shark predation on cephalopods in the mexican and ecuadorian pacific ocean
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Author's Accepted Manuscript
Shark predation on cephalopods in the Mex-ican and Ecuadorian Pacific Ocean
Felipe Galván-Magaña, Carlos Polo-Silva,Sandra Berenice Hernández-Aguilar, AlejandroSandoval-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
PII: S0967-0645(13)00141-0DOI: http://dx.doi.org/10.1016/j.dsr2.2013.04.002Reference: DSRII3360
To appear in: Deep-Sea Research II
Cite this article as: Felipe Galván-Magaña, Carlos Polo-Silva, Sandra BereniceHernández-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 AndrésAbitia-Cárdenas, Shark predation on cephalopods in the Mexican andEcuadorian Pacific Ocean, Deep-Sea Research II, http://dx.doi.org/10.1016/j.dsr2.2013.04.002
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Shark predation on cephalopods in the Mexican and Ecuadorian Pacific Ocean Felipe Galván-Magaña 1 Carlos Polo-Silva2,6 Sandra Berenice Hernández-Aguilar1 Alejandro Sandoval- Londoño4 Maria Ruth Ochoa- Díaz3 Nallely Aguilar- Castro1 David Castañeda-Suárez5Alejandra Cabrera Chavez-Costa1 Álvaro Baigorrí-Santacruz4 Yassir Eden Torres-Rojas1,7, Leonardo Andrés Abitia-Cárdenas1
1 Centro Interdisciplinario de Ciencias Marinas. Instituto Politécnico Nacional. Apdo. Postal 592. La Paz, Baja California Sur, México. 2 Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Apdo. Postal 70–305 Ciudad Universitaria, 04510 México, D.F., México. 3 Centro de Investigaciones Biológicas del Noroeste. Mar Bermejo 195.Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur. C.P. 23090 4 Corporación académica ambiental, Universidad de Antioquia, Calle 67 No. 53-108 Medellín, Colombia. [email protected] 5 Facultad de Biología Marina, Universidad de Bogotá Jorge Tadeo Lozano, Carrera 2 No. 11-68, Edificio Mundo Marino, Rodadero - Santa Marta, Colombia. [email protected]. 6 Present address: Oficina de Generación del Conocimiento y la Información. Autoridad Nacional de Acuicultura y Pesca, Bogotá, Colombia. 7 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 Corresponding author: Felipe Galván-Magaña. Centro Interdisciplinario de Ciencias Marinas. Av. IPN s/n .Apdo. Postal 592. La Paz, Baja California Sur, México.C.P. 23096. Phone 52 (6121270143). Fax 52(6121225322)*[email protected]
ABSTRACT
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 stomach
contents of the silky shark (Carcharhinus falciformis), blue shark (Prionace glauca),
scalloped hammerhead (Sphyrna lewini), smooth hammerhead (S. zygaena),
pelagic thresher shark (Alopias pelagicus), and bigeye thresher shark (A.
2
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 in 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.
Key words: squid, sharks, vertical distribution, Mexico, Ecuador.
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, 1996a; Cherel
and Klages, 1998; Abitia-Cárdenas 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, 1999; Torres et al., 2009;
3
Markaida and Sosa, 2010), billfishes (Abitia-Cárdenas et al., 1997,1998,1999;
Rosas-Alayola et al., 2002; Markaida and Hochberg, 2005), tunas (Galvan et al.,
1985), dolphins (Perrin et al., 1973; Galván-Magaña, 1999), and mahi-mahi
(Aguilar et al., 1998; Olson and Galvan, 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 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
4
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 (> 8 cm) close to the Baja
5
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;
Galvan-Magaña, 1999; Ruiz-Cooley et al., 2004; Estupiñan-Montaño et al., 2009;
Polo 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 (Martinez-Ortiz and Galvan-Magaña, 2007; Cabrera-Chavez-Costa et al.,
2010).
