Ecological energetics of forage fish from the Mediterranean Sea: Seasonal dynamics and interspecific differences

Abstract

Small and medium pelagic fishes play a central role in marine food webs by transferring energy from plankton to top predators. In this study, direct calorimetry was used to analyze the energy density of seven pelagic species collected over four seasons from the western Mediterranean Sea: anchovy Engraulis encrasicolus, sardine Sardina pilchardus, round sardinella Sardinella aurita, horse mackerels Trachurus trachurus and T. mediterraneus, and mackerels Scomber scombrus and S. colias. Inter-specific differences in energy density were linked to spawning period, energy allocation strategies for reproduction and growth, and feeding ecologies. Energy density of each species varied over time, with the exception of S. colias, likely due to its high energetic requirements related to migration throughout the year. In general, higher energy density was observed in spring for all species, regardless of their breeding strategy, probably as a consequence of the late-winter phytoplankton bloom. These results provide new insights into the temporal availability of energy in the pelagic ecosystem of the Mediterranean Sea, which are pivotal for understanding how the population dynamics of small and medium pelagic fishes and their predators may respond to environmental changes and fishing impacts. In addition, the differences found in energy density between species highlighted the importance of using species specific energy-values in ecosystem assessment tools such as bioenergetic and food web models.

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.