Journal of the Marine Biological Association of the United Kingdom, 2018, 98(4), 927 –935.
doi:10.1017/S002531541600179X
# Marine Biological Association of the United Kingdom, 2017
Diet of three shark species in the Ecuadorian
Pacific, Carcharhinus falciformis,
Carcharhinus limbatus and Nasolamia velox
~ o-figueroa2,
colombo estupin~a’n-montan~o1, fabian pacheco-trivin~o2, luis g. ceden
3
1
~ a and jose f. estupin~a’n-ortiz
felipe galva’n-magan
1
Fundación Alium Pacific, Carrera 26 No. 5C– 13, Santiago de Cali, Colombia, 2Universidad Laica “Eloy Alfaro” de Manabı́, Facultad
Ciencias del Mar, Ciudadela Universitaria vı́a San Mateo, Apartado Postal 27 – 32, Manta, Manabı́, Ecuador, 3Instituto Politécnico
Nacional, Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n. La Paz, Baja California Sur, C.P. 23096, México
We analysed the stomach contents of 69 silky sharks Carcharhinus falciformis, 44 blacktip sharks Carcharhinus limbatus and
24 whitenose sharks Nasolamia velox caught in the Ecuadorian Pacific from August 2003 to December 2004. Prey included
bony fishes, elasmobranchs, molluscs, crustaceans and turtles, with bony fishes being the most important to the diets of all
three sharks, suggesting they are piscivorous predators. Based on the index of relative importance, the C. falciformis diet
includes Thunnus albacares, Thunnus sp. and Auxis thazard, as well as some squid, fish and turtles. Similarly, the C. limbatus diet was dominated by T. albacares, Exocoetus monocirrhus, A. thazard, Katsuwonus pelamis, members of the
Ophichthidae family and other elasmobranchs. Meanwhile, N. velox consumed mainly Dosidicus gigas, Larimus argenteus,
Cynoscion sp. and Lophiodes spilurus. There is little competition for food between these tertiary carnivores: C. limbatus
prefers prey from coastal-oceanic habitats; C. falciformis consumes mostly oceanic prey and N. velox focuses on prey from
coastal habitats. The lack of information on the biology of sharks in Ecuador hinders the development of appropriate management and conservation plans to protect shark resources. This study increases our knowledge and understanding of sharks
in Ecuador, thus contributing to their conservation.
Keywords: Silky shark, blacktip shark, whitenose shark, feeding, trophic level, Ecuadorian Pacific
Submitted 17 March 2016; accepted 23 November 2016; first published online 22 February 2017
INTRODUCTION
Elasmobranchs have been exploited in many parts of the
world as part of both the target and by-catch of the tuna,
trawl and longline fishery (Anderson, 1990). The rapid expansion of these activities has led to the collapse of some shark
populations in a short period of time (Anderson, 1990),
causing important changes in the natural renewal rates of
these stocks, which will now require decades to return to
their previous levels (Anderson, 1990). Moreover, since
sharks are apex predators in marine ecosystems, they play
an important role in regulating prey populations at lower
trophic levels (i.e. fish, invertebrates, reptiles, mammals and
birds) (Ellis et al., 1996).
Studies on the trophic ecology, diet composition and
trophic level of sharks shed light on their life histories, roles
in marine ecosystems and species distributions as well as
energy flows, and the impact of predation by different
species (Cortés, 1999). Information regarding important
feeding and breeding areas identified by such studies are
used in conjunction with other biological studies to develop
Corresponding author:
F. Galván-Magaña
Email: galvan.felipe@gmail.com
appropriate strategies for the conservation and management
of shark species (Galván-Magaña et al., 1989).
This information is important as it allows us to make inferences regarding the predator– prey relationship, including
prey abundance, distribution, and preferences, as well as possible ontogenetic changes in diet. Further, understanding
quantitatively the feeding ecology of the shark species is a
very important step to constructing a complex food web
(Navia et al., 2010; Bornatowski et al., 2014a) and ecosystem
models for evaluating the function of each species within an
ecosystem, and predicting possible changes through fishing
effects (Stevens et al., 2000). Additionally, studies of feeding
ecology are important not only for identifying the relative frequency of the particular prey in a shark’s diet, but also for
revealing the importance of species (sharks and batoids) as a
link between the higher and lower levels of the food chain
(Bornatowski et al., 2014b).
Carcharhinidae is the second largest family of sharks of
commercial importance in Ecuador. The silky shark C. falciformis (Müller & Henle, 1839) is the third most important
species for Ecuador’s fisheries. The species is distributed in
tropical and subtropical waters throughout the Eastern
Pacific from Baja California to Peru (Compagno, 1984;
Robertson & Allen, 2002), displaying epipelagic habits and
feeding on a variety of prey, particularly bony fishes, cephalopods, and, to a lesser extent, crustaceans (Fischer et al., 1995).
Another species targeted by Ecuadorian fisheries is the
927
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928
~ a’ n-montan~ o et al.
colombo estupin
blacktip shark Carcharhinus limbatus (Müller & Henle, 1839),
found only infrequently in landings. The species inhabits the
tropical and subtropical waters of the Eastern Pacific from
San Diego, California to Peru, including the Revillagigedo
and Galapagos Islands (Compagno, 1984; Robertson &
Allen, 2002). This species lives mainly in coastal and
oceanic surface waters and is a fast swimmer, allowing it to
feed on shoaling fish, rays and squid (Cervigón et al., 1992;
Fischer et al., 1995). Similarly, the whitenose shark
Nasolamia velox (Gilbert, 1898) is also caught by local fisheries. We know little of this species; however, it is distributed
from Baja California to Peru (Compagno, 1984), and considered endemic to the Eastern Tropical Pacific (Robertson &
Allen, 2002), preferring coastal habitats where it feeds on
fishes, cephalopods and crustaceans (Compagno, 1984).
