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        Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador
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        Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador
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        Feeding habits and trophic level of the smooth hammerhead shark, Sphyrna zygaena (Carcharhiniformes: Sphyrnidae), off Ecuador
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Abstract

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 teutophagous 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.

INTRODUCTION

Some shark species have experienced population declines, mainly due to overfishing, bycatch, pollution and habitat degradation (Dulvy et al., 2008). Recent studies suggest that populations of large sharks have declined by 90% or more in some regions (Myers et al., 2007), making them one of the most threatened group of marine animals worldwide (Heithaus et al., 2010; Lucifora et al., 2011). The implementation of effective strategies for the conservation and management of sharks is often hampered by the lack of information regarding their diet, life history and behaviour (Shiffman et al., 2012). For example, few studies have focused on describing the dietary habits of Sphyrna zygaena around the world. Galván-Magaña et al. (1989) described the diet of S. zygaena in the Gulf of California, Mexico, as being based on pelagic cephalopods (Histioteuthis heteropsis, Onychoteuthis banksii and squids of the family Cranchiidae). Off the coast of South Africa, Smale (1991) noted that the diet of juveniles of S. zygaena was composed mainly of small fishes, followed by cephalopods (e.g. Loligo reynaudii), some elasmobranchs and teleosts (Merluccius capensis, Trachurus capensis and Lepidopus caudatus). The squid Loligo reynaudii, found in coastal habitats, was however the most important prey, indicating a preference for neritic cephalopod species.

Also in South Africa, Smale & Cliff (1998) showed that the diet of small S. zygaena specimens (<100 cm precaudal length) was dominated in both number and mass by neritic cephalopods (of the families Loliginidae and Sepiidae), while that of larger specimens (>100 cm precaudal length) included oceanic squids (Ancistrocheirus lesueurii, Ommastrephes bartramii, Ornithoteuthis volatilis, Sthenoteuthis oualaniensis, 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) described S. zygaena as ichthyophagous and teutophagous, with a preference for coastal areas at the juvenile stage, when its diet is composed mainly of squids of the genus Loligo. Also in Brazil, Bornatowski et al. (2014a) concluded that juveniles of S. zygaena are teutophagous, with a diet based on the inshore squids Doryteuthis spp. and Lolliguncula (Lolliguncula) brevis. Galván-Magaña et al. (2013) and Rosas-Luis et al. (2015) also reported that in the Mexican and Ecuadorian Pacific, respectively, S. zygaena preys on various squid species.

Understanding the ecological role of a species within an ecosystem depends on the knowledge of its trophic relationships (Braga et al., 2012). Trophic studies allow us to understand the functional role of organisms within marine communities (e.g. predator–prey relationships), hence providing important information on resource partitioning, competition, energy transfer, and food dynamics (Navia et al., 2010; Bornatowski et al., 2014a). A quantitative understanding of the feeding ecology of shark species enables researchers to describe complex marine food webs (Navia et al., 2010; Bornatowski et al., 2014a) and develop ecosystem models for evaluating the function of each prey species within the ecosystem, and predicting possible changes due to fishing effects (Stevens et al., 2000). Studies of a species’ feeding ecology are important not only for knowing the relative frequency of each particular prey in its diet, but also for revealing whether this species (of, e.g. shark or batoid) acts as a link between different levels of the food chain (Bornatowski et al., 2014b).

These complex approaches depend on the availability of data describing the species’ basic diet, and are thus affected by the lack of basic knowledge of the diet of some fish species (Bornatowski et al., 2014b). Studies such as this one, in conjunction with other biological studies, will thus ultimately allow more appropriate management and conservation measures to be implemented for elasmobranch species (Galván-Magaña et al., 1989).

Sphyrna zygaena is the fourth most commonly caught shark species in Ecuador (Martínez-Ortíz et al., 2007). It is listed as ‘Vulnerable’ in the International Union for Conservation of Nature (IUCN) Red List (Casper et al., 2005). The aim of this study was (1) to describe the species’ dietary spectrum; (2) to estimate its relative trophic level; and (3) to identify ontogenetic shifts in diet between maturity stages.

