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

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 (delta(13)C) and nitrogen (delta(15)N) are indicators of the foraging areas and trophic levels of consumers, respectively. First, a comparison of delta(13)C and delta(15)N values of different tissues from the same individuals showed that beaks were slightly enriched in C-13 but highly impoverished in N-15 compared with lipid-free muscle tissues. Second, beaks from the same species showed a progressive increase in their delta(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 delta(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 delta(15)N indicate that cephalopods living in slope waters of the subantarctic Kerguelen Islands (n = 18 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. delta(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.