Fishery is one of the most important economic activities in
Ecuador and often includes the capture of sharks. However
there is a lack of studies on the basic biology of sharks in
Ecuador, and only a few management studies, including the
National Plan for the Conservation of Sharks (MICIP,
2006). Some recent studies have focused on shark dietary
habits (Estupiñán-Montaño et al., 2009; Polo-Silva et al.,
2009, 2013; Loor-Andrade et al., 2015) and reproduction
(Romero-Caicedo et al., 2014). However, to date no studies
have examined the biology of silky sharks C. falciformis, blacktip sharks C. limbatus and whitenose sharks N. velox. Thus,
the goal of this paper was to investigate the diet and trophic
positions of these three shark species, to generate baseline
information to improve our knowledge and serve as a starting
point for further research on sharks in the country, and thus
contribute to scientific knowledge on these species.
MATERIALS AND METHODS
We collected stomachs of 69 Carcharhinus falciformis (43
females, 26 males) from January to December 2004; 44 C. limbatus (four females, 40 males) and 24 Nasolamia velox (17
females, seven males) from August 2003 to March 2004,
caught in Ecuadorian waters and landed in the port of
Manta (Ecuador). The study area extended from 028N to
028S and from the coast to 848W. For each shark, the total
length (TL) was recorded and the digestive tract was
removed by dissection. Stomach contents were removed and
screened through a 1.5 mm sieve. Prey were identified to the
lowest possible taxon considering the state of digestion and
subsequently placed in plastic bags and preserved on ice for
transportation to the laboratory.
For the taxonomic identification, we consulted different
identification keys; for fishes we used those by Clothier
(1950), Rubio (1988), Fischer et al. (1995), Chirichigno
(1998) and Garcı́a-Godos (2001); whereas to identify cephalopods, we used Wolff (1982, 1984) and Clarke (1986). Due to
the advanced state of digestion, cephalopods were identified
by their mandibular apparatus and crustaceans were classified
based on their exoskeletons following Fischer et al. (1995).
We quantified the stomach contents numerically (N),
gravimetrically (W), and in terms of the frequency of occurrence (FO) (Hyslop, 1980). We also used Pinkas et al.’s
(1971) index of relative importance (IRI), which incorporates
the three measurements in the following formula: IRI ¼
(%W + %P) × %FO. Cortés (1997) subsequently transformed this formula in order to obtain values as percentages
and facilitate comparison:
%IRIi = (IRIi /
IRIi ) × 100
Similarly, we also determined the breadth of the trophic niche
using Levin’s standardized index (Krebs, 1989):
Bi = 1/n − 1{(1/
Pij2 ) − 1}
where n is the number of prey items and Pij is the proportion
of the diet of predator i composed of prey j. This index ranges
from 0 to 1; values ,0.6 indicated specialist predators that
consume only certain types of prey, while values ≥0.6 indicated the diets of opportunistic predators that use resources
indiscriminately (Labropoulou & Eleftheriou, 1997).
We also used the Morisita –Horn index to assess the degree
of trophic overlap (Smith & Zaret, 1982):
Cl = 2
n
(Pxi ∗ Pyi )
i=1
n
i=1
Pxi2 +
n
i=1
Pyi2
where Cl is the Morisita-Horn index between species x and y,
Pxi is the proportion of prey i relative to the total prey consumed by predator x, Pyi is the proportion of prey i relative
to the total prey consumed by y, and n is the total number
of prey. Values for this index range from 0 to 1; those
closest to zero indicate dietary differences, while values
closer to one indicate similarities in the prey consumed
(Langton, 1982).
In addition, we also assessed the trophic overlap using the
‘mh’ function in the ‘divo’ package of R software, applying
bootstraping (nboot ¼ 1000) and setting the confidence level
at 95%; this function generates a matrix of the overlap
between variables and is represented by a dendrogram.
Finally, to evaluate the uncertainty of our classification, we
used the ‘pvclust’ package to calculate the P-value quantiles
using bootstrapping (bootstrap ¼ 1000). The approximately
unbiased (AU) P-value is calculated via multi-scale bootstrapping, while the bootstrap probability (BP) P-value is calculated
using standard bootstrapping. The AU is the best approximation of the P-value; AU values .95% strongly support the
information (R Core Team, 2014).
To determine the average trophic level of the different prey
items identified in the stomachs analysed we used the following formula proposed by Cortés (1999):
ITR = 1 +
n
j=1
Pj × ITRj
where ITRj is the trophic level of each prey taxa j and Pj is the
proportion of each of the categories of prey j in the predator’s
diet based on %N (Cortés, 1999). We obtained the trophic
levels for different prey species from Froese & Pauly (2015)
(www.fishbase.org); when no data were available, we used
the average trophic level for the corresponding group: cartilaginous fishes (3.65), cephalopods (3.2), teleosts (3.24) and
crustaceans (2.52) (Cortés, 1999). All calculations were
carried out using the R software (R Core Team, 2014).
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Prey species
Mollusks
Ancistrocheirus lesueurii
Argonauta sp.
Dosidicus gigas
Gonatus sp.
Ommastrephes bartramii
Octopus sp.
Pholidoteuthis boschmaii
Thysanoteuthis rhombus
Vitreledonella richardi
Squid remains
Octopus remains
Teleost fishes
Anchoa sp.
Auxis thazard
Benthosema panamense
Caulolatilus sp.
Coryphaena hippurus
Cynoscion sp.
Diodon sp.
Euthynnus lineatus
Exocoetus monocirrhus
Belonidae Family
Ophichthidae Family
Ophidiidae Family
Scombridae Family
Tetraodontidae Family
Isacia conceptionis
Katsuwonus pelamis
Larimus argenteus
Lophiodes spilurus
Merluccius gayi
Myrophis vafer
Normanichthys crockeri
Ophichthus sp.
