Trophic niche of squids: Insights from isotopic data in marine systems worldwide

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Abstract

Cephalopods are an important prey resource for fishes, seabirds, and marine mammals, and are also voracious predators on crustaceans, fishes, squid and zooplankton. Because of their high feeding rates and abundance, squids have the potential to exert control on the recruitment of commercially important fishes. In this review, we synthesize the available information for two intrinsic markers (δ15N and δ13C isotopic values) in squids for all oceans and several types of ecosystems to obtain a global view of the trophic niches of squids in marine ecosystems. In particular, we aimed to examine whether the trophic positions and trophic widths of squid species vary among oceans and ecosystem types. To correctly compare across systems, we adjusted squid δ15N values for the isotopic variability of phytoplankton at the base of the food web provided by an ocean circulation–biogeochemistry–isotope model. Studies that focused on the trophic ecology of squids using isotopic techniques were few, and most of the information on squids was from studies on their predators. Our results showed that squids occupy a large range of trophic positions and exploit a large range of trophic resources, reflecting the versatility of their feeding behavior and confirming conclusions from food-web models. Clear differences in both trophic position and trophic width were found among oceans and ecosystem types. The study also reinforces the importance of considering the natural variation in isotopic values when comparing the isotopic values of consumers inhabiting different ecosystems.

Introduction

Cephalopods are widely distributed throughout all oceans and inhabit diverse ecosystems, such as coastal shelves, open oceans and the deep-sea. Approximately 800 species of cephalopods have been described, including demersal species (e.g. octopuses and cuttlefish) and pelagic cephalopods (primarily squids) (Boyle and Rodhouse, 2005). The squids (order Teuthida) is a diverse group of cephalopods with approximately 300 species classified into 29 families, with large differences in size, feeding patterns and other biological traits. In general, benthic and shallow-water squids are better studied than their pelagic or deep-sea relatives, mainly due to sampling limitations (e.g., Cherel et al., 2009). During recent decades, however, important advances have been made in understanding the ecology of squids in many marine ecosystems (Cherel and Hobson, 2005, Cherel et al., 2009, Olson and Young, 2007).

Cephalopods are important organisms in terms of their economic and ecological value. From an economic perspective, approximately 76% of the world cephalopod catch in 2005 was squids, according to Food and Agriculture Organization (FAO) of the United Nations (Jerb and Roper, 2005, Rodhouse and Nigmatullin, 1996). Ecologically, squids comprise large biomasses in marine communities and occupy medium to top trophic positions in food webs (Amaratunga, 1983, Coll et al., 2013). Squids are an important prey resource for fishes, seabirds and marine mammals, and are voracious predators of crustaceans, squid, fishes and zooplankton (e.g., Cherel and Duhamel, 2004, Clarke, 1996, Croxall and Prince, 1996, Kaschner et al., 2001, Klages, 1996, Olson and Young, 2007, Rodhouse and Nigmatullin, 1996, Smale, 1996, Stergiou and Karpouzi, 2001, Xavier and Croxall, 2007, Hoving and Robison, in press). Because of their high feeding rates and generalist trophic strategy, squids have the potential to exert trophodynamic control on the recruitment of the early life stages of economically important fishes (Hunsicker and Essington, 2008, Rodhouse and Nigmatullin, 1996). In addition, cephalopods in general, and squids in particular, have been highlighted as indicators of fisheries and climate change impacts on marine ecosystems (Dawe et al., 2000, Sakurai et al., 2000, Bellido et al., 2001, Coll et al., 2013).

Despite their ecological importance in comparison with other marine organisms, trophic studies on cephalopods in general, and squids in particular, are scarce. Consequently, it is important to improve our understanding of the ecological role of squids in the marine environment. Stable isotopes are intrinsic markers that are increasingly being used to examine the trophic ecology of squids. The use of stable isotope values of nitrogen and carbon provide information on trophic position, trophic pathways and niche width for individuals to communities (see the recent review by Layman et al., 2011), and complement information from stomach-content analyses and food-web models (Coll et al., 2013). Stable isotope analysis is based on the fact that standardized stable isotope ratios of nitrogen, i.e. 15N/14N, (δ15N) and carbon, i.e. 13C/12C, (δ13C) are transformed from dietary sources to consumers in a predictable manner (Layman et al., 2011). δ15N values show a predictable increase from one trophic level to the next, with typical enrichment of about 3‰ per trophic level (Post, 2002) in marine food webs (Navarro et al., 2011). Carbon isotope ratios show little change due to trophic transfer, but are useful indicators of dietary sources of carbon (Fry and Sherr, 1984, Michener and Schell, 1994). Furthermore, by analyzing both δ15N and δ13C data together it is possible to estimate trophic width of species, populations and ecosystems by calculating isotopic area (Layman et al., 2011).