6
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 1 =
intact or nearly intact, 2 = soft parts partially digested, 3 = whole or nearly whole
skeletons without flesh (or comparable state for nonfish taxa), and 4 = 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
7
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 (% iN ) and
percent weight (% iW ) were calculated for each sample to provide mean and
variability estimates (Bizarro et al., 2007; Chipps and Garvey, 2007). For prey
counts,
1
1
1% 100P
iji Q
jij
i
NN
P N=
=
⎛ ⎞⎜ ⎟⎜ ⎟=⎜ ⎟⎜ ⎟⎝ ⎠
∑∑
(1)
where % iN is 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,
1
1
1% 100P
iji Q
jij
i
WW
P W=
=
⎛ ⎞⎜ ⎟⎜ ⎟=⎜ ⎟⎜ ⎟⎝ ⎠
∑∑
(2)
where % iW is 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),
8
( ), ,1
2 2, ,
1
2n
x i y iin
x i y ii
P PC
P P
μ =
=
•=
+
∑
∑
where Cμ is the Morisita-Horn index, Px,i is the proportion of i-th prey with respect to
all prey of predator x; Py,i is the proportion of the i-th 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 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).
9
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 (Table 1 and 2).
3.1 Sharks in the eastern Pacific
Scalloped hammerhead (Sphyrna lewini) (Baja California Sur: n = 131, eastern
equatorial Pacific: n = 82).
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 = 46; eastern
equatorial Pacific: n =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 O. banksii were the most important species (Table 1). In the eastern
10
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. lesueuri (Table 2).
Blue shark (Prionace glauca) (Baja California Sur: n = 210)
The cephalopods were the prey most consumed by blue sharks in number (79%)
and weight (98%) (Table 1). The main prey by number were Onychoteuthis banksii,
Gonatus californiensis, and D. gigas. By weight, Gonatus californiensis, A.
lesueurii, and D. gigas were the most important species (Table 1).
Silky shark (Carcharhinus falciformis) (Baja California Sur: n =142)
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 = 91)
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 = 107)
11
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 Abraliopsis 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 Gonatus
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 o the blue shark P. glauca consumed larger squids on average than did
12
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
Sphyrna 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 Prionace 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, whereas the bigeye thresher shark A.
superciliosus consumes epipelagic and mesopelagic cephalopods, followed by
13
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 eastern Pacific Ocean. These cephalopods are
also consumed by other upper-level predators (birds, fishes, and marine mammals)
(Imber et al., 1992; Clarke, 1996a), 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.
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.
14
the blue and bigeye thresher sharks, dive to deep waters to prey on cephalopods
(Carey and Scharold, 1990; Polo-Silva 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 to 9 cephalopod species.
Scalloped hammerhead shark (Sphyrna lewini)
15
Studies in the Gulf of California have found that the scalloped hammerhead shark
preys on several cephalopod species, such as Mastigoteuthis sp., A. lesueuri,
Moroteuthis robusta, Octopus spp., Dosidicus gigas, Rossia sp., Vampyroteuthis
infernalis, and H. heteropsis (Klimley, 1983; Galvan et al., 1989). Torres et al.
(2009) in the area off Mazatlan, Sinaloa, México found the diet of juvenile
scalloped hammerhead sharks were dominated by L. diomedeae and A. affinis.
The cephalopod prey in our study are similar to the species reported by Torres 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 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,
mesopelagic, and neritic cephalopods (Duncan and Holland, 2006; Torres 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,
1988) 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. lesueuri, Octopoteuthis, and Taningia danae. They also
found other cephalopods as Chiroteuthis, Cranchidae (Teuthowenia),
16
Histoteuthidae (H. miranda and H. 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.
Smooth Hammerhead shark (Sphyrna 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 et al.,
1998). The Ommastrephidae and Ancistrocheiridae families were the most
important prey in the diet of this shark in both geographic areas. Castañeda-
Suárez 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 Dosidicus 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
17
been conducted to determine the vertical movements to associate it with different
cephalopod species consumed by this shark species.
Blue shark (Prionace glauca)
The feeding habits of blue sharks off Mexico revealed a diet composed of
mesopelagic cephalopods (H. heteropsis, A. lesueuri, and H. atlanticus), epipelagic
cephalopods (Argonauta sp, Gonatus californiensis, and D. gigas), and
bathypelagic squids (V. infernalis, Architeuthis sp.) off the coast of the Baja
California Peninsula (Hernández, 2008; Markaida and Sosa, 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, 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 (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
Ancistrocheirus lesueuri in Brazilian waters (Vaske-Junior and Rincon, 1998). Off
18
SW Ireland, blue sharks consumed Haliphron 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 °C.
Silky shark (Carcharhinus 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 time)
during day and night between the surface and 50 m at water temperatures
between 24 and 31 °C.
Bigeye thresher (Alopias superciliosus).
19
We sampled bigeye thresher sharks in Ecuadorian waters, where they consumed
mainly Dosidicus 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).
Pelagic thresher (Alopias pelagicus).
