Trophic Level and Isotopic Composition of δ13C and δ15N of Pacific Angel Shark, Squatina californica (Ayres, 1859), in the Southern Gulf of California, Mexico
O. Escobar- Sanchez,
F. Galvan- Magana
L.A. Abitia- Cardenas
δ13C and δ15N stable isotopes were used to determine trophic level and the assimilated food components of Pacific angel shark, Squatina californica and its variation between size, sexes and seasonally in the southern Gulf of California, Mexico. Muscle tissues were collected during 2001 to 2003. The quantification of δ13C and δ15N stable isotopes was realized by isotope ratio mass spectrometry. The values of stable isotope of carbon (δ13C) ranged from -16.55 to -15.06 (average -15.94 ±0.34) and nitrogen (δ15N) was between 18.30 to 19.52 (average 18.90 ±0.27), we found that as male as female feeds on same zones and not differences were found among years and seasons, therefore the angel shark present a same trophic level to feed on benthic prey in the coast zone. The trophic level was determined for S. californica with 4.5, therefore is considered a tertiary consumer in the southern Gulf of California. We concluded that Pacific angel shark present a same trophic pattern during migration to deep areas en the Gulf of California, feeding on benthic species with same trophic level.
to cite this article:
O. Escobar- Sanchez, F. Galvan- Magana and L.A. Abitia- Cardenas, 2011. Trophic Level and Isotopic Composition of δ13C and δ15N of Pacific Angel Shark, Squatina californica (Ayres, 1859), in the Southern Gulf of California, Mexico. Journal of Fisheries and Aquatic Science, 6: 141-150.
May 25, 2010; Accepted: July 19, 2010;
Published: August 13, 2010
The Pacific angel shark, Squatina californica Ayres, 1859 is a demersal
species that inhabit muddy and sandy bottoms of temperate and tropical waters.
This shark is found in depth not more that 200 m, with preference between 3-45
m (Natanson and Cailliet, 1986). Their distribution
is from southern Alaska to the Gulf of California and perhaps from Peru to southern
Chile (Kato and Hernández-Carvallo, 1967; Compagno
et al., 1995). In the Gulf of California, the maximum size recorded
is 95.5 cm (Escobar-Sanchez et al., 2006) and
show a seasonal presence within the Gulf of California, indicating a migration
during summer associated to reproduction (Galvan-Magana
et al., 1989).
In contrast to others sharks, S. californica is an ambush predator species associated with the marine bottom, where they remained to bury to capture its preys when swimming near to them. This specie is caught commercially and few biological information has been published to do a fisheries management in Mexico, because their populations have been decreased in the Gulf of California.
The trophic studies of S. californica have been done in the Pacific
Ocean using observations in situ to examine the feeding behavior (Fouts
and Nelson, 1999) and stomach content analysis (Pittenger,
1984; Galvan-Magana et al., 1989; Escobar-Sanchez
et al., 2006). The use of stomach contents in sharks (Estrada
et al., 2003) have been important to know the role of sharks associated
to ecosystems; however, this method provide specific information on the recent
feeding habits of sharks, while the stable isotope analysis give more information
about the assimilated food and their origin (benthic or pelagic, oceanic and
coastal prey) (Hesslein et al., 1993; Harvey
and Kitchel, 2000). The most important isotopes used in this kind of analysis
are carbon and nitrogen (Schell et al., 1998),
which permit to know the energy flow and feeding relationships within aquatic
food webs (Minagawa and Wada, 1984; Cabana
and Rasmussen, 1994; Zanden et al., 1997,
2000). The carbon isotopes are used to identify consumption
from coastal or pelagic sources. While nitrogen isotopes are fractionated, leaving
3.4 δ15N to be integrated into the consumers tissue.
This enrichment causes a stepwise increase in 15N as the consumers
trophic level increases (Deniro and Epstein, 1981; Minagawa
and Wada, 1984).
