SCRS/2007/173
Collect. Vol. Sci. Pap. ICCAT, 62(6): 1883-1891 (2008)
FISHERY BIOLOGY ON PELAGIC STINGRAY PTEROPLATYTRYGON VIOLACEA CAUGHT OFF SOUTHERN BRAZIL BY LONGLINERS SETTLED IN SAO PAULO STATE (2006-2007) C.C. Ribeiro-Prado1, A.F. Amorim2 SUMMARY The pelagic stingray (Pteroplatytrygon violacea) is cosmopolitan and it is usually caught by Sao Paulo longliners as bycatch. The species is considered Least Concern by the IUCN Red List. From August to September 2006 and January to September 2007, 157 specimens (77% male and 23% female) were received from the mentioned fleet that operates off Southern Brazil. A total of 157 stomachs were analyzed. From that total, 99 stomachs were empty and 58 presented some content. Mollusca was the most common group, with predominance of Loligo sp. Actinopterygii was present in 19% and Crustacea in 17% of stomach contents. The male matures from 43.5 cm DW and 10.4 cm CL, and female from 46 cm DW on. According to Gonadosomatic Index, the females were larger in January, and it could indicate that they were near birth period. Two females were caught with embryos in different developing stages, in January 1992 and in April 2002. Females were most frequently caught near the surface and the males in deeper water. New areas of occurrence were registered. This paper aims to study the biological aspects of the P. violacea as a contribution for its conservation. RÉSUMÉ La Pastenague violette (Pteroplatytrygon violacea) est une espèce cosmopolite, généralement capturée par les palangriers de Sao Paulo en tant que prise accessoire. Cette espèce est considérée comme Préoccupation mineure par la Liste rouge de l’IUCN. Du mois d’août jusqu’au mois de septembre 2006 et de janvier à septembre 2007, 157 spécimens (77% mâles et 23% femelles) ont été reçus de la flottille susmentionnée opérant au sud du Brésil. Au total, 157 estomacs ont été analysés. Parmi ceux-ci, 99 estomacs étaient vides et 58 présentaient un contenu. Les mollusques étaient le groupe le plus répandu, avec une majorité de Loligo sp. Les contenus stomacaux se composaient d’actinoptérygiens (19%) et de crustacés (17%). Les mâles étaient matures à partir de 43,5 cm en poids manipulé et de 10,4 cm de longueur à la fourche, et les femelles à partir de 46 cm en poids manipulé. D’après l’indice gonadosomatique, les femelles étaient plus grandes au mois de janvier et cela pourrait indiquer qu’elles étaient proches de leur période de procréation. Deux femelles ont été capturées avec des embryons se trouvant dans diverses phases de développement, en janvier 1992 et en avril 2002. Les femelles étaient capturées le plus fréquemment près de la surface et les mâles plus en profondeur. Leur présence a été enregistrée dans de nouvelles zones. Ce document vise à étudier les aspects biologiques de la P. violacea afin de contribuer à sa conservation. RESUMEN La raya látigo violeta (Pteroplatytrygon violacea) es cosmopolita y por lo general los palangreros de Sao Paulo la capturan como captura fortuita. Esta especie es considerada de mínima inquietud por la Lista Roja de IUCN. Desde agosto hasta septiembre de 2006 y de enero a septiembre de 2007, 157 ejemplares (77% machos y 23% hembras) fueron recibidos de la mencionada flota que opera frente al sur de Brasil. Se analizó un total de 157 estómagos. De estos, 99 estómagos estaban vacíos y 58 presentaban algún contenido. El grupo más común eran los moluscos, con predominancia de Loligo sp. Actinopterygii estaba presente en el 19% y crustáceos en el 17% de los contenidos estomacales. Los machos maduran desde los 43,5 cm DW y 10,4 cm CL, y las hembras desde 46 cm DW en adelante. De acuerdo con el índice gonadosomático, las hembras eran más grandes en enero, lo que podría indicar que estaban cerca del periodo de parto. Dos hembras fueron capturadas con embriones en diferentes etapas de desarrollo, en enero de 1992 y abril de 2002. Las hembras se capturan con más frecuencia cerca de la superficie y los machos en aguas más profundas. Se registraron nuevas zonas de presencia. Este documento tiene como objetivo estudiar los aspectos biológicos de la P. violacea como una contribución a su conservación. 1 2
M.Sc. Student. Instituto de Pesca - APTA/SAA. Santos, SP.