Oxyporhamphus micropterus
Paralichthys sp.
Polydactylus opercularis
Pontinus sierra
Scomberomorus sierra
Carcharhinus falciformis
Carcharhinus limbatus
Trophic∗ level
Nasolamia velox
%N
%W
%FO
%IRI
%N
%W
%FO
%IRI
%N
%W
%FO
%IRI
31.79
4.71
7.06
1.18
–
1.18
–
1.18
1.18
7.06
8.24
–
67.08
2.35
5.88
–
–
1.18
–
2.35
1.19
–
–
–
–
3.53
7.06
–
3.53
–
–
–
–
–
–
–
–
–
–
1.18
5.54
2.86
0.01
1.32
–
0.01
–
0.01
0.02
0.01
1.3
–
90.42
0.34
5.84
–
–
0.94
–
0.49
3.66
–
–
–
–
0.62
2.26
–
2.44
–
–
–
–
–
–
–
–
–
–
0.01
–
5.08
5.08
1.69
–
1.69
–
1.69
0.69
6.78
11.86
–
–
1.69
8.47
–
–
1.69
–
1.69
1.69
–
–
–
–
5.08
5.08
–
3.39
–
–
–
–
–
–
–
–
–
–
1.69
11.86
1.85
1.73
0.2
–
0.1
–
0.1
0.11
2.31
5.46
–
87.83
0.22
4.77
–
–
0.17
–
0.23
0.39
–
–
–
–
1.02
2.28
–
0.97
–
–
–
–
–
–
–
–
–
–
0.1
4.00
–
–
–
–
–
–
–
–
–
4.00
–
84.00
–
8.00
4.00
–
–
–
–
–
20
4.00
4.00
4.00
–
4.00
–
8.00
8.00
–
–
–
–
–
–
–
–
–
–
0.17
–
–
–
–
–
–
–
–
–
0.17
–
89.43
–
14.49
,0.01
–
–
–
–
–
2.68
0.24
16.96
,0.01
–
1.19
–
12.91
,0.01
–
–
–
–
–
–
–
–
–
–
5.56
–
–
–
–
–
–
–
–
–
5.56
–
–
–
11.11
5.56
–
–
–
–
–
11.11
5.56
5.56
5.56
–
5.56
–
11.11
5.56
–
–
–
–
–
–
–
–
–
–
1.22
–
–
–
–
–
–
–
–
–
1.22
–
92.21
–
13.18
1.17
–
–
–
–
–
13.29
1.24
6.14
1.17
–
1.52
–
12.25
2.34
–
–
–
–
–
–
–
–
–
–
14.71
–
–
5.88
2.94
–
2.94
–
–
–
–
2.94
67.65
–
–
2.94
2.94
–
17.65
–
–
–
–
–
5.88
–
–
2.94
–
8.82
2.94
2.94
2.94
2.94
2.94
2.94
2.94
2.94
2.94
–
63.35
–
–
62.82
0.19
–
0.01
–
–
–
–
0.33
27.59
–
–
0.01
0.01
–
0.01
–
–
–
–
–
0.38
–
–
0.01
–
2.22
10.53
0.50
0.01
0.01
0.01
3.60
0.16
7.72
2.42
–
–
–
–
8.33
8.33
–
8.33
–
–
–
–
8.33
–
–
–
8.33
8.33
–
8.33
–
–
–
–
–
8.33
–
–
8.33
–
16.67
8.33
8.33
8.33
8.33
8.33
8.33
8.33
8.33
8.33
–
25.51
–
–
22.46
1.02
–
0.96
–
–
–
–
1.07
34.74
–
–
0.96
0.96
–
5.77
–
–
–
–
–
2.05
–
–
0.96
–
7.22
4.40
1.12
0.96
0.96
0.96
2.14
1.01
3.49
1.75
–
–
3.20
3.20
3.20
3.20
3.20
3.20
3.20
3.20
3.20
–
–
–
2.70
4.33
3.20
3.24
4.50
3.24
4.00
3.24
3.24
3.24
3.24
3.24
3.24
3.24
3.24
4.30
3.24
3.24
4.30
3.24
3.24
3.24
3.24
3.24
3.60
3.24
4.50
Habitat
–
Mesopelagic
–
Mesopelagic
Mesopelagic
Mesopelagic
Benthic
Bathy-Mesopelagic
Epi-Mesopelagic
Pelagic
–
–
–
Coastal
Epipelagic
Mesopelagic
Coastal
Coastal/Oceanic
Coastal
Coastal
Oceanic
Oceanic
Coastal/Oceanic
Benthic
Benthic
Coastal/Oceanic
Coastal
Demersal
Oceanic
Coastal
Benthic
Benthic
Benthic
Demersal
Benthic
Oceanic
Benthic
Benthic
Benthic
Benthic
Continued
diet of sharks in the ecuadorian pacific
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Table 1. Trophic spectrum for C. falciformis, C. limbatus, and N. velox in the Ecuadorian Pacific expressed numerically (%N) and gravimetrically (%W) as well as in terms of the frequency of occurrence (%FO) and the
index of relative importance (%IRI).
929
~ a’ n-montan~ o et al.
colombo estupin
930
–
Benthic
–
The C. falciformis individuals measured from 95 to 310 cm
total length (TL) (mean + SD ¼ 174.1 + 35.7 cm TL). Of
the 69 (43 female, 26 males) stomachs analysed, 83% (59 stomachs) contained food. We were able to identify 19 dietary
components to the lowest taxon: 12 teleosts and eight cephalopods, as well as the remains of fishes, cephalopods and
turtles. Based on the %IRI, teleosts contributed most to the
C. falciformis diet (Table 1). The most important prey were
the Scombridae fishes Thunnus albacares (%IRI ¼ 22.4%),
Thunnus sp. (12.9%) and Auxis thazard (4.77%) (Table 1,
Figure 1). The trophic spectrum of both females and males
consisted of teleosts and cephalopods; females also consumed
turtles (Table 2). The most important prey species for males
were the cephalopods Ancistrocheirus lesueurii (13.2%) and
Vitreledonella richardi (8.8%), while females preferred the
fishes T. albacares (29.7%), Thunnus sp. (12.0%) and A.
thazard (5.88%) (Table 2).
