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Contenido estomacal del cazon bironche del Pacifico, Rhizoprionodon longurio (Carcharhiniformes, Carcharhinidae) en el sector suroriental del Golfo de California.

Stomach contents of the Pacific sharpnose shark, Rhizoprionodon longurio (Carcharhiniformes, Carcharhinidae) in the southeastern gulf of California.

INTRODUCTION

The Pacific sharpnose shark, Rhizoprionodon longurio (Jordan & Gilbert, 1882) is a small shark (<1.5 m) of the eastern Pacific coastal waters. Its distribution ranges from California to Peru (Compagno, 1984), it is exploited by the artisanal fishing fleets operating along the Mexican coasts from Baja California to Chiapas, and it appears in the bycatch of industrial trawl fisheries (Marquez-Farias et al, 2005).

Its presence in Sinaloa coastal waters shows a strong, possibly temperature-related seasonal pattern, since it is present only between November and MarchApril of each year when R. longurio, as well as the pups and juveniles of the scalloped hammerhead, Sphyrna lewini (Griffith & Smith, 1834), are important target species for the artisanal fishery of the state of Sinaloa, where these species are the bulk of the captures of small sharks, and the 453 ton of cazon landed in 2011 (small sharks), were close to 20% of the total production of small sharks of the Mexican Pacific fishing fleets (SAGARPA-CONAPESCA, 2011).

Although it is fished intensively, studies on its general biology are scarce. In particular, information on its feeding habits is limited (Marquez-Farias et al., 2005) and is mostly confined to grey literature (Saucedo-Barron et al., 1982; Alatorre-Ramirez, 2003; Conde-Moreno, 2009). Aiming to add information on its feeding ecology in the SE Gulf of California, we determined the stomach contents of specimens of this species caught by the artisanal fishing fleet operating off Mazatlan, Sinaloa, and NW Mexico.

MATERIALS AND METHODS

Samples were obtained between December 2007 and March 2008 in two important landing sites (Playa Sur and Chametla) for the local artisanal fishing fleet. This fleet operates on a gently sloping platform, in depths of 18 to 91 m with soft terrigenous sediments (AlbaCornejo et al., 1979), between the locations Marmol (23[degrees]11'N, 106[degrees]30'W) and Chametla (23[degrees]45'25"N, 106[degrees]05'15"W). The boats (pangas) are fiberglass, 6 to 7.5 m long, with 75-200 HP outboard motors, and each boat operates two 1500-m bottom longlines with 300 hooks #4 or H5.

Both landing sites were visited once weekly, the total length (TL) and wet weight (WW) of the landed specimens of R. longurio were obtained with a measuring tape and a digital scale ([+ or -] 0.5 cm y 50 g), and their sex was determined from the presence/absence of claspers. The females and males of this species reach first maturity at 83 and 86 cm TL, respectively (Castillo et al., 1996). Consequently, specimens with values lower than these sizes were considered juveniles.

The whole stomachs were obtained through a longitudinal slit in the abdominal region and preserved frozen (-30[degrees]C) until analysis. Upon defrosting, the fullness of each stomach was assessed as: 0 = empty, 1 = 1-25%, 2 = 26-50%, 3 = 51-75% and 4 = 76-100% (Stillwell & Kohler, 1982). The contents were sieved through a 0.1 mm sieve to retain the prey items, which were counted, weighed to the nearest 0.1 g and identified to the lowest possible taxon depending on the state of digestion. This was evaluated as: 1: preys complete, undigested; 2: whole body, no skin, no eyes, bare muscles; 3: only parts of the body and axial skeleton present; 4: only hard structures present, and 5: organic material not identifiable (OMNI) (Galvan-Magana, 1999).

Complete, undigested fish were identified with the manuals by Miller & Lea (1972); Walker & Rosenblatt (1988); Allen & Robertson (1994) and Fischer et al. (1995). Fish remains (states of digestion 2 and 3) were identified by their vertebral characteristics with the keys by Clothier (1950) and Miller & Jorgensen (1973), using as reference the collection of fish skeletons of the Laboratory of Fish Ecology of the Centro Interdisciplinario de Ciencias Marinas (CICIMAR) of La Paz, BCS. State 4 items were fish otoliths, cephalopod beaks and crustacean exoskeletons (complete or parts), which were identified using the keys by Fitch & Brownell Jr. (1968), Clarke (1962, 1986), Iverson & Pinkas (1971) and Wolff (1982, 1984).

The importance of each prey was determined using the traditional numeric (%N), gravimetric (%W) and frequency of observation (%F) indexes (Hyslop, 1980), which were used to calculate the composite index of relative importance IRI = (%N+%V) %F by Pinkas et al. (1971), but using gravimetric (W%), rather than volumetric (V%) data, as suggested by Stevens et al. (1982).

