SCRS/2011/134 Collect. Vol. Sci. Pap. ICCAT, 68(4): 1594-1600 (2012)

STOMACH CONTENTS ANALYSIS OF SWORDFISH (XIPHIAS GLADIUS) CAUGHT OFF SOUTHERN BRAZIL: A BAYESIAN ANALYSIS

Guilherme R. Gorni1, Selene Loibel2, Roberto Goitein3, and Alberto F. Amorim4

SUMMARY

This study proposes to ascertain the importance of each alimentary category in the Xiphias gladius diet composition, as well as to reinforce the use of the Bayesian approach for analysis of these data. Swordfish were collected during fishing cruises carried out by the longline fleet of Santos and Guarujá, São Paulo State, from July 2007 to June 2009. The collection of the stomachs was done on board during evisceration. The stomach contents have been identified to the smallest possible taxa. For Bayesian model formulation, each alimentary item was clustered in four food categories previously defined as: teleost fishes, cephalopod molluscs, crustaceans, and others. After the stomach contents analysis, 550 food items were identified, which belonged to 19 taxa. Following the calculation, the most important food category of X. gladius is comprised of cephalopod molluscs (PM= 0.5051), followed by teleost fishes. (PM=0.4362). The food category composed of crustaceans presents a low contribution for the swordfish feeding habit (PM=0.0634), and in this case it could be considered to be an accidental food item. The Bayesian approach should be useful to analyse great top predators, which are usually caught in small numbers.

RÉSUMÉ

La présente étude se propose de déterminer l’importance de chaque catégorie alimentaire dans la composition du régime alimentaire du Xiphias gladius et de renforcer également l'utilisation de l’approche bayésienne pour analyser ces données. Les espadons ont été collectés pendant des campagnes de pêche réalisées par les flottilles palangrières de Santos et Guarujá, Etat de Sao Paulo, entre juillet 2007 et juin 2009. La collecte des contenus stomacaux s'est effectuée à bord pendant l'éviscération. Les contenus stomacaux ont été identifiés jusqu'aux plus petits taxons possibles. Aux fins de la formulation du modèle bayésien, chaque aliment a été classé dans les quatre catégories alimentaires antérieurement définies comme étant : poissons téléostéens, mollusques céphalopodes, crustacés et autres. Au terme de l’analyse des contenus stomacaux, 550 aliments ont été identifiés, lesquels appartenaient à 19 taxons. A la suite des calculs, la catégorie alimentaire la plus importante de X. gladius est composée de mollusques céphalopodes (PM= 0,5051), suivis des poissons téléostéens (PM=0,4362). La catégorie alimentaire composée de crustacés présente une faible contribution aux habitudes trophiques de l'espadon (PM=0,0634), et elle pourrait être considérée dans ce cas comme un aliment accidentel. L'approche bayésienne devrait être utile pour analyser les principaux grands prédateurs, qui sont généralement capturés en faibles nombres.

RESUMEN

En este estudio se propone determinar la importancia de cada categoría alimentaria en la composición de la dieta de Xiphias gladius, así como reforzar la utilización del enfoque bayesiano para los análisis de esos datos. Se recogieron peces espada durante mareas de pesca realizadas por la flota de palangre de Santos y Guarujá, Estado de São Paulo, desde julio de 2007 hasta julio de 2009. La recogida de muestras estomacales se realizó a bordo durante la evisceración. Los contenidos estomacales se identificaron hasta el taxón más pequeño posible. Para la formulación del modelo bayesiano, cada elemento alimentario se agrupó en cuatro

1 Departamento de Ciências Biológicas e da Saúde, UNIARA, Araraquara (SP) ; [email protected] 2 Instituto de Geociências e Ciências Exatas, UNESP, Rio Claro (SP); [email protected] 3 Instituto de Biociências, UNESP, Rio Claro (SP); [email protected] 4 Instituto de Pesca, APTA-SAA, Santos (SP); [email protected] 1594 categorías alimentarias previamente definidas como: peces teleósteos, moluscos cefalópodos, crustáceos y otros. Tras el análisis de los contenidos estomacales, se identificaron 550 productos alimentarios, que pertenecían a 19 taxones. Tras realizar los cálculos, se halló que la categoría alimentaria más importante para el X. gladius eran los moluscos cefalópodos (PM = 0,5051), seguidos por los peces teleósteos. (PM=0,4362). La categoría alimentaria compuesta de crustáceos presenta una baja contribución a los hábitos alimentarios del pez espada (PM 0,0634) y, en este caso, puede considerarse un producto alimentario accidental. El enfoque bayesiano debería ser útil para analizar a los grandes depredadores, que generalmente se capturan poco.