–
–
–
–
–
–
–
–
–
0.97
–
0.97
–
–
–
–
–
–
–
–
–
–
–
8.33
–
–
–
–
–
–
–
–
–
0.03
–
0.03
%IRI
%FO
%W
–
–
–
–
–
–
–
–
–
2.94
–
2.94
27.34
–
–
12.57
5.29
1.34
3.95
–
–
1.27
1.27
–
11.11
–
–
16.67
–
5.56
5.56
–
–
–
5.56
–
∗
22.43
0.65
12.99
41.61
–
–
–
0.43
0.43
–
–
–
10.17
1.69
10.17
27.12
–
–
–
–
1.69
–
–
–
35.47
6.87
18.41
13.07
–
–
–
4.08
4.08
–
–
–
10.59
1.18
8.24
18.82
–
–
–
1.18
1.18
–
–
–
Thunnus albacares
Thunnus obesus
Thunnus sp.
Fish remains
Cartilaginous fishes
Dasyatis longa
Batoid remains
Turtles
Turtle remains
Crustaceans
Portunus sp.
Crustacean remains
From: www.fishbase.org (2015), Cortés (1999), Pauly et al. (1998), Hobson & Welch (1992).
38.66
–
–
2.3
10.06
0.59
9.47
–
–
0.34
0.34
–
%FO
%W
%N
%IRI
%W
%N
%FO
8.00
–
–
12.00
2.00
1.00
1.00
–
–
4.00
4.00
–
%N
Carcharhinus limbatus
%IRI
Nasolamia velox
Carcharhinus limbatus
Prey species
Carcharhinus falciformis
Table 1. Continued
Carcharhinus falciformis
4.30
4.40
4.30
–
–
3.65
3.65
–
2.40
–
2.52
2.52
Trophic∗ level
Epipelagic
Epipelagic
Epipelagic
–
–
Benthic
–
Habitat
RESULTS
The C. limbatus specimens measured from 132 to 224 cm TL
(188.7 + 15.9 cm TL). Of the 44 (four females, 40 males) stomachs analysed, 19 (43.2%) had stomach contents, including
12 identifiable dietary components (10 teleosts, one elasmobranch and one crustacean) and the remains of cephalopods,
fishes and batoids. Based on the %IRI, teleosts were the most
important group followed by elasmobranchs, crustaceans and
cephalopods (Table 1); the fishes T. albacares (27.34%),
Exocoetus monocirrhuns (13.29%), A. thazard (13.18%),
Katsuwonus pelamis (12.25%) and members of the
Ophichthidae family (6.14%) were the most important to C.
limbatus diet (Table 1, Figure 1). The small sample size for
females (N ¼ 4) impeded the trophic analysis based on sex.
Considering each sex separately, 12 prey species were consumed by males (10 teleosts, one batoid and one crustacean),
of which the most important prey were: T. albacares (%IRI ¼
18.7%), A. thazard (8.7%), Larimus argenteus (8.1%) and K.
pelamis (8%) (Table 2). Of the four females analysed, only
two had stomach contents, which included the remains of teleosts (25.1%) and batoids (75%) (Table 2).
Nasolamia velox
A total of 24 (17 females, seven males) specimens measured
between 67 and 192 cm TL (151 + 31.1 cm TL) were analysed, of which 12 (50%) had stomach contents; we identified
17 dietary components as well as the remains of unidentified
organisms. Based on the %IRI, the N. velox diet was composed
of teleosts, cephalopods and crustaceans (Table 1); the most
important prey were the cephalopod Dosidicus gigas
(22.46%), L. argenteus (7.22%), Cynoscion sp. (5.77%) and
Lophiodes spilurus (4.4%) (Table 1, Figure 1). The male diet
was dominated by teleosts and cephalopods, with the most
important prey being the fishes L. spilurus (27.18%),
Polydactylus opercularis (21.13%) and L. argenteus (13.29%)
(Table 2). In contrast, the female diet also included crustaceans, of which D. gigas (%IRI ¼ 26.87%), members of the
Ophidiidae family (2.7%) and Oxyporhamphus micropterus
(2.67%) were the most important (Table 2).
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diet of sharks in the ecuadorian pacific
Fig. 1. Trophic spectrums for C. falciformis, C. limbatus and N. velox in Ecuadorian waters showing the most important prey based on the index of relative
importance (%IRI).
Trophic niche, trophic overlap and trophic
level
The trophic niches calculated for Carcharhinus falciformis
(Bi ¼ 0.57), C. limbatus (Bi ¼ 0.40) and Nasolamia velox
(Bi ¼ 0.34) indicate that all three are specialist predators.
The trophic niche for male and female of C. falciformis
was 0.65 and 0.43, respectively. For C. limbatus and N.
velox, this analysis was not performed due to low number
of samples of each sex. We use the trophic overlap
Morisita– Horn index (Cl ,0.5), indicating low food competition between these three predators (Table 3, Figure 2).
The trophic levels calculated for C. falciformis (4.57), C. limbatus (4.28) and N. velox (4.25) suggest they are tertiary
carnivores.
DISCUSSION
Carcharhinus falciformis
The trophic spectrum of the Carcharhinus falciformis in the
present study is consistent with observations made elsewhere
in the world. In Colombia, the main prey include members of
the Scombridae and Coryphaenidae families, the coastal cephalopod Lolligo sp., and a small percentage of crustaceans (Euphylax
robustus) and turtles (Chelonia mydas) (Acevedo, 1996).
