Reproductive Biology of the Common Torpedo, Torpedo Torpedo (Linnaeus, 1758) (Pisces, Torpedinidae) from the Coast of Senegal (Eastern Tropical Atlantic)

Miscel.lania Zoologica 23.1 (2000) 9 - -- Reproductive biology of the common torpedo, Torpedo torpedo (Linnaeus, 1758) (Pisces, Torpedinidae) from the coast of Senegal (Eastern Tropical Atlantic)

C. Capapé, A. A. Seck & Y. Diatta

Capape, C., Seck, A. A. & Diatta, Y., 2000. Reproductive biology of the cornrnon torpedo, Torpedo torpedo (Linnaeus, 1758) (Pisces, Torpedinidae) frorn the coast of Senegal (Eastern Tropical Atlantic). Misc. ZOOI., 23.1: 9-21.

Reproductive biology of the common torpedo, Torpedo torpedo (Linnaeus, 1758) (Pisces, Torpedinidae) from the coast of Senegal (Eastern Tropical Atlantic).- Among the five species of genus Torpedo recorded from the coast of Senegal, the common torpedo, Torpedo torpedo is that most cornrnonly caught in the area. Adult males and fernales studied were over 300 rnrn and 310 rnrn total length (TL), respectively, with the largest male and the largest female recorded being 445 rnrn and 550 rnrn TL respectively. Size at birth was between 102 and 125 mrn TL (mean 112.12 mrn; s.e.rn. 5.58). Weight of eggs ranged frorn 6.2 to 8.0 g (rnean: 7.07; s.e.m. 0.5). Gestation lasts longer, from 6 to 8 rnonths, than in the Mediterranean specimens. A calculated chernical balance of development based on rnean dry weights of the fully developed fetuses and ripe oocytes was 1.58 for 7: torpedo. This value shows that this torpedinid is not a pure lecithotrophic species, and the role of the rnother during gestation is not negligible. The fecundity (s.1.) of 7: torpedo ranges from 5 to 28 in Senegalese specimens as cornpared to 1 to 9 in Mediterranean specirnens. Male ernbryos and fully developed fetuses are more nurnerous than fernales. Among the free-living specimens, nurnber of males and fernales is practically the same. The cornrnon torpedos from the coast of Senegal are larger and the eggs are heavier than Mediterranean specirnens.

Key words: Pisces, Torpedinidae, Torpedo torpedo, Reproductive biology, Senegal, Eastern Tropical Atlantic.

(Rebut: 28 XII 99; Acceptació condicional: 27 111 00; Acc. definitiva: 20 VI 00)

Christian Capapé, Laboratoire d'lchtyologie, Université Montpellier 11, Sciences et Techniques du Languedoc, 34095 Montpellier cedex 05, France (France). - A. A. Seck, lnstitut fondamental d'Afrique noire Cheikh Anta Diop, Musée de la Mel; Gorée, Sénégal (Senegal).- Y: Diatta, Département de Biologie animale, Faculté des Sciences et Techniques, Université Cheikh Anta Diop, BP 5005, Dakal; Sénégal (Senegal).

