Abstract
Abstract Predicting the implications of ongoing ocean climate warming demands a better understanding of how short‐term thermal variability impacts marine ectotherms, particularly at beyond‐optimal average conditions during summer heatwaves. Using a globally important model species, the blue mussel Mytilus, in a 5‐week‐long experiment, we (a) assessed growth performance traits under 12 scenarios, consisting of four thermal averages (18.5, 21, 23.5 and 26℃) imposed as constant or daily fluctuating regimes with amplitudes of 2 or 4℃. Additionally, we conducted a short‐term assay using different mussel individuals to (b) test for the species capacity for suppression and recovery of metabolic performance traits (feeding and aerobic respiration) when exposed to a 1‐day thermal fluctuation regime (16.8–30.5℃). Using this high‐resolution data, we (c) generated short‐term thermal metabolic performance curves to predict and explain growth responses observed in the long‐term experiment. We found that daily high‐amplitude thermal cycles (4℃) improved mussel growth when fluctuations were imposed around an extreme average temperature of 26℃, representing end‐of‐century heatwaves. In contrast, thermal cycles negatively affected mussel growth at a less extreme average temperature of 23.5℃, resembling current peak summer temperature scenarios. These results suggest that fluctuations ameliorate heat stress impacts only at critically high average temperatures. The short‐term assay demonstrated that during the warming phase, animals stopped feeding between 24 and 30℃ while gradually suppressing respiration. In the subsequent cooling phase, feeding and respiration partially and fully recovered to pre‐heating rates respectively. Furthermore, nonlinear averaging of short‐term feeding responses (upscaling) well‐predicted longer term growth responses to fluctuations. Our findings suggest that fluctuations can be beneficial to or detrimental for the long‐term performance of ectothermic animals, depending on the fluctuations' average and amplitude. Furthermore, the observed effects can be linked to fluctuation‐mediated metabolic suppression and recovery. In a general framework, we propose various hypothetical scenarios of fluctuation impacts on ectotherm performance considering inter‐ or intra‐species variability in heat sensitivity. Our research highlights the need for studying metabolic performance in relation to cyclic abiotic fluctuations to advance the understanding of climate change impacts on aquatic systems. A free Plain Language Summary can be found within the Supporting Information of this article.
Highlights
Thermal variations in marine ecosystems, in coastal and shallow-water zones, can occur on short time-scales of minutes to days, due to changes in irradiance, up and downwelling and tides (Boyd et al, 2016; Choi et al, 2019)
We conducted a short-term assay using different mussel individuals to (b) test for the species capacity for suppression and recovery of metabolic performance traits when exposed to a 1-day thermal fluctuation regime (16.8–30.5°C). Using this high-resolution data, we (c) generated short-term thermal metabolic performance curves to predict and explain growth responses observed in the long-term experiment
We propose a simple framework that may explain this context dependency based on possible scenarios of acclimation- or stress- induced changes in an ectotherm's capacity for thermal metabolic performance
Summary
Thermal variations in marine ecosystems, in coastal and shallow-water zones, can occur on short time-scales of minutes to days, due to changes in irradiance, up and downwelling and tides (Boyd et al, 2016; Choi et al, 2019). Such predictions assume that an organism's instant thermal response, as defined by its TPC, remains constant over time (i.e. lack of time-dependent effects; sensu Kingsolver et al, 2015; Sinclair et al, 2016) This assumption limits predictions on the consequences of thermal fluctuations for marine ectotherms with remarkable capacities for suppressing and recovering their (organism level) metabolic performance. Refuge fluctuation effects on the long-term performance can be projected using metabolic TPCs generated on short time-scales of hours to days via an upscaling approach (Chesson et al, 2005; Denny, 2019; Denny & Benedetti-Cecchi, 2012) Such short-term TPCs usually show convex (decelerating) drops at the higher beyond-optimal end, manifesting heat-induced suppression of metabolic performance (Figure S1). The effects of temperature fluctuations on these mussels can be experimentally assessed without considering tidally induced aerial exposure as a covariate
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