A systematic map of studies testing the relationship between temperature and animal reproduction

Liam R. Dougherty; Fay Frost; Maarit I. Maenpaa; Melissah Rowe; Benjamin J. Cole; Ramakrishnan Vasudeva; Patrice Pottier; Eva Schultner; Erin L. Macartney; Ina Lindenbaum; Jamie L. Smith; Pau Carazo; Marco Graziano; Hester Weaving; Berta Canal Domenech; David Berger; Abhishek Meena; Tom Rhys Bishop; Daniel W. A. Noble; Pedro Simões; Julian Baur; Merel C. Breedveld; Erik I. Svensson; Lesley T. Lancaster; Jacintha Ellers; Alessio N. De Nardo; Marta A. Santos; Steven A. Ramm; Szymon M. Drobniak; Matteo Redana; Cristina Tuni; Natalie Pilakouta; Z. Valentina Zizzari; Graziella Iossa; Stefan Lüpold; Mareike Koppik; Regan Early; Clelia Gasparini; Shinichi Nakagawa; Malgorzata Lagisz; Amanda Bretman; Claudia Fricke; Rhonda R. Snook; Tom A. R. Price

doi:10.1002/2688-8319.12303

A systematic map of studies testing the relationship between temperature and animal reproduction

Liam R. Dougherty^* (Corresponding Author), Fay Frost, Maarit I. Maenpaa, Melissah Rowe, Benjamin J. Cole, Ramakrishnan Vasudeva, Patrice Pottier, Eva Schultner, Erin L. Macartney, Ina Lindenbaum, Jamie L. Smith, Pau Carazo, Marco Graziano, Hester Weaving, Berta Canal Domenech, David Berger, Abhishek Meena, Tom Rhys Bishop, Daniel W. A. Noble, Pedro SimõesJulian Baur, Merel C. Breedveld, Erik I. Svensson, Lesley T. Lancaster, Jacintha Ellers, Alessio N. De Nardo, Marta A. Santos, Steven A. Ramm, Szymon M. Drobniak, Matteo Redana, Cristina Tuni, Natalie Pilakouta, Z. Valentina Zizzari, Graziella Iossa, Stefan Lüpold, Mareike Koppik, Regan Early, Clelia Gasparini, Shinichi Nakagawa, Malgorzata Lagisz, Amanda Bretman, Claudia Fricke, Rhonda R. Snook, Tom A. R. Price

^*Corresponding author for this work

Aberdeen Centre For Environmental Sustainability

Research output: Contribution to journal › Article › peer-review

Abstract

Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction. We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits). Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species. The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled. This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.

Original language	English
Article number	e12303
Number of pages	17
Journal	Ecological Solutions and Evidence
Volume	5
Issue number	1
Early online date	1 Feb 2024
DOIs	https://doi.org/10.1002/2688-8319.12303
Publication status	Published - 1 Mar 2024

Bibliographical note

ACKNOWLEDGEMENTS
We thank two anonymous reviews for suggestions that improved the manuscript. This work was funded by the European Society for Evolution (which funds a Special Topic Network on Evolutionary Ecology of Thermal Fertility Limits to CF, AB, RRS and TARP), the Natural Environment Research Council (NE/P002692/1 to TARP, AB and RRS, NE/X011550/1 to LRD and TARP), the Biotechnology and Biological Sciences Research Council (BB/W016753/1 to AB, TARP and RRS) and a Heisenberg fellowship from the German Research Foundation (FR 2973/11-1 to CF).

Keywords

climate change
egg
evidence map
sperm
sterility
systematic review
thermal fertility limit
thermal tolerance

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1002/2688-8319.12303Licence: CC BY

Dougherty_etal_ESE_A_Systematic_Map_VoR
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2024 The Authors. Ecological Solutions and Evidence published by John Wiley & Sons Ltd on behalf of British Ecological Society https://creativecommons.org/licenses/by/4.0/
Final published version, 2.29 MBLicence: CC BY

Cite this

Dougherty, L. R., Frost, F., Maenpaa, M. I., Rowe, M., Cole, B. J., Vasudeva, R., Pottier, P., Schultner, E., Macartney, E. L., Lindenbaum, I., Smith, J. L., Carazo, P., Graziano, M., Weaving, H., Canal Domenech, B., Berger, D., Meena, A., Bishop, T. R., Noble, D. W. A., ... Price, T. A. R. (2024). A systematic map of studies testing the relationship between temperature and animal reproduction. Ecological Solutions and Evidence, 5(1), Article e12303. https://doi.org/10.1002/2688-8319.12303

Dougherty, LR, Frost, F, Maenpaa, MI, Rowe, M, Cole, BJ, Vasudeva, R, Pottier, P, Schultner, E, Macartney, EL, Lindenbaum, I, Smith, JL, Carazo, P, Graziano, M, Weaving, H, Canal Domenech, B, Berger, D, Meena, A, Bishop, TR, Noble, DWA, Simões, P, Baur, J, Breedveld, MC, Svensson, EI, Lancaster, LT, Ellers, J, De Nardo, AN, Santos, MA, Ramm, SA, Drobniak, SM, Redana, M, Tuni, C, Pilakouta, N, Zizzari, ZV, Iossa, G, Lüpold, S, Koppik, M, Early, R, Gasparini, C, Nakagawa, S, Lagisz, M, Bretman, A, Fricke, C, Snook, RR & Price, TAR 2024, 'A systematic map of studies testing the relationship between temperature and animal reproduction', Ecological Solutions and Evidence, vol. 5, no. 1, e12303. https://doi.org/10.1002/2688-8319.12303