MATERIALS AND METHODS

The diet of 335 smooth hammerhead sharks, Sphyrna zygaena (Linnaeus, 1758), was determined using stomach content analysis. A total of 156 sharks (72 males and 84 females) were caught between July and December 2003 (rainy season), and 179 more (95 males and 84 females) were caught between January and June 2004 (dry season). The sharks were caught in Ecuadorian waters and landed in the port of Manta (Ecuador). The study area extended from 02°N to 02°S, and from the coast to 84°W. For each shark specimen, total length was measured and sex was determined before extracting the digestive tract. Stomach contents were removed and filtered through a 1.5-mm mesh sieve, stored in plastic bags, and preserved on ice for transportation to the laboratory.

To determine whether the number of stomachs was adequate to describe the diet of S. zygaena, cumulative prey curves were constructed using the Shannon method, and samples were randomized 500 times with the ‘sample-based rarefaction’ routine in EstimateS 9.10 software (Colwell, 2013). The coefficient of variation (CV = 0.05) served as the basis for determining whether the number of stomachs was sufficient. In addition, a quantitative criterion for assessing sample-size sufficiency was used to determine whether the cumulative prey curves approached an asymptote, by comparing the slope of the line generated from the curve's four last points to a slope of zero through a Student's t-test. If the slopes were not significantly different (P > 0.05), the prey curve was considered to approach an asymptote (Bizzarro et al., 2007). Sample-size sufficiency could not be tested for individual size classes because of the small number of individuals in each class.

To assess the importance of each prey taxon to the diet of S. zygaena, the Index of Relative Importance (IRI; Pinkas et al., 1971) was calculated as follows: IRI = (%N + %W) (%FO); where %N is the number of a given prey type as a percentage of the total number of prey taxa (Hyslop, 1980), %W is the mass of a given prey type as a percentage of the total mass of prey consumed, and %FO is the percentage of frequency of occurrence of each prey type (Hyslop, 1980). IRI values were standardized to percentages according to Cortés (1997).

Diet niche breadth was estimated using Levin's index (B i): B i = (ΣP ij2)–1 (Krebs, 1999), where P ij is the fraction by N of each food j in the diet (ΣP j = 1). B i values were standardized (B A) so that they ranged from 0 to 1 by using the equation: B A = (B i–1) (N–1)–1, where N is the number of classes (Krebs, 1999). Low B A values indicate narrow, specialized diets, whereas high values indicate generalist diets.

Trophic overlap was assessed by calculating the Morisita–Horn index (C λ; Smith & Zaret, 1982) to detect possible differences in diet between sexes and size classes:

$$C_{\rm \lambda} = 2\displaystyle{{\mathop \sum \nolimits_{i = 1}^n (\,p_{xi} \times p_{yi})} \over {\mathop \sum \nolimits_{i = 1}^n P_{xi}^2 + \mathop \sum \nolimits_{i = 1}^n P_{yi}^2}}$$

where P xi is the proportion of the ith prey with respect to all prey of predator x; P yi is the proportion of the ith prey with respect to all prey of predator y, and n is the total number of prey species. This index ranges from 0 to 1, with values 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 stages, a one-way non-parametric permutational multivariate analysis of variance (PERMANOVA) was used (Anderson, 2001). This method allows multivariate data to be analysed based on any distance or dissimilarity measure, with P values obtained using 500 permutations.

The maturity stage of each shark was recorded using the criteria proposed by Nava & Márquez-Farías (2014), where the size at first maturity is 194 cm total length for males, and 200 cm total length for females. The specimens of S. zygaena measuring 90 to 300 cm total length were grouped into three size classes (Size I = 90.0–142.5 cm; Size II = 142.5–195.0 cm; Size III = 195.0–300.0 cm).

The standardized trophic level (TL) of sharks was calculated using the trophic index proposed by Cortés (1999):

$${\rm T}{\rm L}_k = 1 + \left( {\mathop \sum \limits_{\,j = 1}^n P_j \times {\rm T}{\rm L}_j} \right)$$

where TLk is the trophic level of each prey taxon j and P j is the proportion of each prey category j in the predator's diet, based on %N values (Cortés, 1999). The trophic level was estimated for each specimen of S. zygaena, and then was averaged. The trophic levels of prey were obtained from Cortés (1999), Hobson & Welch (1992), www.fishbase.org (Froese & Pauly, 2015) and www.seaaroundus.org (Pauly & Zeller, 2015).

RESULTS

Cumulative prey curves

Of the 335 Sphyrna zygaena specimens examined (130 males, 171 females and 34 unsexed individuals), 91.9% (N = 308) had food in their stomach, that is, 86.92% of the males (N = 113) and 94.15% of the females (N = 161). Fifty-three prey items could be identified, together with fish and squid remains.

