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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.
It has been proposed that growth and reproduction of animals is frequently limited by multiple nutrients simultaneously. To improve our understanding of the consequences of multiple nutrient limitations (i.e. co-limitation) for the performance of animals, we conducted standardized population growth experiments using an important aquatic consumer, the rotifer Brachionus calyciflorus. We compared nutrient profiles (sterols, fatty acids and amino acids) of rotifers and their diets to reveal consumerdiet imbalances and thus potentially limiting nutrients. In concomitant growth experiments, we directly supplemented potentially limiting substances (sterols, fatty acids, amino acids) to a nutrient-deficient diet, the cyanobacterium Synechococcus elongatus, and recorded population growth rates. The results from the supplementation experiments corroborated the nutrient limitations predicted by assessing consumerdiet imbalances, but provided more detailed information on co-limiting nutrients. While the fatty acid deficiency of the cyanobacterium appeared to be of minor importance, the addition of both cholesterol and certain amino acids (leucine and isoleucine) improved population growth rates of rotifers, indicating a simultaneous limitation by sterols and amino acids. Our results add to growing evidence that consumers frequently face multiple nutrient limitations and suggest that the concept of co-limitation has to be considered in studies assessing nutrient-limited growth responses of consumers.