The diversity of the diet as indicated by the stomach contents was estimated with the Shannon-Weaver diversity (H') and equitability (E) indexes H' = - [sigma](pi)ln(pi) and E = H'/MH5, where pi is the proportion of species i, MH is the index of maximum diversity: -ln(1/S), and S is the number of species (Pielou, 1975).

The dietary breadth was determined with the standardized version Ba = (B-1)/(n-1) of Levin's index of niche breadth B = 1/[sigma][Pj.sup.2] where B is Levin's index, Pj is the proportion of the diet consisting in prey j, and n is the number of prey categories (Krebs, 1999; Navia et al., 2007). Ba ranges from 0 to 1: values close to 0 indicate dominance of few prey items (specialist feeder), and generalist feeders have values close to 1.0 (Hurlbert, 1978).

The presence of overlap of trophic habits of males and females and of organisms of different size (age) was determined using analysis of similarities (ANOSIM) tests, performed with the PRIMER Software package (Clarke & Gorley, 2006). The values of the resulting statistic (R) range from 1 to 0. R = 1 indicates that the samples are within the same groups (no overlap), and R values close to 0 indicate that similarities and dissimilarities are not related to the groups (overlap).

RESULTS

The total number of sharks used for this study was 250 (135 males and 115 females). Sizes ranged from 52 to 120 cm and from 60 to 120 cm TL for females and males, respectively. The common mean TL was 77.7 [+ or -] 12.8 cm and the TL distribution frequency diagram showed two clearly defined modal groups of equal size, hereinafter defined as juveniles (size range 52-80 cm TL, modal value 72.5 cm), and adults (TL 85-140 cm, modal value 92.5 cm) (Fig. 1).

The accumulated diversity curves reached close to asymptotic values after 25 to 30 stomachs for juveniles (both sexes) and male adults. The total number of female adults was 26, and the accumulated diversity increased by 0.25% between 20 and 26 stomachs (Osuna-Peralta, 2010). Most of the stomachs were in fullness class 1 (78.4%), and 6% were totally empty. Class 2 was 12.4% and classes 3 and 4 represented 1.2% y 2.0% of the total, respectively. The total number of preys found in the 193 stomachs with contents between stages of digestion 1 to 4 was 395. More than 73% were at stages of digestion 3 and 4, and OMNI was 17%.

Trophic spectrum

The preys identified were 395. Those identified at the specific level were 52 (13.2%), and 311 (79%) were identified at the generic level. The remaining 32 were identified at the family level, for a total of 11 species, 18 genera and 15 families (17 fish, 4 cephalopods and 1 crustacean) (Table 1).

Numeric index

Pelagic cephalopods and fish made up approximately

76.9 and 20.7% of the preys, while crustaceans were the remaining 2.3%. The most frequent and abundant cephalopods were Argonauta spp. (73.7%), this was followed by Lolliguncula diomedae andMastigoteuthis dentata, which jointly represented <2.5%. The most common fish were Oligoplites refulgens (6.8%), Oligoplites spp. (3.3%) and Chloroscombrus orqueta (1.0%) (Table 1).

[FIGURE 1 OMITTED]

Gravimetric index

The total weight of the preys identified was 570.3 g; 506.4 g (88.8%) were fish, cephalopod beaks were 10.8% and crustaceans 0.4%. Additionally, 317 g of OMNI were found in 83 stomachs (Table 1).

Gravimetrically, the most important prey items were the belonid fish Tylosurus crocodrilus fodiator (25.7%) and the carangid O. refulgens (13.9%). The beaks of Argonauta spp. were only 10.8%, which was closely followed by fishes Opisthonema libertate, Oligoplites spp. and Caranx spp. (9.7%, 8.4% and 7.8%, respectively) (Table 1).

Frequency of occurrence

The most frequent prey items were molluscs (46.8%), followed by fishes and crustaceans (26.0 and slightly less than 3% of the stomach contents examined, respectively). Among molluscs, the most frequent were Argonauta spp. (43.4%), followed by L. diomedae and M. dentata, with 2.1 and 1.7%. Among fish, O. refulgens, Oligoplites spp. and C. orqueta were 6.8%, 4.3% and 1.7% respectively (Table 1).

Index of relative importance

The main preys were cephalopods, with IRI values >3600 (>93%). Among these, the most important were Argonauta spp. (92.9%), followed by O. refulgens (3.6%) and Oligoplites spp. (1.3%). All remaining preys were <1% (Table 1). The relative importance of Argonauta spp. was similar for males and females (91.0 and 92.8%, respectively), but the value calculated for juveniles (95.4%) was almost 12% higher than for adults (83.7%). As a consequence, the relative importance of other preys such as Oligoplites spp. was higher for adults than for juveniles (8.8% and 2.9%, respectively).