The accumulated information in muscle is approximately 3 months of isotopic signatures, which allows knowing the origin of assimilated prey by the predator. This technique is useful when there are a high percentage of empty stomachs with little information on consumed prey. Therefore, the goal of the present analysis was recognize the trophic level and the origins of food components by means of δ13C and δ15N isotopic analysis by sex, size, season and locality in the southern Gulf of California.
MATERIALS AND METHODS
The samples were collected from February 2001 to March 2003 in the following
fishing camps: El Pardito (PAR) (24°51 42=N; 110°35
22= W), El Portugués (PORT) (24°47 38= N; 110°39
39= W) and Ensenada de muertos (EMTOS) (23°58 38 N; 109°49
57 W), located in the southern Gulf of California, Mexico (Fig.
1). The sharks were caught using a multifilament gill net of mesh size between
10 and 30 cm.
|| Study area. Indicating the fishing camps in the southern
Gulf of California
The nets were set during the sunset and reviewed the following morning. In
the field, Total Length (TL) and sex were recorded. The state of maturity of
angel shark was determined following to Marqueda-Cava et
al. (2003), it which considered to juveniles with a total length less
than 80 cm, while the sharks with a TL more than 80 cm were considered like
For isotopic analysis, the muscles from the anterior-dorsal region of 38 angel sharks were collected and preserved frozen. The muscles were lyophilized (LABCONCO) to -45°C and a pressure of 24-27x10-3 MBAR during 24 h to extract humidity. The lipid extraction were realized in a microwave (Microwave Assisted Extraction-MAE model 1000 (CEM, Matthews, NL) with temperature and pressure controlled during 20 min. Each dried samples was ground and weighed (±0.001 g) in an analytical balance and put into tin capsules (8x5 mm). The isotope ratios of carbon and nitrogen were measured with a mass spectrometer (EMRI) (20-20 mass spectrometer, PDZ Europe, Scientific Sandbach, United Kingdom, UK) at the University of California in Davis (USA).
The δ values of stable isotopes were calculated according to the following
where, Rsample for δ15N is the proportion between
its isotopes 15N/14N, while by δ13C is
the proportion of the isotopes of 13C/12C. The standards
used for carbon (δ13C) and nitrogen (δ15N) were
Pee Dee Belemnite limestone (PDB) and atmospheric nitrogen (AIR), respectively.
The relative Trophic Level (TL) was determined using the following equation
established by Post (2002):
where, λ is the trophic position of the specie used to estimate δ15N
Base, Δn is the enrichment in δ15N
per trophic level (the mean aquatic enrichment of 3.4 was assumed for
all trophic estimations according to Minagawa and Wada (1984)
and δ15NPredator is the direct signature of δ15N
for the predator to evaluate. According to Post (2002),
to determine the δ15NBase it is necessary to use
prey species that should share the same habitat as the predator to evaluate
the isotopic signature of the food web. We used the fish Diplectrum pacificum
as the 15N Base, which is located in the Gulf of California
and it was categorized as secondary consumer with a trophic level of 3.99.
The normality of isotope data was tested using the Kolmogorov-Smirnov (KS) (p>0.05). The data were normally distributed (d = 0.091 p>0.05 for δ15N; d = 0.049 p>0.05 for δ13C); therefore we used an Analysis of Variance (ANOVA) to determine the possible differences by categories (sex, location). Also we used a linear regression analysis to examine the possible relationship and trend between total length and the δ15N signatures.
Stable isotopes signatures: The stable isotope analysis was applied
to 38 angel sharks muscle that representing different sex, season, size, location
and capture year. The stable isotopes of angel shark muscles showed δ13C
values of -16.55 to -15.06 (av. -15.94 ±0.34 sd); whereas
the δ15N values were 18.30 to 19.52 (av. 18.90 ±0.27)
||Mean and standard deviation δ13C and δ15N
stable isotope values of Squatina californica in the Southern Gulf
||δ13C and δ15N isotopic values
of Squatina californica by location (PAR = El Pardito, PORT = El
Portugués, EMTOS = Ensenada de muertos)
|| Isotopic composition (δ13C and δ15N
presented in ) of Pacific angel shark, Squatina californica
in the southern Gulf of California
|PAR: El Pardito, PORT: El Portugués, EMTOS: Ensenada
We did not found significant differences by location (ANOVA, p>0.05) (Fig.