Based on the constructed cumulative prey curves, sample size was adequate to describe the general diet of S. zygaena (Nmin = 31; Student's t-test: t = –1.73, P = 0.18) as well as that of males (Nmin = 42; t = –1.73, P = 0.18) and females (Nmin = 36; t = 0.65, P = 0.56; Figure 1).

Fig. 1. Prey accumulation curves for Sphyrna zygaena caught in Ecuador (A: males, B: females and C: both sexes combined).

Diet

The diet of S. zygaena was mainly composed of cephalopods and teleosts, cephalopods making up the highest percentage in number, weight and frequency of occurrence. The %IRI indicated that Dosidicus gigas, Sthenoteuthis oualaniensis and Ancistrocheirus lesueurii were the most important prey in the stomach contents (Table 1).

Table 1. Trophic spectrum of Sphyrna zygaena caught in Ecuador and trophic level (TL) of each prey species.

%N, percentage in number; %W, percentage in weight; %FO, percentage in frequency of occurrence; and %IRI, percentage Index of Relative Importance.

a Taken from: Froese & Pauly (2015), Cortés (1999), Pauly et al. (1998), Hobson & Welch (1992) and Pauly & Zeller (2015).

Within years, males and females did not show significant dietary differences, both sexes consuming Dosidicus gigas and Sthenoteuthis oualaniensis (global F = 10.14, P = 0.38 for 2003; P = 0.69 for 2004; Table 3). However, S. oualaniensis made a much smaller contribution to the diet of females compared with that of males (Table 2). When comparing the males and females between years, however, significant dietary differences were found (F = 10.14, P = 0.02 for both males and females; Table 3).

Table 2. Trophic spectrum by sex and year of Sphyrna zygaena caught in Ecuador based on the percentage Index of Relative Importance (%IRI).

Table 3. Permutational multivariate analysis of variance (PERMANOVA) based on Euclidean distance matrix of prey data from stomach contents of Sphyrna zygaena off Ecuador, for sexes (M = males; F = females), size classes and years.

df, Degrees of freedom; F, F-value; P, P-value (0.05).

The most important prey of sharks of all sizes was Dosidicus gigas (for Size-I2003, Size-I2004, Size-II2003, Size-II2004, Size-III2003 and Size-III2004) and, to a much lesser extent, Lolliguncula (Loliolopsis) diomedeae (for Size-I2004 and Size-II2004 sharks), Sthenoteuthis oualaniensis (for Size-I2004, Size-II2003, Size-II2004 and Size-III2004 sharks), Ancistrocheirus lesueurii (for Size-II2003, Size-III2003 and Size-III2004 sharks) and Mastigoteuthis spp. (for Size-III2003 sharks), suggesting ontogenetic changes in diet, both within and between years (global F = 7.88, P = 0.02; Figure 2; Table 3).

Fig. 2. Trophic spectrum by size class of Sphyrna zygaena caught in Ecuador, based on the percentage Index of Relative Importance (%IRI).

The trophic analysis by maturity stage showed that both juveniles and adults consume a large proportion of D. gigas (IRI = 83.58% and 82.22%, respectively). However, juveniles complement their diet with the squids S. oualaniensis and L. (Loliolopsis) diomedeae (IRI = 6.73% and 4.04%, respectively), while adults complement theirs with the squids Mastigoteuthis spp. and A. lesueurii (IRI = 6.14% and 5.89%, respectively). Overall, this suggests that sharks at different maturity stages have a similar diet (global F = 0.82, P = 0.62; Figure 3).

Fig. 3. Trophic spectrum by maturity stage of Sphyrna zygaena caught in Ecuador, based on the percentage Index of Relative Importance (%IRI).

The trophic analysis by season showed that in both the rainy and dry season, sharks consumed D. gigas (IRI = 84.6% and 57.8%, respectively), S. oualaniensis (IRI = 6.66% and 22.4%, respectively), A. lesueurii (IRI = 5.11% and 0.67%, respectively) and L. (Loliolopsis) diomedeae (IRI = 1.94% and 5.46%, respectively; global F = 28.7, P = 0.002).

Niche breadth and trophic overlap

Values of standardized Levin's niche breadth were <0.6 for males, females and both sexes combined (Table 4), which indicates that S. zygaena is a specialized predator.

