Journal of the Marine Biological Association of the United Kingdom, 2019, 99(3), 673–680. # Marine Biological Association of the United Kingdom, 2018 doi:10.1017/S0025315418000474 Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador colombo estupin~a’ n-montan~o1,2, luis ceden~o-figueroa3, jose’ f. estupin~a’ n-ortiz1, felipe galva’ n-magan~a4, alejandro sandoval-london~o1,5, david castan~eda-suarez6 and carlos j. polo-silva6 1Fundacio´n Alium Pacific, Carrera 26 No. 5C–13, Cali, Colombia, 2Servicio Nacional de Aprendizaje, Centro Agroindustrial y Pesquero de la Costa Pacı´fica, La Chiricana km 21, Tumaco, Colombia, 3Facultad Ciencias del Mar, Universidad Laica “Eloy Alfaro” de Manabı´, Manta, Ecuador, 4Instituto Polite´cnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, La Paz, Baja California Sur, C.P. 23096, Mexico, 5Corporacio´n Acade´mica Ambiental, Universidad de Antioquia, Calle 70 No. 52-21, Medellı´n, Colombia, 6Facultad de Ciencias Naturales e Ingenierı´a, Programa de Biologı´a Marina, Universidad de Bogota´ Jorge Tadeo Lozano, Santa Marta, Colombia As apex predators, sharks are known to play an important role in marine food webs. Detailed information on their diet and trophic level is however needed to make clear inferences about their role in the ecosystem. A total of 335 stomachs of smooth hammerhead sharks, Sphyrna zygaena, were obtained from commercial fishing vessels operating in the Ecuadorian Pacific between January and December 2004. A total of 53 prey items were found in the stomachs. According to the Index of Relative Importance (%IRI), cephalopods were the main prey (Dosidicus gigas, Sthenoteuthis oualaniensis, Ancistrocheirus lesueurii and Lolliguncula [Loliolopsis] diomedeae). Sphyrna zygaena was thus confirmed to be a teutopha- gous species. The estimated trophic level of S. zygaena was between 4.6 and 5.1 (mean + SD: 4.7 + 0.16; males: 4.7; females: 4.8). Levin’s index (BA) was low (overall: 0.07; males: 0.08; females: 0.09), indicating a narrow trophic niche. We found that sharks ,150 cm in total length consumed prey of coastal origin, whereas sharks ≥150 cm foraged in oceanic waters and near the continental shelf. The analyses indicate that S. zygaena is a specialized predator consuming mainly squids. Keywords: Diet, Ecuador, ontogeny, top predator, food web, seasonal variations Submitted 10 February 2017; accepted 7 June 2018; first published online 13 July 2018 INTRODUCTION Onychoteuthis banksii and squids of the family Cranchiidae). Off the coast of South Africa, Smale (1991) Some shark species have experienced population declines, noted that the diet of juveniles of S. zygaena was composed mainly due to overfishing, bycatch, pollution and habitat deg- mainly of small fishes, followed by cephalopods (e.g. Loligo radation (Dulvy et al., 2008). Recent studies suggest that reynaudii), some elasmobranchs and teleosts (Merluccius populations of large sharks have declined by 90% or more capensis, Trachurus capensis and Lepidopus caudatus). The in some regions (Myers et al., 2007), making them one of squid Loligo reynaudii, found in coastal habitats, was the most threatened group of marine animals worldwide however the most important prey, indicating a preference (Heithaus et al., 2010; Lucifora et al., 2011). The implementa- for neritic cephalopod species. tion of effective strategies for the conservation and manage- Also in South Africa, Smale & Cliff (1998) showed that the ment of sharks is often hampered by the lack of diet of small S. zygaena specimens (,100 cm precaudal information regarding their diet, life history and behaviour length) was dominated in both number and mass by neritic (Shiffman et al., 2012). For example, few studies have cephalopods (of the families Loliginidae and Sepiidae), while focused on describing the dietary habits of Sphyrna zygaena that of larger specimens (.100 cm precaudal length) included around the world. Galva´n-Magan˜a et al.(1989) described oceanic squids (Ancistrocheirus lesueurii, Ommastrephes bar- the diet of S. zygaena in the Gulf of California, Mexico, as tramii, Ornithoteuthis volatilis, Sthenoteuthis oualaniensis, being based on pelagic cephalopods (Histioteuthis heteropsis, Todarodes filippovae and Todarodes spp.), which suggests a change in habitat use as sharks mature. Off the southern coast of Brazil, Bornatowski et al.(2007) Corresponding author: described S. zygaena as ichthyophagous and teutophagous, F. Galva´n-Magan˜a with a preference for coastal areas at the juvenile stage, when Email: [email protected] its diet is composed mainly of squids of the genus Loligo.Also 673 Downloaded from https://www.cambridge.org/core. IP address: 186.29.4.34, on 02 Apr 2020 at 21:54:00, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315418000474 674 colombo estupin~ a’ n-montan~ o et al. in Brazil, Bornatowski et al.