Ecological energetics of forage fish from the Mediterranean Sea: Seasonal dynamics and interspecific differences
Introduction
The amount of energy available to an individual during its lifecycle affects its ability to grow and reproduce and this in turn, affects ecological energetics, that is, how energy is acquired, retained and transferred from one trophic level to another in the food web (Rossoll et al., 2012). Ecosystem energetics underpins many food web models that are increasingly being used to assist ecosystem-based fisheries and conservation management (Christensen and Maclean, 2011). Knowing the energetic value of the main ecological groups is needed in these models to understand energy transfer from lower to higher trophic levels and also to validate model outputs. One of the most cost-effective and quantitative ways to assess ecological energetics is through energy density analysis which provides a direct measure of the nutritional condition and quality of an individual or population. Energy density is positively correlated with lipid content (Rand et al., 1994, Van Pelt et al., 1997), which is important for energy storage and often the first macro-molecule to be catabolized (Lloret et al., 2014). Instead, proteins and carbohydrates remain rather constant in most species and have a much lower energy density than lipids (Anthony et al., 2000, Lloret et al., 2014).
Energy storage and nutritional quality of fish may fluctuate during the year due to different biological processes (i.e. growth, maintenance or reproduction) and external factors (i.e. temperature). In temperate regions, pelagic marine environments show important seasonal fluctuations with cyclical changes in temperature and food availability (Coma et al., 2000, Mazzocchi and Ribera d’Alcalà, 1995). In response to this, marine organisms have developed different life-history and energy allocation strategies in order to optimise their reproduction and population growth (Houston et al., 2006). Some marine species acquire and store energy in periods of high food abundance, which is then used for reproduction (they are named ‘capital breeders’). Others use their current energy income for reproduction (named ‘income breeders’), and there are also intermediate strategies (Alonso-Fernández and Saborido-Rey, 2012, McBride et al., 2015).
Species of fish with faster life cycles and smaller body size, such as small and medium sized pelagic fish, also known as forage fish, are thought to respond rapidly to environmental fluctuations that have been shown to have important implications for fish recruitment and ecosystem structure (Perry et al., 2005, Peck et al., 2013). Changes in the energy density of forage fish have been shown to be responsible for declines in top-predator populations through negatively impacting their breeding success and fitness (Doney et al., 2012, Österblom et al., 2008). For example, the decline of the common guillemots (Uria aalge) in the North Sea was linked to a reduction in the energetic value of their main prey (sprat Sprattus sprattus and lesser sandeels Ammodytes marinus) (Wanless et al., 2005). Furthermore, the decline of Steller sea lions (Eumetopias jubatus) in the Gulf of Alaska was partially related to a reduction of fattier fishes such as herring (Clupea harengus) within their feeding grounds (Rosen and Trites, 2000). Moreover, small and medium pelagic fishes are a good source of food nutrition for humans and in some areas, such as sub-Saharan countries, their consumption represent the main protein supply (Kawarazuka and Béné, 2011, Tacon and Metian, 2013).
In the Mediterranean Sea, small pelagic fishes such as Sardina pilchardus (sardine), Engraulis encrasicolus (anchovy) and Sardinella aurita (round sardinella), and medium pelagic fishes such as Trachurus spp. (horse mackerels) and Scomber spp. (mackerels) play key roles in the food-web, due to their high abundances and fast population turnover rates (Coll et al., 2008, Palomera et al., 2007). Despite this, while the energy density of multiple forage fishes has been reported in the Atlantic and the Pacific Oceans (Anthony et al., 2000, Dubreuil and Petitgas, 2009, Pedersen, 2001, Spitz and Jouma’a, 2013), such data are very scarce in the Mediterranean Sea (Tirelli et al., 2006, Harmelin-Vivien et al., 2012).
In the present study, we investigated the ecological energetics of seven forage fishes, E. encrasicolus, S. pilchardus, S. aurita, T. trachurus, T. mediterraneus, S. scombrus and S. colias, that are ecologically and economically important in the western Mediterranean Sea (see Table 1). The study aims were to (1) provide reference values of the energy densities of their whole-body, (2) examine potential seasonal changes, and (3) make inter-specific comparisons. These results are needed to better understand the different life-history strategies of these fishes and regional ecological energetics. Energy density analyses are relevant as input data for bioenergetics and food web models, increasingly used to predict the cumulative effects of climate change and fishing impacts on population and ecosystem dynamics.
Section snippets
Study area
The present study was conducted in the continental shelf and upper slope areas associated with the Ebro River Delta, northwestern Mediterranean Sea (Fig. 1). As a consequence of particular oceanographic conditions, such as wind conditions, vertical mixing and river discharges (Salat et al., 2002), this area is an important fishing ground of the Mediterranean Sea (Lleonart and Maynou 2003) and has been identify as a priority area for conservation (Coll et al., 2015, Piante, C., Ody, D., 2015.
Inter-specific differences in energy density
The annual energy density was significantly different between species (Pseudo-F6,348= 22.45; p-value<0.01) with the lower values for E. encrasicolus and the higher values for S. scombrus (Table 2; Fig. 2). Within small pelagic fish, S. pilchardus showed significantly higher energy density than E. encrasicolus and similar to Trachurus spp. S. aurita had similar energy density to both, E. encrasicolus and S. pilchardus. Within the medium pelagic fishes, T. trachurus and T. mediterraneus had
Discussion
This study reports new energetic data on 354 individuals of seven ecological and economical important pelagic fish species in the Mediterranean Sea. Results revealed clear differences in energy density between species and between seasons. These differences are related to species life-history and energy allocation strategy in addition to their feeding ecology. In consequence, predators of these small and medium sized pelagic fish could gain more or less energy per unit of food intake depending
Acknowledgements
We would like to thank all of the participants of the ECOTRANS Project, fishermen and crew on board the R.V. Ángeles Alvariño. We are especially grateful to Raquel Sáez who helped in the samplings and dissections and to Ignacio Catalán for his logistical support. M.A.-P. was supported by a predoctoral contract of the FPI program (BES-2012–054267, Spanish Ministry of Economy and Competitiveness). J.N. was supported by the Andalucía Talent Hub Program (Andalusian Knowledge Agency, European Marie
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