Shark predation on cephalopods in the Mexican and Ecuadorian Pacific Ocean

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SHARK PREDATION ON CEPHALOPODS IN THE MEXICAN AND ECUADORIAN PACIFIC OCEAN

FELIPE GALVÁN‐MAGAÑA, CARLOS POLO‐SILVA, SANDRA BERENICE HERNÁNDEZ‐AGUILAR, ALEJANDRO SANDOVAL‐ LONDOÑO, MARIA RUTH OCHOA‐DÍAZ, NALLELY AGUILAR‐CASTRO, DAVID CASTAÑEDA‐SUÁREZ, ALEJANDRA CABRERA CHAVEZ‐COSTA, ÁLVARO BAIGORRÍ‐SANTACRUZ, YASSIR EDEN TORRES‐ROJAS, LEONARDO ANDRÉS ABITIA‐CÁRDENAS

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Deep-Sea Research II ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Shark predation on cephalopods in the Mexican and Ecuadorian Pacific Ocean Felipe Galván-Magaña a,n, Carlos Polo-Silva b,1, Sandra Berenice Hernández-Aguilar a, Alejandro Sandoval-Londoño d, Maria Ruth Ochoa-Díaz c, Nallely Aguilar-Castro a, David Castañeda-Suárez e, Alejandra Cabrera Chavez-Costa a, Álvaro Baigorrí-Santacruz d, Yassir Eden Torres-Rojas a,2, Leonardo Andrés Abitia-Cárdenas a a

Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, Apdo. Postal 592, La Paz, Baja California Sur, Mexico Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apdo. Postal 70-305 Ciudad Universitaria, 04510 México, D.F., Mexico c Centro de Investigaciones Biológicas del Noroeste, Mar Bermejo 195, Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur, C.P. 23090, Mexico d Corporación académica ambiental, Universidad de Antioquia, Calle 67, No. 53-108, Medellín, Colombia e Facultad de Biología Marina, Universidad de Bogotá Jorge Tadeo Lozano, Carrera 2, No. 11-68, Edificio Mundo Marino, Rodadero—Santa Marta, Colombia b

art ic l e i nf o

Keywords: Squid Sharks Vertical distribution Mexico Ecuador

a b s t r a c t Pelagic predators such as sharks have been shown to be effective cephalopod samplers, because they have high consumption rates and swimming speeds. The stomach contents of these predators allow us to determine the distribution and abundance of cephalopods, considering the scarcity of biological information and the difficulty of catching squids and octopi using traditional methods. The silky shark (Carcharhinus falciformis), blue shark (Prionace glauca), scalloped hammerhead (Sphyrna lewini), smooth hammerhead (Sphyrna zygaena), pelagic thresher shark (Alopias pelagicus), and bigeye thresher shark (Alopias superciliosus) were caught off both coasts of Baja California Sur, Mexico, and in the Ecuadorian Pacific Ocean. Cephalopod sizes (mantle lengths, ML) were calculated based on the beak measurements to determine the size of cephalopods consumed by the sharks. We identified 21 cephalopod species based on beak items found in the shark stomachs. The most abundant cephalopods consumed by sharks in both areas were Dosidicus gigas, Ancistrocheirus lesueurii, Onychoteuthis banksii, Sthenoteuthis ovalaniensis, Argonauta spp., Abraliopsis affinis, and Mastigoteuthis dentata. The cephalopod's habitat provides information about the depth at which these sharks capture their prey. The blue shark feeds on cephalopods in epipelagic, mesopelagic, and bathypelagic waters; the silky shark feeds on cephalopods in epipelagic waters; and the scalloped hammerhead shark preys on cephalopods in neritic (bottom) and oceanic waters (epipelagic and mesopelagic). The pelagic thresher shark consumed epipelagic and neritic species; whereas the bigeye thresher shark feeds mainly on epipelagic and mesopelagic squids in Ecuadorian waters. The smooth hammerhead preys on epipelagic and mesopelagic squids off Mexico and Ecuador. & 2013 Elsevier Ltd. All rights reserved.

1. Introduction The ecological role of cephalopods in marine ecosystems is important because they are the main prey of large pelagic fishes, marine mammals, and sharks, allowing the flow of energy from one trophic level to another (Clarke, 1996; Cherel and Klages, 1998; Abitia-Cardenas et al., 1999; Ruiz-Cooley et al., 2004; Cherel et al., 2009). The main predators of cephalopods in the eastern Pacific Ocean are sharks (Galván-Magaña et al., 1989; Galván-Magaña,

n Correspondence to: Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, Apdo, Postal 592, La Paz, Baja California Sur, México, C.P. 23096, Mexico.

Tel.: +52 6121270143; fax: 52 6121225322.

E-mail address: galvan.felipe@gmail.com (F. Galván-Magaña).

1 Present address: Oficina de Generación del Conocimiento y la Información, Autoridad Nacional de Acuicultura y Pesca, Bogotá, Colombia.

2 Present address: Instituto de Ciencias del Mar y Limnologia, UNAM, Av. Joel Montes Camarena S/N, Apartado Postal 811,C.P. 82040, Mazatlán, Sin., México.

1999; Torres-Rojas et al., 2009; Markaida and Sosa-Nishizaki, 2010), billfishes (Abitia-Cárdenas et al., 1997, 1999; AbitiaCardenas et al., 1998; Rosas-Alayola et al., 2002; Markaida and Hochberg, 2005), tunas (Galván-Magaña et al., 1985), dolphins (Perrin et al., 1973; Galván-Magaña, 1999), and dolphinfish (Aguilar-Palomino et al., 1998; Olson and Galván-Magaña, 2002).

One of the main problems in analyzing the stomach contents of these large predators is the identification of prey because of the advanced state of digestion. For cephalopods, the mandibles (beaks) are the structure most frequently found in predator stomachs because their chemical composition is chitin, which resists the gastric acid of predators (Cherel and Hobson, 2005; Lu and Ickeringill, 2006; Kim et al., 2011). Sometimes mantle tissue is found, although it is not possible to identify squid prey from partially-digested body tissues.

Cephalopod beaks have been analyzed by several researchers (Wolff, 1984; Clarke, 1986; Kubodera, 2005, Erick Hochberg—Santa Barbara Museum of Natural history) to identify cephalopods to family or species. Roeleveld (1998) mentioned that the systematics

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of the cephalopods has advanced slowly compared with that of other marine taxa, which is the reason that knowledge of the ecology and biology of cephalopods is scarce. Any new biological information on cephalopods, including where they live and their distribution, will increase the understanding of this important group.

The waters off southern Baja California Sur are considered a transition zone, with a complicated oceanographic structure. At the surface, three water masses can be detected: (1) cold California Current water with a low salinity, (2) warm eastern tropical Pacific water with intermediate salinity, and (3) warm, highly saline Gulf of California water (Alvarez-Borrego, 1983). This area has deep waters close to the coast, as off Cabo San Lucas with a depth of 3500 m close to the coast (Thomson et al., 2000). The Ecuadorian waters are characterized by the presence of the Humboldt Current, the warm Panama Current, and the Subequatorial Cromwell Current (Banks, 2002). These oceanographic characteristics allow the distribution of nutrients contributing to the generation of productive habitats for several shark and cephalopod species (Palacios, 2002).

Additionally, in these regions there is a midwater layer of oxygen-depleted water (Fiedler and Talley, 2006), called the oxygen minimum layer (OML). This stable hypoxic zone typically extends from 100 m to 1000 m off the Baja California peninsula (Helly and Levin, 2004), and 250 m to 1000 m in the Pacific close to the coast of Ecuador and Peru (Thamdrup et al., 2006; Hamersley et al., 2007). These hypoxic mesopelagic habitats are from the microbial metabolism of sinking organic material generated by high surface productivity (Roden, 1964; Alvarez-Borrego and Lara-Lara, 1991). The low oxygen levels influence the vertical distribution and ecology of marine animals, such as sharks and squids (Weng and Block, 2004; Gilly et al., 2006; Jorgensen et al., 2009; Rosa and Seibel, 2010), which are generally precluded from hypoxic depths in these strong oxygen-minimum zones.