The pelagic thresher shark in Ecuadorian waters was found to consume Dosidicus
gigas as their main prey, and the mesopelagic fish Benthosema 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 is due to overlap in predation on the same
squid species, and less so on fishes and crustaceans, as revealed by the diet
indices.
20
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,
2003; Polo et al., 2007, 2009). The sizes of D. gigas consumed by several sharks
off Mexico are nearly uniform (226 to 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 to 217 mm ML) than for thresher sharks (138 to 171 mm
ML).
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 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.
4.1 Cephalopods as prey of sharks
Dosidicus 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
21
(Markaida and Sosa, 2003; Polo 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- to 10-cm
ML), they are located above the thermocline at depths of 15 - 50 m, whereas the
adults (> 15 cm ML) feed in groups of 50 to 60 organisms during the night at the
surface. During the day they descend probably to depths of 500 to 1000 m (Zuev
and Nesis, 1971).
Abraliopsis 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, A. pacificus, and A. noury. While it is possible to identify these
22
octopods to species if the shell is almost complete, it is difficult to identify them
based on the beaks in the stomach contents alone.
Ancistrocheirus lesueuri 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 to
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’onguia 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 weight = 100 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).
23
Onychoteutis 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) were 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 Histioteuthis heteropsis (> 6 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).
Haliphron atlanticus were prey of only blue sharks and were reported inhabiting
depths between the surface and 3200 m (Roper and Young, 1975).
24
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 to
800 m during the day, and at night between 300 and 500 m (Roper and Young,
1975; Russell, 1996).
Vampyroteuthis 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 18° N,
25° W, the vampire squid had a distribution between 700 and 1200 m (Clarke and
Lu, 1975).
25
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).
4. 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:
Dosidicus gigas, Ancistrocheirus lesueurii, Onychoteuthis banksii, Sthenoteuthis
ovalaniensis, Argonauta spp., Abraliopsis affinis and Mastigoteuthis 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 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.
26
Acknowledgements
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. 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.
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40
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 equations 1 and 2 for calculations of %N and %W. S. lewini S. zygaena P. glauca C. falciformis %N %W %N %W %N %W %N %W Cephalopo
