A single heat-stress bout induces rapid and prolonged heat acclimation in the California mussel,Mytilus californianus

Abstract

Climate change is not only causing steady increases in average global temperatures but also increasing the frequency with which extreme heating events occur. These extreme events may be pivotal in determining the ability of organisms to persist in their current habitats. Thus, it is important to understand how quickly an organism's heat tolerance can be gained and lost relative to the frequency with which extreme heating events occur in the field. We show that the California mussel, Mytilus californianus —a sessile intertidal species that experiences extreme temperature fluctuations and cannot behaviourally thermoregulate—can quickly (in 24–48 h) acquire improved heat tolerance after exposure to a single sublethal heat-stress bout (2 h at 30 or 35°C) and then maintain this improved tolerance for up to three weeks without further exposure to elevated temperatures. This adaptive response improved survival rates by approximately 75% under extreme heat-stress bouts (2 h at 40°C). To interpret these laboratory findings in an ecological context, we evaluated 4 years of mussel body temperatures recorded in the field. The majority (approx. 64%) of consecutive heat-stress bouts were separated by 24–48 h, but several consecutive heat bouts were separated by as much as 22 days. Thus, the ability of M. californianus to maintain improved heat tolerance for up to three weeks after a single sublethal heat-stress bout significantly improves their probability of survival, as approximately 33% of consecutive heat events are separated by 3–22 days. As a sessile animal, mussels likely evolved the capability to rapidly gain and slowly lose heat tolerance to survive the intermittent, and often unpredictable, heat events in the intertidal zone. This adaptive strategy will likely prove beneficial under the extreme heat events predicted with climate change.

An integrated, multi‐level analysis of thermal effects on intertidal molluscs for understanding species distribution patterns

“…Both congeners are likely to experience temperatures in these ranges in the field, so the costs of maintaining haemocyte populations and, by extension, populations of other types of cells as well could be substantial components of sublethal thermal stress. Note that cardiac critical temperatures for M. californianus are always above 32 C, regardless of latitude (Logan, Kost & Somero, 2012) or vertical position (Moyen et al, 2019) of the sampled populations. Thus, considerable amounts of thermal damage at the cellular level may ensue before an organ-level property like cardiac critical temperature manifests during thermal stress.…”

“…one important consideration to incorporate into experimental design. For example, Moyen et al (2019) showed that the rate of heating (in air) in a laboratory setting could lead to significant variation in critical temperature of cardiac function in M. californianus. Specimens from low and high intertidal sites differed in their responses; only high-site individuals exhibited changes in critical temperature with heating rate.…”

“…Wang, Peng & Dong, 2020b). Periodicity of stress is also important in the context of how long an adaptive acclimatization response persists relative to the periodicity of occurrence of stressful thermal conditions (Moyen et al, 2020b(Moyen et al, , 2020c.…”

Heat hardening enhances mitochondrial potential for respiration and oxidative defence capacity in the mantle of thermally stressed Mytilus galloprovincialis

“…In this prism, Connor and Gracey 75 reported that M. californianus exhibits phenotypic plasticity with respect to transcriptomic expression during cycles of aerial exposure and that it may produce a type of “heat hardening”, thus promoting homeostasis in the intertidal environment and enhanced tolerance to low-tide heating events. Moyen et al 34 recently reported that this adaptive strategy via phenotypic plasticity will likely prove beneficial for M. californianus and other mussel species under the extreme heat events projected with progressing climate change.…”

“…These changes in the expression pattern and thresholds of the transcriptional induction of stress response genes during heat hardening play an important role in development of the heat-tolerant phenotypes of animals 29 – 33 . Such phenotypic plasticity in response to heat hardening have been proposed as an adaptive strategy under the extreme heat events predicted with climate change for marine mussels including Mytilus californianus (Conrad, 1837) 34 . However, the physiological and molecular mechanisms of heat hardening are not well understood in marine ectotherms, including mussels, and require further investigation to assess the potential mechanisms underlying the organism’ ability to cope with extreme weather events such as marine heat waves.…”