Diversity, equitability, dietary breadth and trophic overlap

There were no significant sex-related differences in the mean diversity of the stomach content of both sexes, although the mean diversity values calculated for juveniles were significantly lower than those of the respective adults. In all cases, the low values of the accumulated diversity, equitability and dietary breadth indexes indicated a monotonous diet, strongly dominated by a small number of prey items, and the global R value obtained with the ANOSIM routine was 0.02, indicating similar dietary habits for juveniles and adults of the two sexes (Table 2).

DISCUSSION

All information available on the trophic habits of R. longurio was obtained in southern Sinaloa waters during winter months, when samples are available from the local artisanal fishing fleets. According to these previous data, the most important preys of this species are fish (Saucedo-Barron et al., 1982; Castillo et al., 1996; Alatorre-Ramirez, 2003; Marquez-Farias et al., 2005), which does not coincide with our results, since the frequency, abundance and high IRI value of the pelagic octopod Argonauta spp. beaks indicate that, in spite of their low %W due to the advanced degree of digestion of these preys, this was the most important prey in all our samples.

Argonauta spp. are epipelagic organisms of tropical and subtropical oceanic waters (Roper et al, 1984; Heeger et al., 1992), although they may appear in high numbers in coastal areas, generally associated with the presence of oceanic water masses (Demicheli et al.,

2006). They are frequent in the vicinity of floating objects, and are known to form long chains of up to 20 specimens (Nesis, 1977; Walton & Houston, 2001), which might explain the high numerical and relative importance indexes (>70 N% and >90% IIR), although their frequency of occurrence was below 45%.

The presence of Argonauta in the stomach contents of R. longurio, caught in the southeast of the Gulf of California, was reported only by Conde-Moreno (2009), but it has been mentioned by several authors as a common and sometimes important food item for other predators, such as billfish (Abitia-Cardenas et al., 2002, 2010; Arizmendi-Rodriguez et al., 2006; AmezcuaGomez, 2007) and dolphinfish (Amezcua-Gomez, 2007), among others.

R. longurio has been considered a generalist predator by all authors who described its feeding habits (Saucedo-Barron et al., 1982; Castillo et al., 1996; Alatorre-Ramirez, 2003; Marquez-Farias et al., 2005), but the low value of Levin's index obtained in this study suggests the feeding behaviour of a specialist predator.

However, as is the case for electivity indices which may be influenced by external food availability (Strauss, 1979; Gras & Saint-Jean, 1982), this is probably due to a high dominance in the pelagic community of the more frequent and abundant prey items found in the stomachs of this species. As suggested for other sharks, by Wetherbee et al. (1990), this feeding strategy combines maximum consumption with minimum energy used for its capture. This is consistent with the suggestion by Conde-Moreno (2009), that R. longurio should be considered an opportunistic, rather than a generalist feeder.

DOI: 103856/vol42-issue3-fulltext-5

Received: 4 April 2013; Accepted: 2 May 2014

ACKNOWLEDGMENTS

The help of Dr. Felipe Galvan and his associates Yassir Torres and Vanessa Alatorre during a training stage for stomach contents identification at the Fish Ecology Laboratory of Centro Interdisciplinario de Ciencias Marinas, La Paz, Baja California Sur, is gratefully acknowledged.

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Yolene R. Osuna-Peralta (1), Domenico Voltolina (2) Ramon E. Moran-Angulo (1) & J. Fernando Marquez-Farias (1)

(1) Facultad de Ciencias del Mar, Universidad Autonoma de Sinaloa Paseo Claussen s/n, Col. Los Pinos, CP 82000, Mazatlan, Sinaloa, Mexico

(2) Laboratorio UA4-CIBNOR, Centro de Investigaciones Biologicas del Noroeste Ap. Postal 1132, CP 82000, Mazatlan, Sinaloa, Mexico

Corresponding author: Domenico Voltolina (voltolin04@cibnor.mx)
Table 1. Absolute and relative (%) number of specimens (N, N%), mass
(grams: G, G%), frequency of occurrence (FO, FO%), and absolute and
relative indexes of relative importance (IRI, IRI%) of preys
identified in the stomach contents of Rhizoprionodon longurio, landed
in Mazatlan, Sinaloa, Mexico.

