Alliance of ecologists and physiologists to study the effect of size and food quantity on muscle metabolism in the European sardine Sardina pilchardus

This blog post is provided by Elisa Thoral, Claire Saraux and Loïc Teulier and tells the #StoryBehindThePaper for the paper ‘Changes in foraging mode caused by a decline in prey size have major bioenergetic consequences for a small pelagic fish’, which was recently published in the Journal of Animal Ecology. Elisa Thoral (PhD student) and Loïc Teulier (her thesis co-director), are from the University of Lyon in France. Claire Saraux is a Researcher from the CNRS in France.

The effect of global warming on individual body size has been a topic of high interest in marine ecology recently, especially with the now well documented shrinking of fish. A decrease in fish size of key species can have strong deleterious consequences both in terms of ecosystem functioning and economy and resource management. The European sardine Sardina pilchardus has been a source of worry in the western Mediterranean Sea over the past 10 years: its size and body condition have been declining, and the oldest individuals have disappeared from the Gulf of Lions. Individual hypotheses including the possible effects of migration, overfishing, epizootic diseases, or increased predation have all been refuted in explaining this phenomenon. Scientists are now taking a new approach, looking at what sardines eat, to test if “bottom up” effects could be responsible for the decline in sardine condition.

It is by combining their expertise across fields, that a physiologist, Loïc Teulier, and a quantitative ecologist, Claire Saraux, at the time Senior Lecturer at the University of Lyon (UMR LEHNA) and Researcher at Ifremer (UMR MARBEC), Sète, respectively, tackled this question. Both researchers belonged to structures with a common interest: water and the species which live in it, but with very different perspectives. While one measured the metabolism of fish from the cell to the whole organism, the other had a vision that extends from the individual to the population and ecosystem. To bridge the gap between these two scales, they collaborated through the supervision of Elisa Thoral, a Masters student. Loïc and Elisa went to Palavas-Les-Flots, on the shores of the Mediterranean Sea, in February 2017 to join Claire Saraux and her colleagues from the Ifremer experimental station.

Accompanied by their high-precision Oxygraphs Oroboros®, they first adapted their usual protocols to measure mitochondrial respiration in Gilthead Sea bream and European sardine muscles. Strong from this first success, an idea was born in the scientists’ minds. What if the physiologists from Lyon, took part in the large-scale study that started a few months ago to study the mechanisms through which food size and quantity might affect sardines? While sardine prey size had been suggested to decrease in the wild based on stomach contents, the mechanisms underlying the effects of prey size on sardine condition and energetics remained entirely new questions. Sardines are known to use two different feeding modes according to the size of their prey: they will directly capture the largest prey, but use filtration for the smallest prey. Could this be the reason for the important demographic changes observed in the Gulf of Lions’ sardines? Their hypothesis was that filtering small prey would result in higher energy costs than hunting large prey, as it would require a longer swimming time to assimilate the same amount of energy. Thanks to resourceful zootechnicians, the Ifremer team was able to capture wild sardines, bring them back to the experimental station and maintain them in captivity.

In June 2017, the Lyon team of physiologists and ecophysiologists came back to Palavas-Les-Flots for a few weeks, surrounded by their ecologist colleagues from Ifremer, to measure mitochondrial respiration and energy production within the muscle of sardines fed for 7 months under four different treatments (two different food quantities and two different food sizes). This alliance made it possible to have a robust analysis of the data, but also to look at the relationship between purely physiological measurements, such as basal mitochondrial respiration, and more integrative measures more often used by ecologists such as body condition index.

The results were convincing: while caloric restriction appeared to have effects at the individual level, with marked effects on body condition in particular, particle size had consequences at both individual and mitochondrial levels. Indeed, a smaller particle size led to a decrease in body condition, regardless of the amount of food delivered, and also led to a decrease in mitochondrial fluxes, but with an improved coupling between oxygen consumption and energy production in the form of ATP. Yet, this is when things got complicated. How to reconcile the larger perspective from the ecologists with the detailed mechanistic approach of the physiologists in a paper? After months of writing, proofreading, corrections and animated discussions, the article saw the light of day, to the great pleasure of all co-authors, proving that it was possible to understand each other, despite very different fields of study, and to learn from each other to produce an eco-physiology paper. By linking both ecological questions and rather physiological answers, this paper showed that the filtration of small particles represents an energetic challenge compared to the capture of larger particles, which may support the bottom-up effect hypothesis that could be linked to climate changes consequences.

Read the paper

Read the full paper here: Thoral, E., Queiros, Q., Roussel, D., Dutto, G., Gasset, E., McKenzie, D. J., Romestaing, C., Fromentin, J.-M., Saraux, C., & Teulier, L. (2021). Changes in foraging mode caused by a decline in prey size have major bioenergetic consequences for a small pelagic fish Journal of Animal Ecology, 00, 1– 13.

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