INTRODUCTION
The gulper shark Centrophorus granulosus (Schneider, 1801) is a widespread deepwater species, from the western and eastern Atlantic and Mediterranean, western Indian Ocean, and western Pacific out onto the Pacific Plate (Musick et al., Reference Musick, Harbin, Compagno and Carrier2004). In both Mediterranean and eastern Atlantic European areas, the gulper shark is frequently reported in different papers about fisheries, distribution or assemblages (Alagador & Costa, Reference Alagador and Costa2003; Politou et al., 2003; Sion et al., Reference Sion, Bozzano, D'Onghia, Capezzuto and Panza2004; Figueiredo & Bordalo, Reference Figueiredo and Bordalo2005).
The aim of this paper is to provide biological data relating to C. granulosus caught in Galicia waters (north-eastern Atlantic) in order to suggest a best discrimination within the Centrophorus species complex.
MATERIALS AND METHODS
This investigation was made as part of the EC FAIR project: Developing deep-water fisheries (CT 95/655), and preliminary results were given by Casas et al. (Reference Casas, Piñeiro and Bañón2001).
Specimens were captured in waters of 500–1300 m depth during two experimental surveys with bottom trawl and longline carried out on commercial vessels in the period 1996–1998, along the continental slope of Galician waters (ICES Divisions VIIIc and IXa) and the Galician Bank (ICES Division IXb). Additional information was provided by sampling the catches of commercial longliners.
Specimens were identified, counted and weighted on board. Total length (TL) by sex was measured to the nearest centimetre, from the tip of the snout to the extremity of the upper lobe of the tail when depressed, and the maturity determined following the method described by Stehmann (Reference Stehmann1987; Table 1). Length at maturity, ovarian fecundity, uterine fecundity and size at birth were also recorded when possible. Ovarian fecundity was estimated counting the number of mature oocytes in mature females (Stage C). Uterine fecundity was determined from pregnant females with well-formed embryos with reduced yolk sacs (Stage F). Size at birth was estimated from measuring near-term and term embryos.
Maturity scale used during surveys (Stehman, 1987).
RESULTS
Centrophorus granulosus
Centrophorus granulosus is more abundant in the Galician Bank (IXb Division), where we caught the majority of the specimens with longline.
A total of 268 specimens were caught between 741–1211 m depth, including 265 with longline and 3 with bottom trawl. Length–frequency data were available for 268 specimens (Figure 1). They ranged from 44 to 166 cm; with males between 73 and 127 cm (N = 12) and females between 44 and 166 cm (N = 256). Females outnumbered males (sex ratio male:female = 1:21.3) and the χ2-test showed that this difference regarding 1:1 was very highly significant (P < 0.001). The size at 50% maturity was 147 cm for females. From males, size at 50% maturity could not be determined due to the low number of males in the sampling. The smallest mature female measured 138 cm and the largest immature female 153 cm, whereas the smallest mature male measured 118 cm and the largest immature male 115 cm.
Length distribution in catches of Centrophorus granulosus.
Of the 10 males examined, 7 (70%) were immature (Stage B) and 3 (30%) were mature (Stage C). The bathymetric distribution by maturity stages in females is illustrated in Figure 2. Of the 156 females examined, 76 (49%) were immature (Stages A–B), 30 (19%) had ripe oocytes (Stage C), 49 (31%) were gravid, with embryos at various stages of development (Stages D–F) and only 1 (1%) were postnatal (Stage G).
Distribution in number of maturity stages according to depth in females of Centrophorus granulosus.
Ovarian fecundity observed in 37 mature specimens (Stages C–F) ranged from 1 to 10 ova, with a mean of 5 ova per female. This number varied between 1 and 5 in the right ovary (mean = 2.5) and between 1 and 8 in the left ovary (mean = 2.5). The diameter of mature oocytes measured in 25 females ranged from 55 to 80 mm (mean = 69 mm).
Uterine fecundity from 32 gravid females ranged from 1 to 6 embryos, with a mean of 3 embryos. Females exhibiting a single or two functional uterus were recorded. The size at birth, based on 13 near-term embryos, ranged from 35–47 cm with a mean of 40 cm.
DISCUSSION
The obtained biological data differ from those compiled in the literature (Table 2) suggesting different populations or different species.
Comparison of reproductive Atlantic specimen data of Centrophorus granulosus.
* precaudal length; E. Medit., eastern Mediterranean; C. Medit., central Mediterranean; W. Medit., western Mediterranean.
