Reproductive cycle of two commercial species of sea cucumber (Echinodermata: Holothuroidea) from Caribbean Panama

The reproductive status of the holothuroid species Isostichopus badionotus (Selenka, 1867) and Holothuria mexicana (Ludwig, 1875) was studied over 16 months in Bocas del Toro (Panama), from November 1999 to February 2001. Sexual reproduction was evaluated by the gonad index method, and by histology of gonad development. In addition, population structure was assessed based on sex ratio, minimum reproductive size, and length and weight distributions of males and females. The sex ratio in both species was 1:1, with a unimodal population distribution composed mainly of mature individuals. The minimum reproductive length and weight were 13–20 cm and 150 g, respectively, for both species, although reproductive individuals 10 cm in length were also found. A consistently higher gonad index was observed in H. mexicana, due to a high proportion of mature females and males and high gonad indices in most monthly samples. Gametogenesis and spawning patterns seemed to occur throughout the year, with periods of enhanced activity. Two periods of maximum reproductive activity were tentatively identified: July–November for I. badionotus and February–July for H. mexicana, but neither species had a single, sharply defined annual spawning event. Further work on these exploited holothuroids should examine the relationships between reproduction and environmental factors and between reproductive status and recruitment. Introduction During the two last decades, numerous holothuroid species have been fished to critical levels, causing the imminent collapse of local and regional populations (Sloan 1985; Richards et al. 1994; Conand 1990, 1997; Herrero-Pérezrul et al. 1999). The demand for Bêchede-mer in the Asian market, which has led to overfishing, has underlined the need for basic studies on the natural history of holothuroids so that the resource can be managed wisely. In particular, the reproductive biology of species of commercial importance has been a priority in different areas of the world, especially for the families Stichopodidae and Holothuriidae (Conand 1993a; Chao et al. 1994; Reichenbach et al. 1996; Herrero-Pérezrul et al. 1999; Ramofafia et al. 2000). Other studies have focused on the extrinsic factors influencing the reproductive cycle of the Holothuroidea, such as temperature (Ong-Che 1990; Sewell 1992; Hopper et al. 1998), precipitation (Kubota and Tomari 1998), salinity (Ong-Che 1990), monsoon runoff (Krishnaswamy and Krishnan 1967), lunar phase (Kubota and Tomari 1998), and active photosynthetic radiation (Catalan and Yamamoto 1994). The information available on this fundamental process for commercially important Caribbean holothuroids, however, is mostly limited to subtropical areas (Engstrom 1980; Mosher 1982; van Veghel 1993; PiresNogueira et al. 2001), and more precise studies on reproduction have been recommended (Buitrago and Boada 1996; de la Fuente-Betancourt et al. 2001). The highest gonad index for Isostichopus badionotus was observed during late spring (October–November) and summer (January–February) months in subtropical Atlantic Brazil, and spawning was reported only in January when water temperature was maximal (PiresNogueira et al. 2001). Spawning in I. badionotus was observed after the full moon of August in tropical Bonaire, Netherlands Antilles (Graaf et al. 1999). Similarly, gametogenesis and spawning of Holothuria mexicana Marine Biology (2003) 142: 271–279 DOI 10.1007/s00227-002-0939-x Communicated by J.P. Grassle, New Brunswick H.M. Guzmán (&) Æ C.A. Guevara Æ I.C. Hernández Smithsonian Tropical Research Institute, Apartado Postal 2072, Balboa, Panama Mailing address: H.M. Guzmán Smithsonian Tropical Research Institute, Unit 0948, APO AA, 34002-0948, USA e-mail: [email protected] Fax: +1-507-2128790 from southern Florida occurred during spring–summer and late summer, respectively (Engstrom 1980; Mosher 1982). Resorption of relict gametes followed, but the breeding season was considered unclear due to the presence of enlarged gonads full of mature gametes from September–November (Engstrom 1980). Van Veghel (1993) reported spawning for >70% of H. mexicana individuals within the