Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids

Abstract

Cephalopods play a key role in the marine environment but knowledge of their feeding habits is limited by lack of data. Here, we have developed a new tool to investigate their feeding ecology by combining the use of their predators as biological samplers together with measurements of the stable isotopic signature of their beaks. Cephalopod beaks are chitinous hard structures that resist digestion and the stable isotope ratios of carbon (d 13 C) and nitrogen (d 15 N) are indicators of the foraging areas and trophic levels of consumers, respectively. First, a comparison of d 13 C and d 15 N values of different tissues from the same individuals showed that beaks were slightly enriched in 13 C but highly impoverished in 15 N compared with lipid-free muscle tissues. Second, beaks from the same species showed a progressive increase in their d 15 N values with increasing size, which is in agreement with a dietary shift from lower to higher trophic levels during cephalopod growth. In the same way, there was an increase in the d 15 N signature of various parts of the same lower beaks in the order rostrum, lateral walls and wings, which reflects the progressive growth and chitinization of the beaks in parallel with dietary changes. Third, we investigated the trophic structure of a cephalopod community for the first time. Values of d 15 N indicate that cephalopods living in slope waters of the subantarctic Kerguelen Islands (nZ18 species) encompass almost three distinct trophic levels, with a continuum of two levels between crustacean-and fish-eaters and a distinct higher trophic level occupied by the colossal squid Mesonychoteuthis hamiltoni. d 13 C values demonstrated that cephalopods grow in three different marine ecosystems, with 16 species living and developing in Kerguelen waters and two species migrating from either Antarctica (Slosarczykovia circumantarctica) or the subtropics (the giant squid Architeuthis dux). The stable isotopic signature of beaks accumulated in predators' stomachs therefore revealed new trophic relationships and migration patterns and is a powerful tool to investigate the role of the poorly known cephalopods in the marine environment.

Extreme food webs: Foraging strategies and diets of scavenging amphipods from the ocean’s deepest 5 kilometers

“…Thus, detrivory or feeding on small carcasses offers a means to sustain energetic requirements between episodes of large carrion fall (Dahl 1979). Notably, chitin tends to be significantly impoverished in d 15 N as compared to muscle tissue (Cherel and Hobson 2005). Since juvenile amphipods tend to exhibit a higher chitin to muscle mass ratio than adults, it is possible that chitin additively biases this ontogenetic pattern to some degree.…”

Uncommon pelagic and deep-sea cephalopods in the Mediterranean: new data and literature review

“…As mentioned earlier, however, such infrequency most probably reflects the inefficiency of the sampling gears, which are not designed to collect oceanic cephalopods, because the stomach content analyses of their predators indicate that they are abundant in the open waters (e.g. Bello, 2000;Cherel & Hobson, 2005). Furthermore, there could be differences in capturing them even between the experimental and commercial bottom trawlers using different mesh sizes and vertical openings (Maiorano et al, 1999;Lefkaditou et al, 2003a,b).…”

Species identification of <i>Ommastrephes bartramii, Dosidicus gigas, Sthenoteuthis oualaniensis</i> and <i>Illex argentinus</i> (Ommastrephidae) using beak morphological variables

“…The allometric regression models between beak size versus mantle length and body weight of cephalopods can yield estimates of cephalopod biomass (Lu and Ickerignill 2002). Other biological attributes of beaks, such as pigment deposits (Ivanovic and Brunetti 1997, Hernandez-García et al 1998), rings (Hernández-López et al 2001) and stable isotopes (Cherel and Hobson 2005), can also help improve our understanding of cephalopod life history and ecology. For example, the stable isotopic signatures of beaks found in predators´ stomachs can be used to determine trophic relationships and migration patterns, and thus are a powerful tool for investigating the role played by poorly known cephalopods in the marine environment Cherel 2006, Xavier et al 2007).…”

“…Morphological characteristics of body and hard structures have often been used to identify cephalopod species with close affinities (Roper et al 1984, Jackson 1995, Doubleday et al 2006. Since chitinous beaks have a relatively consistent shape (Smale 1996, Clarke 1996, 1998, Neige and Boletzky 1997 and are more resistant to fragmentation than other hard structures, such as the statolith and inner shell, they have been proven to be valuable for studying cephalopod predators (Lu andIckeringill 2002, Cherel andHobson 2005).…”

“…The other three species have a much more limited geographical distribution and do not overlap with each other. These four important squid support a world fishery that had a annual catch ranging from 1.1 to 1.65 million tonnes in 2005to 2007(FIGIS 2009). In addition, they play a vital role in their marine ecosystems, in particular as important prey for predators such as tuna, swordfish, sharks and whales (Desportes and Mouritsen 1988, Clarke 1996, Benjamins 2000.…”