Ocean Acidification Amplifies the Olfactory Response to 2-Phenylethylamine: Altered Cue Reception as a Mechanistic Pathway?

Abstract

With carbon dioxide (CO2) levels rising dramatically, climate change threatens marine environments. Due to increasing CO2 concentrations in the ocean, pH levels are expected to drop by 0.4 units by the end of the century. There is an urgent need to understand the impact of ocean acidification on chemical-ecological processes. To date, the extent and mechanisms by which the decreasing ocean pH influences chemical communication are unclear. Combining behaviour assays with computational chemistry, we explore the function of the predator related cue 2-phenylethylamine (PEA) for hermit crabs (Pagurus bernhardus) in current and end-of-the-century oceanic pH. We demonstrate that this dietary predator cue for mammals and sea lampreys is an attractant for hermit crabs. Furthermore, we show that the potency of the cue increases at pH levels expected for the year 2100. In order to explain this increased potency, we assess changes to PEA’s conformational and charge-related properties as one potential mechanistic pathway. Using quantum chemical calculations validated by NMR spectroscopy, we characterise the different protonation states of PEA in water. We show how protonation of PEA could affect receptor-ligand binding, using a possible model receptor for PEA (human TAAR1). Investigating potential mechanisms of pH dependent effects on olfactory perception of PEA and the respective behavioural response, our study advances the understanding of how ocean acidification interferes with the sense of smell and thereby might impact essential ecological interactions in marine ecosystems.

Behavioural stress feedback loops in benthic invertebrates caused by pH drop-induced metabolites

“…Here, we observed an increased escaping tendency of C. maenas in response to S. aurata control metabolites in pH drop but not in control pH. Although this was not the main focus of our study, it could mean that pH drop renders predator odour more potent for its prey, for example through pH-dependent changes in odour molecular structure, receptor binding, or information processing (Munday et al, 2009; Roggatz et al, 2016, 2019; Schirrmacher et al, 2020).…”

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

“…Here, we observed an increased escaping tendency of C. maenas in response to S. aurata control metabolites in pH drop but not in control pH. Although this was not the main focus of our study, it could mean that pH drop renders predator odour more potent for its prey, for example through pH-dependent changes in odour molecular structure, receptor binding, or information processing (Munday et al, 2009;Roggatz et al, 2016Roggatz et al, , 2019Schirrmacher et al, 2020). Our results contrast with earlier reports of decreased predator avoidance (e.g., in snails; see Jellison et al, 2016;Froehlich and Lord, 2020).…”

“…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). In addition, it should be mentioned that although there is little literature disentangling the behavioural effects of pH drop vs. high CO2, an increasing body of recent research evidenced the role of pH-dependent altered chemical communication (Roggatz et al, 2016;Schirrmacher et al, 2020;Porteus et al, 2021;Velez et al, 2021).…”

Ocean acidification alters foraging behaviour in Dungeness crab through impairment of the olfactory pathway

“…The olfactory systems of decapod crustaceans, in general, are considered to be similar (Harzsch & Krieger, 2018) suggesting parallel impacts of ocean acidification on olfaction can be expanded to other taxa. Lastly, an important consideration that cannot be discounted is the effect of seawater pH on the functionality of chemical cues that has been demonstrated to perturb the detection and perception of these cues, arising in altered behaviours of marine crabs (Porteus et al, 2021;Roggatz et al, 2016;Schirrmacher et al, 2020).…”

“…In crabs, reduced sea water pH has been shown to disrupt behaviours pertaining to decision-making and resource assessment (e.g. shell selection), egg ventilation, foraging and feeding, and predator-prey interactions (de la Haye et al, 2011Haye et al, , 2012Dodd et al, 2015;Kim et al, 2016;Manríquez et al, 2021;Richardson et al, 2021;Schirrmacher et al, 2020;Wang et al, 2018).…”