Toward a Mechanistic Understanding of Marine Invertebrate Behavior at Elevated CO2

Thomas, Jodi T.; Munday, Philip L.; Watson, Sue‐Ann

doi:10.3389/fmars.2020.00345

Cited by 20 publications

(30 citation statements)

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“…Recent studies show that increased pCO 2 levels can affect the growth, survivorship and physiology of some marine fishes [3][4][5][6][7]. Elevated CO 2 has also been shown to alter behaviours in a wide variety of fish [8][9][10] and invertebrates [11][12][13]. However, most experimental studies focus on short-term exposure to elevated pCO 2 and do not account for phenotypic variation that may enable populations to adapt over the time scale at which OA will occur [2,14].…”

Section: Introductionmentioning

confidence: 99%

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Molecular basis of parental contributions to the behavioural tolerance of elevated pCO₂in a coral reef fish

et al. 2021

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Knowledge of adaptive potential is crucial to predicting the impacts of ocean acidification (OA) on marine organisms. In the spiny damselfish, Acanthochromis polyacanthus , individual variation in behavioural tolerance to elevated pCO 2 has been observed and is associated with offspring gene expression patterns in the brain. However, the maternal and paternal contributions of this variation are unknown. To investigate parental influence of behavioural pCO 2 tolerance, we crossed pCO 2 -tolerant fathers with pCO 2 -sensitive mothers and vice versa, reared their offspring at control and elevated pCO 2 levels, and compared the juveniles' brain transcriptional programme. We identified a large influence of parental phenotype on expression patterns of offspring, irrespective of environmental conditions. Circadian rhythm genes, associated with a tolerant parental phenotype, were uniquely expressed in tolerant mother offspring, while tolerant fathers had a greater role in expression of genes associated with histone binding. Expression changes in genes associated with neural plasticity were identified in both offspring types: the maternal line had a greater effect on genes related to neuron growth while paternal influence impacted the expression of synaptic development genes. Our results confirm cellular mechanisms involved in responses to varying lengths of OA exposure, while highlighting the parental phenotype's influence on offspring molecular phenotype.

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Section: Introductionmentioning

confidence: 99%

“…affect the growth, survivorship and physiology of some marine fishes [3][4][5][6][7]. Elevated CO 2 has also been shown to alter behaviours in a wide variety of fish [8][9][10] and invertebrates [11][12][13]. However, most experimental studies…”

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confidence: 99%

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO₂in a coral reef fish

et al. 2021

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“…Elevated CO 2 levels are known to alter a range of behaviours in a variety of fishes (Munday et al, 2019). Elevated CO 2 -induced behavioural alterations also occur in some marine invertebrates, including in cnidarians, polychaetes, echinoderms, arthropods and molluscs, across a variety of behavioural traits (reviewed in Clements and Hunt, 2015;Nagelkerken and Munday, 2015;Thomas et al, 2020). The behavioural effects of elevated CO 2 are variable.…”

Section: Introductionmentioning

confidence: 99%

“…A mechanistic understanding of behavioural change at elevated CO 2 is important to determine why there is such variability in behavioural alterations and to identify which animals will be most vulnerable to rising CO 2 levels. However, the mechanisms underlying behavioural change at elevated CO 2 across the diverse range of marine invertebrates are poorly understood (Thomas et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

The role of ligand-gated chloride channels in behavioural alterations at elevated CO2 in a cephalopod

Thomas

Spady

Munday

et al. 2021

Journal of Experimental Biology

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Projected future carbon dioxide (CO2) levels in the ocean can alter marine animal behaviours. Disrupted functioning of γ-aminobutyric acid type A (GABAA) receptors (ligand-gated chloride channels) is suggested to underlie CO2-induced behavioural changes in fish. However, the mechanisms underlying behavioural changes in marine invertebrates are poorly understood. We pharmacologically tested the role of GABA-, glutamate-, acetylcholine- and dopamine-gated chloride channels in CO2-induced behavioural changes in a cephalopod, the two-toned pygmy squid (Idiosepius pygmaeus). We exposed squid to ambient (∼450 µatm) or elevated (∼1,000 µatm) CO2 for seven days. Squid were treated with sham, the GABAA receptor antagonist gabazine, or the non-specific GABAA receptor antagonist picrotoxin, before measurement of conspecific-directed behaviours and activity levels upon mirror exposure. Elevated CO2 increased conspecific-directed attraction and aggression, as well as activity levels. For some CO2-affected behaviours, both gabazine and picrotoxin had a different effect at elevated compared to ambient CO2, providing robust support for the GABA hypothesis within cephalopods. In another behavioural trait, picrotoxin but not gabazine had a different effect in elevated compared to ambient CO2, providing the first pharmacological evidence, in fish and marine invertebrates, for altered functioning of ligand-gated chloride channels, other than the GABAA R, underlying CO2-induced behavioural changes. For some other behaviours, both gabazine and picrotoxin had a similar effect in elevated and ambient CO2, suggesting altered function of ligand-gated chloride channels was not responsible for these CO2-induced changes. Multiple mechanisms may be involved, which could explain the variability in the CO2 and drug treatment effects across behaviours.

