Literature DB >> 33081621

The biophysical basis of thermal tolerance in fish eggs.

Benjamin T Martin1,2,3, Peter N Dudley2,3, Neosha S Kashef2,3, David M Stafford2,3, William J Reeder4, Daniele Tonina4, Annelise M Del Rio5, J Scott Foott6, Eric M Danner2,3.   

Abstract

A warming climate poses a fundamental problem for embryos that develop within eggs because their demand for oxygen (O2) increases much more rapidly with temperature than their capacity for supply, which is constrained by diffusion across the egg surface. Thus, as temperatures rise, eggs may experience O2 limitation due to an imbalance between O2 supply and demand. Here, we formulate a mathematical model of O2 limitation and experimentally test whether this mechanism underlies the upper thermal tolerance in large aquatic eggs. Using Chinook salmon (Oncorhynchus tshawytscha) as a model system, we show that the thermal tolerance of eggs varies systematically with features of the organism and environment. Importantly, this variation can be precisely predicted by the degree to which these features shift the balance between O2 supply and demand. Equipped with this mechanistic understanding, we predict and experimentally confirm that the thermal tolerance of these embryos in their natural habitat is substantially lower than expected from laboratory experiments performed under normoxia. More broadly, our biophysical model of O2 limitation provides a mechanistic explanation for the elevated thermal sensitivity of fish embryos relative to other life stages, global patterns in egg size and the extreme fecundity of large teleosts.

Entities:  

Keywords:  egg; embryo; metabolic rate; oxygen limitation; temperature; thermal tolerance

Mesh:

Substances:

Year:  2020        PMID: 33081621      PMCID: PMC7661308          DOI: 10.1098/rspb.2020.1550

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  16 in total

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Authors:  J H Stillman; G N Somero
Journal:  Physiol Biochem Zool       Date:  2000 Mar-Apr       Impact factor: 2.247

2.  Thermal tolerance patterns across latitude and elevation.

Authors:  Jennifer Sunday; Joanne M Bennett; Piero Calosi; Susana Clusella-Trullas; Sarah Gravel; Anna L Hargreaves; Félix P Leiva; Wilco C E P Verberk; Miguel Ángel Olalla-Tárraga; Ignacio Morales-Castilla
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-06-17       Impact factor: 6.237

3.  Thermal bottlenecks in the life cycle define climate vulnerability of fish.

Authors:  Flemming T Dahlke; Sylke Wohlrab; Martin Butzin; Hans-Otto Pörtner
Journal:  Science       Date:  2020-07-03       Impact factor: 47.728

4.  Phenomenological vs. biophysical models of thermal stress in aquatic eggs.

Authors:  Benjamin T Martin; Andrew Pike; Sara N John; Natnael Hamda; Jason Roberts; Steven T Lindley; Eric M Danner
Journal:  Ecol Lett       Date:  2016-11-28       Impact factor: 9.492

5.  Physical constraints on body size in teleost embryos.

Authors:  S Kranenbarg; M Muller; J L Gielen; J H Verhagen
Journal:  J Theor Biol       Date:  2000-05-07       Impact factor: 2.691

6.  Adult and offspring size in the ocean over 17 orders of magnitude follows two life history strategies.

Authors:  A B Neuheimer; M Hartvig; J Heuschele; S Hylander; T Kiørboe; K H Olsson; J Sainmont; K H Andersen
Journal:  Ecology       Date:  2015-12       Impact factor: 5.499

7.  Differences in thermal tolerance among sockeye salmon populations.

Authors:  Erika J Eliason; Timothy D Clark; Merran J Hague; Linda M Hanson; Zoë S Gallagher; Ken M Jeffries; Marika K Gale; David A Patterson; Scott G Hinch; Anthony P Farrell
Journal:  Science       Date:  2011-04-01       Impact factor: 47.728

8.  Ventilation, gill perfusion and blood gases in dourado, Salminus maxillosus Valenciennes (teleostei, characidae), exposed to graded hypoxia.

Authors:  R H de Salvo Souza; R Soncini; M L Glass; J R Sanches; F T Rantin
Journal:  J Comp Physiol B       Date:  2001-08       Impact factor: 2.200

9.  Provenance matters: thermal reaction norms for embryo survival among sockeye salmon Oncorhynchus nerka populations.

Authors:  C K Whitney; S G Hinch; D A Patterson
Journal:  J Fish Biol       Date:  2013-03-12       Impact factor: 2.051

10.  Oviparous elasmobranch development inside the egg case in 7 key stages.

Authors:  Syafiq M Musa; Molly V Czachur; Holly A Shiels
Journal:  PLoS One       Date:  2018-11-06       Impact factor: 3.240

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  2 in total

1.  Differential sensitivity to warming and hypoxia during development and long-term effects of developmental exposure in early life stage Chinook salmon.

Authors:  Annelise M Del Rio; Gabriella N Mukai; Benjamin T Martin; Rachel C Johnson; Nann A Fangue; Joshua A Israel; Anne E Todgham
Journal:  Conserv Physiol       Date:  2021-07-08       Impact factor: 3.079

2.  Temperature and Diet Acclimation Modify the Acute Thermal Performance of the Largest Extant Amphibian.

Authors:  Chun-Lin Zhao; Tian Zhao; Jian-Yi Feng; Li-Ming Chang; Pu-Yang Zheng; Shi-Jian Fu; Xiu-Ming Li; Bi-Song Yue; Jian-Ping Jiang; Wei Zhu
Journal:  Animals (Basel)       Date:  2022-02-21       Impact factor: 2.752

  2 in total

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