[email protected] Instituto de Pesca - APTA/SAA. Santos, SP.
[email protected]
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KEYWORDS Pteroplatytrygon violacea, incidental catches, longline, pelagic stingray, reproduction, stomach content
1. Introduction The pelagic ray, Ptheroplatytrygon violacea (Bonaparte, 1832) is considered cosmopolitan and is present in tropical and subtropical areas of the Atlantic, Pacific and Indian Oceans (Wilson and Beckett, 1970; Sadowsky and Amorim, 1977; Lamilla et al., 1995; Menni et al., 1995; McKinnell e Seki, 1998; Benson et al., 2001; Chapman, 2001; McEachran e Carvalho, 2002; Bromhead et al., 2003; Dávalos-Dehullu e González-Navarro, 2003; Letourneur et al., 2004; Domingo et al., 2004; FIP, 2004; Francis et al. 2005; Molina et al., 2005; Ward and Myers, 2005). It is incidentally caught by the tuna longliner fleet settled in São Paulo State that operates off Southern Brazil (Sadowsky and Amorim, 1977). The pelagic stingray was included on the Red List of the Threatened Species, considered as “Least Concern”, although its conservation status must be carefully monitored, because the fishing effort was intensified in the area of ray’s occurrence. So its conservation status can be changed to threatened species, if fishermen keep fishing the rays and discarding the dead animals in the ocean (Chapman, 2001; Otway et al., 2004; IUCN, 2007). There are a few studies on fisheries biology of this species (Rosenberger, 2001; Mollet and Cailliet, 2002; Musick, 2004; Peach and Rouse, 2004; Schwartz, 2005), that are important source of data for the species conservation. This paper intends to study the biological aspects of P. violacea, as long as to contribute to data related to its distribution in the Southern Brazil, aiming at the species conservation. 2. Material and methods One hundred and fifty-seven specimens of pelagic rays Pteroplatytrygon violacea (Bonaparte, 1832) were collected in August and September 2006 and from January to September 2007, from the longliners fishing companies from Santos and Guarujá Cities, in Sao Paulo State. Fisheries information were also collected, including numbers of fishing days, number of sets, kind of bait used and the area where the capture of rays occurred. For each exemplar the following data were taken: sex, total length (TL), total weight (TW), gonad weight (GW) and Liver Weight (LW). The Gonadossomatic Index (GSI) and Liversomatic Index (LSI) were calculated according to Vazzoler (1981): GSI=GW/TW*100; LSI=LW/TW*100. The stomach content was identified according to Figueiredo (1988), Dávalos-Dehullu and González-Navarro (2003), Thomas (1993) and Pineda et al. (2002). 3. Results and discussion According to the fishermen, Pteroplatytrygon violacea is always present in the longliner fisheries that aim swordfish, tunas and sharks. The total of P. violacea on sampling represents a small part of the total catch. The rays are discarded alive, although the fisherman injures the animals, in order to get rid of the hooks, what can lead to death. The fishermen also mentioned the preference of the rays for light stick and squids, which occur in waters with higher temperatures. It was also observed the prevalence of females in sets where the hooks were closer to the surface and the males in deeper sets. From 157 specimens caught up to now, 121 were males and 36 were females. The smallest sampling specimen was a female of 87 cm TL, 36.5 cm DW, 1,082 g Wt, with the left uterus weighing 2.0 g, caught in June of 2007 at 25°10’S and 44°30’W, in the area about 800 meters deep. The largest specimen was a female with 129 cm TL, 68.5 DW and 7,780 g TW, presenting only the left uterus developed (87 g), without embryos, caught in August 2007, at 28°00’S and 44º30’W. 1884
