Pelagic cephalopods in the western Indian Ocean: New information from diets of top predators

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Abstract

Using a combination of diverse large predatory fishes and one seabird, we collected information on the cephalopod fauna of the western Indian Ocean. We analyzed the stomach contents of 35 fishes representing ten families (Xiphiidae, Istiophoridae, Scombridae, Carangidae, Coryphaenidae, Alepisauridae, Dasyatidae, Carcharhinidae, Alopiidae and Sphyrnidae) and of the sooty tern Onychoprion fuscata of the Mozambique Channel from 2000 to 2010. Both fresh and accumulated beaks were used for identifying cephalopod prey. Cephalopods were important prey for twelve predators; swordfish Xiphias gladius had the highest cephalopod proportion; sooty tern (O. fuscata) and bigeye tuna (Thunnus obesus) had high proportions too. We recovered 23 cephalopod families and identified 38 species. Ten species from four Teuthida families (Ommastrephidae, Onychoteuthidae, Histioteuthidae and Ancistrocheiridae) and two Octopoda families (Argonautidae and Bolitaenidae) occurred very frequently in the stomach contents, while Sepiida were rare. Ommastrephidae were the most cephalopod food sources: the purpleback flying squid Sthenoteuthis oualaniensis was the most prevalent prey by far, Ornithoteuthis volatilis was important for eleven predators and few but large specimens of the neon flying squid Ommastrephes bartramii were recovered in the stomachs of swordfish in the Indian South Subtropical Gyre province only. Predators' groups were identified based on cephalopod prey composition, on depth in which they forage, and on prey size. Surface predators' diets were characterized by lower cephalopod diversity but greater average numbers of cephalopod prey, whereas the deep-dwelling predators (swordfish and bigeye tuna) preyed on larger specimens than surface predators (O. fuscata or yellowfin tunas Thunnus albacares). Our findings emphasized the usefulness of a community of marine predators to gain valuable information on the biology and the distribution of the cephalopod forage fauna that are discussed with regard to biogeographic province, marine predator, fishing gear to catch the large pelagic fishes, and size of the beaks recovered in the stomachs.

Introduction

Cephalopods are widely distributed in the open ecosystems of the world ocean: they are among the most abundant in number and biomass of nektonic organisms (Jereb and Roper, 2010), and are a dominant component in marine food webs both as predators and as food for top predators (Rodhouse and White, 1995, Clarke, 1996, Boyle and Rodhouse, 2005). In addition they are a valuable direct human resource and are heavily exploited for bait by fisheries. Several important families such as the Ommastrephidae family (e.g., Illex argentinus, Dosidicus gigas) support major fisheries in both neritic and oceanic waters around the world (Rodhouse, 1997, Hunsicker et al., 2010). This commercial importance has made the large ommastrephids the target of many scientific investigations and their biology is consequently reasonably well-known (Nigmatullin et al., 2001, Zuyev et al., 2002, Bower and Ichii, 2005, Markaida, 2006, Parry, 2006, Parry, 2008, Xinjun et al., 2007). However, the biology and ecological role of the unexploited squid species remain poorly known in many areas of the world ocean, including the tropical and equatorial ecosystems of the Indian Ocean. Much more investigations are needed on cephalopods in order to better understand their role in the marine ecosystems. But research cruises devoted to the study of squids are very few, and in addition, cephalopods are difficult to collect by nets. Large predatory fishes (e.g., tunas, billfishes, swordfish, etc.), marine mammals and seabirds can be efficient biological samplers for collecting information on cephalopods, due to their opportunistic feeding behavior (Rodhouse, 1990, Cherel and Weimerskirch, 1999, Cherel et al., 2004, Cherel et al., 2007, Potier et al., 2007). Indeed, cephalopod predators capture larger specimens and a greater diversity of species than does sampling gear. In stomach contents, cephalopod beaks are diagnostic hard part structures that resist digestion and that can accumulate over time (beaks without flesh attached and/or eroded). Therefore, both fresh and accumulated beaks in good condition are a helpful source of information for identifying cephalopod prey ingested by predators (Clarke, 1986). Investigations on the dietary habits of large marine predators can thus provide new information on species composition, abundance, and distribution of cephalopods occurring within the predator foraging range (Cherel et al., 2004).

In this study, our main objective was to collect information on the cephalopod community of the western Indian Ocean using a combination of several large fish predators and one seabird as biological samplers. We used an extensive dataset of stomach samples collected from a diverse community of large predatory fishes representing ten families (Xiphiidae, Istiophoridae, Scombridae, Carangidae, Coryphaenidae, Alepisauridae, Dasyatidae, Carcharhinidae, Alopiidae and Sphyrnidae). Fishes were caught in the area by fishery vessels from 2000 to 2010. In addition, we used an extra dataset from dietary habit of sooty tern Onychoprion fuscata investigated during the breeding seasons on three islands of the Mozambique Channel (Europa, Juan de Nova and Glorieuses). The sooty tern is the most abundant marine bird species in all tropical waters. The cephalopod diversity recovered in the stomach contents of these marine predators is constrained by local prey availability and the foraging behavior of predators, including vertical distribution for fishes arising from physiological abilities. These varying sources of information allowed us to investigate the usefulness of cephalopod eaters for describing the importance of cephalopods in the pelagic food webs of the western Indian Ocean.

Section snippets

Sample collection

From 2000 to 2010, 35 large predatory fishes (sharks, billfishes, scombrids, carangids and other osteichthyes) were sampled in the western Indian Ocean from longline and purse seine cruises, and from troll lines, in three biogeographic provinces of Longhurst (1998): the Indian Monsoon Gyres province (MONS), the Indian South Subtropical Gyre province (ISSG), the Eastern Africa Coastal province (EAFR) (Fig. 1 and Table 1). Longhurst's division is based on biogeochemical properties of the

Cephalopods in the diet of the predators

Fish prey dominated by wet mass (>50%) the diet of 18 predators among the 35 fish predators investigated in our study, and the diet of the sooty tern (Table 2). For seven species, fish were the only food source. Cephalopods constituted the majority of the mollusc prey by wet mass except for Decapterus macarellus. Twenty-one predators had fresh remains of cephalopods in their diet. No predator had only accumulated beaks. A total of 3684 lower beaks were recovered in predators' stomachs: 2360

Discussion

Overall the micronekton fauna of the western Indian Ocean is poorly documented. To our knowledge this study is the first in the western Indian Ocean that investigates the importance of pelagic cephalopods using an extensive number of marine predators as biological samplers of the cephalopod fauna. Potier et al. (2007) analyzed the prey composition and the resource partitioning among three large pelagic fish predators caught by longline in the waters surrounding the Seychelles Islands. These

Acknowledgment

We wish to thank the institutions and projects which provided vessels for the different cruises and contributed financially to the lease of those platforms: IRD, the Paul Emile Victor Institute (IPEV), the Agulhas Somali Currents Large Marine Ecosystem (ASCLME) project, the South West Indian Ocean Fisheries Project (SWIOFP), and the Fonds Français pour l'Environnement Mondial (FFEM). Funding was also provided by the IOSSS project (European Fisheries Funds UE-FEP 2007–2013 No. 31122/DRAM/2009

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