Reproductive Biology of the Island Grouper (Mycteroperca Fusca) in the Canary Islands, Northwest Coast of Africa

Scientia Marina 74(3) September 2010, 613-619, Barcelona (Spain) ISSN: 0214-8358 doi: 10.3989/scimar.2010.74n3613 Reproductive biology of the island grouper (Mycteroperca fusca) in the Canary Islands, northwest coast of Africa ROCÍO BUSTOS, ÁNGEL LUQUE and JOSÉ G. PAJUELO Departamento de Biología, Universidad de Las Palmas de Gran Canaria, Campus de Tafira, 35017 Las Palmas de Gran Canaria, Spain. E-mail: [email protected] SUMMARY: This is the first time that the reproductive characteristics of Mycteroperca fusca have been analyzed over the whole area of its distribution, using the parameter of the histological analysis of the gonads. This species is a protogynous hermaphrodite with a marked predominance of females (1:4.9). The males and females displayed marked differences in the distribution of the sizes. The females were distributed over all the size ranges analyzed (229-725 mm total length), whereas the males were observed within the larger sizes, as of 428 mm. One transitional specimen (610 mm total length) was observed. The size at which the females first reached sexual maturity was 335 mm total length whereas the size at which 95% of females reached sexual maturity was 398 mm total length. The average size at which 50% of the females had inverted to the male condition was found to be 678 mm total length. The range of sizes at which the process of sexual inversion took place was broad, between 428 and 725 mm total length. The reproductive period was long, almost covering the annual cycle, although the maximum activity was observed between April and October, with a peak in spawning in June-July. Keywords: Mycteroperca fusca, island grouper, sex change, maturity, spawning. RESUMEN: Biología reproductora del abade (Mycteroperca fusca) en las Islas Canarias, costa noroeste de África . – Este es el primer estudio que aborda las características reproductoras de Mycteroperca fusca, en toda su área de distribución, utilizando el estudio histológico de las gónadas. La especie se caracteriza por un hermafroditismo proterogíni- co. Existe una marcada predominancia de las hembras (1:4.9). Los machos y las hembras muestran marcadas diferencias en la estructura de tallas. Las hembras se distribuyen en todo el rango de tallas analizado (229-725 mm de longitud total) mientras que los machos sólo fueron observados en las tallas superiores, por encima de los 428 mm de longitud total. Se analizó un ejemplar intersexual de 610 mm de longitud total. La talla a la cual las hembras alcanzan la madurez sexual es 335 mm de longitud total, mientras que la talla a la cual el 95% de las hembras se consideran maduras es 398 mm de longitud total. La talla media a la cual el 50% de las hembras han invertido a la condición de macho fue 678 mm de longitud total. El rango de tallas en el que el proceso de inversión sexual tiene lugar es amplio, entre 428 y 725 mm de longitud total. El periodo reproductivo es amplio, cubriendo casi el ciclo anual completo, aunque el máximo de actividad se localiza entre los meses de abril y octubre, con un máximo de puesta en junio-julio. Palabras clave: Mycteroperca fusca, abade, inversión sexual, madurez, puesta. INTRODUCTION species, is characterized by the large size of individuals (Heemstra and Randall, 1999). The main characteris- The large species of the Serranidae family are tics of the life cycle of most of these species are well generally of great importance in marine ecosystems, known, given the high level of fishing interest in their and play a basic role in the food chain since they are areas of distribution (Heemstra and Randall, 1999). often the main predators of the ecosystems into which However, in the case of Mycteroperca fusca (Lowe, they are integrated. In the Serranidae family, the genus 1836), despite the ecological and fishing interests in Mycteroperca, at present represented by 15 different the Atlantic waters around the islands of Madeira, the 614 • R. BUSTOS et al. Azores, the Savage Islands, the Canary Islands and ded in paraffin, sectioned at 5 µm and stained with Har- Cape Verde, there is no information whatsoever with ris haematoxylin followed by eosin counter stain. Sec- respect to the characteristics of its life cycle. This is tioned and stained tissue was subsequently examined because for many years M. fusca was confused with under a light microscope. The sex and the maturation Mycteroperca rubra (Bloch, 1793), until Heemstra stage were determined from the histological sections. (1991) established that the species found in the Maca- Fish were identified as females, males or in transition ronesian region was M. fusca, with the distribution of from female to male following Sadovy and Shapiro M. rubra limited to the west coast of Africa and Medi- (1987) and Brulé et al. (2003a,b). Using the sexual terranean waters. classes as