(2014a) concluded that juveniles of basis for determining whether the number of stomachs was S. zygaena are teutophagous, with a diet based on the inshore sufficient. In addition, a quantitative criterion for assessing squids Doryteuthis spp. and Lolliguncula (Lolliguncula) brevis. sample-size sufficiency was used to determine whether the Galva´n-Magan˜a et al.(2013) and Rosas-Luis et al.(2015)also cumulative prey curves approached an asymptote, by compar- reported that in the Mexican and Ecuadorian Pacific, respect- ing the slope of the line generated from the curve’s four last ively, S. zygaena preys on various squid species. points to a slope of zero through a Student’s t-test. If the Understanding the ecological role of a species within an slopes were not significantly different (P . 0.05), the prey ecosystem depends on the knowledge of its trophic relation- curve was considered to approach an asymptote (Bizzarro ships (Braga et al., 2012). Trophic studies allow us to under- et al., 2007). Sample-size sufficiency could not be tested for stand the functional role of organisms within marine individual size classes because of the small number of indivi- communities (e.g. predator–prey relationships), hence pro- duals in each class. viding important information on resource partitioning, com- To assess the importance of each prey taxon to the diet of S. petition, energy transfer, and food dynamics (Navia et al., zygaena, the Index of Relative Importance (IRI; Pinkas et al., 2010; Bornatowski et al., 2014a). A quantitative understanding 1971) was calculated as follows: IRI ¼ (%N + %W) (%FO); of the feeding ecology of shark species enables researchers to where %N is the number of a given prey type as a percentage describe complex marine food webs (Navia et al., 2010; of the total number of prey taxa (Hyslop, 1980), %W is the Bornatowski et al., 2014a) and develop ecosystem models mass of a given prey type as a percentage of the total mass for evaluating the function of each prey species within the eco- of prey consumed, and %FO is the percentage of frequency system, and predicting possible changes due to fishing effects of occurrence of each prey type (Hyslop, 1980). IRI values (Stevens et al., 2000). Studies of a species’ feeding ecology are were standardized to percentages according to Corte´s(1997). important not only for knowing the relative frequency of each Diet niche breadth was estimated using Levin’s index (Bi): 2 –1 particular prey in its diet, but also for revealing whether this Bi ¼ (SPij) (Krebs, 1999), where Pij is the fraction by N of species (of, e.g. shark or batoid) acts as a link between different each food j in the diet (SPj ¼ 1). Bi values were standardized levels of the food chain (Bornatowski et al., 2014b). (BA) so that they ranged from 0 to 1 by using the equation: –1 These complex approaches depend on the availability of BA ¼ (Bi –1) (N–1) , where N is the number of classes data describing the species’ basic diet, and are thus affected (Krebs, 1999). Low BA values indicate narrow, specialized by the lack of basic knowledge of the diet of some fish diets, whereas high values indicate generalist diets. species (Bornatowski et al., 2014b). Studies such as this one, Trophic overlap was assessed by calculating the Morisita– in conjunction with other biological studies, will thus ultim- Horn index (Cl; Smith & Zaret, 1982) to detect possible differ- ately allow more appropriate management and conservation ences in diet between sexes and size classes: measures to be implemented for elasmobranch species (Galva´n-Magan˜a et al., 1989). n ( × ) = i=1 pxi pyi Sphyrna zygaena is the fourth most commonly caught Cl 2 n n P2 + P2 shark species in Ecuador (Martı´nez-Ortı´z et al., 2007). It is i=1 xi i=1 yi listed as ‘Vulnerable’ in the International Union for th Conservation of Nature (IUCN) Red List (Casper et al., where Pxi is the proportion of the i prey with respect to all th 2005). The aim of this study was (1) to describe the species’ prey of predator x; Pyi is the proportion of the i prey with dietary spectrum; (2) to estimate its relative trophic level; respect to all prey of predator y, and n is the total number and (3) to identify ontogenetic shifts in diet between maturity of prey species. This index ranges from 0 to 1, with values stages. close to zero indicating dietary differences, and values close to one, similarity in the prey consumed. To test for shifts in diet between years, sexes and maturity MATERIALS AND METHODS stages, a one-way non-parametric permutational multivariate analysis of variance (PERMANOVA) was used (Anderson, The diet of 335 smooth hammerhead sharks, Sphyrna zygaena 2001). This method allows multivariate data to be analysed (Linnaeus, 1758), was determined using stomach content ana- based on any distance or dissimilarity measure, with P lysis.