The females, although less frequently captured, presented higher disc width average than the males (Figure 1). Capapé (1993) reports the same variation of sizes between sexes on stingray Dasyatis centroura. Concerning to the sexual maturity, the studied males presented L50= 43.5 cm DW and 10.4 cm of Clasper Length, when the structure is rigid (Table 1), and the females probably from 46.0 cm on, where the left uterus was significantly more developed than the right one. Studying recent female maturity, it was not observed the presence of embryos. It was observed just one uterus with flaccid appearance, weighing 196 g and 160 cm long by 10.0 cm wide, caught in January 2007 that suggests a recent spawning (Vazzoler, 1981; Querol et al., 2002). The females were larger in January, when high values could indicate that they were near birth period. Nevertheless, two females were caught with embryos in different developing stages. According to Amorim (personal communication) there is a report of a female with three embryos (two females and one male) about five centimeters long without pigmentation pattern (yellowish white). It was brought by Taihei Maru longliner in January 1992, caught off 24°14’–24°59’S and 43°14’-41°33’W. According to Oddone (personal communication), in April 2002, a female with two embryos was found on a boat near Cape Santa Marta Grande (28°46’S-48°40’W). These embryos were about 15 cm long and had a dark color similar to a newborn (Figure 2). Probably the parturition period can occur around April. According to the Gonadosomatic Index, the females presented higher average in January. From February to April, the females had not been caught, and the males presented a little variation of the Gonadosomatic index (Figure 3). Histological analysis will be necessary to determine more precisely the female maturity, that whenever were mature presented only the left uterus developed, although there was not remarkable difference in the weight and dimensions among the ovaries. The male presented both testicles homogeneously developed, with little differences in weight between the pairs, although the left testicle was usually more elongated and narrower than the right one. The Liversomatic Index of the males and females seems highest values in January. For the females, in June it is possible to observe an increasing trend, and for the males the values are more stable (Figure 4). The Liversomatic Index seems to be more related to the concentration of energetic reservoirs, same reported in Querol et al. (2002). In the length-weight relationship, there is a strong correlation between the variables of Disc Width and Total Weight for females, males and clustered sexes (Figure 5), where the Disc Width proved to be more dependable than the length from the tip of the snout to the tip of the tail (Total Length), due to the tail fragility and susceptibility to lose parts, so it was adopted as a pattern measure. It was observed the presence of dermic scutella (Capapé, 1993) in the female skins collected in August and September 2007. A strong correlation between the average of body covered with dermic scutella and weight of the left uterus R²=0,78 (Figure 6) can be related with the influence of female hormone to the presence of the dermic scutella, that appeared most frequently in August and September, 2007, may be the months that the gonad development to the reproduction period began. The males collected in the sample presented the dermic scutella just on the tail. A total of 157 stomachs of P. violacea were analyzed during the studied period. From that total, 99 stomachs were empty (63%) and 58 (37%) presented some contents. Mollusca were the most common group, present in 50% of stomachs with some contents, with predominance of Loligo sp. and unidentified material was present in 26%. Actinopterygii fishes were present in 19% and Crustacea in 17% of stomach contents (Table 2). The occurrence area of the pelagic stingray P. violacea was reported previously by Domingo et al. (2005). In this paper, the occurrence area of the species ranged from 19°30’ to 32°40’ S and 44°30’ to 28°00’ W (always close to continental slope), adding new areas to the literature (Figure 7). 4. Conclusion The analyzed males were mature with measures from 39.7 cm Disc Width on, and 10.5 cm of Clasper Length. When the female gonads were more developed, only the left uterus was developed. Males were most frequent in sets where the fishing gear was placed deeper (up to 800 meters) and the females in low depths (from 60 meters on). The females give birth probably from January to April off Southern Brazil, based on the Gonadosomatic Index and the preterit data of presence of the embryos.