In marine systems, applications of stable isotope analysis have grown substantially in recent decades as analytical costs of have decreased, the capabilities of laboratories and the statistical methodologies for interpretation of isotopic data have improved, being more accessible for non-specialist researchers (Jackson et al., 2011, Layman et al., 2011). Recent studies have used stable isotope analysis to examine the trophic ecology of squids or the trophic relationships among squid guilds (e.g., Cherel and Hobson, 2005, Cherel et al., 2009, Fanelli et al., 2012, Hunsicker et al., 2010, Jackson et al., 2007, Lorrain et al., 2011, Ruiz-Cooley et al., 2010). However, the majority of available isotopic information on squids is dispersed in studies of the trophic ecology of numerous marine predators (Fig. 1), in which the isotope values of squids were analyzed to interpret the isotope values of their predators (e.g., Cardona et al., 2012, Ciancio et al., 2008, Hobson and Montevecchi, 1991, Navarro et al., 2009, Praca et al., 2011). Therefore a synthesis of the available isotopic data for squids is desirable.

An important limitation when comparing nitrogen isotope values of consumers from different geographic locations is the fact that the isotopic composition of seawater varies greatly at different locations, resulting in high isotopic variability of the primary producers at the base of each food web. Since the natural range of nitrogen isotopes in seawater (∼0–12‰) (Somes et al., 2010) is larger than the step-wise increase per trophic level (∼3‰), this must be accounted for when estimating trophic position. One approach is to adjust the isotopic values of consumers by the isotopic values of organisms located at the base of the food webs, such as phytoplankton or zooplankton (Post, 2002, Carscallen et al., 2012).

In this study, we synthesized the available stable isotope data from different oceans and ecosystems and adjusted squid δ15N values for baseline isotopic variability derived from an ocean circulation–biogeochemistry–isotope model to obtain a global picture of the trophic niche of squids in marine ecosystems. In particular, we aimed to (1) examine whether the trophic position inferred from baseline-adjusted δ15N values and (2) the trophic widths (isotopic area using δ15N and δ13C values) of squid species vary among oceans and among ecosystem types.

Section snippets

Stable isotope records

We collected stable isotope data for squids from published sources worldwide (Fig. 2a) (complete list of species and references in Table S1), using the electronic bibliographic database ISI Web of Knowledge and keywords “squid” and “stable isotopes” and the Google Scholar database.

For each publication we recorded the species, geographical sampling location, ocean, ecosystem type, number of samples analyzed, type of tissue analyzed, mean and standard deviation of δ15N and δ13C and main focus of

Stable isotope dataset

We compiled stable isotope data (δ15N and δ13C values) for 89 squid species in 62 published studies from 57 geographical locations (Figs. 1 and 2a, Table S1). The first study we found that reported stable isotope values for a squid was published in 1982, and the first study that focused on the trophic ecology of a squid based on stable isotopes was in 2004 (Fig. 1). Forty-six studies included stable isotope values of squids to investigate the diets of their predators (seabirds, marine mammals

Discussion

In this study, we present the first review of available data on two trophic markers, δ15N and δ13C, for squids, contributing to the knowledge of the trophic ecology of these abundant invertebrates in marine ecosystems. Since squids proliferate in a variety of ecosystems, some highly exploited by fisheries (Dawe et al., 2000, Sakurai et al., 2000, Bellido et al., 2001, Coll et al., 2013), it is desirable to improve our understanding of the ecological role of these organisms and their importance

Acknowledgments

JN was supported by a postdoctoral contract of the Juan de la Cierva program of the Spanish Government. MC was supported by a research contract of the Ramon y Cajal program of the Spanish Government. CS was supported by the SFB754 project of the German Research Foundation (DFG). This paper is a contribution to a CLIOTOP initiative to develop understanding of squid in pelagic ecosystems.

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