Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages

James W.E. Dickey; Neil E. Coughlan; Jaimie T.A. Dick; Vincent Médoc; Monica McCard; Peter R. Leavitt; Gérard Lacroix; Sarah Fiorini; Alexis Millot; Ross N. Cuthbert

doi:10.1007/s10530-021-02542-3

Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages

James W.E. Dickey^*, Neil E. Coughlan, Jaimie T.A. Dick, Vincent Médoc, Monica McCard, Peter R. Leavitt, Gérard Lacroix, Sarah Fiorini, Alexis Millot, Ross N. Cuthbert

^*Corresponding author for this work

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

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Abstract

The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species’ impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages.

Original language	English
Pages (from-to)	2831-2847
Number of pages	17
Journal	Biological Invasions
Volume	23
Issue number	9
DOIs	https://doi.org/10.1007/s10530-021-02542-3
Publication status	Published - 30 Apr 2021

Bibliographical note

Funding Information:
This project has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No 871081 (AQUACOSM) as well as financial support from the Regional Council of Ile-de-France under the DIM Program R2DS I-05-098/R and 2015-1657. It has received a support under the French program “Investissements d’Avenir” with the references ANR-10-EQPX-13-01 Planaqua and ANR-11-INBS-0001 AnaEE France. It has benefited from technical and human resources provided by CEREEP Ecotron IleDeFrance (CNRS/ENS UMS 3194), with JWED also supported by Inland Fisheries Ireland (IFI), RNC by the Alexander von Humboldt Foundation and Department for the Economy Northern Ireland, and NEC by Environmental Protection Agency (EPA). PRL thanks the Canada Research Chair program. Thanks also to the Natural Environment Research Council (NERC).

Publisher Copyright:
© 2021, Crown.

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

Climate change
Functional responses
Hypoxia
Invasive alien species
Neogobius melanostomus

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology

UN SDGs

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

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Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages
Copyright 2021 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited.
Final published version, 951 KBLicence: CC BY

Ecological impacts and behaviour interactions of the notorious invasive lionfish (Pterois volitans)
McCard, M. (Author), Kregting, L. (Supervisor) & Dick, J. (Supervisor), Dec 2023
Student thesis: Doctoral Thesis › Doctor of Philosophy

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Cite this

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title = "Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages",

abstract = "The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species{\textquoteright} impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages.",

keywords = "Climate change, Functional responses, Hypoxia, Invasive alien species, Neogobius melanostomus",

author = "Dickey, {James W.E.} and Coughlan, {Neil E.} and Dick, {Jaimie T.A.} and Vincent M{\'e}doc and Monica McCard and Leavitt, {Peter R.} and G{\'e}rard Lacroix and Sarah Fiorini and Alexis Millot and Cuthbert, {Ross N.}",

note = "Funding Information: This project has received funding from the European Union{\textquoteright}s Horizon 2020 research and innovation programme under grant agreement No 871081 (AQUACOSM) as well as financial support from the Regional Council of Ile-de-France under the DIM Program R2DS I-05-098/R and 2015-1657. It has received a support under the French program “Investissements d{\textquoteright}Avenir” with the references ANR-10-EQPX-13-01 Planaqua and ANR-11-INBS-0001 AnaEE France. It has benefited from technical and human resources provided by CEREEP Ecotron IleDeFrance (CNRS/ENS UMS 3194), with JWED also supported by Inland Fisheries Ireland (IFI), RNC by the Alexander von Humboldt Foundation and Department for the Economy Northern Ireland, and NEC by Environmental Protection Agency (EPA). PRL thanks the Canada Research Chair program. Thanks also to the Natural Environment Research Council (NERC). Publisher Copyright: {\textcopyright} 2021, Crown. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

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doi = "10.1007/s10530-021-02542-3",

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AU - Dickey, James W.E.

AU - Coughlan, Neil E.

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AU - Médoc, Vincent

AU - McCard, Monica

AU - Leavitt, Peter R.

AU - Lacroix, Gérard

AU - Fiorini, Sarah

AU - Millot, Alexis

AU - Cuthbert, Ross N.

N1 - Funding Information: This project has received funding from the European Union’s Horizon 2020 research and innovation programme under grant agreement No 871081 (AQUACOSM) as well as financial support from the Regional Council of Ile-de-France under the DIM Program R2DS I-05-098/R and 2015-1657. It has received a support under the French program “Investissements d’Avenir” with the references ANR-10-EQPX-13-01 Planaqua and ANR-11-INBS-0001 AnaEE France. It has benefited from technical and human resources provided by CEREEP Ecotron IleDeFrance (CNRS/ENS UMS 3194), with JWED also supported by Inland Fisheries Ireland (IFI), RNC by the Alexander von Humboldt Foundation and Department for the Economy Northern Ireland, and NEC by Environmental Protection Agency (EPA). PRL thanks the Canada Research Chair program. Thanks also to the Natural Environment Research Council (NERC). Publisher Copyright: © 2021, Crown. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/4/30

Y1 - 2021/4/30

N2 - The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species’ impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages.

AB - The influence of climate change on the ecological impacts of invasive alien species (IAS) remains understudied, with deoxygenation of aquatic environments often-overlooked as a consequence of climate change. Here, we therefore assessed how oxygen saturation affects the ecological impact of a predatory invasive fish, the Ponto-Caspian round goby (Neogobius melanostomus), relative to a co-occurring endangered European native analogue, the bullhead (Cottus gobio) experiencing decline in the presence of the IAS. In individual trials and mesocosms, we assessed the effect of high, medium and low (90%, 60% and 30%) oxygen saturation on: (1) functional responses (FRs) of the IAS and native, i.e. per capita feeding rates; (2) the impact on prey populations exerted; and (3) how combined impacts of both fishes change over invasion stages (Pre-invasion, Arrival, Replacement, Proliferation). Both species showed Type II potentially destabilising FRs, but at low oxygen saturation, the invader had a significantly higher feeding rate than the native. Relative Impact Potential, combining fish per capita effects and population abundances, revealed that low oxygen saturation exacerbates the high relative impact of the invader. The Relative Total Impact Potential (RTIP), modelling both consumer species’ impacts on prey populations in a system, was consistently higher at low oxygen saturation and especially high during invader Proliferation. In the mesocosm experiment, low oxygen lowered RTIP where both species were present, but again the IAS retained high relative impact during Replacement and Proliferation stages at low oxygen. We also found evidence of multiple predator effects, principally antagonism. We highlight the threat posed to native communities by IAS alongside climate-related stressors, but note that solutions may be available to remedy hypoxia and potentially mitigate impacts across invasion stages.

KW - Climate change

KW - Functional responses

KW - Hypoxia

KW - Invasive alien species

KW - Neogobius melanostomus

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DO - 10.1007/s10530-021-02542-3

M3 - Article

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VL - 23

SP - 2831

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JO - Biological Invasions

JF - Biological Invasions

IS - 9

ER -

Breathing space: deoxygenation of aquatic environments can drive differential ecological impacts across biological invasion stages

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

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Student theses

Ecological impacts and behaviour interactions of the notorious invasive lionfish (Pterois volitans)

Cite this