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According to the fishermen, the pelagic stingray prefers artificial attractors like light stick, and baits like squids, the most frequent stomach content. Although Pteroplatytrygon violacea is frequently caught, it is rarely brought on board, because the species is not sold in the fish market. Attaining a high level of accuracy on the studies of this species is difficult, due to the reduced number of samples collected. 5. Acknowledgements We wish to thank all the people who supported this study, especially: Manuel Gonzalez (NUPEC), Luiza Ishikawa Ferreira (PUC-Campinas), Dra. María Cristina Oddone (FURG) for the information and the photos of the embryos, the fishing companies Imaipesca (Mr. Maeda) and Itafish (Mr. Fernando), Jean Miranda; the interns Juliana Silva, Natália Della Fina, Natália Piva, Roberta Schmidt, Pedro Cecílio, Pedro Osse, Eduardo Oliveira and the fishermen Alemão, Dedé, Sandro, Gilberto, Dirceu, Jorge, Dinho e Almir for the sampling and the friendship. The present work was made possible by funding from the Secretaria Especial de Aqüicultura e Pesca da Presidência da Republica do Brasil. References BENSON, A.J., G.A. MacFarlane, J.R. King. 2001. A Phase “0” Review of Elasmobranch Biology, Fisheries, Assessment and Management. Ottawa. Research Document. 2001/129. BROMHEAD, D., S. Graham, J. Kalish. 2003. National Fishery Report 2003 – Australia. IOTC-SC-Inf. 13. Camberra. CAPAPÉ, C. 1993. New data on the reproductive biology of the thorny stingray, Dasyatis centroura (Pisces: Dasyatidae) from off the Tunisian coasts. Environmental Biology of Fishes 38: 7340. CHAPMAN, L. 2001. By-catch in the Tuna Longline Fishery. Secretariat of the Pacific Community. 2nd SPC Heads of Fisheries Meeting. Working Paper 5. New Caledonia. DÁVALOS-DEHULLU, E., E. González-Navarro. 2003. Stomach Content of One Pelagic Ray Dasyatis violacea (Bonaparte, 1832) (Rajiformes: Dasyatidae) from the Gulf of California, Mexico. Oceánides. Baja Califórnia Sur. 18(1): 43-44. DOMINGO, A., R.C. Menni, R. Forselledo. 2005. By-catch of the Pelagic Stingray Dasyatis violacea in Uruguayan Longline Fisheries and Aspects of Distribution in the Southwestern Atlantic. Scientia Marina 69(1):161-166. FIP. 2005. Proyecto FIP. Lineamientos Básicos para desarrollar El Plan de Acción Nacional de Tiburones. Informe Final. Volumen 2: Estado Actual de la Biología y Pesquería de los Condrictios en Chile. Universidad Austral de Chile. Valdivia. FRANCIS, M.P., L.H. Griggs, S.J. Baird. 2001. Pelagic Shark Bycatch in the New Zealand Tuna Longline Fishery. Marine Freshwater Research, 2001, 52, 165-78. IUCN. 2007. More Oceanic Sharks Added to the IUCN Red List. Oxford. England. Disponível em http://www.iucn.org/en/news/archive/2007/02/22_pr_sharks.htm LAMILLA, J.G., G.R. Pequeño, I.U. Kong. 1995. Dasyatis brevis (GARMAN, 1880) Segunda Especie de Dasyatidae Registrada para Chile (Chondrichthyes, Myliobatiformes). Estudios Oceanologicos 14: 23-27. LETOURNEUR, Y, P. Chabanet, P. Durville, M. Taquet, E. Teissier, M. Parmentier, J.C. Quéro, K. Pothin. 2004. An Updated Checklist of the Marine Fish Fauna of Reunion Island, South-Western Indian Ocean. Cybium. 28(3): 199-216. McEACHRAN, J.D., M.R. Carvalho. 