KEYWORDS

Longliner, Bayesian approach, alimentary category, diet composition, food item

1. Introduction

The swordfish, Xiphias gladius (Linnaeus 1758), is a cosmopolitan fish with epi and meso-pelagic habits and is most often found between 45°N and 45°S latitudes. Its distribution includes tropical and temperate oceans and it can tolerate wide water temperature variations (Palko et al., 1981; Zavala-Camin, 1981; Nakamura, 1985). According to Carey and Robison (1981), this species can reach depths greater than 600 meters and generally inhabiting deeper water during the day and migrating to the surface at night.

Considered to be an opportunistic predator, the swordfish has an ample trophic spectrum, feeing on cephalopods, fish and crustaceans (Clarke et al., 1995; Figueiredo and Menezes, 2000). Studies of the dietary composition of this predator have been conducted in the Mediterranean Sea (Bello, 1991), Pacific Ocean (Ibáñez et al., 2004; Castillo et al., 2007; Letelier et al., 2009), Indian Ocean (Potier et al., 2007) and Atlantic Ocean (Stillwell and Kohler, 1985; Simões and Andrade, 2000; Satoh et al., 2004; Chancollon et al., 2006). There are few studies of this fish species in Brazilian waters, the exceptions being the works of Zavala-Camin (1981), Mello (1992) and Vaske-Júnior (2000).

This study proposes to analyse (1) diet of swordfish, (2) ascertaining the importance of each alimentary category for the diet composition, and (3) reinforce the use of the Bayesian approach for analysis of fish stomach contents.

2. Material and methods

2.1 Study site

This study was carried out in association with the longline commercial fleet settled in Santos and Guarujá cities, São Paulo State. This fleet operates in the southern coast off Brazil, including the area comprised within 17-35°S and 27-52°W, at the side of the continental platform (Figure 1). According to the longliner autonomy, the trips extend from 15 to 20 days, limiting the fishing distance.

2.2 Feeding analysis

Fish were collected during fishing cruises performed between July/2007 to June/2009. The collection of the stomachs was made on board during the evisceration. The stomach was labeled, closed, and deposited in a 50 l box containing a formalin solution at 10%.

In the laboratory the stomach contents were washed and drizzled in mesh of 1 mm and conditioned in flasks with alcohol 70%. The whole material kept has been identified until the smallest possible taxa, following criteria adopted for Nesis (1987), Figueiredo and Menezes (2000), Figueiredo et al. (2002) and Vaske-Junior (2006). For Bayesian model formulation, each alimentary item was clustered in four food categories previously defined as: (1) Teleost fishes; (2) Cephalopod molluscs; (3) Crustaceans; and (4) Others. 2.3 Bayesian inference

1595 See details of the formulation in Gorni et al. (2011). The priori means was based on expert information extracted from Zavala-Camin (1981).

3. Results and discussions

The swordfishes caught were 101 individuals whose size varied from 60 to 275 centimetres (LJFL). After the stomach contents analysis 550 food items were identified, which belonged to 19 taxa. They were mainly composed by molluscs and fishes (see details in Table 1).

Table 2 presents the Bayesian estimations of the proportions of each food category (θ) in composing the diet of X. gladius. The table is composed of the posterior modes (PM) and their respective credibility intervals (γ = 95%).

The most important food category of X. gladius is cephalopod mollusks (PM = 0.50), followed by teleost fishes, with posterior mode of 0.43. Crustaceans and others are the least important food categories, accounting for PM values of 0.06 and 0.02 in the diet, respectively (see Table 2).

The results show that the diet of X. gladius, in the study area and period, was composed mainly of cephalopod mollusks and secondarily of fish. These results are similar to those reported for the species in the South Atlantic (Zavala-Camin, 1981), Northwest Atlantic (Stillwell and Kohler, 1985) and Pacific (Ibáñez et al., 2004; Castillo et al., 2007; Letelier et al., 2009). However, studies conducted in the Mediterranean (Relini et al., 1995), Northeast Atlantic (Chancollon et al., 2006) and Indian Ocean (Marsac and Potier, 2001; Potier et al., 2007) show just the opposite pattern, classifying X. gladius as primarily an ichthyophagous predator. Crustaceans in these studies were reported as having low importance in the diet, even being considered accidental prey (Letelier et al., 2009). Among these animals, specimens of the Decapoda order were also reported by Zavala-Camin (1981) and Chancollon et al. (2006).

