Mechanisms Involving Sensory Pathway Steps Inform Impacts of Global Climate Change on Ecological Processes

Rivest, Emily B.; Jellison, Brittany M.; Ng, Gabriel; Satterthwaite, Erin V.; Bradley, Hannah L.; Williams, Susan L.; Gaylord, Brian

doi:10.3389/fmars.2019.00346

Cited by 15 publications

(12 citation statements)

References 155 publications

(199 reference statements)

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“…Even though we predicted an overall increase in the amount of suitable habitat for mackerel sharks at the end of the 21st century, temperature acclimatization comes with an energetic cost that impacts other functions such as reproduction, growth, foraging and swimming. Changes in the marine environment may result in novel ecosystems requiring predators to alter foraging behaviors and adapt to new prey species (Nagelkerken and Munday, 2016;Rivest et al, 2019). Under such stresses, individuals become less competitive with decreases in reproduction and population density (Beaugrand and Kirby, 2018) and may exploit habitat heterogeneity by undertaking vertical migrations to suitable temperatures to maximize biological efficiency and minimize physiological adjustment costs (Chin et al, 2010;Beaugrand and Kirby, 2018).…”

Section: Discussionmentioning

confidence: 99%

Future Distribution of Suitable Habitat for Pelagic Sharks in Australia Under Climate Change Models

et al. 2020

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Global oceans are absorbing over 90% of the heat trapped in our atmosphere due to accumulated anthropogenic greenhouse gases, resulting in increasing ocean temperatures. Such changes may influence marine ectotherms, such as sharks, as their body temperature concurrently increases toward their upper thermal limits. Sharks are high trophic level predators that play a key role in the regulation of ecosystem structure and health. Because many sharks are already threatened, it is especially important to understand the impact of climate change on these species. We used shark occurrence records collected by commercial fisheries within the Australian continental Exclusive Economic Zone (EEZ) to predict changes in future (2050-2099) relative to current (1956-2005) habitat suitability for pelagic sharks based on an ensemble of climate models and emission scenarios. Our predictive models indicate that future sea temperatures are likely to shift the location of suitable shark habitat within the Australian EEZ. On average, suitable habitat is predicted to decrease within the EEZ for requiem and increase for mackerel sharks, however, the direction and severity of change was highly influenced by the choice of climate model. Our results indicate the need to consider climate change scenarios as part of future shark management and suggest that more broad-scale studies are needed for these pelagic species.

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Section: Discussionmentioning

confidence: 99%

Future Distribution of Suitable Habitat for Pelagic Sharks in Australia Under Climate Change Models

et al. 2020

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“…Ocean acidification has been suggested to have detrimental effects on olfactory driven behaviour of fish, and other marine organisms, including food-search, predator avoidance and homing/selection of settling sites (reviewed in Kelley et al, 2018;Leduc et al, 2013;Rivest et al, 2019). In contrast to freshwater fish, in marine fish the mechanism has been suggested to be due to central nervous effects, particularly on GABA A receptor function (Nilsson et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Independent effects of seawater pH and high PCO2 on olfactory sensitivity in fish: possible role of carbonic anhydrase

