Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)

Abstract Elevated concentrations of CO 2 in seawater can disrupt numerous sensory systems in marine fish. This is of particular concern for Pacific salmon because they rely on olfaction during all aspects of their life including during their homing migrations from the ocean back to their natal strea...

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Published in:Global Change Biology
Main Authors: Williams, Chase R., Dittman, Andrew H., McElhany, Paul, Busch, D. Shallin, Maher, Michael T., Bammler, Theo K., MacDonald, James W., Gallagher, Evan P.
Other Authors: National Institute of Environmental Health Sciences, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Washington Sea Grant, University of Washington, National Oceanic and Atmospheric Administration, University of Washington
Format: Article in Journal/Newspaper
Language:English
Published: Wiley 2018
Subjects:
Online Access:http://dx.doi.org/10.1111/gcb.14532
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spelling crwiley:10.1111/gcb.14532 2024-06-23T07:55:54+00:00 Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch) Williams, Chase R. Dittman, Andrew H. McElhany, Paul Busch, D. Shallin Maher, Michael T. Bammler, Theo K. MacDonald, James W. Gallagher, Evan P. National Institute of Environmental Health Sciences National Marine Fisheries Service, National Oceanic and Atmospheric Administration Washington Sea Grant, University of Washington National Oceanic and Atmospheric Administration University of Washington National Marine Fisheries Service, National Oceanic and Atmospheric Administration 2018 http://dx.doi.org/10.1111/gcb.14532 https://api.wiley.com/onlinelibrary/tdm/v1/articles/10.1111%2Fgcb.14532 https://onlinelibrary.wiley.com/doi/pdf/10.1111/gcb.14532 https://onlinelibrary.wiley.com/doi/full-xml/10.1111/gcb.14532 https://onlinelibrary.wiley.com/doi/am-pdf/10.1111/gcb.14532 en eng Wiley http://onlinelibrary.wiley.com/termsAndConditions#am http://onlinelibrary.wiley.com/termsAndConditions#vor Global Change Biology volume 25, issue 3, page 963-977 ISSN 1354-1013 1365-2486 journal-article 2018 crwiley https://doi.org/10.1111/gcb.14532 2024-06-13T04:22:50Z Abstract Elevated concentrations of CO 2 in seawater can disrupt numerous sensory systems in marine fish. This is of particular concern for Pacific salmon because they rely on olfaction during all aspects of their life including during their homing migrations from the ocean back to their natal streams. We investigated the effects of elevated seawater CO 2 on coho salmon ( Oncorhynchus kisutch ) olfactory‐mediated behavior, neural signaling, and gene expression within the peripheral and central olfactory system. Ocean‐phase coho salmon were exposed to three levels of CO 2 , ranging from those currently found in ambient marine water to projected future levels. Juvenile coho salmon exposed to elevated CO 2 levels for 2 weeks no longer avoided a skin extract odor that elicited avoidance responses in coho salmon maintained in ambient CO 2 seawater. Exposure to these elevated CO 2 levels did not alter odor signaling in the olfactory epithelium, but did induce significant changes in signaling within the olfactory bulb. RNA‐Seq analysis of olfactory tissues revealed extensive disruption in expression of genes involved in neuronal signaling within the olfactory bulb of salmon exposed to elevated CO 2 , with lesser impacts on gene expression in the olfactory rosettes. The disruption in olfactory bulb gene pathways included genes associated with GABA signaling and maintenance of ion balance within bulbar neurons. Our results indicate that ocean‐phase coho salmon exposed to elevated CO 2 can experience significant behavioral impairments likely driven by alteration in higher‐order neural signal processing within the olfactory bulb. Our study demonstrates that anadromous fish such as salmon may share a sensitivity to rising CO 2 levels with obligate marine species suggesting a more wide‐scale ecological impact of ocean acidification. Article in Journal/Newspaper Ocean acidification Wiley Online Library Pacific Global Change Biology 25 3 963 977