ISSN: 021 1-6529 O 2000 Museu de Zoologia Capapé et al. - lntroduction Specimens from the observed sample were weighed to the nearest gram. Measurements According to CADENAT(1950) and CAPAPÉ & also included clasper length (CL, mm) from DESOVITER(1990), five species of genus Torpedo the forward rim of the pelvic girdle to the have been recorded from the coast of Senegal tip of the claspers according to COLLENOT (eastern tropical Atlantic): the common (1969), and diameter or length and weight torpedo, Torpedo torpedo; the marbled to the nearest decigram for oocytes, eggs, torpedo, T: marmorata; the Bauchot's torpedo embryos and fetuses. Developing oocytes ray T: bauchotae; the electric ray, T: nobiliana were measured while they were still in the and the McKay's torpedo ray 1: mackayana. ovaries, whilst ripe oocytes were removed Among these species, T. torpedo is from the ovaries and undeveloppeu eggs, currently caught in this marine locality but embryos and fetuses were removed from little is known about its reproductive the uteri, then counted, measured and biology. Only scarce information was weighed. Fetuses and also embryos were summarized by CAPAPE et al. (1995). New sexed whenever possible. records of specimens in the marine area allow The onset of sexual maturity was deter- us to expand these previous data. In this mined when possible by the relationship paper, we also give details on size at sexual between clasper length and total length. The maturity, size at birth, reproduction, linear regression was expressed in decimal fecundity and sex-ratio of the common logarithmic coordinates. Correlations were torpedo. These data are compared and assessed by least-squares regression. According contrasted with other data previously to Bnss et al. (1975) and STEVENS & LYLE(1989), provided by QUIGNARD(1973) and QUIGNARD the claspers of juvenile males are short and & CAPAPE(1974) from specimens caught off flexible. Males are considered to be mature the Tunisian coasts (Central Mediterranean). when the claspers are elongated and calcified. These features were verified in torpedinids to avoid underestimation of size at maturity. Material and methods Size of females at sexual maturity was determined from the condition of the ovaries The torpedinids were caught off the Cape and the morphology of the reproductive Verde Peninsula in commercial gill-nets from tract. Three categories of females were 1994 to 1998. A total of 183 specimens were considered: juveniles, having small whitish observed, including 91 males and 92 females. ovaries with oocytes of microscopic size, The specimens were generally captured by membranous oviducts and inconspicuous demersal gill-nets and by anglers, in the nidamental glands; subadults with ovaries shallow coastal waters ata depth of 80 m to showing translucent oocytes and a dif- a maximum, on sandy andlor muddy ferentiated genital duct; and adults having bottoms, but rarely among macroalgae. They functional ovaries with yellow-yolked oocytes were landed at the fishing site of Ouakam, and a fully developed genital duct. 5 km from Dakar, where they were examined To investigate the embryonic develop- (fig. 1). ment and the role of the mother during The month of collection, the sex and gestation, a chemical balance of develop- condition of the observed specimens are ment (CBD) was considered. CBD is based described in table 1. In addition, 152 embryos on the mean dry weight of fertilized eggs and 81 fetuses were studied. Embryos still and fully developed fetuses. CBD can be had an umbilical stalk and a yolk stalk. These computed as the mean dry weight of fully features were completely reabsorbed in fully developed fetuses divided by the mean dry developed fetuses, and a scar marked the weight of fertilized eggs. Water content of site of the umbilical stalk. 50% in ova and 75% in fully developped T: torpedo is caught al1 year round, but fetuses can be taken as standard values, adult individuals of both sexes are most based' on chemical analyses of the small- frequently captured from March to October. spotted catshark, Scyliorhinus canicula, by The specimens were measured to the MELLINGER& WRISEZ (1989). CBD is a tentative nearest millimetre for total length (TL). estimate. Miscel.lania Zoologica 23.1 (2000) 11

C -50 ------___..-..___.--___.-- * ,'- .," l. Yoff -.---__e-- 12 Capapé et al. - - - A-

Table l. Monthly collection of Torpedo torpedo caught off the coast of Senegal. Recolección mensual de Torpedo torpedo capturados frente a la costa de Senegal.

Months Jan. Feb. Mar. Apr. May. Jun. Jul. Aug. Sep. Oct. Nov. Dec. Total Males Newborn - - - - 610 - -16 Juvenile 2 3 6 - 1 4 6 2 - 2 - - 26 Subadult - 3 3 2 1 1 1 2 - - - - 13 Adult -39783231--- 36 Total 2 918 9108 9 7 712 - -91 Females m----

Subadult 2 1 3 2 2 312 53 6 5 9 22 14 27 31 26

Results throughout life. All the males having over 300 mm TL were adult. The largest male was Onset of sexual maturity 445 mm TL and weighed 1,400 g.

Males Females The CL to TL relationship (fig. 2) shows two The smallest rnature female which also was inflexions indicating the three stages of sexual the smallest gravid female was 310 mm in development in males. The first stage includes length. Among the adults, 19 were non- the juveniles and the relationship is: gravid and 25 were gravid. Among the lag [CL] = 0.764 lag TL - 0.143 former, 11 had developing oocytes in their n = 26, r = 0.899 ovari, 7 had ripe oocytes, and one specimen, The second stage concerns the subadults which was probably in a quiescent phase, with: did not exhibit any vitellogenetic activity. 10g [CL] = 2.049 lag TL - 3.169 Of the 25 gravid females, 10 possessed n = 13, r = 0.982 fertilized eggs or ova in their uteri, 10 had The third phase concerns the aduits, with: early-stage embryos and 5 presented fully log [CL] = 0.625 log TL + 0.067 developed fetuses. Females over 500 mm TL n = 19, r = 0.968 were often captured. The largest female vvas According to these relations, the claspers 550 mm TL and weighed 2,305 g. grew fastest during the second stage. Juveniles and adults had short, uncalcified flexible Reproduction claspers. Those of adults were elongated, calcified, rigid and functional. The third The common torpedo is an aplacental relation shows that they grew allometrically viviparous species. The two ovaries and the Miscel.lania Zoologica 23.1 (2000) 13 -- .- -