Cephalopods are common in the eastern Pacific Ocean. Young (1972) and Okutani (1980) found ten cephalopod species of commercial size (48 cm) close to the Baja California peninsula.

Roper et al. (1984) mentioned the presence of 28 species in the eastern Pacific, including off Mexico. Roper et al. (1995) recorded 22 cephalopod species in the FAO 77 area (eastern tropical Pacific Ocean). Cruz et al. (2003) recorded four species of cephalopods in Ecuadorian waters. As prey, the abundant squids and octopi in the eastern Pacific Ocean attract large predators of commercial or ecological importance (sharks, tunas, billfishes, mahi mahi, wahoo, sperm whales, dolphins, and sea lions) (Abitia-Cardenas et al., 1998; Galván-Magaña, 1999; Ruiz-Cooley et al., 2004; EstupiñanMontaño et al., 2009; Polo-Silva et al., 2009).

Our study provides information about the cephalopod species occurring in the southwestern and southeastern areas off the Baja California peninsula and in the eastern equatorial Pacific Ocean.

We also include comments about the feeding habitats of sharks based on the vertical migration of the cephalopods.

2. Methods We sampled sharks from August 2000 to July 2003 in the fishing camps of Baja California Sur and Manta, Ecuador. In these locations, the fishermen put their nets or longlines 30 or 40 miles offshore, mainly at sunset and then retrieve the shark catch early the next morning. The main time for catching sharks was during the night (Martínez-Ortiz and Galván-Magaña, 2007; CabreraChávez-Costa et al., 2010).

We identified the sharks with the Compagno (1984) keys. The total length (mm) of each shark was measured, the gender determined, and the stomach excised and preserved in ice or in

Formalin. The samples were processed in the Fish Ecology Laboratory of the Centro Interdisciplinario de Ciencias Marinas (CICIMAR) in La Paz, Mexico. In the laboratory, stomachs were thawed and prey items were identified to the lowest taxon possible, and the prey were weighed and enumerated when individuals were recognizable. The counts of paired structures, such as cephalopod mandibles and fish otoliths, were divided by two to estimate numbers of individual prey items. We categorized the digestion state of the prey as 1¼ intact or nearly intact, 2 ¼soft parts partially digested, 3 ¼ whole or nearly whole skeletons without flesh (or comparable state for nonfish taxa), and 4¼ only hard parts remaining (primarily fish otoliths and cephalopod mandibles) (Galván-Magaña, 1999). We measured the length of the individual prey. For cephalopods, we recorded the mantle length when it was possible.

The identification of the prey depended upon their digestion state. We used Fischer et al. (1995) to identify whole cephalopods and several other keys to identify the cephalopods based on the mandibles (Clarke, 1962; Iverson and Pinkas, 1971; Wolff, 1982, 1984; Clarke, 1986; Kubodera, 2005). The cephalopod collections at the Santa Barbara Museum of Natural History and two research centers of Mexico (CICIMAR and CICESE) were useful for comparison and validation of prey identifications. We used Wolff (1984) and Clarke (1986) to determine the weight and mantle length of cephalopod species from beak measurements. This information was used to compare the cephalopod sizes among shark species.

The only shark species for which we did not estimate the size of the squid prey was the silky shark, because we did not measure the beaks in that species.

The contribution of each prey taxon to the diet of these sharks was quantified with two measurements of dietary composition.

The percent abundance ð%N i Þ and percent weight ð%W i Þ were calculated for each sample to provide mean and variability estimates (Bizzarro et al., 2007; Chipps and Garvey, 2007). For prey counts !

Nij 1 P %N i ¼ ∑ 100 ð1Þ P j ¼ 1 ∑Q N ij i¼1

%N i where is the mean percent by number for prey type i, Nij is the number of individuals of prey type i in shark j, P is the number of sharks with food in their stomachs, and Q is the number of prey types in the pooled samples. For prey weights 0 1 %W i ¼

C 1 P B B W ij C ∑ B C100 A Pj¼1@ Q ∑ W ij

ð2Þ

i¼1

%W i where is the mean percent by weight for prey type i, Wij is the weight of prey type i in shark j, and P and Q are as defined for Eq. (1). To determine the diet overlap between shark species we used the Morisita–Horn index (Horn, 1966; Smith and Zaret, 1982) Cμ ¼

2∑ni¼ 1 ðP x;i P y;i Þ ∑ni¼ 1 P 2x;i þ P 2y;i

where Cμ is the Morisita–Horn index, Px,i is the proportion of ith prey with respect to all prey of predator x; Py,i is the proportion of the ith prey with respect to all prey of predator y; and n is the total number of prey. This index varies from 0, when there are no dietary items in common, to 1, when the diet is the same among species. A significant overlap is traditionally assumed for index values higher than 0.6 (Keast, 1978; Langton, 1982). The bootstrapping techniques based on 500 replications allowed us to estimate 95% confidence intervals for the overlaps indices.

The squid species had different vertical distributions in the water column. Most of them make large vertical migrations during

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the twilight periods, but some stay in the shallow layer both day and night. Therefore, we classified the cephalopods according to their vertical distributions listed in the published literature. The epipelagic cephalopods migrate to the surface at night from about 200 m, whereas the mesopelagic cephalopods migrate from deep waters (200–1000 m) to the surface. The bathypelagic species migrate between 1000 and 2000 m. There are some neritic cephalopods that inhabit depths between 0 and 100 m (Zuev and Nesis, 1971; Roper and Young, 1975; Sato, 1976, Nesis, 1987; Sweeney et al., 1992). We classified the ommastrephids by size according to the beak dimensions. Individuals with rostral length (RL) less than 4.0 mm were considered as epipelagic juveniles, whereas individuals with the RL greater than 4.0 mm were classified as mesopelagic adults (Zuyev et al., 2002).

3. Results Most of the stomachs analyzed had prey in digestion state 4 (70%) and 3 (15%). We separated the data by area, and described the prey of all taxa (fish, crustaceans, and cephalopods) consumed by each shark, to illustrate the importance of cephalopods as prey of sharks in the eastern Pacific (Tables 1 and 2).

3.1. Sharks in the eastern Pacific Scalloped hammerhead (Sphyrna lewini) (Baja California Sur: n ¼131, eastern equatorial Pacific: n ¼82).

Off Baja California Sur, the cephalopods were the most important food source of scalloped hammerhead sharks by number (72%) and weight (68%) (Table 1). The cephalopod species most abundant by number were Dosidicus gigas, Abraliopsis affinis, and Lolliguncula diomedeae. By weight, the main species were D. gigas and Mastigoteuthis dentata (Table 1). In the eastern equatorial Pacific Ocean, the scalloped hammerhead shark consumed cephalopods and fishes in the same percentage by number (48%) (Table 2), although the cephalopods were more important by biomass, where D. gigas, L. diomedeae, Ancitrocheirus lesueurii, and Sthenoteuthis oualaniensis were the dominant species (Table 2).

Smooth hammerhead (Sphyrna zygaena) (Baja California Sur: n ¼46; eastern equatorial Pacific: n ¼ 127).

The cephalopods were the most important prey of smooth hammerhead sharks off Baja California Sur (90% by number, 55% by weight) (Table 1), and D. gigas, A. lesueurii, and Onychoteuthis banksii were the most important species (Table 1). In the eastern equatorial Pacific Ocean, the cephalopods were the main food consumed by this shark, and the dominant prey by number and weight were D. gigas, S. oualaniensis, and A. lesueurii (Table 2).

Blue shark (Prionace glauca) (Baja California Sur: n ¼210).