da 72.4 68.1 90.2 54.7 78.5 97.9 79 50.7
Ancistrocheirus lesueurii _ _ 21.2(27
.3) 8.0
(24.2) 5.0 (13)
15.6 (45.6)
13.3 (32.8)
0.2 (1.8)
Dosidicus gigas
30.3 (43.1)
40.1 (30.2)
36.0 (31)
18.2 (36.7)
8.8 (26.3)
12.4 (15.4)
44.2 (45.9)
43.1 (58.9)
Gonatus californiensis
1 (15) 0.6 (2.5)
0.8 (8.3)
<0.1 (<0.1)
10.5 (27.3)
42 (53.2)
0.2 (1.3)
0.3 (2.7)
Mastigoteuthis dentata
3.6 (15.3)
20.5 (39)
0.62 (7.4)
<0.1 (<0.1)
2.1 (4.5)
0.9 (1.8) _ _
Histioteuthis sp. _ _ _ _ _ 1 (6.5) 0.2
(1.6)
Octopus sp. 0.1 (1.0) _ _ _ _ _ _ _
Lolliguncula diomedeae
6.2 (23.2)
2.5 (14.2) _ _ _ _ _ _
Pholidoteuthis boschmaii
1.2(9.0)
1.7 (7.1)
0.2 (2.0)
<0.1 (<0.1)
4.7 (20.2)
0.3 (1.1) _ _
Thysanoteuthis rhombus
3.9 (15.0)
0.1 (1.8)
0.1 (0.7)
0.3 (1.3) _ _ _ _
Abraliopsis affinis
25.0 (39.1)
0.02 (1.3)
3.8 (11.5)
<0.1 (<0.1) _ _ _ _
Sthenoteuthis oualaniensis _
_ 13 (22.2)
2.8 (9.4) _ _ 2.0
(12.9) 0.5
(3.6)
Octopodoteuthis sicula _ _ 0.1
(0.9) 0.1
(0.3) _ _ _ _
Vitreledonella richardi _ _ <0.1
(<0.1) <0.1
(<0.1) _ _ _ _
Histioteuthis heteropsis _ 2.6
(6.4) _ _ 5.9 (20)
2.2 (3.3) _ _
Onychoteuthis banksii _
_ 13.7 (19.9)
25.4 (40.7)
19.5 (36.3)
0.7 (1.6)
5.1 (19.8)
6.4 (12.4)
Argonauta sp. _ _ 0.7
(8.0) <0.1
(<0.1) 9.2
(26.1) 0.6
(1.2) _ _
Liocranchia reinharti _
_ _ _ 2.6 (15.6)
0.5 (1.1) _ _
Japetella heati _ _ _ _ 4.1
(18.9) <0.1
(<0.1) _ _
Vampyroteuthis infernalis _ _ _ _ 2.6
(12.8) <0.1
(<0.1) _ _
Haliphron atlanticus _ _ _ _ 3.5
(15.6) 22.4 (33) _ _
41
Argonauta cornutus _ _ _ _
13.2 (31.5)
0.3 (1.1)
S. lewini S. zygaena P. glauca C. falciformis %N %W %N %W %N %W %N %W Crustacea 2.0 0.2 _ _ 17.1 1.1 11 0.9
Penaeus californiensis
1 (18.0
)
0.1 (1.2) _ _ _ _ _ _
Pleuroncodes planipes
1 (22.0
) 1 (4.1) _ _ 16.9
(37.4) 1.1
(3.1) 11.0(30.1)
0.8 (5.3)
Squilla biformis _ _ _ _ 0.4
(4.5) <0.1
(<0.1) _ _
Farfantepenaeus californiensis _ _ _ _ _ _ _ 0.1
(1.9) Osteichthyes 25.6 31.5 9.5 45 4.1 1 9.9 48.0 Porichthys analis
0.5 (5.0) 1 (4.7) _ _ _ _ _ _
Decapterus macrosoma
0.5 (3.4) 2 (6.50 _ _ _ _ _ _
Naucrates ductor
0.5 (2.1)
0.5 (3.2) _ _ _ _ _ _
Trachurus symmetricus
0.5 (2.3)
0.1 (1.1) _ _ _ _ 0.7
(5.8) 0.1
(1.7) Trachinotus rhodopus
0.4 (1.8)
0.1 (1.0) _ _ _ _ _ _
Caranx sp. 0.4 (2.5)
1.1 (7.7)
0.2 (2.6)
0.1 (1.1) _ _ _ _
Sardinops caeruleus
4.4 (7.5) 1 (3.9) 3.5
(17.2) 8.5
(23.6) _ _ _ _
Coryphaena hippurus
0.5 (3.5)
0.2 (1.7)
0.1 (0.9)
0.1 (0.6) _ _ 0.9
(5.4) 17.1
(32.1)
C. equiselis _ _ _ _ _ _ 1.4 (11.6)
18.2 (35.4)
Gymnothorax sp.
1 (3.6) 1 (4.0) _ _ _ _ _ _
Paralichthys woolmani
0.5 (1.4)
0.1 (1.3) _ _ _ _ _ _
Syacium latifrons
0.3 (1.1)
0.1 (1.0) _ _ _ _ _ _
Etropus crossotus
0.4 (2.5)
0.2 (1.6) _ _ _ _ _ _
Heteropriacantus cruentatus
1 (4.2) 1 (3.9) _ _ _ _ 0.9
(6.1) 3.6
(8.5)
S. lewini S. zygaena P. glauca C.
falciformis
%N %W %N %W %N %W %N %W
Paralabrax maculatofasciatus 0.8 (4.5) 2.1 (4.3) _ _ _ _ _ _
Diplectrum pacificum 0.3 (3.2) 0.4 (2.7) <0.1 (<0.1) 5.5 (23.5) _ _ _ _
Scomber japonicus 3 (8.5) 3.4 (40.1) 0.5 (3.9) 5.5
(21.3) 3.2
(15.4) 0.7 0.5 (4.6
0.6 (3.