1.4 1 I I I I I I) 2.1 2.2 2.3 2.4 2.5 2.6 2.7 log TL

Fig. 2. Clasper length (CL) versus total length (T in decimal logarithmic co-ordinates. Longitud de los apéndices copuladores en relación con la Ion macho de Torpedo torpedo expresado en coordenadas de logaritmo decimal.

two uteri are both functional. The ovaries observations suggest that gestation begins produced cohorts of oocytes similar in size in spring and ends in late summer and early and in weight. One of these cohorts autumn. Gestation probably lasts from a developed into ripe oocytes, the other minimum of 6 months to a maximum of oocytes degenerated. The diameter and the 8 months. weight of ripe oocytes ready to be ovulated During gestation the ovaries were in a increased as the size of the female grew resting phase. In contrast, 14 adult females (table 2). However, these oocytes features exhibited a phase of active vitellogenic reduced as the number of oocytes increased. activity with developing or ripe oocytes in This was also the case for fertilized eggs their ovaries, whilst their uteri were in a found in the uteri (table 3). resting phase. Vitellogenetic activity lasted Table 4 reveals that al1 the pregnant approximatively six months and the complete femalcs were caught from April to October. reproductive cycle did not exceed one year. Females with oocytes and with fertilized eggs Developing and ripe oocytes were slightly in their uteri were captured in April and in more numerous in the left ovary than in the May and females with fully developed right. The opposite was observed for eggs, fetuses in September and in October. These embryos or fetuses. In a single specimen, 14 Capapé et al.

Table 2. Oocytes features according to total length (TL, mm) in adult female Torpedo torpedo from the coast of Senegal. Característícas de los oocitos en función de la longitud total (TL, mm) en hembras adultas de Torpedo torpedo de la costa de Senegal,

Diameter (mm) Weíght (g) TL N Range Mean s.e.m. Ranqe Mean s.e.m.

these features were equally distributed in each uterus. In al1 cases, the weight of fully developed fetuses was significantly higher that the weight of the fertilized ovum (t- test, P < 0.05). Eggs, embryos and fetuses were not encapsulated but were free in the uteri. Throughout gestation, the uterine contents were protected by a jelly-like structure.

Size at birth

The total length of 76 fully developed fetuses ranged from 100 mm to 125 mm (R = 112.13 mm; s.e.m. 5.58 ). Twenty-six individuals, 16 males and 10 females were collected by scuba divers in shore waters between 5 and 10 m depth, during September and October. They exhibited an unhealed scar on their ventral face and a conspicuous interna1 vitelline vesicle. These specimens were probably the young of the year. The smallest free living specimens observed ranged from 102 mm to 118 mm.

Chemical balance of develo~ment

Fresh weights of the 17 largest ova ranged from 6.2 g to 8.0 g (X = 7.07, s.e.m. 0.53) and of 81 fully developed fetuses from Miscel.lania Zoologica 23.1 (2000)

Table 4. Reproductive cycle of female Torpedo torpedo, condition of ovaries and uteri during gestation: M. Month of capture; N. Number of females; F. Size range of females (TL, mm); Ova. Ovarian activity; Ooc. Oocyte condition; Ood. Oocyte diameter range (mm); Uc. Uteri content; Ucl. Uteri content lenght range (TL, mm). Ciclo reproductor de la hembra de Torpedo torpedo, estado de los ovarios y útero durante la gestación: M. Mes de captura; N. Numero de hembras; E Variación de la talla de las hembras (TL, mm); Ova. Actividad ovárica; Ooc. Desarrollo de los oocitos; Ood. Variación del diámetro de los oocitos (rnm); Uc. Contenido del útero; Ucl.