The cephalopods were the prey most consumed by blue sharks in number (79%) and weight (98%) (Table 1). The main prey by number were O. banksii, Gonatus californiensis, and D. gigas. By weight, G. californiensis, A. lesueurii, and D. gigas were the most important species (Table 1).

Silky shark (Carcharhinus falciformis) (Baja California Sur: n ¼142).

Cephalopods and fishes had similar importance by biomass (51% and 48%) in the diet of silky sharks. The cephalopods were the main food by number (79%) in the diet of this predator (Table 1). D. gigas and O. banksii were the most important species by weight, though by number they were D. gigas, A. lesueurii, Argonauta cornutus, and O. banksii (Table 1).

Pelagic thresher shark (Alopias pelagicus) (Ecuadorian waters: n ¼91).

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Pelagic thresher sharks consumed similar percentages of cephalopods and fishes by number (50% and 49%). However, the cephalopods were more dominant in biomass (68% versus 31%) (Table 2). The main prey by number and weight were the squids D. gigas and S. oualaniensis and the mesopelagic fish Benthosema panamense (Table 2).

Bigeye thresher shark (Alopias superciliosus) (Ecuadorian waters: n ¼107) Fishes were the most important food source of bigeye thresher sharks by number (78%) in comparison with the cephalopods (21%), whereas by weight the cephalopods and fishes had similar contributions (51% and 49%) (Table 2). The main prey by number were the fishes B. panamense, Larimus argenteus, Sardinops sagax, and Merluccius gayi, whereas A. affinis, A. lesueurii, and D. gigas were the most important squids. The dominant squid prey by biomass were D. gigas, L. argenteus, L. diomedeae, A. affinis, and M. gayi (Table 2).

3.2. Trophic overlapping between shark species When comparing pairs of shark species in each area, we found that off Mexico, the trophic overlap was significantly higher among S. lewini and P. glauca (Table 3a) than among the other shark pairs. S. lewini and P. glauca share three similar cephalopod species as prey, the ommastrephid D. gigas, the gonatid G. californiensis, and the mastigoteuthid M. dentata (Table 1). The other shark species had very low overlap indices (Table 3a). In the Pacific off Ecuador, none of the overlap indices between the pairs of shark species were significantly different (Table 3b). The greatest overlap indices were for A. superciliosus with S. zygaena (0.72), whereas the values for all the sharks were similar. All the sharks sampled off Ecuador shared two similar cephalopod prey that were important by number and biomass, the ommastrephids D. gigas and S. oualaniensis (Table 2).

3.3. Shark feeding behavior associated with cephalopod size We analyzed the size distributions of cephalopod prey in both geographic areas. Off Mexico the blue shark P. glauca consumed larger squids on average than did S. lewini (Table 4). S. zygaena prey on large species, such as A. lesueurii (342 mm ML on average), D. gigas (223 mm ML), and S. oualaniensis (142 mm ML) (Table 4).

Off Ecuador the sizes of cephalopods in the stomachs of all sharks were similar, being slightly larger in A. superciliosus and S. lewini (Table 5). D. gigas prey were larger in S. zygaena (217.1 mm ML) and S. lewini (181.3 mm ML) than in A. superciliosus (138.3 mm ML) and A. pelagicus (170.5 mm ML). We found that all sharks fed on adult ommastrephids (D. gigas and S. oualaniensis) (Table 5).

3.4. Vertical distribution of cephalopods and sharks Based on published vertical distributions of cephalopods and sharks, we found that the silky shark C. falciformis consumes mainly epipelagic cephalopods, which migrate to the surface at night (0–200 m) and some mesopelagic cephalopods, which migrate from deep waters (200–700 m). The scalloped hammerhead shark S. lewini consumes cephalopods from various depths. Off Mexico S. lewini feeds mainly on epipelagic and mesopelagic cephalopods, whereas off Ecuador this shark consumes mesopelagic and bathypelagic squids, which are found between 700 and 2000 m, and some neritic species, depth range 0–100 m.

The blue shark P. glauca consumes cephalopods from various depths, mainly epipelagic cephalopods, followed by mesopelagic and bathypelagic species. The pelagic thresher shark A. pelagicus consumes epipelagic cephalopods and some neritic species,

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Table 1 Mean (standard deviation) percent by number (%N) and percent by weight (%W) of prey found in stomachs of four species of shark off both coasts of Baja California Sur, Mexico. See Eqs. (1) and (2) for calculations of %N and %W. S. lewini

Cephalopoda Ancistrocheirus lesueurii Dosidicus gigas Gonatus californiensis Mastigoteuthis dentata Histioteuthis sp.

Octopus sp.

Lolliguncula diomedeae Pholidoteuthis boschmaii Thysanoteuthis rhombus Abraliopsis affinis Sthenoteuthis oualaniensis Octopodoteuthis sicula Vitreledonella richardi Histioteuthis heteropsis Onychoteuthis banksii Argonauta sp.

Liocranchia reinharti Japetella heati Vampyroteuthis infernalis Haliphron atlanticus Argonauta cornutus

S. zygaena

P. glauca

C. falciformis

%N

%W

%N

%W

%N

%W

%N

%W

72.4

68.1 _ 40.1 (30.2) 0.6 (2.5) 20.5 (39) – – 2.5 (14.2) 1.7 (7.1) 0.1 (1.8) 0.02 (1.3) – – – 2.6 (6.4) – – – – – – –

90.2 21.2(27.3) 36.0 (31) 0.8 (8.3) 0.62 (7.4) – – – 0.2 (2.0) 0.1 (0.7) 3.8 (11.5) 13 (22.2) 0.1 (0.9) o 0.1 (o 0.1) – 13.7 (19.9) 0.7 (8.0) – – – – –

54.7 8.0 (24.2) 18.2 (36.7) o 0.1 (o 0.1) o 0.1 (o 0.1) – – – o 0.1 (o 0.1) 0.3 (1.3) o 0.1 (o 0.1) 2.8 (9.4) 0.1 (0.3) o 0.1 (o 0.1) – 25.4 (40.7) o 0.1 (o 0.1) – – – – –

78.5 5.0 (13) 8.8 (26.3) 10.5 (27.3) 2.1 (4.5) – – – 4.7 (20.2) – – – – – 5.9 (20) 19.5 (36.3) 9.2 (26.1) 2.6 (15.6) 4.1 (18.9) 2.6 (12.8) 3.5 (15.6) –

97.9 15.6 (45.6) 12.4 (15.4) 42 (53.2) 0.9 (1.8) – – 0.3 (1.1) – – – – – 2.2 (3.3) 0.7 (1.6) 0.6 (1.2) 0.5 (1.1) o 0.1 ( o0.1) o 0.1 ( o0.1) 22.4 (33) –

79 13.3 (32.8) 44.2 (45.9) 0.2 (1.3) _ 1 (6.5) – – – – – 2.0 (12.9) – – – 5.1 (19.8) – – – – – 13.2 (31.5)

50.7 0.2 (1.8) 43.1 (58.9) 0.3 (2.7) _ 0.2 (1.6) – – – – – 0.5 (3.6) – – – 6.4 (12.4) – – – – – 0.3 (1.1)

30.3 (43.1) 1 (15) 3.6 (15.3) – 0.1 (1.0) 6.2 (23.2) 1.2(9.0) 3.9 (15.0) 25.0 (39.1)

– – – – – –

Crustacea Penaeus californiensis Pleuroncodes planipes Squilla biformis Farfantepenaeus californiensis

2.0 1 (18.0) 1 (22.0) –

0.2 0.1 (1.2) 1 (4.1) – –

– – – – –

– – – – –

17.1 – 16.9 (37.4) 0.4 (4.5) –

1.1 – 1.1 (3.1) o 0.1 ( o0.1) –

11 – 11.0(30.1) – –

0.9 – 0.8 (5.3) – 0.1 (1.9)

Osteichthyes Porichthys analis Decapterus macrosoma Naucrates ductor Trachurus symmetricus Trachinotus rhodopus Caranx sp.