Velez

Costa

Wang

et al. 2021

Journal of Experimental Biology

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Ocean acidification may alter olfactory-driven behaviour in fish by direct effects on the peripheral olfactory system; olfactory sensitivity is reduced in CO2-acidified seawater. The current study tested whether this is due to elevated PCO2 or the consequent reduction in seawater pH and, if the former, investigate the possible involvement of carbonic anhydrase, the enzyme responsible for the hydration of CO2 and production of carbonic acid. Olfactory sensitivity to amino acids was assessed by extracellular multi-unit recording from the olfactory nerve of the gilthead seabream (Sparus auratus L,) in normal seawater (pH ∼8.2), and after acute exposure to acidified seawater (pH ∼7.7, but normal PCO2; ∼340 µatm) and high PCO2 seawater (∼1400 µatm) at normal pH (∼8.2). Reduced pH in the absence of elevated PCO2 caused reduction in olfactory sensitivity to L-serine, L-leucine, L-arginine and L-glutamine, but not L-glutamic acid. Increased PCO2 in the absence of changes in pH caused reduced olfactory sensitivity to L-serine, L-leucine and L-arginine, including increases in their thresholds of detection, but had no effect on sensitivity to L-glutamine and L-glutamic acid. Inclusion of 1 mM acetazolamide (a membrane-permeant inhibitor of carbonic anhydrase) in the seawater reversed the inhibition of olfactory sensitivity to L-serine caused by high PCO2. Ocean acidification may reduce olfactory sensitivity by reduction in seawater pH and intracellular pH (of olfactory receptor neurones); the former by reducing odorant-receptor affinity, and the latter by reducing the efficiency of olfactory transduction. The physiological role of carbonic anhydrase in the olfactory receptor neurones remains to be explored.

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“…The costs associated with decreased olfactory abilities include physiological, behavioural and unquantified energetic costs incurred by maintaining or increasing signal production while coping with physiological stress (Rivest et al, 2019), as described for Carcinus maenas (Reid et al, 1997). However, most of these costs have not been proven directly (Nagelkerken et al, 2019).…”

Section: Wider Effects and Knowledge Gapsmentioning

confidence: 99%

“…Furthermore, the evolution of chemical signalling systems will be slow and costly if it involves changes to odorant production pathways and active sites in receptors. Receptor plasticity and changes to selection are known to drive odorant-receptor evolution in insects but this remains unproven in aquatic organisms (Rivest et al, 2019). Evidence for adaptation of olfactory systems to acidification stress is lacking, even in studies of CO 2 vent systems, which may be thousands of years old.…”

Section: Wider Effects and Knowledge Gapsmentioning

confidence: 99%

Acidification can directly affect olfaction in marine organisms

Porteus

Roggatz

Velez

et al. 2021

Journal of Experimental Biology

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In the past decade, many studies have investigated the effects of low pH/high CO2 as a proxy for ocean acidification on olfactory-mediated behaviours of marine organisms. The effects of ocean acidification on the behaviour of fish vary from very large to none at all, and most of the maladaptive behaviours observed have been attributed to changes in acid–base regulation, leading to changes in ion distribution over neural membranes, and consequently affecting the functioning of gamma-aminobutyric acid-mediated (GABAergic) neurotransmission. Here, we highlight a possible additional mechanism by which ocean acidification might directly affect olfaction in marine fish and invertebrates. We propose that a decrease in pH can directly affect the protonation, and thereby, 3D conformation and charge distribution of odorants and/or their receptors in the olfactory organs of aquatic animals. This can sometimes enhance signalling, but most of the time the affinity of odorants for their receptors is reduced in high CO2/low pH; therefore, the activity of olfactory receptor neurons decreases as measured using electrophysiology. The reduced signal reception would translate into reduced activation of the olfactory bulb neurons, which are responsible for processing olfactory information in the brain. Over longer exposures of days to weeks, changes in gene expression in the olfactory receptors and olfactory bulb neurons cause these neurons to become less active, exacerbating the problem. A change in olfactory system functioning leads to inappropriate behavioural responses to odorants. We discuss gaps in the literature and suggest some changes to experimental design in order to improve our understanding of the underlying mechanisms and their effects on the associated behaviours to resolve some current controversy in the field regarding the extent of the effects of ocean acidification on marine fish.

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Mechanisms Involving Sensory Pathway Steps Inform Impacts of Global Climate Change on Ecological Processes

Cited by 15 publications

References 155 publications

Future Distribution of Suitable Habitat for Pelagic Sharks in Australia Under Climate Change Models

Future Distribution of Suitable Habitat for Pelagic Sharks in Australia Under Climate Change Models

Independent effects of seawater pH and high PCO2 on olfactory sensitivity in fish: possible role of carbonic anhydrase

Acidification can directly affect olfaction in marine organisms

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