January 2 345-455 vitellogenesis developing 15-18 resting - February 2 325-335 vitellogenesis developing 17-20 resting -

July 4 340-505 resting - embryos 35-44

August 2 480-500 resting -- - embryos 55-63

September 3 41 - fetuses 102-115 fetuses 105-115

December 4 500-535

20.5g to 25.5g (X = 22.23, s.e.m. 0.87). to 550 mm. UF ranged from 5 to 20 (X = 3.88, CBD, based on mean dry weights calculated s.e.m. 3.53). The relationship between UF for Torpedo torpedo, is 1.58. and TL is: UF = 0.035 TL - 1.252, n = 24, r = 0.741 Fecundity These two types of fecundity are correlat- ed with females TL and they slowly increase Ovarian fecundity (OF) was based on the with females size (fig. 3). number of ripe oocytes counted in 19 females, their TL ranging from 325 to Sex ratio 535 mm. OF ranged from 10 to 28 (R =16.84, s.e.m. 4.71). ihe relationship between OF Table 5 shows that among the embryos and and female TL was: the fully developed fetuses, males were more OF = 0.058TL - 8.395, n = 19, r = 0.053 abundant than females. This was also true However, uterine fecundity (UF) based for juveniles, but was not the case for on the number of fertilized eggs, embryos subadults and adults. The sex ratio of the or fully developed fetuses was counted in uterine contents in individual females was 25 specimens, their TL ranging from 31 0 mm similar to the mean sex ratio for uterine 16 Capapé et al.

N 30 • Ripe oocytes • Embryos or fetuses n Eggs 25 •

• •

n • A 20 q n n q q z!, • n qq 15 n q • n n •

q n n • q Alk 10 • • n

350 400 450 500 550 LT (mm)

Number of ripe oocytes, eggs, embryos and/or fetuses versus total length (TL, mm) in female Torpedo torpedo. Número de oocitos maduros, embriones y/o fetos en relación ala longitud total (TL, en hembras de Torpedo torpedo.

contents of .all gravid females. Among the hypohaline and hyperhaline lagoons and free-living specimens, the numbers of females estilaries (BEN BRAHIM et al, 1998; PANDARE et and males was practically the same. in the al., 1997). total sample of 363 specimens, the males Off Senegal, size at first sexual maturity were significantly more abundant than the was closely related in both sexes. Hovvever, females (x2, P < 0.05) and the pooled ratio the females were generally larger and heavier was 1.10 (9:d). than the males. Off Naples, Lo BIANCO (1899) noted that the smallest gravid female was 230 mm TL and the largest female was Discussion 450 mm TL. In Tunisian waters, specimens of both sexes were adults over 190 mm TL The common torpedo is an Atlanto-Mediterra- (QUIGNARD, 1973; QUIGNARD & CAPAPÉ, 1974). nean species that generally prefers warm- The largest male was 390 mm TL and weighed temperate and subtropical waters. in this area, 848 g, the largest female was 410 mm TL and T torpedo is one of the rare elasmobranch weighed 1,005 g, but the heaviest female species which enters and reproduces in both weighed 1,254 g and was 390 mm in TL. Miscel•lània Zoològica 23.1 (2000) 17