Sardinops caeruleus Coryphaena hippurus C. equiselis Gymnothorax sp.

Paralichthys woolmani Syacium latifrons Etropus crossotus Heteropriacantus cruentatus Paralabrax maculatofasciatus Diplectrum pacificum Scomber japonicus Auxis thazard Auxis sp.

Remora remora Zu cristatus Selar cromenophthalmus Fam. Balistidae Etrumeus teres Paralabrax sp.

Euthynnus lineatus Bodianus diplotaenia Scorpaena histrio Synodus evermanni Cheilopogon pinnatibarbatus Prionurus punctatus Synchiropus atrilabiatus Apterichtus equatorialis Merluccius productus Macrocystis pyrifera Mugil cephalus Vinciguerria lucetia Fodiator acutus Hippoglossina stomata Brotula sp.

Gerres cinereus

25.6 0.5 (5.0) 0.5 (3.4) 0.5 (2.1) 0.5 (2.3) 0.4 (1.8) 0.4 (2.5) 4.4 (7.5) 0.5 (3.5) – 1 (3.6) 0.5 (1.4) 0.3 (1.1) 0.4 (2.5) 1 (4.2) 0.8 (4.5) 0.3 (3.2) 3 (8.5) 1.3 (3.2) – – – – – 0.3 (3.1) 0.5 (5.0) 0.3 (3.1) – 0.3 (3.0) 4.4 (10.2) 1 (2.8) 0.3 (2.7) 0.5 (3.1) 1 (3.1) – – – – – – – –

31.5 1 (4.7) 2 (6.50) 0.5 (3.2) 0.1 (1.1) 0.1 (1.0) 1.1 (7.7) 1 (3.9) 0.2 (1.7) – 1 (4.0) 0.1 (1.3) 0.1 (1.0) 0.2 (1.6) 1 (3.9) 2.1 (4.3) 0.4 (2.7) 3.4 (40.1) 4.7 (22.1) – – – – – o 0.1 (0.9) 2.1 (5) 1.2 (3.5) – 0.7 (6.1) 3.5 (12) 0.5 (3.2) 0.5 (3.5) 0.1 (1.2) 0.2 (1.7) – – – – – o 0.1(o 0.1) – –

9.5 – – – – – 0.2 (2.6) 3.5 (17.2) 0.1 (0.9) – – – – – – – o 0.1 (o 0.1) 0.5 (3.9) – – – – – – – – – –

45 – – – – – 0.1 (1.1) 8.5 (23.6) 0.1 (0.6) – – – – – – – 5.5 (23.5) 5.5 (21.3) – – – – 0.1 (1.2) – – – – – 9.2 (25.4) – – – – 0.9 (9.1) – 2.3 (8.2) 1.0 (4.2) 4.3 (18.6) – 0.1 (0.8) 0.1 (0.6)

1 – – – – – – – – – – – – – – – – 0.7 – – o 0.1 ( o0.1) o 0.1 ( o0.1) – – – – – – – – – – – – – o 0.1( o 0.1) – – – – – –

9.9 – – – 0.7 (5.8) – – – 0.9 (5.4) 1.4 (11.6) – – – – 0.9 (6.1) – – 0.5 (4.6) 1.4 (11.6) 1.3 (11.6) – – – 1.4 (11.6) – – – 1.4 (11.6) – – – – – – – – – – – – – –

48.0 – – – 0.1 (1.7) – – – 17.1 (32.1) 18.2 (35.4) – – – – 3.6 (8.5) – – 0.6 (3.9) 0.1 (1.5) 2.2 (5.2) – –

2.5 (9.6) – – – – – – 1 (4.7) 0.2 (2.6) 0.3 (3.9) 7.7 (24.8) 0.6 (7.9) 0.6 (7.9)

4.1 – – – – – – – – – – – – – – – – 3.2 (15.4) – – 0.8 (9.0) 0.4 (4.5) 0.3 (1.3) – – – – – – – – – – – o 0.1 ( o0.1) 1.5 (10.5) – – – – – –

Please cite this article as: Galván-Magaña, F., et al., (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.002i

1.1 (7.2) – – – 0.2 (1.8) – – – – – – – – _ – – –

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Table 2 Mean (standard deviation) percent by number (%N) and percent by weight (%W) of prey found in the stomachs of four species of sharks off Ecuador. See Eqs. (1) and (2) for calculations of %N and %W. S. lewini

S. zygaena

A. pelagicus

A. superciliosus

%N

%W

%N

%W

%N

%W

%N

%W

Cephalopoda Dosidicus gigas Lolliguncula diomedeae Ancistrocheirus lesueurii Sthenoteuthis oualaniensis Histioteuthis sp.

Onychoteuthis banksii Octopodoteuthis sicula Mastigoteuthis dentata Pholidoteuthis boschmai Gonatus sp.

Argonauta sp.

Abraliopsis affinis Vitreledonella richardi Octopus sp.

Thysanoteuthis rhombus

48.1 8.6 (19.5) 5.3 (18.5) 6.3 (16.9) 2.3 (9.8) 2.7 (10.4) – 2.5(12.6) 12.9(25) 0.7(4.3) 0.1( o0.1) – 0.5 (3.9) – 6.2 (17.7) 0.1 (1.1)

85.7 41.2 (59) 4.1 (13.5) 11.4 (30.2) 23 (36.2) 2.8 (5.3) – 1.8 (4.3) 0.4 (1.60) 0.8 (3.5) 0.1 (1.4) – o0.1 ( o 0.1) – o0.1 ( o 0.1) 0.1 (1.3)

86.7 52.7 (34.3) 1.5 (5.7) 8.6 (14.6) 12.6 (25.2) 0.4 (3.2) 0.1 (1.2) 2.0 (4.8) 4.9 (11.8) 0.1 (0.6) 0.06 (0.3) 0.06 (0.5) – 0.5 (2.2) – 3.1 (8.1)

88.2 67.7 (36.9) 0.4 (4.6) 5.9 (15.5) 12.9 (26.6) 0.5 (4.4) o0.1 ( o 0.1) 0.3 (1.1) 0.1 (0.4) 0.1 (0.7) o0.1 ( o 0.1) o0.1 ( o 0.1) – o0.1 ( o 0.1) – 0.2 (2.8)

50.5 42.2(62.4) 0.7 (6.7) 1.0 (5.4) 5.7 (13.9) – – – 0.4 (3.6) 0.4 (4.3) – – 0.1 (1.2) – – –

68.3 60.2 (43.5) o0.1 ( o 0.1) o0.1 ( o 0.1) 8.0 (19.5) – – – o0.1 ( o 0.1) o0.1 ( o 0.1) – – o0.1 ( o 0.1) – – –

21.1 5.7 (18.3) 0.1 (0.4) 6.0 (15.2) 1.1 (4) 0.2 (1.1) – – 0.3 (2.0) 0.1 (1.2) – – 7.5 (20.2) – – 0.1 (1.3)

51.1 25 (40.7) 8.4 (12.8) 0.1 (1.30) 5.3 (17.2) 2.4 (3.6) – – 2.4 (3.4) 0.2 (1.0) – – 7.0 (24.8) – – 0.3 (1.4)

Crustacea Penaeus stylirostris Solenocera agassizi Heterocarpus vicarius Fam.Penaeidae Fam. Xantidae

4.4 – 1.4 (7.0) 2 (10) 0.5 (4.4) 0.7 (5.9)

0.2 – 0.1 (1.6) 0.1 (1) o0.1 ( o 0.1) o0.1 ( o 0.1)

– – – – – –

– – – – – –

– o0.1 ( o 0.1) – – –

– 0.1 (0.3) – – – –

– – – – – –

– – – – – –

Osteichthyes Synodus sp.

Auxis thazard Oxyporhamphus micropterus Exocoetus monocirrhus Katsuwonus pelamis Canthidermis maculatus Sardinops sagax Larimus argenteus Coryphaena hippurus Remora remora Benthosema panamense Fam. Carangidae Fistularia sp.

