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...
Published in: | PLOS Biology |
---|---|
Main Authors: | , , , , , , |
Other Authors: | |
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 |
---|---|
record_format |
openpolar |
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 |
_version_ |
1785571822007222272 |