Table 4. Trophic overlap (based on the Morisita–Horn index, C λ), trophic level (TL) and niche breadth (B A) estimated in Sphyrna zygaena off Ecuador for different size classes and years.

The trophic overlap index showed that similar prey were consumed by males and females (C λ−overall = 0.98, 95% CI = 0.97–0.98; C λ2003 = 0.98, 95% CI = 0.97–0.98; and C λ2004 = 0.84, 95% CI = 0.82–0.87) and by sharks of different size classes (Table 4).

Relative trophic level

The mean trophic level estimated for both sexes combined was 4.7 ± 0.16 (mean ± SD; TL2003 = 4.8 ± 0.13; TL2004 = 4.0 ± 0.13). The mean trophic level of males was 4.7 (TL2003 = 4.8; TL2004 = 4.5), and that of females, 4.8 (TL2003 = 4.9; TL2004 = 4.5). When estimated by size class, mean trophic level ranged from 4.6 to 5.1, increasing with size, indicating that the smooth hammerhead shark is a tertiary carnivore (Table 4; Cortés, 1999).

DISCUSSION

The diet of Sphyrna zygaena was dominated by three cephalopod species: Dosidicus gigas, Sthenoteuthis oualaniensis and Ancistrocheirus lesueurii. Other studies worldwide have reported that this shark species consumes a variety of teleosts (e.g. anchovies, saltwater catfish, perch, mackerel, snapper), smaller sharks, guitarfish, rays, shrimps, crabs, as well as squids and other cephalopods (see, among others, Bigelow & Schroeder, 1948; Bass et al., 1975; Compagno, 1984; Stevens, 1984; Bornatowski et al., 2014b).

Our trophic analysis showed similarity in the diets of males and females (C λ = 0.98): in the same year, both sexes used the same food resources, although in different proportions (D. gigas, S. oualaniensis, A. lesueurii and Lolliguncula (Loliolopsis) diomedeae). However, males consumed more S. oualaniensis and less A. lesueurii and L. (Loliolopsis) diomedeae than females, which suggests that they spend most of their time feeding in oceanic areas, while females search for food in both coastal and oceanic areas. This may reflect a temporary sex segregation that occurs when females migrate toward the coast to give birth, as was reported for Sphyrna lewini (Torres-Rojas et al., 2015). However, for both sexes dietary differences were found between years, and even within the same year. This may be due to temporal variations in prey abundance in the sampling area, because sharks were caught in the same area in both years (30 to 60 nautical miles from the coast).

We also found dietary differences between seasons. These differences may be due to this shark species feeding more on L. (Loliolopsis) diomedeae during the dry season, and more on the squid A. lesueurii during the rainy season.

Other studies have reported similar feeding habits in other hammerhead sharks (e.g. S. lewini), with sharks consuming coastal squids (Torres-Rojas et al., 2006; Estupiñán-Montaño et al., 2009) and coastal fishes (Torres-Rojas et al., 2006; Avendaño-Alvarez et al., 2013), females feeding in coastal areas, and males spending more time in the oceanic zone (Estupiñán-Montaño et al., 2009).

In the Mexican Pacific, S. zygaena was reported to feed mostly on cephalopods (Galván-Magaña et al., 1989). In a study conducted off Brazil, however, Bornatowski et al. (2007, 2014a) categorized S. zygaena as ichthyophagous and teutophagous, consuming a high proportion of the squids Loligo spp., Doryteuthis spp. and Lolliguncula (Lolligunculla) brevis. Galván-Magaña et al. (2013) and Rosas-Luis et al. (2015) also reported that S. zygaena preys on various squid species in the Mexican and Ecuadorian Pacific. Our results agree with the studies cited above. Indeed, the diet of S. zygaena consisted mainly of cephalopods, teleosts being consumed in smaller proportion and elasmobranchs being absent from the stomach contents. In the Eastern Tropical Pacific, the diets of S. zygaena and S. lewini were shown to include similar groups of prey, with a predominance of cephalopods (Torres-Rojas et al., 2006; Estupiñán-Montaño et al., 2009; Galván-Magaña et al., 2013; Bornatowski et al., 2014a; Rosas-Luis et al., 2015). The predominance of this prey item may be related to its abundance and broad distribution in this part of the Pacific (Taipe et al., 2001).