The maximum recorded size of 166 cm is greater than Mediterranean specimens of 128 cm (Capapé et al., 1985), greater also than 96 or 100 cm of western Atlantic specimens (Carpenter, Reference Carpenter2002; Kiraly et al., Reference Kiraly, Moore and Jasinski2003) and than 105–110 cm of the general information for this species (Compagno et al., Reference Compagno, Dando and Fowier2005).
Most of the results about reproductive biology differ from those compiled in previous research papers.
Size at 50% maturity in C. granulosus was 147 cm for females, much higher than for Mediterranean specimens, of 90 cm (Capapé, Reference Capapé1985) and 94 cm (Guallart, Reference Guallart1998).
The range of 1–10 mature oocytes is higher than 1–2 reported in the literature and their diameter, between 55–80 mm is lower than reported previously (Capapé, Reference Capapé1985; Megalofonou & Chatzispyrou, 2006). Embryo sizes are slightly greater than reported in other works (Gullart & Vicent, 2001; Compagno et al., Reference Compagno, Dando and Fowier2005) and the number of embryos, up to 6 by female, is greater than 1–2 observed in other areas (Capapé, Reference Capapé1985; Guallart, Reference Guallart1998; Guallart & Vicent, Reference Guallart and Vicent2001; Compagno et al., Reference Compagno, Dando and Fowier2005). The vitellogenesis and gestation of C. granulosus are continuous, developing simultaneously oocytes and embryos and have only one functional uterus in which a single embryo (Capapé, Reference Capapé1974, Reference Capapé1985; Guallart, Reference Guallart1998; Golani & Pisanty, Reference Golani and Pisanty2000) or up to two (Compagno et al., Reference Compagno, Dando and Fowier2005) is developed.
In our sample, there were no females with a single mature oocyte and only two (5.4%) had two mature oocytes. Of 32 females with embryos, 6 of them (19%) between 147 and 155 cm had 1 embryo and 9 (28%) between 142 and 159 cm had 2, but all these had in their ovaries between 2 and 10 mature oocytes.
The differences found in size and reproductive parameters in Galician specimens could indicate a marked distinctiveness of Mediterranean and Atlantic populations. Geographical variation in reproductive and growth parameters has been reported for elasmobranch species (Leloup & Olivereau, Reference Leloup and Olivereau1951; Pawson & Ellis, Reference Pawson and Ellis2005). Different length range occurs also in another deep-water shark, the Portuguese dogfish Centroscymnus coelolepis, usually recorded in the Mediterranean Sea, which are much smaller than those reported in the Atlantic and Pacific Oceans (Sion et al., Reference Sion, Bozzano, D'Onghia, Capezzuto and Panza2004; Tosti et al., 2006), indicating different populations isolated by geographical areas and physical barriers such as the Strait of Gibraltar.
The hypothesis of a misidentification was also taken into account. According to the biological data, the most similar Centrophorus species and therefore our principal candidate for this possible misidentification is the Taiwan gulper shark Centrophorus niaukang Teng, 1959. This is probably the larger Centrophorus species, with maximum size to about 170 cm TL, 1–6 pups/litter, size at birth to 30–45 cm TL, males matures at 90–110 cm TL and females at 130–149 cm TL (Yano & Kugai, Reference Yano and Kugai1993; Fowler, Reference Fowler2003; Compagno et al., Reference Compagno, Dando and Fowier2005).
There is little information published about C niaukang. Their distribution is wide, if sporadic, in the Atlantic and Indo-West Pacific. In the north-eastern Atlantic they were reported between 29° and 31° N (Muñoz-Chapuli & Ramos, 1989) and, toward the north, Compagno et al. (Reference Compagno, Dando and Fowier2005) question their distribution in Iberian Peninsula waters. In the north-western Atlantic, Kiraly et al. (Reference Kiraly, Moore and Jasinski2003) reported from USA specimens of C. granulosus, with litters consisting of 4–6 pups that measure approximately 35 cm; we consider that these could be misidentifications of C. niaukang, also described in this paper. The other C. niaukang biological parameters (maximum reported size of 169 cm, males mature at 110 cm and females at 146 cm) are very similar to C. granulosus of Galician waters.
The genus Centrophorus needs a revision and until then, and according to our results, it is probable that C. granulosus is distributed only in the Mediterranean Sea, as Guallart et al. (Reference Guallart, Serena, Mancusi, Casper, Burgess, Ebert, Clarke and Stenberg2006) has already pointed out and therefore, the species present in Galician waters could be C. niaukang. The recognition of C. niaukang in the eastern Atlantic is the key to resolve some of the taxonomic confusion surrounding the genus Centrophorus in the literature.
