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. Living in intertidal environments, hermit crabs face large pH fluctuations in their current habitat in addition to climate-change related ocean acidification. We demonstrate that the dietary predator cue PEA for mammals and sea lampreys is an attractant for hermit crabs, with the potency of the cue increasing with decreasing pH levels. 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.

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).…”

“…The observed lower antennular flicking rates in response to chemical cues with high CO 2 exposure is consistent with work on intertidal (de la Haye et al, 2012) and deep‐sea (Kim et al, 2016) hermit crabs despite a ~10‐fold difference in p CO 2 levels between these studies and ours, which reflects the distinct marine ecosystems that these crabs inhabit. Whether reduced antennular flicking with cadaverine is the result of changes in the structure of the odorant in low pH altering perception and detection, the energetic demands of living in elevated CO 2 (Porteus et al, 2021; Roggatz et al, 2016; Schirrmacher et al, 2020), or decreased sensitivity to chemical cues (Porteus et al, 2018) in the marine environment, high CO 2 levels has a negative impact on this important olfactory response.…”

“…A decrease in sensitivity and a lower detection threshold of the olfactory nerve of marine fishes exposed to elevated CO 2 corresponded with a reduction in anti‐predator behavioural responses (Porteus et al, 2018, 2021; Velez et al, 2019), suggesting parallel mechanisms of olfactory impairment does occur across different marine animal phyla with ocean acidification. pH‐dependent effects on odorant molecule conformation, protonation state, odorant receptor–ligand binding, and potency are also potential mechanisms for the impacts of ocean acidification on the sense of smell of marine animals (Porteus et al, 2021; Roggatz et al, 2016; Schirrmacher et al, 2020). Cadaverine (C 5 H 16 N 2 2+ ) and ammonium (NH 4 + ) are both ionic compounds with pH‐dependent speciation (National Center for Biotechnology Information, 2022), and in this study each compound was dissolved in either clean control seawater or clean CO 2 ‐acidified seawater before being applied to the antennules of control or elevated CO 2 ‐exposed crabs, respectively.…”

“…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, 2011, 2012; Dodd et al, 2015; Kim et al, 2016; Manríquez et al, 2021; Richardson et al, 2021; Schirrmacher et al, 2020; Wang et al, 2018). To date, the physiology, morphology, and gene expression underlying sensory impairment leading to maladaptive olfactory‐mediated behaviours associated with ocean acidification remain largely unknown in aquatic crustaceans.…”

Becoming nose‐blind—Climate change impacts on chemical communication

“…Electrophysiological and transcriptomic measurements show that elevated CO 2 levels impair the olfactory system of sea bass (Porteus et al, 2018) and sea bream (Velez et al, 2019) (D). The altered chemoreception can be attributed to changes in the infochemical (C), the olfactory receptor or the olfactory epithelium (Schirrmacher et al, 2021; Velez et al, 2019) (D). Additionally, ocean acidification has been shown to interfere with neurotransmitter functioning as the internal compensation for elevated CO 2 conditions can lead to altered brain ion gradients (Nilsson et al, 2012) (E and F).…”