42
) 9)
Auxis thazard 1.3 (3.2) 4.7 (22.1) _ _ _ _
1.4 (11.6)
0.1 (1.5)
Auxis sp. _ _ _ _ _ _ 1.3 (11.6)
2.2 (5.2)
Remora remora _ _ _ _ 0.8 (9.0) <0.1 (<0.1)
_ _
Zu cristatus _ _ _ _ 0.4 (4.5) <0.1 (<0.1)
_ _
Selar cromenophthalmus _ _ _ _ 0.1 (1.2) 0.3
(1.3) _ _
Fam. Balistidae _ _ _ _ _ _ 1.4 (11.6)
1.1 (7.2)
Etrumeus teres 0.3 (3.1) <0.1 (0.9) _ _ _ _ _ _
Paralabrax sp. 0.5 (5.0) 2.1 (5) _ _ _ _ _ _ Euthynnus lineatus 0.3 (3.1) 1.2 (3.5) _ _ _ _ _ _
Bodianus diplotaenia _ _ _ _ _ _ 1.4 (11.6)
0.2 (1.8)
Scorpaena histrio 0.3 (3.0) 0.7 (6.1) _ _ _ _
Synodus evermanni 4.4 (10.2) 3.5 (12) 2.5 (9.6) 9.2
(25.4) _ _ _ _
Cheilopogon pinnatibarbatus 1 (2.8) 0.5 (3.2) _ _ _ _ _ _
Prionurus punctatus 0.3 (2.7) 0.5 (3.5) _ _ _ _ _ _ Synchiropus atrilabiatus 0.5 (3.1) 0.1 (1.2) _ _ _ _ _ _
Apterichtus equatorialis 1 (3.1) 0.2 (1.7) _ _ _ _ _ _
Merluccius productus _ _ _ _ 0.9 (9.1)
<0.1 (<0.1)
_ _
Macrocystis pyrifera _ _ _ _ 1.5 (10.5)
<0.1(<0.1)
_ _
Mugil cephalus _ _ 1 (4.7) 2.3 (8.2) _ _ _ _ Vinciguerria lucetia _ _ 0.2 (2.6) 1.0 (4.2) _ _ _ _
Fodiator acutus _ _ 0.3 (3.9) 4.3 (18.6) _ _ _ _
Hippoglossina stomata _ _ <0.1(<0.1) 7.7
(24.8) _ _ _ _
Brotula sp. _ _ 0.6 (7.9) 0.1 (0.8) _ _ _ _ Gerres cinereus _ _ 0.6 (7.9) 0.1 (0.6) _ _ _ _
43
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 equations 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 48.1 85.7 86.7 88.2 50.5 68.3 21.1 51.1
Dosidicus gigas
8.6 (19.5)
41.2 (59)
52.7 (34.3)
67.7 (36.9)
42.2(62.4)
60.2 (43.5)
5.7 (18.3)
25 (40.7)
Lolliguncula diomedeae
5.3 (18.5)
4.1 (13.5)
1.5 (5.7)
0.4 (4.6) 0.7 (6.7) <0.1
(<0.1) 0.1
(0.4) 8.4
(12.8) Ancistrocheirus lesueurii
6.3 (16.9)
11.4 (30.2)
8.6 (14.6)
5.9 (15.5) 1.0 (5.4) <0.1
(<0.1) 6.0
(15.2) 0.1
(1.30) Sthenoteuthi
s oualaniensis
2.3 (9.8) 23 (36.2)
12.6 (25.2)
12.9 (26.6)
5.7 (13.9)
8.0 (19.5) 1.1 (4) 5.3
(17.2)
Histioteuthis sp.
2.7 (10.4) 2.8 (5.3) 0.4
(3.2) 0.5
(4.4) _ _ 0.2 (1.1)
2.4 (3.6)
Onychoteuthis banksii _ _ 0.1
(1.2) <0.1
(<0.1) _ _ _ _
Octopodoteuthis sicula
2.5(12.6
) 1.8 (4.3) 2.0
(4.8) 0.3
(1.1) _ _ _ _
Mastigoteuthis dentata 12.9(25) 0.4
(1.60 4.9
(11.8) 0.1
(0.4) 0.4 (3.6) <0.1 (<0.1)
0.3 (2.0)
2.4 (3.4)
Pholidoteuthis boschmai
0.7(4.3) 0.8 (3.5) 0.1
(0.6) 0.1
(0.7) 0.4 (4.3) <0.1 (<0.1)
0.1 (1.2)
0.2 (1.0)
Gonatus sp.