Barranco (2008) studied the C. falciformis diet at two locations in Mexico, noting that their main prey included the
crustacean Portunus xantusii affinis, the pelagic cephalopod
Argonauta sp. and the epipelagic fish Euthynnus lineatus.
Cabrera-Chávez-Costa et al. (2010) recorded that silky shark
Table 2. Trophic spectrum by sex in C. falciformis, C. limbatus and N. velox in Ecuadorian waters, expressed in Index of Relative Importance (%IRI).
Prey species
Ancistrocheirus lesueurii
Auxis thazard
Cynoscion sp.
Dosidicus gigas
Tetraodontidae Family
Gonatus sp.
Katsuwonus pelamis
Larimus argenteus
Lophiodes spilurus
Polydactylus oppercularis
Thunnus sp.
Thunnus albacares
Vitreledonella richardi
Batoid remains
Turtle remains
Cephalopod remains
Fish remains
C. falciformis
C. limbatus
N. velox
Males
Females
Males
Females
Males
Females
13.23
1.93
–
–
4.68
–
0.77
5.88
–
–
1.03
–
–
–
–
–
12.03
29.72
–
–
0.38
–
43.90
–
8.70
–
–
–
–
8.03
8.05
–
–
–
18.70
–
–
–
–
39.30
–
–
–
–
–
–
–
–
–
–
–
–
–
74.99
–
–
25.05
–
–
–
–
–
4.91
–
13.29
27.18
21.13
–
–
–
–
–
–
19.94
–
–
7.65
26.87
–
–
–
1.36
–
–
–
–
–
–
–
–
48.48
–
–
–
11.41
1.61
8.80
–
–
33.40
17.30
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Table 3. Trophic overlap between C. falciformis, C. limbatus and N. velox
in the Ecuadorian Pacific based on the Morisita-Horn index (Cl).
C. falciformis
C. limbatus
N. velox
C. falciformis
C. limbatus
N. velox
1
–
–
0.31
1
–
0.01
0.16
1
predate mainly on crustacean Pleuroncondes planipes (Baja
California Sur, Mexico), the cephalopod D. gigas and the
pelagic-coastal fish Scomber japonicus. Duffy et al. (2015)
examined the stomach contents of C. falciformis in the
Eastern Pacific Ocean (EPO), finding that: (1) this species’
diet varies based on the abundance of different prey, (2) the
species displays few ontogenetic changes, (3) they are piscivorous consumers, with over 50% of their prey belonging to
Scombridae family (K. pelamis, T. albacares, Thunnus sp.
and Auxis sp.) and (4) they consume a variety of prey items,
suggesting that they are opportunistic predators.
Although our study was based on a small number (69) of
stomachs, our observations are similar to those reported by
Duffy et al. (2015). In our study, the most important prey
species were fish from the Scombridae family (Thunnus sp.),
making them piscivorous. It is clear that both off the coast
of Ecuador as well as throughout the EPO, this species
prefers fish; however, the trophic spectrum of this species in
other parts of the world indicated a more varied diet, including prey from benthic (some crustaceans) and oceanic-coastal
(fish and turtles) habitats. This pattern is likely related to differences in size, sex and sexual maturity; however, Duffy et al.
(2015) found no differences in diet based on size in the EPO
and too little is known about the biology of this species in
the Ecuadorian Pacific to confirm this suggestion.
We found changes in the diet of C. falciformis comparing
different studies, these changes would be because juveniles
of this species are more frequent in areas near the coast,
where they consume abundant and easy (e.g. epipelagic crustaceans) prey to save energy during capture; while adults are in
oceanic waters feeding on big prey such as tuna, which supply
more energy. The C. falciformis in this study prefer to
consume prey of oceanic waters (e.g. tuna) because the
shark fleet in Ecuador performs their catch in oceanic areas.
The studies used to compare the diet in this shark species
include catches by small boats close to coastal areas or big
boats (e.g. tuna purse seiner), which are used in oceanic
waters. This would explain the different prey items consumed
by this shark in different areas in the Eastern Pacific Ocean.
Carcharhinus limbatus
We found that the shark species’ diet in Ecuadorian waters
includes prey from the same groups or with similar characteristics to those observed previously by Castro (1996), Tavares &
Provenzano (2000), Barry (2002) and Tavares (2008), who
report that teleosts are the most important prey for this piscivorous predator. Moreover, Castro (1996) also reports that
both sharks and rays are included in their diet. This supports
our findings, which included one longtail stingray D. longa
and the remains of batoids.
Castro (1996) and Barry (2002) have noted that small
numbers of crustaceans are included in the C. limbatus diet;
we also identified one crustacean, Portunus sp., although
based on a small sample. Gaitán-Espitia & López-Peña
(2008) identified the remains of fish vertebrae and cephalopod
beaks in the stomachs of juvenile C. limbatus.
In the south-eastern USA, Castro (1996) reported that the
Atlantic menhaden Brevoortia tyrannus was the most abundant prey; other prey species included the elasmobranchs
Rhinoptera banasus, Rhizoprionodon terraenovae and
Sphyrna tiburo, as well as some shrimp and small teleosts.
In contrast, Barry (2002) mentioned that off the coast of
Louisiana, USA, the most important prey were Brevoortia
patronus and Micropogonias undulatus. Meanwhile in Los
Roques Archipelago, Venezuela, Tavares & Provenzano
(2000) only reported the presence of teleost fishes, of which
the following were the most important: Opisthonema
oglinum, Gerres cinereus, Albula vulpes and Haemulon sciurus.
