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.

Keywords: heat acclimatization; heat hardening; heat wave; intertidal zone; physiological plasticity; thermal tolerance.

Figure 1.

Schematic of the experimental design for the survival tests. Mussels first underwent a sublethal heat-stress bout for 2 h (temperature according to the treatment group: 25, 30 or 35°C, or no sublethal heat-stress control), and then recovered in an aquarium for a certain number of days (i.e. recovery time, 1–28 days), before being subjected to an extreme heat-stress bout (40°C for 2 h). After the extreme heat-stress bout, mussels were placed back into the flow-through aquaria for four weeks, and survival was assessed every 2–3 days throughout that period. The colours after the number of recovery days indicate which groups were tested for each condition. Note that control mussel groups were tested for all conditions (but there are no grey boxes noted on the diagram). The 25°C group was only tested for recovery days 1–4 since we found no differences between the control and 25°C groups; see ‘Methods’ for details.

Figure 2.

Mussel survival based on sublethal heat-stress temperature and number of recovery days between consecutive heat-stress bouts. (a) Kaplan–Meier survival curves for each of the experimental (sublethal heat exposure) and control groups over the four-week monitoring period after mussels underwent the extreme heat-stress bout. The number at the top of each panel indicates the recovery time (in days) between the sublethal and extreme heat-stress bouts. Survival probability is indicated on the y-axis, where 1.0 is 100% survival. A separate control group was used for each recovery day. The ‘no extreme heat’ subplot shows mussel survival for four weeks after the sublethal heat-stress bouts alone; only one mussel died after the 35°C sublethal heat-stress bout. (b) Percent survival across the four-week monitoring period (y-axis) based on the number of recovery days between the sublethal and extreme heat-stress bouts (x-axis), separated by experimental groups (25°C in blue, 30°C in yellow and 35°C in red). Each bar on the plot was corrected for by subtracting the control group's final percent survival from each of the experimental group's final percent survival. Superscript symbols indicate significant differences: from the control group*, the 30°C group^‡ or the 35°C group^† (all p < 0.05) based on the Pearson chi-square tests (see ‘Results’ and electronic supplementary material, table S3 for further details).

Figure 3.

Frequency of two consecutive heat-stress bouts based on field Robomussel data. Field data from Robomussels at Hopkins Marine Station [37], where Robomussel temperatures were collected every 10 min for 6–13 consecutive months in each of the years shown in the figure (2005, 2007, 2009 and 2014). The frequency of heat-stress bouts (on the y-axis) is relative to the total number of heat-stress bouts for that given year. The x-axis indicates the total number of days between any two consecutive heat-stress bouts, where a heat-stress bout was defined as any temperature from 28 to 41°C for at least two consecutive hours (see ‘Methods’ for more details). The numbers above the bars indicate the frequency (as a percentage) with which any two heat-stress bouts occurred for that specific number of days apart, relative to the total number of heat bouts for that given year (e.g. in 2007, 37% of heat events occurred 2 days apart). The yellow and red shading behind the bar plots shows the results from our laboratory-based findings for the 30 and 35°C groups, respectively. Note that the primary y-axis values are not applicable to the yellow- and red-shaded trapezoids, which are only meant as a pictorial representation to synthesize the data from the laboratory with the field body temperature data; the secondary y-axis label of ‘Increasing survival’ is simply to show that the trapezoidal shading indicates when survival increased and decreased over time for each of the two experimental groups. Heat tolerance was improved 1 and 2 days after the initial 30 and 35°C sublethal heat-stress bouts, respectively, and starts to decay at 14 and 21 days later, respectively. Note that the 25°C experimental group data are not pictured here as this treatment did not improve survival.