Use of valvometry as an alert tool to signal the presence of toxic algae Alexandrium catenella by Mytilus edulis

Abstract

Valvometry is a non-invasive technique used to continuously monitor gaping behaviour of bivalves at high frequency. In previous laboratory studies, valvometry has revealed a behavioural sensitivity of bivalves to the presence of toxic microalgae in seawater. However, the application of valvometry as an early-warning system for detecting natural occurrences of toxic microalgae and their resulting toxicity in bivalves remains largely unexplored. In this study, valvometry was used to characterise changes in blue mussels (Mytilus edulis) gaping behaviour during gradual exposure to the toxic dinoflagellate, Alexandrium catenella, which produces paralytic shellfish toxins (PST). Laboratory experiments were first performed to identify specific gaping behaviour changes and these responses were subsequently validated in natural seawater conditions in a second experiment. Under both laboratory and natural seawater conditions, mussels exposed to A. catenella tended to remain open (yawning) longer than non-exposed mussels. This change in gaping behaviour was observed at PST concentration as low as 30 μg STXeq 100 g–1 of mussel tissue. We suggest that increased opening is likely related to temporary muscular paralysis induced by toxic algae, as this mechanism has been previously reported in other bivalve species. Furthermore, we observed that biological rhythms of valve behaviour related to tidal and daily rhythms were modified when mussels were intoxicated by PSP (Paralytic Shellfish Poisoning). In conclusion, the effects of toxic algae on mussel gaping behaviour reveals that valvometry could be used as an early-warning tool for the presence of toxic Alexandrium sp. in the environment prior to mussels reaching the regulatory threshold (80 μg STXeq 100 g–1) for harvest interdiction.

Impact of the Toxic Dinoflagellate Alexandrium catenella on the Valve Movement of Mytilus edulis: A Comparison between Two Populations with Contrasting Histories Exposure

“…After this initial 24 h period, A. catenella was introduced at a concentration of 10,000 cells L −1 for 42 h (T1 period). This A. catenella concentration aligns with the maximum concentration used by Durier et al ( 2022) [14] and ensured the regulatory limit for bivalve harvest. Following the T1 period, the water in each of the tanks was completely replaced, and mussels were exposed to Tetraselmis suecica, a non-toxic alga, at a concentration of 5000 cell mL −1 for the next 24 h (T2 period).…”

“…When mussels were exposed to A. catenella in the current study, the most notable response was an avoidance behaviour with a recorded rise in the number of valve closures and a prolonged valve closure duration. It is noteworthy that Durier et al (2022) [14] reported a contrasting behavioural response, since mussels in that study displayed a decrease in valve closures in the presence of toxic dinoflagellates. The contrasting behavioural responses between the two studies could perhaps be due to different concentrations of A. catenella which was higher in the present study than in Durier et al (2022) [14].…”

“…Deploying bivalve sentinel species equipped with valvometry sensors may provide an early warning of harmful algal blooms (HAB) [12][13][14]. Such a warning system could minimize the economic losses by harvesting some of the cultured stock prior to a PST outbreak.…”

“…Such a warning system could minimize the economic losses by harvesting some of the cultured stock prior to a PST outbreak. Blue mussels (Mytilus edulis) may have such sentinel attributes since (1) their valve-gaping behaviours are known to be sensitive to harmful algae [14], (2) they can be easily transferred between areas, and (3) they continue pumping water under challenging conditions, including in contaminated environments [15,16]. In more detail, when M. edulis was exposed to natural seawater containing A. catenella its valve gaping behaviours was altered, resulting in longer valve openings (yawning) of longer durations, which in turn suggested a partial and temporary muscle paralysis [14].…”

“…Blue mussels (Mytilus edulis) may have such sentinel attributes since (1) their valve-gaping behaviours are known to be sensitive to harmful algae [14], (2) they can be easily transferred between areas, and (3) they continue pumping water under challenging conditions, including in contaminated environments [15,16]. In more detail, when M. edulis was exposed to natural seawater containing A. catenella its valve gaping behaviours was altered, resulting in longer valve openings (yawning) of longer durations, which in turn suggested a partial and temporary muscle paralysis [14]. This behavioural change was detected at low A. catenella concentrations, up to a week before the toxin accumulation in mussels triggered a harvest prohibition.…”