3; Table 1), therefore, the isotopic data by different
categories were analyzed in general data. The δ15N values were
similar in both locations (PAR and POR), where the means were of 18.91
±0.31 and 18.91 ±0.23 respectively, while, in EMTOS the
isotopic ratio was of 18.88 ±0.28; while the δ13C
by areas were 16.22 ±0.30 (EMTOS), 15.69 ±0.28
(POR) and 16.00 ±0.26 (PAR).
|| δ13C and δ15N isotopic values
of Squatina californica by sex and size (juveniles and adults)
||δ13C and δ15N isotopic values
of Squatina californica by season during the period 2001-2003 in
the southern Gulf of California, Mexico
Stable isotope signatures by categories: Not significant differences
in δ13C and δ15N were found between male (δ15N=
18.91 ±0.29; δ13C= -16.06 ±0.32) and
female (δ15N= 18.89 ±0.26; δ13C
= -15.87 ±0.34) of angel sharks (ANOVA, p>0.05) (Fig.
4), but some males presented negative values of carbon and some females
with positive values.
The stable carbon isotope ratios by size (juveniles and adults), were similar with means of 15.91 ±0.39 and 15.96 ±0.30, respectively (Fig. 4). Likewise, the nitrogen isotope ratios, the juveniles presented a mean of 18.93 ±0.31 and adults of 18.87 ±0.23.
The ratio of stable isotopes in warm season was 16.09 ±0.37 (δ13C) and 19.86±0.28 (δ15N); while in cold season the values had an overall mean of 15.86 ±0.30 (δ13C) and 18.92±0.27 (δ15N) (Fig. 5). When we compared the annual isotopic analysis, there were no significant differences among years (2001, 2002 and 2003) (Fig. 6).
In the Table 2 and Figure 7, we showed the isotopic values of δ13C and δ15N of different marine species located in the Gulf of California. Including others predators like sharks, marine mammals, rays and some prey of S. californica. We compared the isotopic values of this species with respect to isotopic values of Pacific angel shark. No significant relationship between δ15N and total length of this shark was observed (R2 = 0.014, N = 38, p = 0.47).
||Isotopic values of δ13C and δ15N
of different marine species (*shark, **ray, +marine mammal),
located in the Gulf of California (GC) and some important preys reported
in stomach contents of S. californica. In marine mammal, the tissue
analyzed was skin, while in the others species was muscle tissue
|a: Taken of fishbase, b: Main prey of
S. californica reported by Escobar-Sanchez et
||δ13C and δ15N isotopic values
by year in Squatina californica in the Southern Gulf of California,
||Mean comparison of δ13C and δ15N
isotopic values of different species caught in the Gulf of California
Trophic level: The trophic level of S. californica was 4.5±0.1
(range of 4.3-4.7), whereas by categories (juveniles-adults, males and females)
the trophic level was the same (4.5 TL).
Considering that organisms associated to benthic food chain have an enrichment
with 13C (Jennings et al., 1997),
the observed isotopic values of carbon for angel shark (-15.94 ±0.34)
are within the range of carnivorous fishes that feed on benthic prey (18.0
to 15.9) reported by Jennings et al.
(1997) for Mediterranean fishes. The accumulate information of 13C
of predator, indicated a similarity with the food content of angel shark, therefore,
the angel sharks diet is considered benthic-coastal.