Similarly, Tavares (2008) noted that the main prey consumed by C. limbatus in the Los Roques Archipelago,
Venezuela, included Eucinostomus argenteus, O. oglinum
and G. cinereus; suggesting a shift over time in this predator’s
alimentary preferences in the area. In our study, the main prey
consumed by C. limbatus in Ecuadorian waters included the
fishes T. albacares, E. monocirrhus, A. thazard, K. pelamis
and members of the Ophichthidae family. This is not consistent with the results of other studies, and may be related to prey
diversity and availability in the different geographic areas
examined as well as the influence of the age-class of the specimens examined. Finally, both the present study and previous
research on the C. limbatus diet indicate that, regardless of
geographic area, their diet is based on high consumption of
fish from both coastal and oceanic areas including prey
from pelagic, and sometimes even benthic habitats.
Nasolamia velox
In Ecuadorian waters, N. velox feed on various groups of
organisms, including fish, shellfish, and crustaceans, with a
preference for fish, suggesting they are piscivorous, similar
to Compagno (1984). They feed on coastal habitats and
consume prey from the seabed (benthic and demersal
species) with 47% of the 19 prey species identified coming
from benthic environments, 16% from both coastal and mesopelagic environments, 11% from demersal coastal habitats,
and 5% from oceanic and oceanic-coastal areas (Table 1).
Nasolamia velox is common in shallow coastal areas (15 –
24 m, sometimes to 192 m) (Compagno, 1984). This habitat
and the presence of fishes from the Sciaenidae (e.g.
Cynoscion sp., L. argenteus), Lophiidae (L. spilurus) and
Polynemidae (P. opercularis) families, which inhabit coastal
zones in sandy and muddy habitats (Robertson & Allen,
2002), suggest that whitenose shark feed in this habitats.
Trophic niche, trophic overlap and trophic
level
Based our results, we consider C. falciformis to be a specialist
predator; this is consistent with Barranco (2008),
Cabrera-Chávez-Costa et al. (2010) and Duffy et al. (2015),
who consider C. falciformis a specialist predator, because
although consuming many prey species, some prey are more
important in their diet. Duffy et al. (2015) report that this
shark species has a preference for fishes of the Scombridae
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diet of sharks in the ecuadorian pacific
Fig. 2. Trophic overlap between C. falciformis, C. limbatus and N. velox in the Ecuadorian Pacific based on the Morisita – Horn index. AU ¼ p-valor multi-scale
(1000 replicates).
family (T. albacares and Thunnus sp.). Although our study area
was small and we analysed few (69) stomachs, our results are
similar to those obtained by Duffy et al. (2015) who examined
786 stomachs. Silky shark feeding patterns indicate that this
species has a broad trophic niche, suggesting that they make
use of a variety of available resources. In contrast, C. limbatus
(Bi ¼ 0.40) and N. velox (Bi ¼ 0.33) have a reduced trophic
niche. It is worth noting that these are approximations of the
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933
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colombo estupin
niche breadth for the latter two species because we lack information on their diets; the present study is the first to examine
the diets of C. limbatus and N. velox in Ecuador.
While C. falciformis, C. limbatus and N. velox are all
present in the Ecuadorian Pacific, our results suggest low
interaction between them (Table 3) due to the distribution
of resources in the area and differences in the habitat preferences of these shark species; C. falciformis prefers oceanic
habitats, C. limbatus frequents oceanic-coastal habitats and
also feeds on prey from the water column and seabed, and
N. velox is a coastal species that consumes benthic prey.
Thus, these species avoid potential competition for food
even though our calculations place C. falciformis (4.57), C.
limbatus (4.28) and N. velox (4.25) in the same trophic level
(i.e. tertiary consumers).
Very few studies have examined the trophic positions of
these sharks. Of the few studies that have been undertaken,
Cortés (1999) estimated trophic positions for both C. falciformis (4.2) and C. limbatus (4.2), which are similar to those
reported here. Other studies relying on different techniques
have produced results similar to ours. For example, in two
studies involving the stable isotopes analysis of d15N,
Galindo (2014) assigned C. falciformis in a trophic position
between 3.3 and 3.8, while Yunkai et al. (2014) placed this
species between 3.4 and 5.3. Other authors have identified
C. falciformis as secondary (Mearns et al., 1981) or tertiary
consumers (Cortés, 1999) based on a variety of techniques.
Trophic level estimates for N. velox make no mention of
trophic position, illustrating the lack of information regarding
the species.
The information presented here serves as a strong base for
increasing our understanding of the trophic ecology of the different species of sharks found in Ecuadorian waters. Future
studies should focus on examining the diets of these shark
species using complementary techniques (e.g. stable isotope
analysis, etc.). In order to improve our understanding of
their role in the ecosystem, other studies of cartilaginous
fishes are needed, including assessing alimentary ontogeny,
sexual segregation of feeding areas, inter- and intra-specific
competition, and estimating their trophic levels.
(Chondricthyes: Lamniformes) en la Ensenada de Panamá. Thesis.
Facultad de Ciencias, Universidad del Valle, Cali.
Anderson E.D. (1990) Fishery models as applied to elasmobranch fisheries. In Pratt H.L., Gruber S.H. and Taniuchi T. (eds) Elasmobranchs as
living resources: Advances in the biology, ecology, systematics, and the
status of fisheries. US Department of Commerce, NOAA Technical
Report NMFS 90, pp. 473 –484.
Barranco S.L.M. (2008) Hábitos alimenticios y nivel trófico del tiburón
Carcharhinus falciformis, Müller & Henle 2841 (Elasmobranchii:
Carcharhinidae) en el Golfo de Tehuantepec, México por medio del
análisis del contenido estomacal e isótopos estables de d13C y d15N.
Master science thesis. Universidad del Mar, Puerto Ángel, Oaxaca,
México.
Barry K.P. (2002) Feeding habits of blacktip shark, Carcharhinus limbatus, and sharpnose shark, Rhizoprionodon terraenovae, in Louisiana
coastal waters. Thesis. B.S., University of South Alabama, Mobile, AL.
