Ocean acidification boosts reproduction in fish via indirect effects

Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO₂ are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do n...

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Published in:PLOS Biology
Main Authors: Nagelkerken, I., Alemany, T., Anquetin, J.M., Ferreira, C.M., Ludwig, K.E., Sasaki, M., Connell, S.D.
Other Authors: Buckley, Y.
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2021
Subjects:
Online Access:http://hdl.handle.net/2440/129981
https://doi.org/10.1371/journal.pbio.3001033
id ftunivadelaidedl:oai:digital.library.adelaide.edu.au:2440/129981
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spelling ftunivadelaidedl:oai:digital.library.adelaide.edu.au:2440/129981 2023-12-17T10:47:51+01:00 Ocean acidification boosts reproduction in fish via indirect effects Nagelkerken, I. Alemany, T. Anquetin, J.M. Ferreira, C.M. Ludwig, K.E. Sasaki, M. Connell, S.D. Buckley, Y. 2021 application/pdf http://hdl.handle.net/2440/129981 https://doi.org/10.1371/journal.pbio.3001033 en eng Public Library of Science (PLoS) http://purl.org/au-research/grants/arc/FT120100183 http://purl.org/au-research/grants/arc/DP170101722 http://purl.org/au-research/grants/arc/FT0991953 PLoS Biology, 2021; 19(1):1-21 1544-9173 1545-7885 http://hdl.handle.net/2440/129981 doi:10.1371/journal.pbio.3001033 Nagelkerken, I. [0000-0003-4499-3940] Sasaki, M. [0000-0002-4832-2573] Connell, S.D. [0000-0002-5350-6852] © 2021 Nagelkerken et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://dx.doi.org/10.1371/journal.pbio.3001033 Animals Fishes Acids Carbon Dioxide Ecosystem Biodiversity Seawater Population Growth Reproduction Hydrogen-Ion Concentration New Zealand Oceans and Seas Female Male Sexual Behavior Animal Stress Physiological Climate Change Journal article 2021 ftunivadelaidedl https://doi.org/10.1371/journal.pbio.3001033 2023-11-20T23:20:37Z Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO₂ are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO₂ vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO₂ on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO₂ vents, which may further boost reproductive success. These positive indirect effects of elevated CO₂ were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean. Ivan Nagelkerken, Tiphaine Alemany, Julie M. Anquetin, Camilo M. Ferreira, Kim E. Ludwig, Minami Sasaki, Sean D. Connell Article in Journal/Newspaper Ocean acidification The University of Adelaide: Digital Library Ferreira ENVELOPE(-62.050,-62.050,-64.600,-64.600) New Zealand PLOS Biology 19 1 e3001033
institution Open Polar
collection The University of Adelaide: Digital Library
op_collection_id ftunivadelaidedl
language English
topic Animals
Fishes
Acids
Carbon Dioxide
Ecosystem
Biodiversity
Seawater
Population Growth
Reproduction
Hydrogen-Ion Concentration
New Zealand
Oceans and Seas
Female
Male
Sexual Behavior
Animal
Stress
Physiological
Climate Change
spellingShingle Animals
Fishes
Acids
Carbon Dioxide
Ecosystem
Biodiversity
Seawater
Population Growth
Reproduction
Hydrogen-Ion Concentration
New Zealand
Oceans and Seas
Female
Male
Sexual Behavior
Animal
Stress
Physiological
Climate Change
Nagelkerken, I.
Alemany, T.
Anquetin, J.M.
Ferreira, C.M.
Ludwig, K.E.
Sasaki, M.
Connell, S.D.
Ocean acidification boosts reproduction in fish via indirect effects
topic_facet Animals
Fishes
Acids
Carbon Dioxide
Ecosystem
Biodiversity
Seawater
Population Growth
Reproduction
Hydrogen-Ion Concentration
New Zealand
Oceans and Seas
Female
Male
Sexual Behavior
Animal
Stress
Physiological
Climate Change
description Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO₂ are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO₂ vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO₂ on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO₂ vents, which may further boost reproductive success. These positive indirect effects of elevated CO₂ were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean. Ivan Nagelkerken, Tiphaine Alemany, Julie M. Anquetin, Camilo M. Ferreira, Kim E. Ludwig, Minami Sasaki, Sean D. Connell
author2 Buckley, Y.
format Article in Journal/Newspaper
author Nagelkerken, I.
Alemany, T.
Anquetin, J.M.
Ferreira, C.M.
Ludwig, K.E.
Sasaki, M.
Connell, S.D.
author_facet Nagelkerken, I.
Alemany, T.
Anquetin, J.M.
Ferreira, C.M.
Ludwig, K.E.
Sasaki, M.
Connell, S.D.
author_sort Nagelkerken, I.
title Ocean acidification boosts reproduction in fish via indirect effects
title_short Ocean acidification boosts reproduction in fish via indirect effects
title_full Ocean acidification boosts reproduction in fish via indirect effects
title_fullStr Ocean acidification boosts reproduction in fish via indirect effects
title_full_unstemmed Ocean acidification boosts reproduction in fish via indirect effects
title_sort ocean acidification boosts reproduction in fish via indirect effects
publisher Public Library of Science (PLoS)
publishDate 2021
url http://hdl.handle.net/2440/129981
https://doi.org/10.1371/journal.pbio.3001033
long_lat ENVELOPE(-62.050,-62.050,-64.600,-64.600)
geographic Ferreira
New Zealand
geographic_facet Ferreira
New Zealand
genre Ocean acidification
genre_facet Ocean acidification
op_source http://dx.doi.org/10.1371/journal.pbio.3001033
op_relation http://purl.org/au-research/grants/arc/FT120100183
http://purl.org/au-research/grants/arc/DP170101722
http://purl.org/au-research/grants/arc/FT0991953
PLoS Biology, 2021; 19(1):1-21
1544-9173
1545-7885
http://hdl.handle.net/2440/129981
doi:10.1371/journal.pbio.3001033
Nagelkerken, I. [0000-0003-4499-3940]
Sasaki, M. [0000-0002-4832-2573]
Connell, S.D. [0000-0002-5350-6852]
op_rights © 2021 Nagelkerken et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
op_doi https://doi.org/10.1371/journal.pbio.3001033
container_title PLOS Biology
container_volume 19
container_issue 1
container_start_page e3001033
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