Behavioural stress feedback loops in benthic invertebrates caused by 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 minutes 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.

Thermal stress induces a positive phenotypic and molecular feedback loop in zebrafish embryos

“…These results are in agreement with higher activities in rainbow trout embryos facing alarm cues (Poisson et al, 2017) but depart from lower behaviour activities in 24 hpf zebrafish embryos exposed to conspecific alarm cues (Lucon-Xiccato et al, 2020), which suggest that the response depends on the type of the cue and the tested model. Behavioural alteration was also observed in adult zebrafish in response to low pH and fasting stress-induced metabolites (Abreu et al, 2016), and adult marine invertebrates experiencing metabolites from low pH-stressed conspecifics and heterospecifics (Feugere et al, 2021). Third, stress medium conditioned by thermally-stressed embryos induced changes in gene expression patterns in naive conspecific receiver embryos.…”

“…Despite the wealth of information on such biotic stress-induced stress propagation, this phenomenon is only known for a few abiotic stressors, such as low pH or acute fasting (Abreu et al, 2016;Feugere et al, 2021). Evidence of transmission of heat-induced stress between conspecifics comes mainly from a single experiment in crayfish (Hazlett, 1985).…”

“…1a). As alarm and disturbance cues have been defined with respect to biotic stressors, we introduce the term "stress metabolite" referring to such cues putatively induced by abiotic stress (Feugere et al, 2021). To test our hypothesis, zebrafish embryos were exposed to independent and combined treatments of thermal stress and medium putatively containing stress metabolites induced by thermal stress.…”

Effects of pH on Olfactory Behaviours in Male Shore Crabs, Carcinus maenas

“…For a measured total alkalinity of 2500 mmol/kg SW, the pCO 2 was calculated as 537 and 1922 matm in the 8.1 and 7.6 pH water (CO 2 calc software v1.2.0). Seawater parameters were measured daily at 2.30 p.m. for temperature: 20.16 • C ± 1.05 • C, salinity: 35.67 PSU ± 0.26 PSU, and dissolved oxygen: 7.55 mg/L ± 0.16 mg/L (for details of methods, see [25,26]). These tanks contained tubes for the crabs to shelter in.…”

“…The total alkalinity of 2500 µmol/kg SW was measured, and the pCO 2 was calculated as 537 and 1922 µatm for the control and reduced pH tank water, respectively (CO2calc software v1.2.0). Salinity, temperature, and dissolved oxygen were recorded as seawater parameters daily at 2.30 p.m. (mean temperature: 20.16 • C ± 1.05 • C, mean salinity: 35.67 PSU ± 0.26 PSU, mean dissolved oxygen: 7.55 mg/L ± 0.16 mg/L) [26]). The seawater was natural seawater pumped directly from the estuary at Ramalhete and cleaned via fluidised sand filters.…”