Our analysis by size class suggests possible changes in S. zygaena’s diet with size: indeed, the presence of the coastal cephalopod L. (Loliolopsis) diomedeae among the most important prey in the diet of the specimens <140 cm total length suggests that the juveniles feed in coastal areas. This hypothesis agrees with Bornatowski et al. (2007, 2014a), who reported coastal cephalopods of the genera Doryteuthis, Loligo and Lolliguncula as S. zygaena’s most important prey off the southern coast of Brazil.

Lolliguncula (Loliolopsis) diomedeae and its genus, as well as the genera Doryteuthis and Loligo, are demersal squids that inhabit coastal areas or areas near the continental shelf, at a depth of 50 to 200 m (Jereb & Roper, 2010). Their occurrence in the diet of small specimens of S. zygaena suggests that they use coastal habitats. In contrast, squids like D. gigas and S. oualaniensis were the most important prey in the stomach contents of the larger specimens of S. zygaena (≥150 cm total length), which suggests that they forage in oceanic areas or areas near the continental shelf. This shift in habitat would lead to changes in the shark's diet as individuals mature and grow.

Ontogenetic changes in diet are common among sharks and have been documented through both stomach content analysis (Lowe et al., 1996; Marshall et al., 2008; Newman et al., 2012) and stable isotope analysis (Estrada et al., 2006; Kim et al., 2012; Loor-Andrade et al., 2015). These shifts may be associated with increased body size. As they mature and grow, indeed, smooth hammerhead sharks become less susceptible to predation by other sharks, thus promoting horizontal migration from coastal to oceanic areas, where larger prey are available.

Four squid species dominated the diet of S. zygaena in this study: two of the family Ommastrephidae (D. gigas and S. oualaniensis), one of the family Ancistrocheiridae (A. lesueurii), and one of the family Loliginidae (L. (Loliolopsis) diomedeae). In conjunction with Levin's index (B A < 0.6), this finding suggests that S. zygaena is a specialist predator, as was also reported in Brazil by Bornatowski et al. (2014a) and in Peru by Gonzalez-Pestana et al. (2017), consuming coastal prey during the juvenile stage and oceanic prey during the adult stage. This conclusion is supported by the abundance of D. gigas and S. oualaniensis and, to a lesser degree, of other squid species (Histioteuthis spp., Mastigoteuthis spp., Onychoteuthis banksii and Ommastrephes bartramii) in the shark's diet. This specialization may be related to prey availability, with the smooth hammerhead shark specialized in hunting the prey species that are most abundant in the area in order to maximize consumption and optimize energy use. When prey is scarce, in contrast, S. zygaena may be forced to feed on whatever prey is available, which implies a greater expenditure of energy (Wetherbee et al., 1990).

To date, few studies have estimated the trophic level of S. zygaena. Cortés (1999) and Bornatowski et al. (2014a) concluded that this shark is a tertiary predator (TL = 4.2). Our results agree with these studies, as the mean TL estimated here ranged from 4.45 to 4.91 (mean ± SD: 4.73 ± 0.16). As top predators, these sharks would be able to influence lower trophic levels of the food chain through both direct and indirect effects (Stevens et al., 2000; Myers et al., 2007; Heithaus et al., 2008; Navia et al., 2010).

The similarity in the estimated trophic levels of males and females supports the high trophic overlap between sexes and absence of sexual segregation found above, and suggests that both sexes feed on prey at similar trophic levels. It was also shown that as smooth hammerhead sharks increase in size, they tend to consume prey at higher trophic levels, suggesting ontogenetic changes in their diet.

This study seeks to remedy the lack of knowledge on the biology and ecology of S. zygaena off Ecuador, and is one of the first studies to address this topic in detail. Further research is needed, however, to expand upon this initial study and elucidate the species’ feeding patterns and preferences, ontogenetic changes and habitat use.

ACKNOWLEDGEMENTS

We thank the fish butchers at Tarqui beach (Manabí, Ecuador) as well as José Mendez, Vanessa Velázquez and Fabián Pacheco. Thanks to Anika Mora Coral for editing the figures, and Kristin Sullivan and Isabelle Gamache for editing the English text.

FINANCIAL SUPPORT

This study was supported by the Fundación Alium Pacific through a grant to Colombo Estupiñán-Montaño, and by the Instituto Politécnico Nacional through grants from the Estímulos al Desempeño de los Investigadores (EDI; Performance Inc entives for Researchers) and the Comisión de Operación y Fomento de Actividades Académicas (COFAA-IPN; Commission of Operation and Promotion of Academic Activities) to Felipe Galván-Magaña.

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