Thunnus albacares Katsuwonus pelamis Sarda sarda Gempylus serpens Cheilopogon spilonotopterus Ophichthus sp.

Ophichthus sp. morphotype2 Ophichthus sp. morphotype 3 Ophichthus sp. morphotype 4 Ophichthus sp. morphotype 5 Ophichthus sp. morphotype 6 Ophichthus sp. morphotype 7 Myrophys vafer Pseudomyrophis sp.

Paralabrax callaensis Exocoetus monocirrhus Merluccius gayi Symbolophorus evermanni Lagocephalus lagocephalus Brama japonica Ablennes hians Munida sp.

Fam Hemirramphidae Lutjanidae Fam. Scorpaenidae Fam. Serranidae Fam. Scombridae

47.5 – 3.7 (17.1) – – – – – 10.2 (22.8) 0.2 (1.7) – – – – – 0.1 (1.4) – 1.4 (11.8) – 1.4 (7.20 4 (15.2) 0.7 (5.9) – – – – 1.9 (9.9) 1.4 (11.8) – – 6.7 (17.0) – – – – 1.2 (8.1) o0.1 ( o 0.1) 2.6 (14.6) 6 (12.9) 0.5 (3.9) –

14.1 – 0.7 (1.1) – – – – – 0.6 (1.9) 0.1 (1.1) – – – – – 1.5 (3.2) – 0.3 (5.2) – 0.4 (1.6) 1 (2.2) 0.7 (1.4) – – – – 0.8 (3.1) o0.1 ( o 0.1) – – 0.5 (4.2) – – – – 0.2 (2.3) 0.1 (2.7) 0.4 (1.5) 0.4 (1.40) 0.4 (1.5) –

12.9 0.07 (0.8) 2.9 (14.6) 1.1 (5.9) 0.32 (1.6) 0.5 (3.2) 0.1 (0.9) – 1.0 (9.2) 1.2 (9.6) – – 0.7 (8.6) 0.7 (8.6) 2.4 (12.6) 0.5 (3.6) o0.1 ( o 0.1) 0.1 (1.5) 0.5 (3.3) 0.3 (4.3) – –

11.4 o0.1 ( o 0.1) 2.6 (14.3) 0.3 (1.7) o0.1 ( o 0.1) 0.5 (4.5) o0.1 ( o 0.1) – 0.7 (8.6) 1.2 (9.2) – – 0.7 (8.6) 0.7 (8.6) 2.2 (12.4) 0.8 (6.7) o0.1 ( o 0.1) o0.1 ( o 0.1) 0.3 (1.5) 0.3 (2.9) – – – – – – – – – 0.4 (5.3) – – – – – – – – – – 0.3(2.0)

48.9 o0.1 ( o 0.1) 3.0 (12.4) – – – – 1.5 (10.4) 0.2 (1.4) – – 37.3 (46.8) – – – – – 0.2 (1.3) – 0.7 (4.5) 0.1 (1.0) 0.1 (0.5) 0.1 (0.6) 0.1 (0.9) – – – – 0.1 (0.9) – 4.2 (17.3) 0.1 (0.4) 0.1 (1.0) 1.1 (10.4) – – – – – – –

31.4 0.1 (0.3) 1.3 (10.9) – – – – 0.9 (8.1) 0.1 (0.6) – – 24.1 (41.4) – – – – – o0.1 ( o 0.1) – 0.3 (2.0) 0.4 (3.9) o0.1 ( o 0.1) 0.1 (0.7) 0.1 (0.4) – – – – 0.2 (2.3) – 2.5 (14.4) 0.23 (2.0) o0.1 ( o 0.1) 1.1 (10.8) – – – – – – –

78.4 – 3.6 (11.4) – – – – 13.2 (24.70) 20.5 (32.40) 1.3 (7.3) 0.2 (1.2) 22.1 (34.5) – 0.1(0.5) – – – – – 0.8 (4.5) 0.1 (0.3) 1.7 (9.1) – – 0.3 (2.0) 0.1 (0.5) – – – – 12.9 (26) – 0.2 (1.22) – 1.3 (4.4) – – – – – –

48.8 – 5.2 (24.80) – – – – 3.6 (17.2) 15.6 (34.5) 1.5 (3.4) 0.1 4 (17.2) – 0.1 (1.4) – – – – – 2 (7.0) 0.1 (0.4) 0.1 (0.4) – – 0.5 (2.3) 1.2 (1.6) – – – – 12 (28.8) – 0.4 (0.6) – 2.4 (7.0) – – – – – –

– – – – – – 0.7 (8.6)) – – – – – – – – – – 0.2 (1.7)

whereas the bigeye thresher shark A. superciliosus consumes epipelagic and mesopelagic cephalopods, followed by bathypelagic squids. The smooth hammerhead S. zygaena preys mainly on epipelagic and mesopelagic cephalopods.

4. Discussion Our results indicate that pelagic squids and octopods are important prey for sharks in the trophic web of the tropical

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Table 3a Diet overlap estimated by the Morisita–Horn index for each shark species caught off both coasts of Baja California Sur. 95% confidence intervals generated by bootstrap are in parenthesis (500 replicates).

Shark species

S. lewini

P. glauca

C. falciformis

S. zygaena

S. lewini P. glauca C. falciformis S. zygaena

1 0.46 (0.15–0.94) 0 0.001 (0.0001–0.005)

0.46 (0.15–0.94) 1 0.03 (0.01–0.06) 0

0 0.03 (0.01–0.06) 1 0.003 (0–0.009)

0.001 (0.0001–0.005) 0 0.003 (0–0.009) 1

Table 3b Diet overlap estimated by the Morisita–Horn index for each shark caught off the eastern equatorial Pacific Ocean. 95% Confidence intervals generated by bootstrap are in parenthesis (500 replicates).

Shark species

A. pelagicus

A. superciliosus

S. zygaena

S. lewini

A. pelagicus A. superciliosus S. zygaena S. lewini

1 0.52 (0.19–0.86) 0.52 (0.24–0.78) 0.47 (0.36–0.57)

0.52 (0.19–0.86) 1 0.72 (0.51–0.86) 0.64 (0.39–0.80)

0.52 (0.24–0.78) 0.72 (0.51–0.86) 1 0.49 (0.29–0.71)

0.47 (0.36–0.57) 0.64 (0.39–0.80) 0.49 (0.29–0.71) 1

Table 4 Estimated mantle lengths of cephalopods consumed by sharks Prionace glauca, Sphyrna zygaena, and Sphyrna lewini caught off both coasts of Baja California Sur, Mexico. RL: rostral length; HL: hood length; ML: mantle length.

Cephalopod species

Ancistrocheirus lesueurii Gonatus californiensis Histioteuthis dofleini Dosidicus gigas Onychoteuthis banksii Pholidoteuthis boschmai Thysanoteuthis rhombus Mastigoteuthis dentata Haliphron atlanticus Sthenoteuthis oualaniensis Abraliopsis affinis Octopodoteuthis sicula Vitreledonella richardi

Argonauta sp.