institution Open Polar
collection Wiley Online Library
op_collection_id crwiley
language English
description Abstract Elevated concentrations of CO 2 in seawater can disrupt numerous sensory systems in marine fish. This is of particular concern for Pacific salmon because they rely on olfaction during all aspects of their life including during their homing migrations from the ocean back to their natal streams. We investigated the effects of elevated seawater CO 2 on coho salmon ( Oncorhynchus kisutch ) olfactory‐mediated behavior, neural signaling, and gene expression within the peripheral and central olfactory system. Ocean‐phase coho salmon were exposed to three levels of CO 2 , ranging from those currently found in ambient marine water to projected future levels. Juvenile coho salmon exposed to elevated CO 2 levels for 2 weeks no longer avoided a skin extract odor that elicited avoidance responses in coho salmon maintained in ambient CO 2 seawater. Exposure to these elevated CO 2 levels did not alter odor signaling in the olfactory epithelium, but did induce significant changes in signaling within the olfactory bulb. RNA‐Seq analysis of olfactory tissues revealed extensive disruption in expression of genes involved in neuronal signaling within the olfactory bulb of salmon exposed to elevated CO 2 , with lesser impacts on gene expression in the olfactory rosettes. The disruption in olfactory bulb gene pathways included genes associated with GABA signaling and maintenance of ion balance within bulbar neurons. Our results indicate that ocean‐phase coho salmon exposed to elevated CO 2 can experience significant behavioral impairments likely driven by alteration in higher‐order neural signal processing within the olfactory bulb. Our study demonstrates that anadromous fish such as salmon may share a sensitivity to rising CO 2 levels with obligate marine species suggesting a more wide‐scale ecological impact of ocean acidification.
author2 National Institute of Environmental Health Sciences
National Marine Fisheries Service, National Oceanic and Atmospheric Administration
Washington Sea Grant, University of Washington
National Oceanic and Atmospheric Administration
University of Washington
National Marine Fisheries Service, National Oceanic and Atmospheric Administration
format Article in Journal/Newspaper
author Williams, Chase R.
Dittman, Andrew H.
McElhany, Paul
Busch, D. Shallin
Maher, Michael T.
Bammler, Theo K.
MacDonald, James W.
Gallagher, Evan P.
spellingShingle Williams, Chase R.
Dittman, Andrew H.
McElhany, Paul
Busch, D. Shallin
Maher, Michael T.
Bammler, Theo K.
MacDonald, James W.
Gallagher, Evan P.
Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)
author_facet Williams, Chase R.
Dittman, Andrew H.
McElhany, Paul
Busch, D. Shallin
Maher, Michael T.
Bammler, Theo K.
MacDonald, James W.
Gallagher, Evan P.
author_sort Williams, Chase R.
title Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)
title_short Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)
title_full Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)
title_fullStr Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)
title_full_unstemmed Elevated CO 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( Oncorhynchus kisutch)
title_sort elevated co 2 impairs olfactory‐mediated neural and behavioral responses and gene expression in ocean‐phase coho salmon ( oncorhynchus kisutch)
publisher Wiley
publishDate 2018
url http://dx.doi.org/10.1111/gcb.14532
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https://onlinelibrary.wiley.com/doi/pdf/10.1111/gcb.14532
https://onlinelibrary.wiley.com/doi/full-xml/10.1111/gcb.14532
https://onlinelibrary.wiley.com/doi/am-pdf/10.1111/gcb.14532
geographic Pacific
geographic_facet Pacific
genre Ocean acidification
genre_facet Ocean acidification
op_source Global Change Biology
volume 25, issue 3, page 963-977
ISSN 1354-1013 1365-2486
op_rights http://onlinelibrary.wiley.com/termsAndConditions#am
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op_doi https://doi.org/10.1111/gcb.14532
container_title Global Change Biology
container_volume 25
container_issue 3
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