could also explain why the common torpedos Torpedo torpedo sex ratio for from the Senegalese coast are larger than those each category of specimens and for of the Mediterranean (s.1.). That ova of heavier the total same:ple N}. Numberm of weight could produce specimens of greater emales; N{. Number of males; R. weight and size may be concluded. These Ratio observations show that the common torpedos Porcentaje de sexos de Torpedo from Senegalese waters are on the whole torpedo para cada categoría de larger and heavier than the Mediterranean individuos y para ei total de Ia muestra:• specimens. N. Número de hembras; N Número These intraspecific variations in size were also observed among oviparous elasmo- e machos; R. Ratio (Q d). branch species, such as the small-spotted catshark S. canícula. The Mediterranean Ncr specimens appear to be smaller than those of the Atlantic because they mature at a smaller size {LELOUP & OLIVEREAU, 1951; 58 1:1.29 MELLINGER, 1966, 1989; COLLENOT, 1969). LELOUP 8t OLIVEREAU (1951) stated that these 44 1:1.19 intraspecific variations are related to 102 1:1.24 environmental influences, especially light and temperature, on growth. On the contrary, Dono (1983) emphasized that 16 1.1..60 nothing is known about environmental 26 1:1.33 influences on reproduction in viviparous 13 1.38:1 species. lt is therefore interesting to note that in a closely related torpedinid, T. 1.22:1 marmorata there are no intraspecific 91 1.01:1. variations in size between specimens from the Bay of Biscay (MELLINGER, 1971), specimens 193 .1.10 from the Tunisian coasts (CAPAPÉ, 1979) and specimens captured off the coast of Senegal (unpublished data). ln T torpedo from the Senegalese coast, Our observations show that birth occurred as in all torpedinid species studied to date, when term pups were between 102 and oocytes and/or eggs, embryos, and fully 125 mm and weight at birth was between developed fetuses were more numerous on 20.5 and 25.5 g. Off Naples, size at birth ranged the left side than on the right. MELLINGER from 80 mm (Lo BIANCO, 1899) to 88 mm (RANZI, (1974) and QUIGNARD & CAPAPÉ (1974) pointed 1932). This author added that average weight out in T marmorata and in T torpedo at birth was 13.37 g. ln Tunisian waters, respectively that an asymmetry of abdominal QUIGNARD 8t CAPAPÉ (1974) found that size at viscera exists. This morphological character birth was between 80 and 97 mm and weight is due to the fact that the right genital tract at birth between 9 and 16 g. is more developed than the left. The intraspecific geographic variations of A 6-8 months gestation period in the size and weight at birth as a function of the common torpedo off the Senegalese coast marine area are probably related to ova could be considered a possible hypothesis. weight which in turn is subject to variation This period was longer than that of the according to the marine locality (table 6). Mediterranean specimens which generally did Off Senegal, the ova weight ranged from not exceed four months (Lo BIANCO, 1888, 1899; 6.2 to 8.0 g = 7.07 g}. Off Naples, RANZI RANZI, 1932; QUIGNARD & CAPAPÉ, 1974). According (1932) noted that this parameter ranged from to these authors, females produced their brood 5.02 to 6.53 g 6.34 g}. ln Tunisian waters, at the end of August in these areas. The QUIGNARD 8t CAPAPÉ (1974) noted that it ranged parturition occurred during September and from 2 to 7 g (5-< = 4.182). These differences October off the Senegalese coast. 18 Capapé et al.