Aguilar-Castro (2003) analyzed the hammerhead shark,
Sphyrna lewini samples from the southern Gulf of California, recording
a δ15N isotopic ratio of 20.92 ±0.72, where juveniles
had higher values of nitrogen than adults and therefore juveniles had a higher
trophic level because they feed on carnivorous prey from coastal areas. Also
Ochoa-Díaz (2009), found in smooth hammerhead shark Sphyrna zygaena
from the Gulf of California that nitrogen isotope values indicated that this
shark feeds mostly in deep waters, which is confirmed with the stomach contents
analysis, where the main prey were oceanic cephalopods. In silky shark (Carcharhinus
falciformis), Cabrera (2003), found that silky shark
in the western coast of Baja California Sur, had a nitrogen ratio of 16.19
±0.65, with a trophic position smaller than S. lewini. This author
mentioned that silky shark feed in oceanic zone, with a short food chain, because
their main prey (Pleuroncodes planipes) feeds on zooplankton or zooplanktophague
The nitrogen values of angel shark (18.9 ±0.27), were between
S. lewini and C. falciformis results. The main prey of S. lewini
are benthic and pelagic prey; whereas C. falciformis, feed mainly on
red crab (Pleuroncodes planipes), a common crustacean in the column water
from the western coast of Baja California Sur. The other shark species recorded
in the same area than S. californica, showed variations in the isotope
values, which indicated the different feeding habits and distribution of each
shark species in the marine ecosystems and therefore the different trophic level
obtained by Pacific angel shark, using isotopes which is considered a tertiary
consumer (TL = 4.5). Cortes (1999) also classified to
S. californica as a tertiary consumer (TL= 4.1 average). Conde-Moreno
(2009) determined the trophic level for sharpnose shark Rhizoprionodon
longurio in the Gulf of California, which classified this shark species
as a tertiary consumer or a high level carnivorous (TL> 4), because this
shark feed mainly on carnivorous prey.
Two factors would contribute to the 15N enrichment: the first is
the shift of the preferred prey from species with low trophic level and low
δ15N (e.g., crustacean and planktivorous fishes), toward prey
with high trophic level and high δ15N values (e.g., cephalopods
and benthic carnivorous fishes). The second factor is the increase in trophic
position considering the predator size, as reported by Renones
et al. (2002). However, we do not found changes in isotopes values
in angel shark, because the range of isotopic values of δ15N
and δ13C were minimal (1.4 and 1.6, respectively).
The lack of differences in patterns of 15N enrichment by areas and
sizes, suggest that trophic niche is similar in angel sharks. This behavior
was observed also in angel shark stomach contents (Escobar-Sanchez
et al., 2006), where the angel shark feed on prey with similar trophic
level in different areas. Although we found few differences in δ13C
values, we think that angel shark fed on prey with different carbon origin because
they move from different ecosystems (Rau et al.,
1992; Das et al., 2000).
The variability in δ15N and δ13C was minimal, considering that enrichment of δ15N in nature is 3-4 by trophic level and 1 in δ13C. We consider that angel sharks in the coastal area fed on the same trophic level (benthic prey), considering the δ15N values of 18.3 to 19.5 (av.= 18.9 ±0.27 sd) and δ13C of 16.5 to 15.06 (av.= 15.94 ±0.34 sd). These values changed few, which indicate that males, females, juveniles and adults feed on the same resources during years.
By other hand, the isotopic composition would change among organism with different
size or seasonally in each area and this information would be used to know the
migratory behavior of predators (Hesslein et al.,
1993; Overman and Parrish, 2001), however little
information exists on migration of angel sharks. Fishing information indicates
that adults are found in deep waters during the warm season, following their
reproductive cycle. Although, the nitrogen isotope values showed no differences
in the trophic level, then we consider that despite the capture area of angel
sharks, they feed in deep waters, where the prey have a constant trophic level.
More biological information on angel sharks is necessary to know what happen
during the warm season, because the artisanal fishermen do not catch angel shark
in this season. Considering that fishermen put their nets at depths of 70-80
m, would indicate that angel sharks would be in deeper waters during this season.
We would like to thank Instituto Politécnico Nacional (SIP, COFAA and EDI) for funds in the project Trophic ecology of sharks and mantas in the lower Gulf of California. To fishermen of El Pardito, El Portugués and Ensenada de Muertos, mainly to Alejandro Escobar for help in the sampling. The first author thanks to CONACyT and PIFI.
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