P. glauca

S. zygaena

N

Mean RL (mm)

SD

Range

Mantle length (mm)

N

Mean RL (mm)

SD

Range

Mantle length

43 84 13 14 6 9 1 – 27 – – – –

5.7 7.6 3.9 5.5 3.3 2.5 – – 6.2 – – – –

1 0.5 1.6 2.5 0.6 0.8 – – 1.6 – – – –

3.3–7.6 4.9–9.1 1.6–6.5 2.6–10.0 2.6–3.8 1.3–3.5 – – 3.7–10.5 – – – –

192.2 157 64.4 241 172.4 91.7 – – – – – – –

5 1 – 22 13 3 1

9.4 3.4 – 5 3.1 1 4.9 – – 4 – 1 6.8

2.6 – – 3.9 4.5 0.8 – – – 3.3 – 0.8 –

2.4–7.3 – – 9.6–19.3 3.85–8.67 1.8–3 – – – 3.02–14.9 – 9.5–10.3 –

341.8 77.5 – 223.2 160.2 34.1 – – – 141.9 – 16.9 –

Mean HL (mm)

SD

Range

Mantle length (mm)

Mean HL (mm)

SD

Range

3.4

0.8

1.1–10.2

5.7

3.2

–

–

66

10 1 1

1

–

Sphyrna lewini Cephalopod species

N

Mean RL (mm)

SD

Range

Mantle length (mm)

Ancistrocheirus lesueurii Gonatus californiensis Histioteuthis dofleini Dosidicus gigas Onychoteuthis banksii Pholidoteuthis boschmai Thysanoteuthis rhombus Mastigoteuthis dentata Haliphron atlanticus Sthenoteuthis oualaniensis Abraliopsis affinis Octopodoteuthis sicula Vitreledonella richardi

– 2 – 103 35 – – 7 – – 29 – –

– 7.1 – 5.1 2.6 – – 1.8 – – 4.4 – –

– 0.3 – 1.3 0.3 – – 0.2

– 7.0–7.1 – 3.3–10 2.2–3.0 – – 1.5–2.2 – – 3.4–7.2 – –

– 147.9 – 226.7 129.7 – – 105.6 – – 94.28 – –

– 0.8 – –

eastern Pacific Ocean. These cephalopods are also consumed by other upper-level predators (birds, fishes, and marine mammals) (Imber et al., 1992; Clarke, 1996), and in turn are predators of crustaceans, fishes, and other organisms at lower trophic levels.

Standard methods of sampling, such as low speed trawling nets in limited sampling areas, do not effectively sample epipelagic micronekton, including cephalopods. Large predators, however,

are the most efficient samplers of cephalopods because they swim at high speeds and are generalist predators.

Many neritic and oceanic cephalopods were consumed by the different sharks we analyzed. The differences in proportions of cephalopods consumed by these sharks in the waters off Mexico and Ecuador may indicate differences in the squid availability, feeding behavior and habitat used by sharks in the different regions.

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Table 5 Estimated mantle lengths of cephalopods consumed by sharks Sphyrna zygaena and Sphyrna lewini caught off Ecuador. RL: rostral length; HL: hood length; ML: mantle length.

Cephalopod species

Ancistrocheirus lesueurii Gonatus californiensis Histioteuthis heteropsis Dosidicus gigas Onychoteuthis banksii Pholidoteuthis boschmai Thysanoteuthis rhombus Mastigoteuthis dentata Sthenoteuthis oualaniensis Lolliguncula diomedeae Abraliopsis affinis Octopodoteuthis sicula Vitreledonella richardi Gonatus sp.

Octopus sp.

S. zygaena N

Mean RL (mm)

SD

Range

Estimated ML (mm)

N

Mean RL (mm)

SD

Range

Estimated ML (mm)

195 – 4 1050 2 7 80 190 252 18 – 47 19 3 –

4.2 – 5.5 7.3 1.9 4.2 4.1 2.4 6.7 1 – 4.9 4.8 4.4 –

1.6 – 1.6 3.5 – 1.4 1 1 2.3 0.2 – 2.2 1.4 1.2 –

0.9–13.8 – 3.7–6.4 0.8–25 – 2.0–4.7 1.6–6.6 0.2–5.4 1.2–14.1 0.5–1.4 – 2.1–7.8 2.3–6.7 3.0–5.5 –

129.9 – 133.4 217.1 87 157 – 109.3 245 –

26 – 11 45 – 2 1 42 7 90 – 11 – 1

4.5 – 4.5 6.3 – 3.8 4.4 1.9 8.3 1.4 – 8 8.5 4.4

1.4 – 1.3 4.2 – 0.1 – 1.1 3.8 0.2 – 1.6 – –

0.9–13.8 – 2.3–6.7 0.4–28 – 3.7–3.9 – 0.6–5.1 1.2–14.1 0.5–1.6 – 4.2–11.4 – –

142.1 – 112.9 181.3.

– 141.6 – 106.2 306.2 – – 138 – 94.8

Mean HL (mm)

SD

Range

Estimated ML (mm)

5.1

2.5

3.3–6.9

43.1

–

–

–

–

–

Argonauta sp.

3

Cephalopods species

Alopias pelagicus

Ancistrocheirus lesueurii Gonatus californiensis Histioteuthis heteropsis Dosidicus gigas Onychoteuthis banksii Pholidoteuthis boschmai Thysanoteuthis rhombus Mastigoteuthis dentata Sthenoteuthis oualaniensis Lolliguncula diomedeae Abraliopsis affinis Octopodoteuthis sicula Vitreledonella richardi Gonatus sp.

Octopus sp.

S. lewini

84.4 94.8

Alopias superciliosus

N

Mean RL (mm)

SD

Range

Estimated ML (mm)

N

Mean RL (mm)

SD

Range

Estimated of ML (mm)

3 – – 149 – 2 – 6 22 13 1 – – – –

6.0 – – 6.0 – 3.0 – 1.0 6.0 1.0 2.0 – – – –

0.1 – – 0.3 – – – o0.1 0.1 0.0 – – – – –

3–6 – – 1–2 – – – 1–2.5 4–9 1–2 – – – – –

203.2 – – 170.5 – – – 100.6 218.3 – – – – – –

– – 1 19 – 2 – 3 4 – 20 2 – – 1

4.5 – 2.8 5.1 – 2.1 – 1 8.6 1 – 3.5 – – 0.27

1.9 – 0.1 1.7 – 3 – 0 2.3 0.1 – – – – –

1.8–6.6 – 2.7–2.8 1.8–5.9 – – – – 6–10 1–1.3 – – – – –

142.08 – 77.9 138.3 – 76.3 – 100.6 317.6 – – 60.2 – – –

Where and when the sharks attack cephalopods is unknown. A number of squid species are known to undergo diel vertical migration (Young, 1972). This behavior permits squids to inhabit deep waters during part of the daytime, and rise toward the surface often at night where they are available to predators. Some sharks, e.g. the blue and bigeye thresher sharks, dive to deep waters to prey on cephalopods (Carey and Scharold, 1990; PoloSilva et al., 2007; Kubodera et al., 2007).

The stomach contents of all sharks showed a high incidence of prey in an advanced state of digestion (3 and 4), which is mostly associated with the fishing operation and time of the gear in the water (Hazin et al., 1994). Generally the fishermen put out their fishing gear at sunset and retrieve it the following morning. The sharks are caught mainly at night, when their feeding occurs. The high proportions of prey in advanced stages of digestion are due to the long time lapse between capture of the sharks and removal of their stomachs the next day (Henderson et al., 2001; McCord and Campana, 2003).

Electronic tagging of different shark species has shown extensive dives of hundreds of meters during the daytime and smaller vertical excursions to the depth of the thermocline at night (Teo et al., 2004; Weng and Block, 2004; Jorgensen et al., 2009; Stevens et al., 2010; Hammerschlag et al., 2011). This diel difference in shark diving behavior is thought to be associated with the diel vertical movements of their prey (Carey and Scharold, 1990).

Of the six shark species analyzed, the silky, blue, and hammerhead sharks consume between 12 and 13 cephalopod species off Mexico and Ecuador, respectively, whereas thresher sharks prey on 7–9 cephalopod species.

4.1. Scalloped hammerhead shark (S. lewini) Studies in the Gulf of California have found that the scalloped hammerhead shark preys on several cephalopod species, such as Mastigoteuthis sp., A. lesueurii, Moroteuthis robusta, Octopus spp., D. gigas, Rossia sp., Vampyroteuthis infernalis, and Histioteuthis heteropsis (Klimley, 1983; Galván-Magaña et al., 1989). TorresRojas et al. (2009), in the area off Mazatlan, Sinaloa, México, found the diet of juvenile scalloped hammerhead sharks was dominated

by L. diomedeae and A. affinis. The cephalopod prey in our study are similar to the species reported by Torres-Rojas et al. (2009).