0.1(<0.1)
0.1 (1.4) 0.06 (0.3)
<0.1 (<0.1) _ _ _ _
Argonauta sp. _ _ 0.06
(0.5) <0.1
(<0.1) _ _ _ _
Abraliopsis affinis 0.5 (3.9) <0.1
(<0.1) _ _ 0.1 (1.2) <0.1 (<0.1)
7.5 (20.2)
7.0 (24.8)
Vitreledonella richardi _ _ 0.5
(2.2) <0.1
(<0.1) _ _ _ _
Octopus sp. 6.2 (17.7)
<0.1 (<0.1) _ _ _ _ _ _
Thysanoteuthis rhombus 0.1 (1.1) 0.1 (1.3) 3.1
(8.1) 0.2
(2.8) _ _ 0.1 (1.3)
0.3 (1.4)
Crustacea 4.4 0.2 _ _ _ _ _ _ Penaeus
stylirostris _ _ _ _ <0.1 (<0.1) 0.1 (0.3) _ _
Solenocera agassizi 1.4 (7.0) 0.1 (1.6) _ _ _ _ _ _
Heterocarpus vicarius 2 (10) 0.1 (1) _ _ _ _ _ _
Fam.Penaeidae 0.5 (4.4) <0.1
(<0.1) _ _ _ _ _ _
Fam. Xantidae 0.7 (5.9) <0.1
(<0.1) _ _ _ _ _ _
Osteichthyes 47.5 14.1 12.9 11.4 48.9 31.4 78.4 48.8
Synodus sp. _ _ 0.07 (0.8)
<0.1 (<0.1)
<0.1 (<0.1) 0.1 (0.3) _ _
44
Auxis thazard
3.7 (17.1) 0.7 (1.1) 2.9
(14.6) 2.6
(14.3) 3.0
(12.4) 1.3
(10.9) 3.6
(11.4) 5.2
(24.80) S. lewini S. zygaena A. pelagicus A. superciliosus
%N %W %N %W %N %W %N %W Osteichthyes (continued) _ _ _ _ _ _ _ _ Oxyporhamphus micropterus _ _
1.1 (5.9)
0.3 (1.7) _ _ _ _
Exocoetus monocirrhus _ _
0.32 (1.6)
<0.1 (<0.1) _ _ _ _
Katsuwonus pelamis _ _ 0.5
(3.2) 0.5
(4.5) _ _ _ _ Canthidermis maculatus _ _
0.1 (0.9)
<0.1 (<0.1) _ _ _ _
Sardinops sagax _ _ _ _ 1.5
(10.4) 0.9 (8.1) 13.2
(24.70)
3.6 (17.2
)
Larimus argenteus 10.2
(22.8) 0.6
(1.9) 1.0
(9.2) 0.7
(8.6) 0.2 (1.4) 0.1 (0.6) 20.5
(32.40)
15.6 (34.5
)
Coryphaena hippurus 0.2
(1.7) 0.1
(1.1) 1.2
(9.6) 1.2
(9.2) _ _ 1.3 (7.3) 1.5
(3.4) Remora remora _ _ _ _ _ _ 0.2 (1.2) 0.1
Benthosema panamense _ _ _ _
37.3 (46.8)
24.1 (41.4)
22.1 (34.5)
4 (17.2
)
Fam. Carangidae _ _ 0.7
(8.6) 0.7
(8.6) _ _ _ _
Fistularia sp. _ _ 0.7
(8.6) 0.7
(8.6) _ _ 0.1(0.5) 0.1
(1.4)
Thunnus albacares _ _ 2.4
(12.6) 2.2
(12.4) _ _ _ _
Katsuwonus pelamis 0.1
(1.4) 1.5
(3.2) 0.5
(3.6) 0.8
(6.7) _ _ _ _
Sarda sarda _ _ <0.1
(<0.1) <0.1
(<0.1) _ _ _ _
Gempylus serpens 1.4
(11.8) 0.3
(5.2) 0.1
(1.5) <0.1
(<0.1) 0.2 (1.3) <0.1
(<0.1) _ _ Cheilopogon spilonotopterus _ _
0.5 (3.3)
0.3 (1.5) _ _ _ _
Ophichthus sp. 1.4
(7.20 0.4
(1.6) 0.3
(4.3) 0.3
(2.9) 0.7 (4.5) 0.3 (2.0) 0.8 (4.5) 2
(7.0) Ophichthus sp. morphotype2
4 (15.2) 1 (2.2) _ _ 0.1 (1.0) 0.4 (3.9) 0.1 (0.3)
0.1 (0.4)
Ophichthus sp. morphotype 3
0.7 (5.9)
0.7 (1.4) _ _ 0.1 (0.5)
<0.1 (<0.1) 1.7 (9.1)
0.1 (0.4)
Ophichthus sp. morphotype 4 _ _ _ 0.1 (0.6) 0.1 (0.7) _ _ Ophichthus sp. morphotype 5 _ _ _ _ 0.1 (0.9) 0.1 (0.4) _ _ Ophichthus sp. morphotype 6 _ _ _ _ _ _ 0.3 (2.0)
0.5 (2.3)
Ophichthus sp. morphotype 7 _ _ _ _ _ _ 0.1 (0.5)
1.2 (1.6)
S. lewinii S. zygaena A. pelagicus A. superciliosus
45
%N %W %N %W %N %W %N %W Myrophys vafer
1.9 (9.9)
0.8 (3.1) _ _ _ _ _ _
Pseudomyrophis sp.
