Behavioural stress feedback loops in benthic invertebrates caused by pH drop-induced metabolites
Preprint posted on 18 April 2021 https://www.biorxiv.org/content/10.1101/2021.04.16.440165v1
Article now published in Frontiers in Marine Science at http://dx.doi.org/10.3389/fmars.2021.773870
Ocean acidification can directly as well as indirectly affect feeding and avoidance behavior in the benthic community.Selected by Fouzia Haider
Ocean acidification or pH drop is progressing at an alarming rate and poses a great threat to intertidal benthic organisms. A constant shift in water pH level compels these organisms to live at their physiological tolerance limit, making them interesting model species to study the effects of climate change. These organisms rely on different behavioral and physiological pathways to avoid and/or adjust to these changes, among which chemical signaling is a crucial one. However, ocean acidification can disrupt this chemical signaling in the aquatic environment and thus requires more scientific attention.
Although the effect of biotic stressors on chemical communication has been studied in the past, the effect of abiotic stressors, such as pH drop, is still not well studied. Here, Feugere et al. studied the direct and indirect effects of pH drop using a ‘stress metabolite’ approach from conspecific and heterospecific donors to understand the importance of chemical signaling and their dissemination capabilities. Upon dissemination, stress metabolites can cause an indirect stress propagation in the conspecifics and/or heterospecifics creating a positive feedback-loop. Therefore, the authors hypothesize that an acute pH drop will both directly and indirectly cause behavioral change in their sample species (small hermit crab Diogenes pugilator, green shore crab Carcinus maenas, and harbor ragworm Hediste diversicolor).
To test this hypothesis, they exposed the sample species to control pH 8.2 with control metabolite (CM), pH drop 7.6 with control metabolite (pH drop), control pH 8.2 with stress metabolite (SM), and pH 7.6 with stress metabolite (pH drop+SM). The authors also tested the effect of SM from their vertebrate predator gilt-head sea bream Sparus aurata on each sample species. The effects of aforementioned treatments were investigated on the escape mechanisms and ‘time-to-success’ (the time to find a feeding cue for crabs and to bury the head entirely in the sediment for ragworm).
In the small hermit crab, Diogenes pugilator, time-to-success was significantly affected by pH drop and SM from S. aurata (Fig. 1B). Avoidance response in D. pugilator was significantly higher in response to SM from S. aurata (69%), but pH drop did not have any effect (Fig. 2). In green shore crab, Carcinus maenas, time-to-success was not affected by any of the four treatments when exposed to SM from conspecifics. However, when S. aurata was the metabolite donor, lower feeding success was noticed in response to pH drop and SM (Fig. 1). Similarly, when exposed to metabolites from conspecific donor, no effect of CM, pH drop, SM, and pH drop+SM was significant on the avoidance response of C. maenas, but exposure to S. aurata metabolites caused a significant increase in their avoidance activity in pH drop, SM and pH drop+SM treatments (Fig. 2).
Figure 1: Effect of pH drop and donor specific stress metabolite on feeding cue of hermit crab, green shore crab, and harbor ragworm. (B) Interaction of pH drop and donor specific stress metabolite on time-to-success. (C) Kaplan-Meier curves visualizing success probability under each experimental condition over time.
Figure 2: Effects of pH drop and donor specific stress metabolites on the avoidance behavior of hermit crab, green shore crab, and harbor ragworms. (A) Interaction of pH drop and donor specific stress metabolites (conspecific SM first window; heterospecific SM second window) on hermit crab (first column), green shore crab (middle column), and harbor ragworm (third column). (B) Split bars represent the presence (dark area) and absence (light area) of avoidance behavior in the hermit crab, green shore crab, and harbor ragworm.
In case of harbor ragworm, Hediste diversicolor, time-to-success did not depend on donor species, but pH drop and SM had a significant negative impact (Fig. 1B). The effect of conspecific metabolite donor on the burrowing success score of H. diversicolor was more pronounced than that of heterospecific metabolites. Conversely to their time-to-success, their avoidance response was much pronounced when exposed to S. aurata metabolites compared to conspecific metabolites. H. diversicolor exposed to S. aurata metabolite showed different avoidance responses in different treatment group (CM, pH drop, SM, and pH drop+SM) (Fig. 2).
What I like about this preprint
In this preprint the authors tried to unveil the role of chemical signaling in response to an abiotic stressor, pH drop. Climate change is progressively challenging the organisms living in the intertidal zone by impacting the abiotic parameters of the water, and ocean acidification or pH drop is among one of them. The fact that the authors studied the effect of pH drop on an intra- and interspecific level using stress metabolites sheds new light on the study of metabolomics and its importance on the study of eco-physiology. This study also allows us to think about how stress metabolites can propagate from an individual to a population level and create awareness among different organisms.
Future implications and questions to authors
It is very intriguing that the time-to-success and avoidance mechanisms was different depending on the metabolite donors. As the heterospecific metabolite donor caused a difference in the measured parameters, how different was the metabolite composition from S. aurata compared to the conspecific metabolite composition?
What metabolites were the dominant ones and how do these metabolites create an awareness (in which potential pathways) to the studied organisms?
The effects of pH drop on small hermit crab and ragworm are more pronounce compared to green shore crab. Is it possible that this is due to the mobility of the chosen sample species; ragworm and hermit crab having less mobility than shore crab?
Posted on: 19 May 2021 , updated on: 21 May 2021
doi: https://doi.org/10.1242/prelights.29062Read preprint
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