Powell, M., Jones, M. & Lijalad, M. Effects of skeletal deformities on swimming performance and recovery from exhaustive exercise in triploid Atlantic salmon. Dis. Aquat. Org. 85, 59–66 (2009).

    Google Scholar 

  62. Chandra, G., Saini, V. P. & Kumar, S. Fopp-Bayat, D. Deformities in fish: A barrier for responsible aquaculture and sustainable fisheries. Reviews Aquaculture. 16, 872–891 (2024).

    Google Scholar 

  63. Andrades, J. A., Becerra, J. & Fernández-Llebrez, P. Skeletal deformities in larval, juvenile and adult stages of cultured Gilthead sea Bream (Sparus aurata L). Aquaculture 141, 1–11 (1996).

    Google Scholar 

  64. Pörtner, H. O. & Peck, M. A. Climate change effects on fishes and fisheries: towards a cause-and-effect Understanding. J. Fish Biol. 77, 1745–1779 (2010).

    Google Scholar 

  65. Chang, S. L., Lee, W. S. & Munch, S. B. Separating paternal and maternal contributions to thermal transgenerational plasticity. Front. Mar. Sci. 8, (2021).

  66. Bernal, M. A., Ravasi, T., Rodgers, G. G., Munday, P. L. & Donelson, J. M. Plasticity to ocean warming is influenced by transgenerational, reproductive, and developmental exposure in a coral reef fish. Evol. Appl. 15, 249–261 (2022).

    Google Scholar 

  67. Donelson, J. M., Munday, P. L., McCormick, M. I. & Pitcher, C. R. Rapid transgenerational acclimation of a tropical reef fish to climate change. Nat. Clim. Change. 2, 30–32 (2012).

    Google Scholar 

  68. Jonsson, B. & Jonsson, N. Phenotypic plasticity and epigenetics of fish: embryo temperature affects later-developing lift-history traits. Aquat. Biology. 28, 21–32 (2019).

    Google Scholar 

  69. FAO. The State of World Fisheries and Aquaculture. (2020). https://openknowledge.fao.org/server/api/core/bitstreams/02d655dc-06a3-4a37-bd5a-328f45bc2852/content/ca9229en.html (2020).

  70. McIntyre, P. B., Reidy Liermann, C. A. & Revenga, C. Linking freshwater fishery management to global food security and biodiversity conservation. Proc. Natl. Acad. Sci. 113, 12880–12885 (2016).

    Google Scholar 

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Acknowledgements

We would like to thank Kate Chu for her help with aquarium set-up, fish collection and animal husbandry, Simon Wever, Joe Dukes, Tyson Hausler-Breen and Zac Stibbard for technical assistance, Victoria Aese-Bjoerkaa, Polina Mosyagina and Frœya Ullensvang for assisting aquarium maintenance and animal husbandry, and Dr Nikos Andreakis for the use of reagents for clearing and staining.

Funding

This work was supported by the Australian Research Council (J.M.D.: DP230100078).

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All authors were involved in conceiving the study and designing the methodology. L.C.A. and T.L.H. conducted the experiments, and L.C.A. analysed the data, prepared the figures and wrote the original manuscript draft. J.M.D. supervised the project and provided funding and resources. All authors reviewed the manuscript.

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Correspondence to
Lucinda C. Aulsebrook.

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Aulsebrook, L.C., Hosler, T.L. & Donelson, J.M. Developmental warming induces severe deformities and mortality in a thermally tolerant fish species.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-39489-1

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  • DOI: https://doi.org/10.1038/s41598-026-39489-1

Keywords

  • Climate change
  • Heat stress
  • Thermal tolerance
  • Skeletal development
  • Developmental plasticity
  • Gambusia holbrooki


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