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

Abstract

Studies on pH stress in marine animals typically focus on direct or species-specific aspects. We here test the hypothesis that a drop to pH = 7.6 indirectly affects the intra- and interspecific interactions of benthic invertebrates by means of chemical communication. We recorded fitness-relevant behaviours of small hermit crabs Diogenes pugilator, green shore crabs Carcinus maenas, and harbour ragworms Hediste diversicolor in response to short-term pH drop, and to putative stress metabolites released by conspecifics or gilt-head sea bream Sparus aurata during 30 min of acute pH drop. Not only did acute pH drop itself impair time to find a food cue in small hermit crabs and burrowing in harbour ragworms, but similar effects were observed under exposure to pH drop-induced stress metabolites. Stress metabolites from S. aurata, but not its regular control metabolites, also induced avoidance responses in all recipient species. Here, we confirm that a short-term abrupt pH drop, an abiotic stressor, has the capacity to trigger the release of metabolites which induce behavioural responses in conspecific and heterospecific individuals, which can be interpreted as a behavioural cost. Our findings that stress responses can be indirectly propagated through means of chemical communication warrant further research to confirm the effect size of the behavioural impairments caused by stress metabolites and to characterise their chemical nature.

Heat induces multi-omic and phenotypic stress propagation in zebrafish embryos

“…We found these cues to elicit similar phenotypic responses as heat stress itself in naive receivers, which are the characteristics of a positive feedback loop (16). To date, only a few studies have shown that animals communicate to each other upon abiotic stress, such as heat and low pH (17,18). Zebrafish (Danio rerio) is a commonly used experimental model species, including for behavioural assays (19) and "omics" approaches (20).…”

“…Previous studies have focused mostly on cues released upon biotic factors such as injury (14) or disturbance (15). We have recently proposed that abiotic stress such as heat or low pH likewise elicits the release of olfactory cues, which we termed “stress metabolites” (16, 17). We found these cues to elicit similar phenotypic responses as heat stress itself in naive receivers, which are the characteristics of a positive feedback loop (16).…”

Short-Term Microplastic Exposure Impairs Cognition in Hermit Crabs

“…Variables such as microplastic levels, water level, temperature, and pH remained stable across our experiment, rather than fluctuating throughout the day. Daily and seasonal fluctuations in pH, for instance, can impact behavioural responses in marine organisms [ 64 , 65 , 66 ], including crustaceans [ 37 ] and involving stress-induced metabolites [ 67 ]. Such discrepancies may produce different effects in nature, so we recommend studies investigating whether our findings apply to wild hermit crab populations.…”

Consequences of directly- and indirectly-experienced heat stress in a mutagenic environment

“…Frisch, 1938). We previously extended this mechanism to abiotic stress and identified specific classes of social metabolites (Feugere et al, 2021a; 2021b; 2023). Here, we confirm that heat stress responses can be indirectly transmitted between embryos via social metabolites activating immune-, cell structure- and keratin-related genes in receivers.…”

“…Aquatic ectotherms, such as zebrafish (Engeszer et al, 2007), may spawn in shallow waters where offspring experience high temperatures and environmental mutagens such as ultraviolet radiation (UVR) from sunlight (Dahms and Lee, 2010). Moreover, heat-stressed aquatic animals may release “social metabolites” that alter the phenotype of conspecifics not directly experiencing heat stress (Feugere et al, 2021a; 2021b). Embryos developing in clutches may have amplified stress responses to heat through chemical communication, the consequences of which have received little focus.…”