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“…While this may mean that intertidal species are more resilient to climate change due to their acquired tolerances of pH fluctuations, it also forces them to live more frequently near their inhabiting intertidal areas are interesting models to study the effects of short-term pH fluctuations within the IPCC predicted range. A low environmental pH can directly alter animal behaviour through several pathways, which include (i) deviation of energy budgets toward the stress response (Pörtner, 2008), (ii) fleeing to avoid the sources of stress (Pörtner and Peck, 2010;Abreu et al, 2016), (iii) disrupted information detection and processing leading to impaired decision-making (Briffa et al, 2012;Porteus et al, 2018;Thomas et al, 2020;Cothran et al, 2021), and (iv) alteration of the chemical signals themselves impacting the sensory environment and the transfer of information (Wyatt et al, 2014;Roggatz et al, 2016Roggatz et al, , 2019. Behavioural effects triggered by lowered pH are known to occur in different taxonomic groups such as crustaceans (de la Haye et al, 2011), marine ragworms (Bond, 2018), and fish (Munday et al, 2009), although recent research debates both their ubiquitousness and effect size (Clark et al, 2020a;Clements et al, 2020a,b, but see Clark et al, 2020b;Munday et al, 2020;Williamson et al, 2021 for the importance of which comparisons are made).…”

Section: Introductionmentioning

confidence: 99%

Behavioural Stress Propagation in Benthic Invertebrates Caused by Acute pH Drop-Induced Metabolites

Feugere

et al. 2021

Front. Mar. Sci.

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Studies on pH stress in marine animals typically focus on direct or species-specific aspects. We here test the hypothesis that a drop to pH = 7.6 indirectly affects the intra- and interspecific interactions of benthic invertebrates by means of chemical communication. We recorded fitness-relevant behaviours of small hermit crabs Diogenes pugilator, green shore crabs Carcinus maenas, and harbour ragworms Hediste diversicolor in response to short-term pH drop, and to putative stress metabolites released by conspecifics or gilt-head sea bream Sparus aurata during 30 min of acute pH drop. Not only did acute pH drop itself impair time to find a food cue in small hermit crabs and burrowing in harbour ragworms, but similar effects were observed under exposure to pH drop-induced stress metabolites. Stress metabolites from S. aurata, but not its regular control metabolites, also induced avoidance responses in all recipient species. Here, we confirm that a short-term abrupt pH drop, an abiotic stressor, has the capacity to trigger the release of metabolites which induce behavioural responses in conspecific and heterospecific individuals, which can be interpreted as a behavioural cost. Our findings that stress responses can be indirectly propagated through means of chemical communication warrant further research to confirm the effect size of the behavioural impairments caused by stress metabolites and to characterise their chemical nature.

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Toward a Mechanistic Understanding of Marine Invertebrate Behavior at Elevated CO2

Cited by 20 publications

References 231 publications

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO₂in a coral reef fish

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO₂in a coral reef fish

The role of ligand-gated chloride channels in behavioural alterations at elevated CO2 in a cephalopod

Behavioural Stress Propagation in Benthic Invertebrates Caused by Acute pH Drop-Induced Metabolites

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Toward a Mechanistic Understanding of Marine Invertebrate Behavior at Elevated CO2

Cited by 20 publications

References 231 publications

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO2in a coral reef fish

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO2in a coral reef fish

The role of ligand-gated chloride channels in behavioural alterations at elevated CO2 in a cephalopod

Behavioural Stress Propagation in Benthic Invertebrates Caused by Acute pH Drop-Induced Metabolites

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Molecular basis of parental contributions to the behavioural tolerance of elevated pCO₂in a coral reef fish

Molecular basis of parental contributions to the behavioural tolerance of elevated pCO₂in a coral reef fish