The neglected role of environmental fluctuations as modulator of stress
Ongoing changes in ocean climate (e.g., warming trends) are accompanied by increases in frequency and intensity of extreme weather events (e.g., heatwaves), particularly in shallow-water habitats. Traditionally, empirical studies intending to project the ecological impacts of environmental variability have focused on species or community responses to shifts in average conditions (trends), extracted from days to weeks-long experiments under static treatment conditions. As species might express cumulative stress responses under continuous critical exposures, the performance curves based on static experimental conditions commonly show a concave drop over the beyond-optimal interval of the environmental factors in focus. Accordingly, nonlinear averaging usually predicted fluctuations’ adverse effects, neglecting the role of acclimation, stress recovery, and evolutionary adaptation. This thesis provides a general introduction to the above issues and then tries to move forward by investigating (i) the environmental fluctuations’ long-term impacts on fitness-related traits (e.g., growth) at beyond-optimal average conditions, (ii) the role of fluctuation-mediated metabolic suppression and recovery, and (ii) how these relations may be modulated by warm adaptation forces (acclimation and selection). Such practice and its required method development are optimized by focusing on cyclic (daily) temperature fluctuations, i.e., one of the most common and ecologically important environmental forces, and an ecosystem engineer, the mytilid mussel Mytilus spp., from the Western Baltic Sea. The first Chapter describes the Fluorometer and Oximeter equipped Flow-through Setup (FOFS), the experimental design, and data processing protocols for recording metabolic performance (feeding and aerobic respiration) of benthic filter-feeders in response to fine-tuned environmental variability. The FOFS method’s functionality is successfully demonstrated through recording mussels’ responses during short-term (one-day) thermal fluctuation cycles. In the following research, FOFS is used in short-term assays to evaluate mussels’ capacity to suppress and recover their metabolic performance over successive phases of stressful and benign temperatures. Chapter 2 presents a combination of a long-term (5 weeks) experiment, a short-term (one-day) FOFS assay, and an associated upscaling framework (nonlinear averaging). The results show that (i) daily high-amplitude thermal cycles improved mussel growth when fluctuations were imposed around an extreme average condition representative of end-of-century heatwaves. In contrast, (ii) the thermal cycles negatively affected mussel growth at a less extreme average, representing today’s peak summer temperatures in the region. Furthermore, (iii) nonlinear averaging of the short-term (non-acclimated) thermal feeding responses could well predict fluctuation impacts observed on growth rates from the long-term experiment. Merging these findings with physiological and mathematical principles, I propose a simple prediction framework based on various possible time-dependent changes in thermal metabolic performance. The framework explains how fluctuations, mediating metabolic suppression and recovery, can be beneficial or detrimental to ectotherm’s long-term performance, depending on the fluctuations’ average and amplitude. Chapter 3 then tests whether and how intensified summer thermal regimes would result in higher heat tolerance in individuals’ daily thermal metabolic suppression and recovery. Mussels were grown from juveniles (transplanted mussels) or larval recruits (recruited mussels) under current versus warmed (end-of-century extreme) summer regimes in a near-natural mesocosm setting. Then, mussels’ feeding and aerobic respiration rates were assessed in response to a mild temperature for six hours (baseline performances) followed by two 24 h fluctuation cycles in mild to critical temperature range. The results show that the potentially warm-selected recruits were more capable of recovering their feeding and respiration rates in benign phases of daily temperature fluctuations and expressed lower baseline respiration rates (metabolic demand). These findings support the hypotheses that (i) extremely warm events may select for rare heat-tolerant individuals of marine ectotherms at their very early life-history stages, (ii) lower metabolic demand is a mechanism for such heat tolerance, and (iii) the capacity to acquire such tolerance through acclimation is minor. Overall, this research highlights the significance of studying the metabolic performance of ectothermic species at timescales relevant to natural fluctuations to advance our understanding of climate change impacts on aquatic systems. Whether selection-induced shifts in stress tolerance can lead to ectotherms’ evolutionary adaptation to ocean warming is an essential research subject of future studies.