first 5 days following the full moons between August and October on Curaçao reefs, perhaps the only information available for tropical areas. The minimum length at maturity for I. badionotus is reported to be 18 cm (Rodrı́guez-Milliet and Pauls 1998), while lengths of 57.9 and 75.7 cm have been reported for H. mexicana males and females, respectively, from Florida (Engstrom 1980). Non-traditional fishing areas in the Caribbean have been targeted for supplying the Asian market in recent years (Buitrago and Boada 1996; Rodrı́guez-Milliet and Pauls 1998; de la Fuente-Betancourt et al. 2001), with species of commercial importance. In the present study, we describe aspects of the reproductive biology of two of these species, I. badionotus and H. mexicana. Both species are widely distributed throughout the Caribbean. They commonly inhabit shallow waters with sandy, coral, or interspersed seagrass areas, and prefer seagrass meadows (Humann 1992; Hendler et al. 1995). Both species can reach lengths of up to 50 cm (Hendler et al. 1995). Both species, like most of the Holothuroidea, are gonochoric. The goals of the study were: (1) to describe the annual reproductive cycle, using the gonad index (GI) method, confirmed by histological examination of gonads; (2) to compare the annual reproductive cycle data with environmental variables (rainfall, temperature); and (3) to analyze the population structure (size frequency by sex, sex ratio, minimum reproductive size) in the Archipelago of Bocas del Toro, Panama. Materials and methods Sexual reproduction assessment Specimens of Isostichopus badionotus (Selenka, 1867) and of Holothuria mexicana (Ludwig, 1875) were collected at Punta Pondsack (09 17¢19¢¢N; 082 19¢43¢¢W) and at Punta Quarys (09 16¢10¢¢N; 082 23¢18¢¢W), in the archipelago of Bocas del Toro, Panama. Adults and juveniles of both species were commonly found in sandy areas with abundant seagrass (Thalassia testudinum), at depths of up to 5 m. The geology, climate, oceanography, and orography of the archipelago have been described previously (Rodrı́guez et al. 1993; Greb et al. 1996; Guzmán and Guevara 1998). About 30 mature individuals of each species were collected monthly just before or on the day of full moon, from November 1999 to February 2001 (475 and 479 individuals per species, respectively). We expected gonad weight to be maximal at the time of full moon according to van Veghel (1993) and Graaf et al. (1999), who observed spawning after the full moon in Curaçao and Bonaire, respectively. These holothurians were placed in buckets of 10 l of seawater and ca. 5–10 g of MgSO4 for 5–10 min, until completely relaxed and drained, thus facilitating biometric measurements (sensu Ong-Che 1990; Chao et al. 1993). Body length was measured for drained individuals (to within 1 mm). For the extraction of gonads, an incision was made through the ventral body wall, and all internal parts were removed. We measured weight using gutted individuals (to within 0.01 g), defined as body wall wet weight (sensu Conand 1981; Chao et al. 1993, 1995). This weight (gutted) was chosen, since drained weight may include sediments in the digestive tract and water in the respiratory system. We used drained body weight (sensu Conand 1981; Chao et al. 1993) only to obtain the minimum reproductive size, without sacrificing more individuals (Ramofafia et al. 2000). Body length was compared to gutted weight (Fig. 1). A significant but weak relationship was observed for both species, although the r was higher in H. mexicana. This may have been due to the relative rigidity of the body wall in H. mexicana, which allowed more precise measurement, compared to the smoother, more flaccid body wall in I. badionotus. The extracted gonads were weighed separately (0.01 g precision) to develop a gonad index. Gonad index was calculated as follows: GI=[(gonad wet weight)/(gutted weight)]·100. Gonads were then fixed in Bouin’s solution for 24 h, washed alternately in water and 50% ethanol several times, and preserved in 70% Fig. 1 Isostichopus badionotus, Holothuria mexicana. Relationship between body length and wall wet weight. Correlations were statistically significant (P<0.001) as were the regressions (F(1, 473)=104.748 and F(1, 477)=159.735, respectively) 272