However the earlier studies of Klimley (1983) and Galvan et al. (1989) reported a greater number of cephalopod species in the prey composition. This difference could be due to the fact that adults were sampled in the earlier studies, while our analysis was based on juvenile scalloped hammerhead sharks (i.e. less than 150 cm), similar in size to the sharks sampled by Torres-Rojas et al. (2009). We also found more cephalopod species than in other studies, which probably indicates that the sharks were feeding more actively during the night, preying on epipelagic,

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mesopelagic, and neritic cephalopods (Duncan and Holland, 2006; Torres-Rojas et al., 2009). Additionally, in the Gulf of California, Jorgensen et al. (2009) reported that the scalloped hammerhead made dives to depths of 980 m, close to the oxygen-minimum layer (OML), but they spend more time between the surface and 400 m.

Other studies of scalloped hammerhead sharks off South Africa (Smale and Cliff, 1998) indicated that S. lewini preys on cephalopods. The main species were benthic octopods (Octopus vulgaris), neritic squids (familiy Loliginidae), and oceanic squids such as A. lesueurii, Octopoteuthis, and Taningia danae. They also found other cephalopods as Chiroteuthis, Cranchidae (Teuthowenia), Histoteuthidae (Histioteuthis miranda and Histioteuthis dofleini), Lycoteuthis diadema, and Ommastrephidae (Ommastrephes volatilis, S. oualaniensis, and Todarodes spp.).

In the Pacific off Ecuador, Estupiñan-Montaño et al. (2009) found the diet of scalloped hammerhead sharks was dominated by squids of the families Ommastrephidae (D. gigas and S. oualaniensis), Ancistrocheiridae (A. lesueurii), and Mastigoteuthidae (M. dentata), which all inhabit oceanic areas. A similar trend was found in our study, with this shark preying on three mesopelagic squid species (D. gigas, S. oualaniensis, and A. lesueurii), which indicates a possible preference for mesopelagic prey or because of a higher abundance of these cephalopod species in this region.

These squids were also important in the diet of thresher sharks in this area.

4.2. Smooth hammerhead shark (S. zygaena) The smooth hammerhead shark is less studied than the scalloped hammerheads, although they are known to feed on both pelagic and benthic prey (Smale and Cliff, 1998). The Ommastrephidae and Ancistrocheiridae families were the most important prey in the diet of this shark in both geographic areas. CastañedaSuárez and Sandoval-Londoño (2007) reported the same squid species as the most important, while the contribution in weight of D. gigas in their study was slighter greater than in our study. This similarity is likely due to a high abundance of D. gigas in this area.

The ommastrephids D. gigas and S. oualaniensis were previously described as the most dominant species in the tropical Pacific off Ecuador (Markaida and Hochberg, 2005). No electronic tagging of this shark has been conducted to determine the vertical movements to associate it with different cephalopod species consumed by this shark species.

4.3. Blue shark (P. glauca) The feeding habits of blue sharks off Mexico revealed a diet composed of mesopelagic cephalopods (H. heteropsis, A. lesueurii, and Haliphron atlanticus), epipelagic cephalopods (Argonauta sp., G. californiensis, and D. gigas), and bathypelagic squids (V. infernalis, Architeuthis sp.) off the coast of the Baja California Peninsula (Hernández-Aguilar, 2008; Markaida and Sosa-Nishizaki, 2010; Kim et al., 2011).

Blue sharks also preyed on cephalopods in other geographic areas (Stevens, 1973; Clarke and Stevens, 1974; Gubanov and Grigor'ev, 1975; Nigmatulin, 1976; Tricas, 1979; Harvey, 1989; Clarke et al., 1996b; Bello, 1996; Vaske-Junior and Rincon-Filho, 1998; Macnaughton et al., 1998; Henderson et al., 2001).

Nigmatulin (1976) recorded an Architeuthis sp. from a blue shark stomach in the eastern equatorial Atlantic. This cephalopod species also has been recorded in blue shark stomachs from the Baja California peninsula by Markaida and Sosa-Nishizaki (2010).

Clarke et al. (1996b) recorded Histioteuthis bonnellii and Taonius pavo, which are neutrally buoyant cephalopods from mesopelagic or bathypelagic depths, eaten by blue sharks in Azorean waters.

Blue sharks preyed on Chiroteuthis verany, Moroteuthis robsoni, and A. lesueurii in Brazilian waters (Vaske-Junior and Rincon-Filho, 1998). Off SW Ireland, blue sharks consumed H. atlanticus and Todarodes sagittatus (Macnaughton et al., 1998).

From the vertical distribution of cephalopods consumed by the blue shark, we concluded that it is a predator that feeds on cephalopods in epipelagic, mesopelagic, and bathypelagic waters of oceanic areas. In research on the movements of the blue shark, Stevens et al. (2010) reported that the blue shark can be found at 980 m off eastern Australia, although it is more common between the surface and 100 m at water temperatures between 17.5 and 20.0 1C. 4.4. Silky shark (C. falciformis) Cabrera-Chávez-Costa et al. (2010) found that the silky shark off the western coast of Baja California Sur preyed on Gonatus spp.

No other studies have been conducted on the feeding habits of the silky shark, except in the Gulf of California by Galván-Magaña et al.

(1989). Those studies did not find cephalopod species as prey of this shark off Baja California, because it fed mostly on red crabs (Pleuroncodes planipes) in that area. Kohin et al. (2006) reported tagging data for the silky shark in the eastern Pacific Ocean, close to Costa Rica. They found that this shark dives to 370 m, though they are more frequently found (99% of the time) during day and night between the surface and 50 m at water temperatures between 24 and 31 1C. 4.5. Bigeye thresher (A. superciliosus) We sampled bigeye thresher sharks in Ecuadorian waters, where they consumed mainly D. gigas (Table 2). A tagging study in the Gulf of Mexico found that the bigeye thresher inhabited between 300 and 500 m during the day, and between 10 and 100 m during the night. In Hawaii it was found between 400 m and 500 m during the day, and between 10 m and 50 m during the night (Weng and Block, 2004).

4.6. Pelagic thresher (A. pelagicus) The pelagic thresher shark in Ecuadorian waters was found to consume D. gigas as their main prey, and the mesopelagic fish B. panamense, which indicates that this shark moves to mesopelagic waters to feed. No tagging research has been done on this shark to determine the depths at which they consume their prey.

When evaluating diet overlap and resource partitioning among the shark species, it is important to also consider the diet indices for each prey species and the prey-size distributions, in addition to the overlap index. For example, the similarity in the diet of S. lewini and P. glauca off Mexico, based on the Morisita–Horn Index, is less valid when we consider the size of cephalopods preyed upon. P. glauca preyed on larger cephalopods than did S. lewini. Non-significant differences in the Morisita–Horn overlap index among four shark species (A. pelagicus, A. superciliosus, S. lewini, and S. zyagena) off Ecuador are due to overlap in predation on the same squid species, and less so on fishes and crustaceans, as revealed by the diet indices.

The dominance of D. gigas in the diet of most shark species we evaluated suggests that sharks consume their prey in oceanic waters, possibly during the night when the squids are more susceptible to be captured ( Markaida and Sosa-Nishizaki, 2003; Polo-Silva et al., 2007, 2009). The sizes of D. gigas consumed by several sharks off Mexico are nearly uniform (226–241 mm ML) (Table 4) in comparison with the sizes of D. gigas consumed by sharks off Ecuador, which were larger for hammerhead sharks (181–217 mm ML) than for thresher sharks (138–171 mm ML).