2002. FAO Species Identification Guide for Fishery Purposes. The Living Marine Resources of the Western Central Atlantic. Volume 1. Introduction, molluscs, crustaceans, hagfishes, sharks, batoid fishes and chimaeras. Rome. McKINNELL, S., M.P. Seki. 1998. Shark bycatch in the Japanese high seas squid driftnet Fishery in the North Pacific Ocean. Fisheries Research 39 (1998) 127-138. MENNI, R.C., F.H.V. Hazin, R.P. Lessa. 1995. Occurrence of the night shark Carcharhinus signatus, and the pelagic stingray Dasyatis violacea off north-eastern Brazil. Neotropica 41(105−106):105-110. 1886
MOLINA, A.D., R. Sarralde, P. Pallarés, J.C. Santana, R.D. Molina, J. Ariz. 2005. Estimación de Capturas de las Especies Accesorias y de los Descartes en la Pesquería de Cerco de Túnidos Tropicales en el Océano Atlántico Oriental, Entre 2001 y 2004. Collect. Vol. Sci. Pap. ICCAT, 58(1): 385-404. MOLLET, H.F., G.M. Cailliet. 2002. Comparative Population Demography of Elasmobranchs Using Life History Tables, Leslie Matrices and Stage-Based Matrix Models. Marine Freshwater Res. 53:503-516. MUSICK, J. A. 2004. Elasmobranch Fisheries Management Techniques. Chapter 1. Introduction: Management of Sharks and their Relatives (Elasmobranchii). APEC Fisheries Working Group. IUCN. Singapore. OTWAY, N.M., C.J.A. Bradshaw, R.G. Harcourt. 2004. Estimating the Rate of Quasi-Extinction of the Australian Grey Nurse Shark (Carcharias taurus) Population Using Deterministic Age- and StageClassified Models. Biological Conservation. PEACH, M.B., G.W. Rouse. 2004. Phylogenetic Trends in the Abundance and Distribution of Pit Organs of Elasmobranches. Acta Zoologica. 85:233-244. PINEDA, S.D., D.R. Hernández, N.E. Brunetti, B. Jerez. 2002. Morphological Identification of Two Southwest Atlantic Loliginid Squids: Loligo gahi and Loligo sanpaulensis. Rev. Invest. Desarr. Pesq. 15:67-84. QUEROL, M.V.M., E. Querol, N.N.A. Gomes. 2002. Fator de Condição Gonadal, Índice Hepatossomático e Recrutamento como Indicadores do Período de Reprodução de Loricariichthys platymetopon (Osteichthyes, Loricariidae), Bacia do Rio Uruguai Médio, Sul do Brasil. Iheringia, Série Zoológica, Porto Alegre, 92(3): 79-84. ROSENBERGER, L.J. 2001. Pectoral Fin Locomotion in Batoid Fishes: Undulation Versus Oscillation. The Journal of Experimental Biology 204: 379-394. SADOWSKY, V., A.F. Amorim. 1977. Primeiro registro de ocorrência da arraia pelágica Dasyatis violacea (Bonaparte, 1832) nas águas do Atlântico Sul Ocidental. 29ª Reunião Anual-SBPC. Resumos. Suplemento de Ciência e Cultura, SP. 29. (7): 792. SCHWARTZ, F. J. 2005. Tail Spine Characteristics of Stingrays (Order Myliobatiformes) Found in the Northeast Atlantic, Mediterranean, and Black Seas. Electronic Journal of Ichthyology. 1: 1- 9. THOMAS, J. D. 1993. Identification Manual for the Marine Amphipoda: (Gammaridea) I. Common Coral Reef and Rocky Bottom Amphipods of South Florida. Final Report for DEP Contract Number SP290. VAZZOLER, A. E. A. DE M. 1981. Manual de métodos para estudos biológicos de população de peixes. Reprodução e crescimento. Brasilia, CNPq - Programa Nacional de Zoologia. 108p. WARD, P., R.A. Myers. 2005. Shifts in Open-Ocean Fish Communities Coinciding with the Commencement of Commercial Fishing. Ecology, 86(4), 2005, pp. 835-847. WILSON, P. C., J.S. Beckett. 1970. Atlantic Ocean Distribution of the Pelagic Stingray, Dasyatis violacea. Copeia, Vol. 1970, No. 4. pp. 696-707.