@article{c25b54aa45b94134a9df776647daeff5,

title = "A systematic map of studies testing the relationship between temperature and animal reproduction",

abstract = "Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction. We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits). Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species. The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled. This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.",

keywords = "climate change, egg, evidence map, sperm, sterility, systematic review, thermal fertility limit, thermal tolerance",

author = "Dougherty, {Liam R.} and Fay Frost and Maenpaa, {Maarit I.} and Melissah Rowe and Cole, {Benjamin J.} and Ramakrishnan Vasudeva and Patrice Pottier and Eva Schultner and Macartney, {Erin L.} and Ina Lindenbaum and Smith, {Jamie L.} and Pau Carazo and Marco Graziano and Hester Weaving and Berta Canal Domenech and David Berger and Abhishek Meena and Bishop, {Tom Rhys} and Noble, {Daniel W. A.} and Pedro Sim{\~o}es and Julian Baur and Breedveld, {Merel C.} and Svensson, {Erik I.} and Lancaster, {Lesley T.} and Jacintha Ellers and De Nardo, {Alessio N.} and Santos, {Marta A.} and Ramm, {Steven A.} and Drobniak, {Szymon M.} and Matteo Redana and Cristina Tuni and Natalie Pilakouta and Zizzari, {Z. Valentina} and Graziella Iossa and Stefan L{\"u}pold and Mareike Koppik and Regan Early and Clelia Gasparini and Shinichi Nakagawa and Malgorzata Lagisz and Amanda Bretman and Claudia Fricke and Snook, {Rhonda R.} and Price, {Tom A. R.}",

note = "ACKNOWLEDGEMENTS We thank two anonymous reviews for suggestions that improved the manuscript. This work was funded by the European Society for Evolution (which funds a Special Topic Network on Evolutionary Ecology of Thermal Fertility Limits to CF, AB, RRS and TARP), the Natural Environment Research Council (NE/P002692/1 to TARP, AB and RRS, NE/X011550/1 to LRD and TARP), the Biotechnology and Biological Sciences Research Council (BB/W016753/1 to AB, TARP and RRS) and a Heisenberg fellowship from the German Research Foundation (FR 2973/11-1 to CF).",

year = "2024",

month = mar,

day = "1",

doi = "10.1002/2688-8319.12303",

language = "English",

volume = "5",

journal = "Ecological Solutions and Evidence",

issn = "2688-8319",

publisher = "John Wiley and Sons Inc.",

number = "1",

}

TY - JOUR

T1 - A systematic map of studies testing the relationship between temperature and animal reproduction

AU - Dougherty, Liam R.

AU - Frost, Fay

AU - Maenpaa, Maarit I.

AU - Rowe, Melissah

AU - Cole, Benjamin J.

AU - Vasudeva, Ramakrishnan

AU - Pottier, Patrice

AU - Schultner, Eva

AU - Macartney, Erin L.

AU - Lindenbaum, Ina

AU - Smith, Jamie L.

AU - Carazo, Pau

AU - Graziano, Marco

AU - Weaving, Hester

AU - Canal Domenech, Berta

AU - Berger, David

AU - Meena, Abhishek

AU - Bishop, Tom Rhys

AU - Noble, Daniel W. A.

AU - Simões, Pedro

AU - Baur, Julian

AU - Breedveld, Merel C.

AU - Svensson, Erik I.

AU - Lancaster, Lesley T.

AU - Ellers, Jacintha

AU - De Nardo, Alessio N.

AU - Santos, Marta A.

AU - Ramm, Steven A.

AU - Drobniak, Szymon M.

AU - Redana, Matteo

AU - Tuni, Cristina

AU - Pilakouta, Natalie

AU - Zizzari, Z. Valentina

AU - Iossa, Graziella

AU - Lüpold, Stefan

AU - Koppik, Mareike

AU - Early, Regan

AU - Gasparini, Clelia

AU - Nakagawa, Shinichi

AU - Lagisz, Malgorzata

AU - Bretman, Amanda

AU - Fricke, Claudia

AU - Snook, Rhonda R.

AU - Price, Tom A. R.

N1 - ACKNOWLEDGEMENTS We thank two anonymous reviews for suggestions that improved the manuscript. This work was funded by the European Society for Evolution (which funds a Special Topic Network on Evolutionary Ecology of Thermal Fertility Limits to CF, AB, RRS and TARP), the Natural Environment Research Council (NE/P002692/1 to TARP, AB and RRS, NE/X011550/1 to LRD and TARP), the Biotechnology and Biological Sciences Research Council (BB/W016753/1 to AB, TARP and RRS) and a Heisenberg fellowship from the German Research Foundation (FR 2973/11-1 to CF).

PY - 2024/3/1

Y1 - 2024/3/1

N2 - Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction. We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits). Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species. The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled. This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.

AB - Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction. We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits). Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species. The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled. This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.

KW - climate change

KW - egg

KW - evidence map

KW - sperm

KW - sterility

KW - systematic review

KW - thermal fertility limit

KW - thermal tolerance

U2 - 10.1002/2688-8319.12303

DO - 10.1002/2688-8319.12303

M3 - Article

SN - 2688-8319

VL - 5

JO - Ecological Solutions and Evidence

JF - Ecological Solutions and Evidence

IS - 1

M1 - e12303

ER -

A systematic map of studies testing the relationship between temperature and animal reproduction

Abstract

Bibliographical note

Keywords

UN SDGs

Access to Document

Fingerprint

Cite this