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Understanding how variance in environmental factors affects physiological performance, population growth, and persistence is central in ecology. Despite recent interest in the effects of variance in single biological drivers, such as temperature, we have lacked a comprehensive framework for predicting how the variances and covariances between multiple environmental factors will affect physiological rates. Here, we integrate current theory on variance effects with co-limitation theory into a single unified conceptual framework that has general applicability. We show how the framework can be applied (1) to generate mathematically tractable predictions of the physiological effects of multiple fluctuating co-limiting factors, (2) to understand how each co-limiting factor contributes to these effects, and (3) to detect mechanisms such as acclimation or physiological stress when they are at play. We show that the statistical covariance of co-limiting factors, which has not been considered before, can be a strong driver of physiological performance in various ecological contexts. Our framework can provide powerful insights on how the global change-induced shifts in multiple environmental factors affect the physiological performance of organisms.
Understanding animal performance in heterogeneous or variable environments is a central question in ecology. We combine modelling and experiments to test how temperature and food availability variance jointly affect life-history traits of ectotherms. The model predicts that as mean temperatures move away from the ectotherm's thermal optimum, the effect size of joint thermal and food variance should become increasingly sensitive to their covariance. Below the thermal optimum, performance should be positively correlated with food–temperature covariance and the opposite is predicted above it. At lower temperatures, covariance should determine whether food and temperature variance increases or decreases performance compared to constant conditions. Somewhat stronger than predicted, the covariance effect below the thermal optimum was confirmed experimentally on an aquatic ectotherm (Daphnia magna) exposed to diurnal food and temperature variance with different amounts of covariance. Our findings have important implications for understanding ectotherm responses to climate-driven alterations of thermal mean and variance.
In food webs, herbivores are often constrained by low food quality in terms of mineral and biochemical limitations, which in aquatic ecosystems can co-occur with limited oxygen conditions. As low food quality implies that carbon (C) is available in excess, and therefore a regulation to get rid of excess C is crucial for the performance of consumers, we examined the C pathways (ingestion, feces release, excretion, and respiration) of a planktonic key herbivore (Daphnia magna). We tested whether consumer C pathways increase due to mineral (phosphorus, P) or biochemical (cholesterol and fatty acid) limitations and how these regulations vary when in addition oxygen is low. Under such conditions, at least the capability of the upregulation of respiration may be restricted. Furthermore, we discussed the potential role of the oxygen-transporting protein hemoglobin (Hb) in the regulation of C budgets. Different food quality constraints led to certain C regulation patterns to increase the removal of excess dietary C: P-limited D. magna increased excretion and respiration, while cholesterol-limited Daphnia in addition upregulated the release of feces. In contrast, the regulative effort was low and only feces release increased when D. magna was limited by a long-chain polyunsaturated fatty acid (eicosapentaenoic acid, EPA). Co-limiting oxygen did not always impact the discharge of excess C. We found the food-quality-induced upregulation of respiration was still present at low oxygen. In contrast, higher excretion of excess C was diminished at low oxygen supply. Besides the effect that the Hb concentration increased under low oxygen, our results indicate a low food-quality-induced increase in the Hb content of the animals. Overall, C budgeting is phenotypically plastic towards different (co-) limiting scenarios. These trigger specific regulation responses that could be the result of evolutionary adaptations.