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The presence of neritic cephalopods, such as L. diomedeae and A. cornutus, in the diet of hammerhead and thresher sharks indicates the movements of these sharks into coastal waters. A similar behavior was reported by Torres-Rojas et al. (2009) for the scalloped hammerhead in the area off Mazatlan (Gulf of California).

In P. glauca and A. superciliosus we found prey from mesopelagic and bathypelagic habitats. These shark species are known to undertake large vertical migrations (Teo et al., 2004; Weng and Block, 2004; Stevens et al., 2010), because they have a tolerance to low oxygen levels, when searching for prey at great depths.

4.7. Cephalopods as prey of sharks D. gigas is an abundant squid that was consumed by all sharks analyzed off Mexico and Ecuador. This cephalopod makes vertical migrations, occurring at depth during the day and near the surface during the night when they feed (Markaida and Sosa-Nishizaki, 2003; Polo-Silva et al., 2007, 2009). During the day, D. gigas inhabits depths of 400 m (Gilly et al., 2006), although it has been seen jumping at the surface during the day in waters close to Peru and Chile (Roper and Young, 1975), mainly when the abundance is high.

Sthenoteuthis ovalaniensis was consumed only by the silky and smooth hammerhead sharks off Mexico, but off Ecuador it was consumed by scalloped and smooth hammerhead sharks and by pelagic and bigeye thresher sharks. This squid makes vertical migrations during its life history. As juveniles (5–10-cm ML), they are located above the thermocline at depths of 15–50 m, whereas the adults (415 cm ML) feed in groups of 50–60 organisms during the night at the surface. During the day they descend probably to depths of 500–1000 m (Zuev and Nesis, 1971).

A. affinis was consumed only by the scalloped and smooth hammerhead shark off Mexico, but in Ecuador by all sharks analyzed. We do not have much information on this cephalopod, but another species in California Abraliopsis felis, migrates during the day to 300–700 m, and from the surface to 900 m at night (Roper and Young, 1975; Russell, 1996; Arkhipkin, 1997).

Argonauta spp. are epipelagic octopods with a worldwide distribution. They were consumed by silky and blue sharks in Mexican waters and by the smooth hammerhead shark off Ecuador. There are three species in the eastern Pacific, Argonauta cornuta, Aetideus pacificus, and Argonauta noury. While it is possible to identify these octopods to species if the shell is almost complete, it is difficult to identify them based on the beaks in the stomach contents alone.

A. lesueurii is an oceanic species (meso-bathypelagic) found in tropical and temperate waters, which was consumed by all sharks examined off Mexico and Ecuador, except by the scalloped hammerhead off Mexico. The mean mantle length was reported as 39 cm by Roper et al. (1984). The juveniles (15–33 mm ML) have been found at night from the surface to 125 m, but during the day they were found between 100 and 800 m (Roper and Young, 1975; D´Onghia et al., 1997).

Pholidoteuthis boschmai is an oceanic species found between the surface and 200 m. The mean mantle length was reported as 60 cm (Roper et al., 1984; Russell, 1996). In our study, these cephalopods were found during the daytime in the stomach contents of all shark species in both areas, except in the silky shark in Mexican waters.

Thysanoteuthis rhombus was recorded as prey of scalloped and smooth hammerhead sharks in both areas and by the bigeye thresher off Ecuador. This is an epipelagic species (average ML and weight¼100 cm and 20 kg, respectively) (Nigmatulin et al., 1995) that has been caught close to the coast off Japan during the fall and winter. It is common at night near the surface (Roper and Young, 1975).

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O. banksii was consumed by silky and blue sharks in Mexican waters and by smooth hammerhead sharks in both areas. In the Atlantic Ocean, O. banksii (about 5 cm ML) was found from the surface to 150 m, and larger individuals have been caught at night at the surface (Roper and Young, 1975). During the day they were found in deep waters (800–1500 m) (Roper and Young, 1975).

Squids of the family Loliginidae are neritic, inhabiting depths of 30–340 m. During the summer these squids migrate to shallow water to spawn (Roper and Young, 1975; Sánchez, 2003). We found that these cephalopods were prey of scalloped hammerhead sharks off Mexico and of all shark species that feed in the neritic habitat off Ecuador.

Squids of the family Histioteuthidae were consumed by three shark species; however the blue shark consumed more of this species than did S. lewini and S. zygaena. In California waters H. heteropsis (46 mm ML) is common. During the day, these squid move to deep waters (300–700 m), and during the night they migrate from 1000 m to the surface, with higher concentrations at about 400 m (Roper and Young, 1975).

H. atlanticus were prey of only blue sharks and were reported inhabiting depths between the surface and 3200 m (Roper and Young, 1975).

We found that Gonatus spp. were prey of all shark species analyzed, but the blue sharks consumed more of these cephalopods than the other sharks. These squids typically occur at high latitudes. Several species in California (G. onix, G. californiensis, and G. pyros) were reported making vertical migrations between 400 and 1200 m during the day, and 100 and 800 m at night (Roper and Young, 1975).

Mastigoteuthis spp. was consumed by all shark species in both areas, except by the silky shark. Off California, Mastigoteutis pyrodes have been recorded at 600–800 m during the day, and at night between 300 and 500 m (Roper and Young, 1975; Russell, 1996).

V. infernalis were recorded in the stomach contents of only blue sharks. This cephalopod lives off California at depths of 600– 1100 m (Roper and Young, 1975). ROV observations in Monterey Bay, California, suggest that the vampire squid is restricted to the oxygen minimum layer at an average depth of 690 m and oxygen levels of 0.22 mL/L (Hunt, 1996). Off Hawaii, 10 of 11 V. infernalis were captured at depths of 800–1200 m, and two of these were taken by opening–closing nets at depths of about 800–950 m. In the Atlantic Ocean at 181N, 251W, the vampire squid had a distribution between 700 and 1200 m (Clarke and Lu, 1975).

Japetella heathi are small cephalopods that were preyed upon by blue sharks in this study. Off California, it is a mesopelagic species found between 200 and 1200 m (Roper and Young, 1975).

We found the beaks of Vitreledonella richardi in the stomach contents of smooth hammerhead sharks from waters off both Mexico and Ecuador. These squids live between 300 and 1000 m (Roper and Young, 1975).

5. Concluding remarks In summary, we conclude that sharks are effective samplers of the cephalopods in open-ocean ecosystems. High consumption rates and swimming speeds of many sharks make them efficient cephalopod predators. We recorded 21 cephalopod species in the stomach contents of six shark species from waters off Mexico and Ecuador. The cephalopods most consumed by the sharks in both areas were D. gigas, A. lesueurii, O. banksii, S. ovalaniensis, Argonauta spp., A. affinis and M. dentata. We used cephalopod beak dimensions to calculate the sizes of cephalopods commonly consumed by the sharks examined in this study. Published information on cephalopod habitats provided useful clues about

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the foraging depths and habitats of these important apex predators, while the stomach contents of the sharks provided rare insights into the distribution and availability of cephalopod prey.

Our results also provide points of comparison for future changes in the ecosystems off Mexico and Ecuador that may result from anthropogenic activities and/or environmental changes.

Acknowledgments We thank the Instituto Politécnico Nacional (SIP, COFAA, and EDI) for the funds to develop this project. Also we appreciate the help of Unai Markaida (CICESE) and Eric Hochberg (Santa Barbara Natural History Museum) to review some cephalopod beaks. YETR thanks to the Programa de Becas Posdoctorales en la UNAM, Instituto de Ciencias del Mar y Limnologia (ICMyL), Universidad Nacional Autonoma de México (UNAM) for the academic and financial support. Thanks to John Logan, Unai Markaida and Robert Olson for valuable comments to improve the manuscript. Thanks to Dr. Ellis Glazier for reviewing the English-language text. This paper is a contribution to a CLIOTOP initiative to develop understanding of squid in pelagic ecosystems.

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Please cite this article as: Galván-Magaña, F., et al., (2013), http://dx.doi.org/10.1016/j.dsr2.2013.04.002i