Bornatowski H., Braga R.R., Abilhoa V. and Corrêa M.F.M. (2014a)
Feeding ecology and trophic comparisons of six shark species in a
coastal ecosystem off southern Brazil. Journal of Fish Biology 85,
246–263. doi: 10.1111/jfb.12417.
Bornatowski H., Navia A.F., Braga R.R., Abilhoa V. and Corrêa M.F.M.
(2014b) Ecological importance of sharks and rays in a structural food
web analysis in southern Brazil. ICES Journal of Marine Science 71,
1586–1592. doi: 10.1093/icesjms/fsu025.
Cabrera-Chávez-Costa A.A., Galván-Magaña F. and Escobar-Sánchez O.
(2010) Food habits of the silky shark Carcharhinus falciformis (Müller &
Henle, 1839) off the western coast of Baja California Sur, México.
Journal of Applied Ichthyology 26, 499–503.
Castro J.I. (1996) The biology of the blacktip shark, Carcharhinus limbatus, off the southeastern United States. Bulletin of Marine Science 59,
508–522.
Cervigón F., Cipriani R., Fischer W., Garibaldi L., Hendrickx M.,
Lemus A.J., Márquez R., Poutiers J.M., Robaina G. and
Rodriquez B. (1992) Fichas FAO de identificación de especies para
los fines de la pesca: Guı́a de campo de las especies comerciales
marinas y de aguas salobres de la costa septentrional de Sur América.
Rome: FAO, p. 513.
Chirichigno N. (1998) Clave para identificar los peces marinos del Perú.
Callao: Publicación Especial del Instituto del Mar del Perú, p. 496.
Clarke M.R.A. (1986) A handbook for the identification of cephalopod
beaks. Oxford: Clarendon Press, p. 271.
ACKNOWLEDGEMENTS
We thank D. Castañeda, A. Sandoval, A. Baigorrı́, J. Méndez,
J. Figueroa, and the fish butchers of Tarqui Beach in Manta,
Ecuador.
FINANCIAL SUPPORT
FMG thanks the Instituto Politécnico Nacional (IPN; National
Polytechnic Institute) for fellowships provided through the
Estı́mulo al Desempeño de los Investigadores (EDI;
Performance Incentives) and the Comisión de Operación y
Fomento de Actividades Académicas (COFAA; Commission
for the Advancement of Academic Activities).
REFERENCES
Acevedo G. (1996) Contribución al estudio de la biologı́a y la dinámica
poblacional de los tiburones de la familia Carcharhinidae
Clothier C.R. (1950) A key to some southern California fishes based on
vertebral characters. Fishery Bulletin 79, 1–83.
Compagno L.J.V. (1984) Sharks of the world. An annotated and illustrated
catalogue of sharks species known to date. Parts 1–2. Hexanchiformes to
Carcharhiniformes. FAO Fishery Synopsis 125. Rome: FAO, pp. 1–655.
Cortés E. (1997) A critical review of methods of studying fish feeding
based on analysis of stomach contents: application to elasmobranch
fishes. Canadian Journal of Fisheries and Aquatic Sciences 54, 726–
738. doi: 10.1139/f96-316.
Cortés E. (1999) Standardized diet compositions and trophic levels of
sharks. ICES Journal of Marine Science 56, 707–717.
Duffy L.M., Olson R.J., Lennert-Cody C.E., Galván-Magaña F.,
Bocanegra-Castillo N. and Kuhnert P.M. (2015) Foraging ecology
of silky shark Carcharhinus falciformis, captured by the tuna purseseine fishery in the eastern Pacific Ocean. Marine Biology 162, 571–
593. doi: 10.1007//s00227-014.
Estupiñán-Montaño C., Cedeño-Figueroa L.G. and Galván-Magaña F.
(2009) Hábitos alimenticios de la cornuda común Sphyrna lewini en
el Pacı́fico ecuatoriano. Revista de Biologı́a Marina y Oceanografı́a
44, 379–386.
Downloaded from https://www.cambridge.org/core. IP address: 207.241.231.108, on 10 Mar 2020 at 20:34:36, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S002531541600179X
diet of sharks in the ecuadorian pacific
Ellis J.R., Pawson M.G. and Shackley S.E. (1996) The comparative
feeding ecology of six species of shark and four species of ray
(Elasmobranchii) in the north-east Atlantic. Journal of the Marine
Biological Association of the United Kingdom 76, 89–106.
Fischer W., Krupp F., Schneider W., Sommer C., Carpenter K.E. and
Niem V.H. (1995) Guı́a FAO para la identificación de especies para
los fines de la pesca. Pacı́fico Centro-Oriental. Rome: FAO, p. 1813.
Froese R. and Pauly D. (eds) (2015) Fishbase. World Wide Web electronic publication. Available at http://www.fishbase.org, Version (08/
2015).
Gaitán-Espitia J. and López-Peña A. (2008) Presencia de juveniles del
tiburón aletinegro Carcharhinus limbatus (Carcharhiniformes:
Carcharhinus) en la zona norte de la ecoregión Tayrona, Caribe
colombiano. Latin American Journal of Aquatic Research 36, 115–119.
Galindo R.M.A. (2014) Composición isotópica (d15N y d13C) durante el
desarrollo ontogénico del tiburón piloto Carcharhinus falciformis
(Müller & Henle 1839) en la zona oceánica del Pacı́fico Oriental
Tropical. Master science thesis. Centro Interdisciplinario de Ciencias
Marinas – CICIMAR, La Paz, BCS, México.
Galván-Magaña F., Nienhuis H. and Klimley P. (1989) Seasonal abundance and feeding habits of sharks of the lower Gulf of California
Mexico. California Fish and Game 75, 74–84.
Garcı́a-Godos I. (2001) Patrones morfológicos del otolito Sagitta de
algunos peces óseos del mar peruano. Boletı́n del Instituto del Mar
del Perú 20, 4–83.
