Nutritional grouping of marine forage species reveals contrasted exposure of high trophic levels to essential micro‐nutrients

Abstract

By transferring energy and nutrients from plankton to top predators, forage species play a major ecological role in marine food webs. While large differences in energy densities have been demonstrated among these species, other determinants of their quality remain poorly explored. We analysed 78 forage species from the Bay of Biscay, NE Atlantic, for their concentrations in various chemical elements with a documented biological role (i.e. micro-nutrients). Species encompassed jellyfish, crustaceans, cephalopods, cartilaginous and bony fish. Elements included two essential macro-minerals (nitrogen and phosphorous) and nine trace elements (arsenic (As), cobalt, copper (Cu), chromium, iron, manganese, nickel, selenium (Se), zinc). We showed a broad range of elemental composition values across forage species, partly driven by taxonomy (fish versus crustaceans/cephalopods) or their habitat (coastal versus oceanic, pelagic versus benthic). Some elements (As, Cu or Se) were more variable than others, especially in fish for Cu and Se. The 78 forage species were then classified by hierarchical clustering analysis (HCA) into different nutritional groups, based on their composition in eleven elements. Mean concentrations of each element in the diet of eight cetacean species was finally calculated, as well as the importance of each nutritional group (as defined by HCA including all elements) for each predator species. We revealed contrasting diets in terms of exposure to elements. Neritic common dolphins and harbour porpoises but also minke whales were thus mainly supplied by the Se-enriched nutritional group composed of small (pelagic) schooling fish (including sandeels, (horse) mackerel and also some Clupeids), while the diets of pilot whales or Risso's dolphins that mostly consume benthic cephalopods were clearly Cu-enriched. This study raises the issue of essential element composition as another determinant of food quality, and the risk associated with changes in forage species' availability for the proper functioning of marine food webs and ecosystems.

Special issue: Questioning the roles of resources nutritional quality in ecology

“…Because all of the contributions considered at least one explicit variable to quantify the nutritional quality of the resource, none of them falls within the cluster of 'undefined food quality' (in green). Five of the articles of the Special issue(Chouvelon et al 2022, Lowman et al 2022, Mathieu-Resuge et al 2022, Sentis et al 2022, van Deurs et al 2022) fall within the cluster aquatic ecosystem/ stoichiometry-lipids/trophodynamics-fitness, a proportion that mirrors well the actual predominance of those themes within the overall research (Fig.2c). Two more articles of this Special issue (LeGall et al 2022, Zaguri et al 2022) belong to the cluster linking the nutritional geometry to physiological aspects, which is current ranked second in term of contribution to the overall research.…”

“…Research in trophic ecology would certainly largely benefit from combining the different frameworks used for characterizing resources quality and their impacts -keeping in mind that methodologies should be harmonized or at least inter-calibrated between studies (Zaguri et al 2022). -The resource quality should be understood as a multidimensional property and it is hard to imagine explaining all resources constraints in ecosystems while considering only one kind of quality descriptor (Chouvelon et al 2022). As underlined in this special issue, different lifehistory traits of consumers can respond differently to deficiencies in various aspects of resource quality (e.g.…”

“…Biomechanical parameters (including all physical defenses) used to be largely considered in the early 90s but the relative use of this parameter is clearly declining in the recent years. The articles published in this special issue are well representative of these trends since one third of the published articles question resources quality through the consideration of resources elemental content(Chouvelon et al 2022, Lowman et al 2022, Sentis et al 2022, while a second third focuses on resources macro-nutrient contents, alone (LeGall et al 2022, Zaguri et al 2022 or in association with fatty acids(van Deurs et al 2022). Finally, three articles specifically focus on fatty acids/lipids(Hudson et al 2022, Leal et al 2022, Mathieu-Resuge et al 2022).…”

Deciphering Eurasian otter (Lutra lutra L.) and seal (Phoca vitulina L.; Halichoerus grypus F.) diet: Metabarcoding tailored for fresh and saltwater fish species

“…Earlier studies on the diet of common dolphins ( Delphinus delphis ) in the Bay of Biscay showed that not all prey species in the diet of top predators are interchangeable or equivalent (Spitz et al, 2010). Hence, any significant changes in predator diets could affect top predator abundance and ecosystem stability in the area (Chouvelon et al, 2022).…”

“…Hence, any significant changes in predator diets could affect top predator abundance and ecosystem stability in the area (Chouvelon et al, 2022).…”