1.4 (11.8)
<0.1 (<0.1) _ _ _ _ _ _
Paralabrax callaensis _ _ _ _
0.1 (0.9) 0.2 (2.3) _ _
Exocoetus monocirrhus _ _
0.7 (8.6))
0.4 (5.3) _ _ _ _
Merluccius gayi
6.7 (17.0)
0.5 (4.2) _ _
4.2 (17.3) 2.5 (14.4) 12.9 (26)
12 (28.8)
Symbolophorus evermanni _ _ _ _
0.1 (0.4) 0.23 (2.0) _ _
Lagocephalus lagocephalus _ _ _ _
0.1 (1.0) <0.1 (<0.1) 0.2 (1.22)
0.4 (0.6)
Brama japonica _ _ _ _
1.1 (10.4) 1.1 (10.8) _ _
Ablennes hians _ _ _ _ _ _ 1.3 (4.4)
2.4 (7.0)
Munida sp. 1.2
(8.1) 0.2
(2.3) _ _ _ _ _ _ Fam Hemirramphidae
<0.1 (<0.1)
0.1 (2.7) _ _ _ _ _ _
Lutjanidae 2.6
(14.6) 0.4
(1.5) _ _ _ _ _ _ Fam. Scorpaenidae
6 (12.9)
0.4 (1.40 _ _ _ _ _ _
Fam. Serranidae
0.5 (3.9)
0.4 (1.5) _ _ _ _ _ _
Fam. Scombridae _ _
0.2 (1.7)
0.3(2.0) _ _ _ _
46
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 1 0.46 (0.15-
0.94) 0 0.001 (0.0001-
0.005)
P. glauca 0.46 (0.15-0.94) 1 0.03 (0.01-
0.06) 0
C. falciformis 0 0.03 (0.01-
0.06) 1 0.003 (0-0.009)
S. zygaena 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 1 0.52 (0.19-
0.86) 0.52 (0.24-0.78) 0.47 (0.36-0.57) A. superciliosus 0.52 (0.19-0.86) 1 0.72 (0.51-0.86) 0.64 (0.39-0.80)
S. zygaena 0.52 (0.24-0.78) 0.72 (0.51-
0.86) 1 0.49(0.29-0.71)
S. lewini 0.47 (0.36-0.57) 0.64 (0.39-
0.80) 0.49(0.29-0.71) 1
47
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 P. glauca S. zygaena
N Mean RL (mm) SD Rang
e Mantle length
(mm) N Mean RL (mm)
SD
Range
Mantle length (mm)
Ancistrocheirus lesueurii 43 5.7 1 3.3-
7.6 192.2 5 9.4 2.6
2.4-7.3 341.8
Gonatus californiensis 84 7.6 0.5 4.9-
9.1 157 1 3.4 - - 77.5
Histioteuthis dofleini 13 3.9 1.6 1.6-
6.5 64.4 - - - - -
Dosidicus gigas 14 5.5 2.5 2.6-
10.0 241 22 5 3.
9 9.6-19.3 223.2
Onychoteuthis banksii 6 3.3 0.6 2.6-
3.8 172.4 13 3.1 4.
5 3.85-8.67 160.2
Pholidoteuthis boschmai 9 2.5 0.8 1.3-
3.5 91.7 3 1 0.8 1.8-3 34.1
Thysanoteuthis rhombus 1 - - - - 1 4.9
- - -
Mastigoteuthis dentata - - - - - -
- - -
Haliphron atlanticus 27 6.2 1.6 3.7-
10.5 - - -
- -
Sthenoteuthis oualaniensis - - - - - 1
0 4 3.3
3.02-14.9 141.9
Abraliopsis affinis - - - - - -
- - -
Octopodoteuthis sicula - - - - 1 1 0.