Hobson K.A. and Welch H.E. (1992) Determination of trophic relationships within a high Arctic marine food web using d13C and d15N
analysis. Marine Ecology Progress Series 84, 9–8. doi: 10.3354/
meps084009.
Hyslop E.J. (1980) Stomach contents analysis: a review of methods and
their application. Journal of Fish Biology 17, 411–429. doi: 10.1111/
j.1095–8649.1980.tb02775.x.
Krebs C. (1989) Ecological methodology. New York, NY: Harper and Row,
550 pp.
Labropoulou M. and Eleftheriou A. (1997) The foraging ecology of two
pairs of congeneric demersal fish species: importance of morphological
characteristics in prey selection. Journal of Fish Biology 50, 324–340.
Langton R.W. (1982) Diet overlap between the Atlantic cod Gadus
morhua, silver hake Merluccius bilinearis and fifteen other northwest
Atlantic finfish. Fishery Bulletin 80, 745–759.
Loor-Andrade P., Galván-Magaña F., Elorriaga-Verplancken F.R.,
Polo-Silva C. and Delgado-Huertas A. (2015) Population and individual foraging patterns of two hammerhead sharks using carbon
and nitrogen stable isotopes. Rapid Communications in Mass
Spectrometry 29, 1 –19. doi: 10.1002/rcm.7169.
Mearns A.J., Young D.R., Olson R.J. and Schafer H.A. (1981) Trophic
structure and the cesium-potassium ratio in pelagic ecosystems.
California Cooperative Oceanic Fisheries Investigations Reports 22,
99–110.
Ministerio de Comercio Exterior, Industrialización, Pesca y
Competitividad (MICIP) (2006) Plan de acción nacional para la conservación y manejo de Tiburones de Ecuador – PAT-Ec. Quito, pp 44.
Navia A.F., Cortés E. and Mejı́a-Falla P.A. (2010) Topological analysis of
the ecological importance of elasmobranch fishes: a food web study on
the Gulf of Tortugas, Colombia. Ecological Modelling 221, 2918–2926.
Pauly D., Trites A., Capuli E. and Christensen V. (1998) Diet composition and trophic levels of marine mammals. ICES Journal of Marine
Science 55, 467 –481.
Pinkas L., Oliphant M.S. and Iverson I.L.K. (1971) Food habits of albacore, bluefin tuna and bonito in California waters of the Pacific Ocean.
California Department of Fish and Game, Fish Bulletin 152, 1–105.
Polo-Silva C., Rendón L. and Galván-Magaña F. (2009) Descripción de
la dieta de tiburones zorro (Alopias pelagicus) y (Alopias superciliosus)
durante la época lluviosa en aguas ecuatorianas. Pan-American Journal
of Aquatic Sciences 4, 556–571.
Polo-Silva C., Newsome S.D., Galván-Magaña F., Grijalba-Bendeck M.
and Sanjuan-Muñoz A. (2013) Trophic shift in the diet of the pelagic
thresher shark based on stomach contents and stable isotope analyses.
Marine Biology Research 9, 958–971. doi: http://dx.doi.org/10.1080/
17451000.2013.793802.
R Core Team (2014) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Available at
http://www.R-project.org/. (accessed October 2015).
Robertson D.R. and Allen G.R. (2002) Peces costeros del Pacı́fico Oriental
Tropical: Un sistema de información. [CD-ROM]. Balboa, Panamá:
Instituto Smithsonian de Investigaciones Tropicales.
Romero-Caicedo A.F., Galván-Magaña F. and Martı́nez-Ortiz J. (2014)
Reproduction of the pelagic thresher shark Alopias pelagicus in the
equatorial Pacific. Journal of the Marine Biological Association of the
United Kingdom 94, 1501–1507. doi: 10.1017/s0025315414000927.
Rubio R.E.A. (1988) Peces de importancia comercial para el Pacı́fico
Colombiano. Cali, Colombia: Universidad del Valle – Departamento
de Biologı́a.
Smith P. and Zaret M. (1982) Bias in estimating niche overlap. Ecology
63, 1248–1253.
Stevens J., Bonfil R., Dulvy N.K. and Walker P.A. (2000) The effects of
fishing on sharks, rays, and chimaeras (Chondrichthyans), and the
implications for marine ecosystems. ICES Journal of Marine Science
57, 476–494. doi: 10.1006/jmsc.2000.0724.
Tavares R. (2008) Occurrence, diet and growth of juvenile blacktip sharks,
Carcharhinus limbatus, from Los Roques Archipelago national park,
Venezuela. Caribbean Journal of Science 44, 291–302.
Tavares R. and Provenzano F. (2000) Alimentación de los juveniles de
tiburón macuira, Carcharhinus limbatus (Valenciennes, 1839) en el
Parque Nacional Archipiélago Los Roques, Venezuela. Acta Biologica
Venezuelica 20, 59–67.
Wolff C.A. (1982) A beak key for eight eastern tropical pacific cephalopods species, with relationship between their beak dimensions and
size. Fishery Bulletin 80, 357–370.
Wolff C.A. (1984) Identification and estimation of size from the beaks of
eighteen species of cephalopods from the Pacific Ocean. NOAA
Technical Reports, NMFS 17, 1 –50.
and
Yunkai L.I., Gong Y., Chenn X., Dai X. and Zhu J. (2014) Trophic
ecology of shark in the mid-East Pacific Ocean inferred from stable
isotopes. Journal of Ocean University of China (Oceanic and Costal
Sea Research) 13, 278 –282. doi: 10.1007/s11802-014-2071-1.
Correspondence should be addressed to:
F. Galván-Magaña
Instituto Politécnico Nacional, Centro Interdisciplinario de
Ciencias Marinas, Av. IPN s/n. La Paz, Baja California Sur,
C.P. 23096, México
email: galvan.felipe@gmail.com
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