defined by Brulé et al. (1999) specifically In the Canary Islands, as is the case with most of for Mycteroperca species, and applied extensively as the large serranids, M. fusca is found on rocky and criteria in groupers (Shapiro et al., 1993; Sadovy and sandy-rocky sea-beds from the shore down to a depth Colin, 1995; Brulé et al., 2003 a,b; Tuz-Sulub et al., of 150 m and is most frequent in dips and bays, where 2006), adults were classified as resting, ripening, ripe it swims around large rocks at mid-depths, most fre- and running, or spent (covering both spent and recover- quently alone but sometimes in small shoals (Bustos, ing ovaries). The growing oocytes were classified ac- 2009). The current state of its populations is directly cording to the six histological stages proposed by Moe linked to the degree of human pressure on the species (1969) specifically for groupers, modified by Brulé et (Tuya et al., 2005). In the Canary Islands, where fish- al. (1999) for Mycteroperca species and extensively ing has been developed intensively, the populations used for this genus (Brulé et al., 2003a, b; Tuz-Sulub et are near to collapse and total landings of this species al., 2006): I, primary oocyte; II, immature oocyte; III, have decreased by approximately 95% over the last oocyte in primary vitellogenesis; IV, oocyte in early fifty years (Bustos, 2009). Traditionally, the most secondary vitellogenesis; V, oocyte in late secondary sought-after individuals have corresponded to those of vitellogenesis; VI, mature and hyaline oocyte. The greatest size (>600 mm), although currently the sizes criteria described by Shapiro et al. (1993) for grouper which make up the catch are between 300 and 500 mm. and by Brulé et al. (2003b) for Mycteroperca species, The records of on-site observation of the same xanthic and extensively applied as criteria in grouper species specimens over more than thirty years in the waters (Sadovy and Colin, 1995; Rhodes and Sadovy, 2002), of Madeira confirm that this species can live for more were used to distinguish a resting mature female from than 30 years (Weitz, pers. comm.). In the past, sam- an immature female based on the presence of muscle ples of larger specimens recorded in the Canaries have bundles remnants and connective tissue surrounding reached at least 860 mm in total length, which would blood vessels. Testes were classified according to the correspond to ages of nearly 40 years. No bag limits are most advanced stage of spermatogenesis observed. The currently imposed on its fishery and only a minimum spermatogenesis was classified under four histological size legislation (350 mm) has been implemented as a categories: spermatogonium, spermatocyte, spermatid management strategy. and spermatozoa, based on a modified criteria of Brulé The absence of available data on the biology of this et al. (2003b). Males were classified by the presence or species is particularly worrying if we consider that the absence and relative proportions of germinal stages, in correct management of biological resources should be conjunction with structural aspects of the gonad. based on the most complete information possible with Difference in mean total length between sexes was respect to the ecology of the species involved. The ob- tested using a t-test. The Kolmogorov-Smirnov non- jective of the present study was to establish the pattern parametric Z-test was used to analyze the differences of sexual development of the species, and to determine in the range of male and female sizes (Sokal and Rohlf, its main reproductive characteristics in the Canary 1995). Islands. This information is essential for the proper The proportion of the sexes (males to females) was management of the species in this area. estimated as a total and by size intervals. Sex ratios were tested statistically for significant deviations from MATERIALS AND METHODS the expected 1:1 ratio with a Pearson chi-square good- ness-of-fit test (α=0.05) (Sokal and Rohlf, 1995). A total of 214 specimens of M. fusca were analyzed The reproductive period was defined for both sexes between January 2004 and December 2005. The sam- using the relative proportion of animals in each sexual ples were collected from the small-scale fishery on the stage and by examining seasonal variations in the islands of Fuerteventura and Gran Canaria (Canary gonado somatic index (GSI=100GM/TM) (Brulé et al., Islands, northwest coast of Africa). 2003b). The total length, TL (mm) and the total mass TM Length-at-sexual maturity of female, length at (g), and gonad mass GM (0.01 g) were taken for each which 50% of the specimens had become mature (L50), fish. Unless otherwise indicated, all lengths reported was estimated by fitting a logistic ogive: are total length. All gonads were also fixed and pre- 100 served in 4% buffered formaldehyde and subsequently P , = r L L processed histologically.

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