Prey                     N     N%      G        G%       FO    FO%

Mollusca Cephalopoda
Argonauta spp.           291   73.67   61.51    10.770   102   43.40
Lolliguncula diomedae    5     1.26    0.14     0.020    5     2.13
Mastigoteuthis dentata   4     1.01    0.05     0.010    4     1.70
Onychoteuthis banksii    3     0.76    0.03     0.005    3     1.28
Remains, unidentified    1     0.25    0.01     0.002    1     0.43
Subtotal                 304   76.95   61.74    10.810   115   48.94
Crustacea Decapoda
Pleuroncodes planipes    3     0.76    0.39     0.07     1     0.43
Remains, unidentified    6     1.52    1.73     0.30     6     0.43
Subtotal                 9     2.28    2.12     0.37     7     0.86
Pisces Osteichthyes
Opisthonema libertate    2     0.51    55.22    9.680    2     0.85
Anchoa spp.              1     0.25    1.49     0.260    1     0.43
Carangidae               3     0.76    2.26     0.400    2     0.85
Caranx spp.              2     0.51    44.22    7.750    2     0.85
Chloroscombrus orqueta   4     1.01    7.61     1.330    4     1.70
Decapterus spp.          1     0.25    7.00     1.230    1     0.43
Engraulis mordax         1     0.25    1.85     0.320    1     0.43
Fistularia spp.          1     0.25    24.74    4.340    1     0.43
Gerreidae                1     0.25    5.09     0.890    1     0.43
Menticirrhus undulatus   1     0.25    11.41    2.000    1     0.43
Mugil spp.               1     0.25    24.16    4.240    1     0.43
Oligoplites refulgens    27    6.83    79.09    13.870   16    6.81
Oligoplites spp.         13    3.29    47.99    8.410    10    4.26
Sciaenidae               1     0.25    0.01     0.002    1     0.43
Serranidae               1     0.25    0.01     0.002    1     0.43
Sphoeroides annulatus    1     0.25    7.14     1.250    1     0.43
Sphoeroides spp.         1     0.25    6.00     1.050    1     0.43
Trachinotus spp.         1     0.25    34.29    6.010    1     0.43
Tylosurus crocodilus     1     0.25    146.50   25.690   1     0.43
  fodiator
Remains, unidentified    18    4.56    0.34     0.060    18    7.66
Subtotal                 82    20.72   506.42   88.800   61    28.57
Total                    395   100     570.28   100      235   78.37

Prey                     IRI       IRI%

Mollusca Cephalopoda
Argonauta spp.           3665.82   92.93
Lolliguncula diomedae    2.75      0.07
Mastigoteuthis dentata   1.74      0.04
Onychoteuthis banksii    0.98      0.02
Remains, unidentified    0.11      0
Subtotal                 3671.4    93.06
Crustacea Decapoda
Pleuroncodes planipes    0.35      0.01
Remains, unidentified    4.65      0.12
Subtotal                 5.00      0.13
Pisces Osteichthyes
Opisthonema libertate    8.67      0.22
Anchoa spp.              0.22      0.01
Carangidae               0.98      0.02
Caranx spp.              7.03      0.18
Chloroscombrus orqueta   4.00      0.10
Decapterus spp.          0.63      0.02
Engraulis mordax         0.25      0.01
Fistularia spp.          1.95      0.05
Gerreidae                0.49      0.01
Menticirrhus undulatus   0.96      0.02
Mugil spp.               1.91      0.05
Oligoplites refulgens    140.96    3.57
Oligoplites spp.         49.81     1.26
Sciaenidae               0.11      0
Serranidae               0.11      0
Sphoeroides annulatus    0.64      0.02
Sphoeroides spp.         0.56      0.01
Trachinotus spp.         2.67      0.07
Tylosurus crocodilus     11.04     0.28
  fodiator
Remains, unidentified    35.36     0.91
Subtotal                 268.35    5.91
Total                    3944.75   100

Table 2. Diversity (H'), equitability (E) and diet breadth
(Bi) indexes calculated from the stomach contents of
juveniles and adults (J and A) of the males and females (M
and F) of Rhizoprionodon longurio landed in Mazatlan
between December 2007 and March 2008. F + M =
indexes calculated jointly for both sexes. The different
letters indicate significant differences between juveniles
and adults, in either case with no difference between males
and females (two ways ANOVA, a = 0.05, a < b).

      H'               E      [B.sub.i]

F     0.619a (0.149)   0.26   0.049
J M   0.696a (0.133)   0.27   0.045
F+M   0.796a (0.112)   0.30   0.033
F     1.053b (0.266)   0.48   0.102
A M   0.947b (0.202)   0.38   0.085
F+M   1.283b (0.179)   0.44   0.055
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Title Annotation:articulo en ingles
Author:Osuna-Peralta, Yolene R.; Voltolina, Domenico; Moran-Angulo, Ramon E.; Marquez-Farias, J. Fernando
Publication:Latin American Journal of Aquatic Research
Date:Jul 1, 2014
Words:4295
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