Decreased thermal tolerance under recurrent heat stress conditions explains summer mass mortality of the blue mussel Mytilus edulis

Laurent Seuront,Gerardo I Zardi,Eric Goberville,Katy R Nicastro

doi:10.1038/s41598-019-53580-w

Abstract

Extreme events such as heat waves have increased in frequency and duration over the last decades. Under future climate scenarios, these discrete climatic events are expected to become even more recurrent and severe. Heat waves are particularly important on rocky intertidal shores, one of the most thermally variable and stressful habitats on the planet. Intertidal mussels, such as the blue mussel Mytilus edulis, are ecosystem engineers of global ecological and economic importance, that occasionally suffer mass mortalities. This study investigates the potential causes and consequences of a mass mortality event of M. edulis that occurred along the French coast of the eastern English Channel in summer 2018. We used an integrative, climatological and ecophysiological methodology based on three complementary approaches. We first showed that the observed mass mortality (representing 49 to 59% of the annual commercial value of local recreational and professional fisheries combined) occurred under relatively moderate heat wave conditions. This result indicates that M. edulis body temperature is controlled by non-climatic heat sources instead of climatic heat sources, as previously reported for intertidal gastropods. Using biomimetic loggers (i.e. ‘robomussels’), we identified four periods of 5 to 6 consecutive days when M. edulis body temperatures consistently reached more than 30 °C, and occasionally more than 35 °C and even more than 40 °C. We subsequently reproduced these body temperature patterns in the laboratory to infer M. edulis thermal tolerance under conditions of repeated heat stress. We found that thermal tolerance consistently decreased with the number of successive daily exposures. These results are discussed in the context of an era of global change where heat events are expected to increase in intensity and frequency, especially in the eastern English Channel where the low frequency of commercially exploitable mussels already questions both their ecological and commercial sustainability.

Highlights

Extreme events such as heat waves have increased in frequency and duration over the last decades
Despite an increase in mussel production along the French Atlantic coastline since 200146, blue mussel beds are identified as a Habitat of Principle Importance (HPI) under the Natural Environment and Rural Communities (NERC) Act 2006, as a Priority Marine feature (PMF) under the Marine (Scotland) Act 2010, and included on the OSPAR (Annex V) list of threatened and declining species and habitats
Though the thermal limits of mussels in water are the ones demonstrating plasticity and local selection[70,71,108,109], we focused on M. edulis thermal limits during emersion as the seawater temperatures observed in the eastern English Channel are consistently well below the temperature causing death in this species, which ranged between 25 °C and 41 °C68,70,71,108,110,111

Summary

Introduction

Extreme events such as heat waves have increased in frequency and duration over the last decades. We found that thermal tolerance consistently decreased with the number of successive daily exposures These results are discussed in the context of an era of global change where heat events are expected to increase in intensity and frequency, especially in the eastern English Channel where the low frequency of commercially exploitable mussels already questions both their ecological and commercial sustainability. Despite an increase in mussel production along the French Atlantic coastline since 200146, blue mussel beds are identified as a Habitat of Principle Importance (HPI) under the Natural Environment and Rural Communities (NERC) Act 2006, as a Priority Marine feature (PMF) under the Marine (Scotland) Act 2010, and included on the OSPAR (Annex V) list of threatened and declining species and habitats This is relevant as summer mortalities of both wild and cultured M. edulis have recurrently been reported throughout the world[20,26,47,48,49,50]. In the western Atlantic region, intertidal population of M. edulis have experienced catastrophic mortality directly associated with summer high temperatures and, over the last 50 years, a poleward contraction of the species southern range edge has occurred[51]

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Results

Discussion

Conclusion