8 9.5-10.3 16.9
Vitreledonella richardi - - - - - 1 6.8
- - -
Mean HL (mm) SD Rang
e Mantle length
(mm) Mean HL
(mm) SD
Range
Argonauta sp. 66 3.4 0.8 1.1-10.2 5.7 1 3.2 -
- -
Sphyrna lewini Cephalopod
species N Mean RL
(mm) SD
Range
Mantle length (mm)
Ancistrocheirus lesueurii - - - - - Gonatus californiensis 2 7.1
0.3
7.0-7.1 147.9
Histioteuthis dofleini - - - - -
Dosidicus gigas 103 5.1
1.3
3.3-10 226.7
Onychoteuthis banksii 35 2.6
0.3
2.2-3.0 129.7
Pholidoteuthis - - - - -
48
boschmai Thysanoteuthis rhombus - - - - - Mastigoteuthis dentata 7 1.8
0.2
1.5-2.2 105.6
Haliphron atlanticus - - - - - Sthenoteuthis oualaniensis - - - - -
Abraliopsis affinis 29 4.4 0.8
3.4-7.2 94.28
Octopodoteuthis sicula - - - - - Vitreledonella richardi - - - - - 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. Cephalop
od species
S. zygaena S. lewini
N Mean RL (mm) SD Range Estimated
ML (mm) N Mean RL (mm)
SD
Range
Estimated ML (mm)
Ancistrocheirus lesueurii
195 4.2 1.6
0.9-13.8 129.9 2
6 4.5 1.4
0.9-
13.8
142.1
Gonatus californiensis
- - - - - - - - - -
Histioteuthis heteropsis 4 5.5
1.6
3.7-6.4 133.4 11 4.5 1.
3
2.3-
6.7 112.9
Dosidicus gigas
1050 7.3
3.5
0.8-25 217.1 45 6.3 4.
2 0.4-28 181.3.
Onychoteuthis banksii 2 1.9 - - 87 - - - - -
Pholidoteuthis boschmai
7 4.2 1.4
2.0-4.7 157 2 3.8 0.1
3.7-
3.9 141.6
Thysanoteuthis rhombus
80 4.1 1 1.6-6.6 - 1 4.4 - - -
Mastigoteuthis dentata 190 2.4 1 0.2-5.4 109.3 4
2 1.9 1.1
0.6-
5.1 106.2
Sthenoteuthis oualaniensis
252 6.7 2.3
1.2-14.1 245 7 8.3 3.
8
1.2-
14.1
306.2
Lolliguncul 18 1 0 0.5-1.4 - 9 1.4 0. 0.5 -
49
a diomedeae
.2
0 2 -1.6
Abraliopsis affinis - - - - - - - - -
Octopodoteuthis sicula 47 4.9
2.2
2.1-7.8 84.4 11 8 1.
6
4.2-
11.4
138
Vitreledonella richardi 19 4.8
1.4
2.3-6.7 - 8.5 - - -
Gonatus sp. 3 4.4 1.2
3.0-5.5 94.8 1 4.4 - - 94.8
Octopus sp. - - - -
Mean HL (mm) SD Range Estimated
ML (mm)
Argonauta sp. 3 5.1
2.5
3.3-6.9 43.1 - - - - -
Cephalopods species Alopias pelagicus Alopias superciliosus
N
Mean RL
(mm) SD
Range
Estimated ML (mm) N
Mean RL (mm)
SD
Range
Estimated of ML
(mm)
Ancistrocheirus lesueurii 3
6.0 0.1 3-6 203.2 - 4.5
1.9
1.8-6.6 142.08
Gonatus californiensis - - - - - - - - - -
Histioteuthis heteropsis -
- - - - 1 2.8
0.1
2.7-2.8 77.9
Dosidicus gigas
149 6.0
0.3 1-2 170.5 19 5.1
1.7
1.8-5.9 138.3
Onychoteuthis banksii - - - - - - - - - - Pholidoteuthis boschmai 2 3.0 - - - 2 2.1 3 - 76.3 Thysanoteuthis rhombus - - - - - - - - - -
Mastigoteuthis dentata 6 1.0
<0.1 1-2.5 100.6 3 1 0 - 100.6
Sthenoteuthis oualaniensis 22 6.0
0.1 4-9 218.3 4 8.6
2.3 6-10 317.6
Lolliguncula diomedeae 13 1.0
0.0 1-2 - - 1
0.1 1-1.3 -
Abraliopsis affinis 1 2.0 - - - 20 - - - - Octopodoteuthis sicula - -
- - - 2 3.5 - - 60.2
50
Vitreledonella richardi - -
- - - - - - - -
Gonatus sp. - - - - - - - - - -
Octopus sp. - - - - - 1 0.27 - - -