Vitellogenesis does not proceed in parallel of 0.5 for two squatinids from the Tunisian with gestation. Moreover, the females exhibit coasts. They concluded that Squatina is a a block to oocyte growth during gestation. purely lecithrotrophic genus where the role Egg capsules are lacking. These phenomena of the mother during gestation is not are the rule in torpedinids according to important. On the other hand, the CBD of MELLINGER(1981, 1989). They were also the spiny butterfly ray, Gymnura altavela observed in other elasmobranch species, from the same marine area, 30.6, is the generally those belonging to the family highest value ever computed in elasmo- Squalidae such as Centroscymnus spp. branchs (CAPAPÉet al., 1992). It is a (YANO& TANAKA,1988) and Centrophorus consequence of trophonemata activity granulosus (CAPAPÉ,1985) and to family during gestation and embryonic nutrition. Oxynotidae as Oxynotus centrina (CAPAPÉet It gives an estimate of mother-derived al., 1999). Consequently, the duration of organic molecules to embryonic growth. It the reproductive cycle remains particularly is a case of matrotrophy according to the long in torpedinids whatever the species definitions of WOURMS(1977, 1981) and and whatever the area. The common WOURMSet al. (1988). The computed CBD of torpedo achieves an annual reproductive the common torpedo is 1.58 according to cycle in both Tunisian and Senegalese the theoretical values given by MELLINGER& waters. MELLINGER(1971) stated that the WRISEZ(1989). However, if using the data of reproductive cycle of the marbled electric RANZI (1932), ¡.e. 43% water in ova and 83% ray from the Bay of Biscay lasted two years in newborns of this species, CBD should be at a minimum, CAPAPÉ (1979) emphasized 0.8 for specimens from Naples and 1.10 for that it probably lasted three years for the those from Senegal. These CBD values were specimens from the Tunissian coasts. closely related whatever the marine locality. CAPAPÉet al. (1990) calculated a CBD value Both values show that 7: torpedo is not a Miscel.lania Zoologica 23.1 (2000) pure lecithotrophic species and the role of tud total (TL) superior a 300 mm y 310 mm the mother during gestation is not negligible. respectivamente, la longitud total del ma- Ovarian fecundity is a little higher than cho y la hembra más largos recolectados fue uterine fecundity. This phenomenon is due de 445 mm y 550 mm respectivamente. El to the fact that some ripe oocytes were not tamaño al nacer era entre 102 y 125 mm TL ovulated and were degenerated. Moreover, (R = 112.12 mm; s.e.m. 5,58). El peso de los some gravid females lost their brood when huevos variaba de 6,2 a 8,O g (X = 7,07; caught. Off Naples, Lo BIANCO(1888) stated s.e.m. 0,5) (tablas 2, 3). La gestación dura that common torpedos bore from 3 to 6 más, de 6 a 8 meses, que en los individuos embryos. Moreover, in 1899, he pointed out del Mediterráneo (tabla 4). Un balance quí- a relation between female size and fecundity. mico calculado de desarrollo basado en la According to QUIGNARD& CAPAPÉ(1974), in media del peso seco de todos los fetos com- the 7: torpedo from the Tunisian coasts, pletamente desarrollados y los oocitos ma- ovarian fecundity ranged from 1 to 15 (mean duros fue de 1.58 en T. torpedo. Este valor 4.32) and the uterine fecundity from 1 to 9 indica que este torpedínido no es una espe- (mean 3.38). Both types of fecundity were cie lecitotrófica pura, y que el papel de la lower in the common torpedo from the madre durante la gestación no es negligible. Mediterranean than in specimens from the La fecundidad (s.1.) de 7: torpedo varíaba Senegalese coast. This is probably related to entre 5 y 28 en los invididuos senegaleses y the size difference observed from specimens de 1 a 9 en los mediterráneos (fig. 3). Los of these two marine localities (table 6). embriones masculinos y fetos completamen- The sex-ratio changes of specimens from te desarrollados son más numerosos que los the coast of Senegal agree with the ob- femeninos. Entre los individuos que viven servations of QUIGNARD& CAPAPÉ (1974). Males libres, el número de machos y hembras es embryos, fully developed fetuses and prácticamente el mismo (tabla 5). Los torpe- juveniles are more numerous than females. do común de la costa del Senegal son más The opposite however is seen in subadults largos y sus huevos pesan más que en los and adults. These changes in sex-ratio are del Mediterráneo (tabla 6). not due to a higher rate of mortality in males than in the females but rather to the segregation of the sexes at different depths Acknowledgements during certain stages of the reproductive cycle. During the breeding period, the adult females The authors wish to thank the fishermen generally approach the coastal waters: from the fishing site of Ouakam (Cape Verde numerous gravid specimens were observed peninsula, Senegal) who provided the in our sample, some of which were practically material, and the two referees for their useful at the end of gestation. This phenomenon and helpful comments on the manuscript. seems to be the rule among elasmobranch species (CASTRO,1993; CAPAPÉ et al, 1995). References

Resumen Bnss A. J., D'AUBREYJ. D. & KISTNASAMY,N., 1975. Sharks of the east coast of southern Biología reproductiva del torpedo común Africa. 111. The families Carcharhinidae Torpedo torpedo (Linnaeus, 7758) (Pisces, (excluding Mustelusand Carcharhinus) and Torpedinidae) de la costa de Senegal (Atlán- Sphyrnidae. lnvestl Rep. (S. Afr. Ass. mar. tico tropical oriental) Biol. Res.), 38: 1-100. BENBRAHIM, R., SECK, A. A. & CAPAPE,C., 1998. Entre las cinco especies del género Torpedo Albinisme chez la torpille ocellée, Torpedo recolectadas en las costas del Senegal, el (Torpedo) torpedo (Linnaeus, 1758). torpedo común, Torpedo torpedo es el Cybium, 22: 83-86. torpedínido más recolectado en esta área CAPAPE,C., 1979. La torpille marbrée, Torpedo (fig. 1, tabla 1). Los machos (fig. 2) y hem- marmorata Risso, 1810 (Pisces, Rajiformes) bras adultos recolectados tenían una longi- des c6tes tunisiennes: nouvelles données Capapé et al.

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