As observed by Abid and Idrissi (2006), the diet of X. gladius varies considerably among habitats and seasons, with this result mainly depending on variations in the population dynamics of the different prey species (Letelier et al., 2009). Therefore, to minimize the effects of these environmental variations on the analysis of the dietary composition of the swordfish, the prior information was only composed of the data reported by Zavala-Camin (1981), since it was conducted in the same region investigated in the present study (Southeast Atlantic). Bayesian inference can be a valuable tool, by allowing the incorporation of data from previous studies with the current results, generating more complete information on the matter in question. Besides a point estimate (posterior mode) of the proportion of each food category, this approach generates an estimate by intervals (credibility intervals), permitting comparison between different studies.

According to Wootton (1990), an understanding of the relationship between predators and their prey is particularly valuable when the targets are species with commercial value. However, as mentioned, studies involving large predators face many problems, among them the difficulty of obtaining a satisfactory sample size to permit characterizing these animals’ diets conclusively. Therefore, the proposal to use Bayesian inference in analyzing the stomach contents of top predators like the swordfish can be effective at least to minimize this problem.

4. Acknowledgements

The authors wish to thank to biologists Natalia Della Fina, Natalia Piva Silva and Caio dos Santos Fernandes, to student Bruna Rodrigues Bernardes, to ItaFish Transporte e Comércio de Pescados, to Instituto de Pesca (Santos/SP) and to CAPES for financial support.

1596 5. References

Abid, N., Idrissi, M., 2006, Swordfish. In: Field Manual, Chapter 2.1.9. International Commission for the Conservation of Atlantic Tunas, Madrid, Spain. http://www.iccat.int/Documents/SCRS/Manual/CH2/2_1_9_SWO_ENG.pdf

Amorim, A.F., Arfelli, C.A., Fagundes, L. 1998, Pelagic elasmobranchs caught by longliners off southern Brazil during 1974-97: An overview. Mar. Freshwater Res., 49 (7): 621-632.

Carey, F.G., Robison, B.H. 1981, Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry. Fish. Bull., 79 (2): 277-292.

Castillo, K., Ibánez, C.M., González, C., Chong, J. 2007, Dieta del pez espada Xiphias gladius Linnaeus, 1758 en distintas zonas de pesca frente a Chile central durante el otoño de 2004. Rev. Biol. Mar. Oceanogr., 42 (2): 149-156.

Chancollon, O., Pusineri, C., Ridoux, V. 2006, Food and feeding ecology of northeast Atlantic swordfish (Xiphias gladius) off the Bay of Biscay. ICES J. Mar. Sci., 63: 1075-1085.

Clarke, M.R., Clarke, D.C., Martins, H.R., Silva, H.M. 1995, The diet of swordfish (Xiphias gladius) in Azorean waters. Arquipélago – Life and Marine Science, 13A: 53-69.

Figueiredo, J.L., Menezes, N. 2000, Manual de peixes marinhos do sudeste do Brasil. VI. Teleostei (5). São Paulo, Museu de Zoologia da USP, 116p.

Figueiredo, J.L., Santos, A.P., Yamaguti, N., Bernares, R.A., Wongtschowski, C.L.B. 2002, Peixes da Zona Econômica Exclusiva do Sudeste e Sul do Brasil. Levantamento com rede de meia água. EDUSP, São Paulo, 242 p.

Gorni, G.R., Loibel, S., Goitein, R., Amorim, A.F., 2011 Stomach contents analysis of white marlin (Tetrapturus albidus) caught in Southern off Brazil: a Bayesian analysis. Collect. Vol. Sci. Pap. ICCAT, 66(4): 1779- 1786.

Ibañez, C.M., González, C., Cubillos, L. 2004, Dieta del pez espada Xiphias gladius Linnaeus, 1758, en aguas oceánicas de Chile central en invierno de 2003. Invest. Mar., 32 (2): 113-120.

Letelier, S., Meléndez, R., Carreño, S., Lopez, S., Barria, P. 2009, Alimentación y relaciones tróficas del pez espada (Xiphias gladius Linnaeus, 1758), frente a Chile centro-norte durante 2005. Lat. Am. J. Aquat. Res., 37 (1): 107-119.

Marsac, F., Potier, M. 2001, On-going research activities on trophic ecology of swordfish (Xiphias gladius) in the Western Indian Ocean. IOTC Proceedings, 4: 155-163.