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Table 1. Percentage of Clasper Length, Number of Specimens (N) and Clasper Rigidity of pelagic stingray P. violacea. Clasper Length (cm) 10,5-15,0 10,4 9,5-10,3
N 129 4 10
Clasper Rigid (%) 100 50 0
Clasper Not Rigid (%) 0 50 100
Table 2. Feeding items found in stomach contents of 58 pelagic stingray P. violacea. Items Phyllum Arthopoda Class Crustacea Order Isopoda Order Amphipoda Order Euphausiacea Order Stomatopoda Phyllum Mollusca Class Cephalopoda Order Theutoidea Family Loliginidae Loligo spp. Order Octopoda Family Octopodidae Octopus sp. Phyllum Chordata Class Actinopterygii Unidentified material
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30 25
Average
20 15 10 5 0 38
40
42
44
46
48
50
52
54
56
58
60
62
Disc Width DW male DW female
Figure 1. Disc width frequency distribution of male and female (in centimeters).
Figure 2. Female of P. violacea with embryos caught in April, 2002.
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64
66
68
5,0
GSI
4,0 3,0 2,0 1,0
au g/ 0 se 6 p/ 06 oc t/0 no 6 v/ 0 de 6 c/ 06 ja n/ 07 fe b/ 0 m 7 ar /0 7 ap r/0 m 7 ay /0 7 ju n/ 07 ju l/0 au 7 g/ 0 se 7 p/ 07
0,0
Month GSI Male GSI Female Figure 3. Average Gonadossomatic Index (GSI) by sex and month.
12,0
Average LSI
10,0 8,0 6,0 4,0 2,0
au
g/ 06 se p/ 06 oc t /0 no 6 v/ 0 de 6 c/ 06 ja n/ 07 fe b/ 0 m 7 ar /0 7 ap r/0 m 7 ay /0 7 ju n/ 07 ju l/0 au 7 g/ 07 se p/ 07
0,0
Month LSI Male LSI Female Figure 4. Variation of Liversomatic Index (LSI) by sex and month.
8000
4000
8000
7000
7000
6000
6000
3000 3,0056
Wt
5000
Wt
2,9469
y = 0,0219x 2 R = 0,9573
4000
y = 0,0279x 2 R = 0,7662
2000
Wt
2,9518
2
R = 0,8788
4000 3000
3000 2000
2000
1000
1000
1000 0
A
y = 0,0273x
5000
0
0 0
10
20
30
40
Disc Width
50
60
70
B
0
10
20
30 Disc Width
40
50
60
C
0
10
20
30
40
50
60
70
Disc Width
Figure 5. Length/Weight relationship of the P. violacea collected from August 2006-August 2007: A female, B Male and C: clustered. 1890
60
% dermic scutella
50 40 30 20 2
10
R = 0,7888
0 0
20
40
60
80
100
120
left uterus weight
Figure 6. Relationship between left uterus weight and body (dorsal) percentage covered with dermic scutella.
Figure 7. P. violacea distribution in the southwestern Atlantic Ocean. The squares indicate de areas of occurrence reported in this study, and the crosses indicate P. violacea with embryos in April 2002 according to Amorim (Pers. Comm.) and Oddone (Pers. Comm.).
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