Ocean acidification affects marine chemical communication by changing structure and function of peptide signalling molecules

Ocean acidification is a global challenge that faces marine organisms in the near future with a predicted rapid drop in pH of up to 0.4 units by the end of this century. Effects of the change in ocean carbon chemistry and pH on the development, growth and fitness of marine animals are well documented. Recent evidence also suggests that a range of chemically mediated behaviours and interactions in marine fish and invertebrates will be affected. Marine animals use chemical cues, for example, to detect predators, for settlement, homing and reproduction. But while effects of high CO₂ conditions on these behaviours are described across many species, little is known about the underlying mechanisms, particularly in invertebrates. Here we investigate the direct influence of future oceanic pH conditions on the structure and function of three peptide signalling molecules with an interdisciplinary combination of methods. NMR spectroscopy and quantum chemical calculations were used to assess the direct molecular influence of pH on the peptide cues and we tested the functionality of the cues in different pH conditions using behavioural bioassays with shore crabs (Carcinus maenas) as a model system. We found that peptide signalling cues are susceptible to protonation in future pH conditions, which will alter their overall charge. We also show that structure and electrostatic properties important for receptor-binding differ significantly between the peptide forms present today and the protonated signalling peptides likely to be dominating in future oceans. The bioassays suggest an impaired functionality of the signalling peptides at low pH. Physiological changes due to high CO₂ conditions were found to play a less significant role in influencing the investigated behaviour. From our results we conclude that the change of charge, structure and consequently function of signalling molecules presents one possible mechanism to explain altered behaviour under future oceanic pH conditions

Swarms of swift scavengers: ecological role of marine intertidal hermit crabs in California

This is the author accepted manuscript. The final version is available from Springer via http://dx.doi.org/10.1007/s00227-015-2639-3While marine hermit crabs are well known for being omnivorous filter feeders, less is known about the role they may play as active carrion scavengers in intertidal ecosystems. Prior studies have revealed that intertidal hermit crabs can be attracted to chemical cues from predated gastropods. Yet their attraction is usually assumed to be driven primarily by the availability of new shells rather than by food. We conducted field experiments to assess hermit crabs’ potential role as generalist carrion scavengers on the California Coast, examining their speed of attraction and the size of the aggregations they formed in response to chemical cues from freshly smashed gastropods and mussels, both of which indicated available carrion. Compared to all other marine species, hermit crabs (Pagurus samuelis, P. hirsutiusculus, and P. granosimanus) were the fastest to arrive at the provisioning sites. Hermit crabs also dominated the provisioning sites, accumulating in the largest numbers, with aggregations of up to 20 individuals, which outcompeted all other scavengers for carrion. Notably, hermit crabs arrived equally quickly for both smashed gastropod and mussel, even though the latter does not offer suitable shells for hermit crabs and even though the former only yields shell-related chemical cues over time frames longer than our experiments. These results thus suggest that shell availability is not the only, or even the primary, reason marine intertidal hermit crabs aggregate at carrion sites; they also aggregate to forage, thereby playing an important role as active carrion scavengers in intertidal ecosystems.Research was supported by funding from the Miller Institute at Berkeley to M.L

Hermit crabs as model species for investigating the behavioural responses to pollution

Human impacts on the environment affect organisms at all levels of biological organisation and ultimately can change their phenotype. Over time, phenotypic change may arise due to selection but individual phenotypes are also subject to change via genotype × environment interactions. In animals, behaviour is the most flexible aspect of phenotype, and hence the most liable to change across environmental gradients including exposure to pollution. Here we review current knowledge on the impacts of pollution, broadly defined to include the release of substances, energy, and the effects of carbon emissions, on the behaviour of a highly studied group, the globally distributed hermit crabs. We first show how their obligate association with empty gastropod shells underpins their use as model organisms for the study of resource-assessment, contest, and risk-coping behaviours. Intense study of hermit crabs has advanced our understanding of how animals use information, and we discuss the ways in which pollutants can disrupt the cognitive processes involved. We then highlight current studies of hermit crabs, which paint a clear picture of behavioural changes due to multiple pollutants. Impacts on behaviour vary across pollutants and entire suites of behaviours can be influenced by a single pollutant, with the potential for interactive and cascade effects. Hermit crabs offer the opportunity for detailed behavioural analysis, including application of the repeated measures animal-personality framework, and they are highly amenable to experimental manipulations. As such, we show how they now provide a model system for studying the impacts of pollution on behaviour, yielding insights broadly applicable across animal diversity

The behavioural consequences of reduced sea water pH in decapod crustaceans

The studies presented in this thesis were designed to investigate the effects of reduced sea water pH on the behaviour of intertidal decapod crustaceans, both within the context of the variations occurring naturally in the pH of rock pool habitats, and in relation to predicted changes to ocean pH resulting from ocean acidification and potential carbon dioxide (CO2) leaks from carbon capture storage (CCS) sites. Recent studies on marine fish have shown behavioural disruptions as a result of increased CO2 concentrations in sea water and reduced pH, but the effects on crustaceans are as yet unknown. The first two studies investigated the effects of reduced pH upon the olfactory behaviour of the prawn Palaemon elegans and the hermit crab Pagurus bernhardus, focussing on their responses to food odours. Short-term (five day) exposures to highly reduced pH (pHNBS = 6.60, 6.80) revealed disruptions to the chemo-sensory behaviour of both species with a reduction in their ‘sniffing’ response, and the inability of P. bernhardus to locate the chemical cue. This was also accompanied by elevated haemolymph chloride ions. in In a further study P. bernhardus was subjected to a longer exposure (60 days) and to a range of pH levels (pHNBS = 8.00, 7.90, 7.70, 7.35 and 6.80) in order to detect a threshold for the behavioural disruptions observed, and to determine if there would be any sign of acclimation over a longer period. A clear gradient in the disruptions to the chemo-sensory responses and survival rates of the hermit crabs, and disruption to a physiological marker (elevated haemolymph calcium ions), was found. Possible thresholds for disruption were also identified at levels that match predictions for ocean acidification and leaks from proposed CO2 CCS sites. Some of the crabs in the lower pH treatments exhibited a recovery in their responses by day 60, possibly indicating an acclimation effect. The presence of disruption to haemolymph ion concentrations in both the short and longer term hermit crab studies suggest a mechanism for behavioural disruption. In a final study the effects of reduced sea water pH on a more complex behaviour, involving decision making, was investigated. Reduced sea water pH was shown to disrupt the shell assessment and selection behaviour of P. bernhardus affecting its decision making processes, although not all crabs were affected in the same way. The work presented here therefore demonstrates that reduced sea water pH could have disruptive effects upon both information gathering, via chemo-sensory processes, and decision making in intertidal crustaceans. The mechanism responsible is unlikely to be due to changes in the odour molecule, or physical damage to receptor organs. Rather the observed disruptions could be due (a) to ionic changes, causing metabolic depression or interference with neurotransmitter function, or (b) to disruption to chemoreception per se. Such disturbances to key behavioural processes have implications for inter and intraspecific species interactions and population dynamics in the marine environment. Changes in pH are already experienced by intertidal animals for short periods when rock pools are emersed, but future anthropogencially-induced reductions in sea water pH are likely to cause more sustained and widespread disruptions with, as yet, unpredictable consequences. The differential responses observed between individuals in these studies may warrant further investigation as such differences may provide the basis for selection and adaptation to projected changes in ocean pH