Mello, R.M. 1992, Análise dos conteúdos estomacais, intensidade de alimentação, idade e crescimento do espadarte Xiphias gladius (Xiphioidei: Xiphiidae), no Sul do Brasil. Dissertação de mestrado, Fundação Universidade Federal do Rio Grande, Rio Grande, Brasil. 105 pp.

Nakamura, I. 1985, FAO Species Catalogue. Vol. 5. Billfishes of the World. An annotated and illustrated catalogue of marlins, sailfishes, spearfishes and swordfishes know to date. FAO Fish. Synop., 125 (5). 65 pp.

Nesis, K. 1987, Cephalopods of the world. Squids, cuttlefishes, and allies. T.F.H. Publications Inc. Ltd. 351p.

Palko, B.J., Beardsley, G.L., Richards, W.J. 1981, Synopsis of the biology of the swordfish, Xiphias gladius Linnaeus. FAO Fish. Synop., 127: 1-21.

Potier, M., Marsac, F., Cherel, Y., Lucas, V., Sabatié, R., Maury, O., Ménard, F. 2007, Forage fauna in the diet of three large pelagic fishes (lancetfish, swordfish and yellowfin tuna) in the western equatorial Indian Ocean. Fish. Res., 83: 60-72.

1597 Relini, O., Garibaldi, L.F., Cima, C., Palandri, G. 1995, Feeding of the swordfish, the bluefin and another pelagic nekton in the western Liguria Sea. Col. Vol. Sci. Pap. ICCAT, 44 (1): 283-286.

Satoh, K., Yokawa, K., Saito, H., Matsunaga, H., Okamoto, H., Uozumi, Y. 2004, Preliminary stomach contents analysis of pelagic fish collected by Shoyo-Maru 2002 research cruise in the Atlantic Ocean. Col. Vol. Sci. Pap. ICCAT, 56: 1096-1114.

Simões, P.R., Andrade, J.P. 2000, Feeding dynamics of swordfish (Xiphias gladius) in Azores area. Collect. Vol. Sci. Pap. ICCAT, 51(5): 1642-1656.

Stillwell, C.E., Kohler, N.E. 1985, Food and feeding ecology of the swordfish Xiphias gladius in the western North Atlantic Ocean with estimates of daily ration. Mar. Ecol. Prog. Ser., 22: 239-247.

Vaske-Júnior, T. 2000, Relações tróficas dos grandes peixes pelágicos da região equatorial sudoeste do oceano Atlântico. Tese de Doutorado. Fundação Universidade Federal do Rio Grande, Brasil. 145 p.

Vaske-Júnior, T. 2006, Guia de identificação de cefalópodes costeiros e oceânicos do Atlântico sudoeste equatorial através das mandíbulas (bicos). 1° ed. Olinda: Elógica-livrorápido. 61 p.

Wootton, R.J. 1990, Ecology of teleost fishes. London: Chapman and Hall. 404 pp.

Zavala-Camin, L.A. 1981, Hábitos alimentares e distribuição dos atuns e afins (Osteichthyes – Teleostei) e suas relações ecológicas com outras espécies pelágicas das regiões Sudeste e Sul do Brasil. Tese de doutorado, Instituto de Biociências da Universidade de São Paulo, Brasil. 237 pp.

1598

Table 1. Prey items in the swordfish stomachs. Prey taxa

Chordata: Teleost fish

Acropomatidae

Synagrops bellus Synagrops sp.

Bramidae

Brama brama Brama sp.

Gempylidae Gempylus serpens

Myctophidae

Nomeidae Cubiceps sp.

Scombridae

Auxis spp. Euthynnus alleteratus Scomber colias Thunnus alalunga

Trichiuridae Trichiurus lepturus

Unidentified fish

Mollusca: Cephalopoda

Order Teuthida

Ommastrephidae

Loliginidae

Order Octopoda

Order Sepiida

Arthropoda: Crustacea

Order Decapoda

Other

1599 Table 2. Bayesian estimators of the proportion of each food category (θ) in the diet composition of Xiphias gladius. MP: posteriori mode; Icred. (95%): Bayesian credibility interval (γ = 95%). Food categories PM Icred. (95%)

θ1 (Teleost fishes) 0.4362 (0.4081 ; 0.4672)

θ2 (Cephalopod molluscs) 0.5051 (0.4744 ; 0.5338)

θ3 (Crustaceans) 0.0634 (0.0538 ; 0.0840)

θ4 (Others) 0.0204 (0.0127 ; 0.0294)

Figure 1. Fishing area of the longline fleet of Santos - SP (adapted from Amorim et al., 1998).

1600