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Reproductive Cycle of Edible Echinoderms from the Southwestern Indian Ocean

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Reproductive Cycle of Edible Echinoderms from the Southwestern Indian Ocean Western Indian OceanREPRODUCTIVE J. Mar. Sci. CYCLE Vol. OF 4, EDIBLE No. 1, pp.ECHINODERMS 47–60, 2005 FROM INDIAN OCEAN (I) 47 © 2005 WIOMSA Reproductive Cycle of Edible Echinoderms from the Southwestern Indian Ocean I. Tripneustes gratilla L. (Echinoidea, Echinodermatata) D. Vaïtilingon1, 2 , R. Rasolofonirina1, 2 and M. Jangoux1, 2, 3 1Université Libre de Bruxelles, Laboratoire de Biologie Marine (CP 160/15), 1050 Bruxelles, Belgium; 2Université de Tuléar, Aqua-lab, Institut Halieutique et des Sciences Marines (BP 141), 601 Tuléar, Madagascar; 3Université de Mons-Hainaut, Laboratoire de Biologie Marine, 7000 Mons, Belgium Key words: echinoid, reproductive cycle, maturity index, tripneustes gratilla, abiotic factors Abstract—The reproductive cycle of the edible echinoid Tripneustes gratilla (Linneaus 1758) was investigated in a population located in the southwest coast of Madagascar (Toliara). The reproductive cycle was followed for two consecutive years (October 1999 to October 2001) and characterised by means of gonad and maturity indices. T. gratilla has an annual reproductive cycle mediated by seawater temperature, day length and feeding activity. The histology of the gonads revealed six different maturity stages grouped in three main reproductive phases: growing and maturing, spawning, and spent and recovering. Reproduction is seasonal. Growing and maturing stages occurred from late summer to early winter correlating with decreasing temperatures and day length. Spawning occurred during mid and later winter, when temperatures and day lengths were lowest. Spent and recovering urchins were observed from late summer to early winter. Besides, the reproductive cycle was also influenced by food quantity in the gut, the repletion index was higher after spawning and gametogenesis started when sufficient amount of nutrient reserves accumulated in gut tissues and nutritive phagocytes of the gonads. This study reveals that the maturity index, based on histological analysis of gonads, is more reliable than gonad index in characterising the reproductive cycle of echinoids. In view of fishery management, we recommend harvest of T. gratilla from November to February, when individuals are in the pre-gametogenic stages. INTRODUCTION echinoids are edible and thus of economic interest. An increasing demand for echinoid roe over the The role of echinoid grazing in determining past 15 years has led to overfishing and depletion subtidal community structure is well established of natural stocks (Sloan, 1985; Keesing & Hall, (Lawrence, 1975; Lawrence & Sammarco, 1982; 1998). In view of these ecological and economic Harrold & Pearse, 1987). A marked increase in aspects, considerable interest has developed in the echinoid population has been shown to transform reproductive biology of echinoids. Reproductive kelp beds to barren grounds while a decrease success has a direct influence on larval supply, resulted in a return to an algal dominated system which is one of the factors affecting recruitment (see Harrold & Pearse, 1987 for review). Many and establishment of echinoid population (Pedrotti, Corresponding Author: DV E-mail: [email protected] 48 D. VAÏTILINGON ET. AL. 1993; Lopez et al., 1998; Balch & Scheibling, MATERIALS AND METHODS 2001). Gonad quality is an important criterion for market value. Echinoid gonads are usually eaten at the pre-gametogenic stage and therefore, Samplings and measurements knowledge of the reproductive cycle is essential for fishery management (Byrne, 1990; Lawrence, The population of T. gratilla was located among 2001). Variability in reproductive patterns is the seagrass beds of the Beloza fringing reef lagoon common among shallow-water echinoid species (23° 29.32' S; 43° 45.05' E). This reef forms part and even within populations of a single species of the Toliara reef complex, at the southwest coast (Himmelman, 1978; Pearse & Cameron, 1991; of Madagascar (see Vaïtilingon et al., 2003 for Lozano et al., 1995). This variability is explained further details about the sampling site). Sampling by the fact the reproductive cycle is determined at low tide was monthly from October 1999 to by environmental cues (temperature, photoperiod, October 2001, except in November 2000 and food availability, and hydrodynamism), which are February 2001 (heavy rains were observed killing themselves subjected to periodic cycles whose numerous echinoids and in order not to introduce intensities and patterns vary according to errors in our results, echinoid samplings were geographical localities. avoided on these two months). At each sampling Tripneustes gratilla (Linneaus 1758) is a- time, 30 individuals of test diameters between 7 shallow-water echinoid, ubiquitous in the tropical and 9 cm were randomly collected, brought alive Indo-West Pacific region. Like many other littoral to the laboratory and measured immediately (Table echinoids, it is of economic and ecological interest 1). Two perpendicular ambital test diameters were since it is edible and considered as a primary measured using vernier calipers. Individual fresh herbivore in the various habitats it occupies weight was determined after leaving the specimen (Lawrence & Agatsuma, 2001). Studies dealing on absorbent paper for three minutes to remove with its reproductive cycle indicated variable excess water. They were then dissected to spawning periods according to its geographical determine the fresh weight of the digestive tract distribution (Chen & Chang, 1981; Lawrence & with its contents and of the gonads. One of the Agatsuma, 2001). A single previous study in the five gonads was fixed in Bouin’s fluid for further Indian Ocean, from the north coast of Madagascar, histological investigation (see below). reported continuous gametogenic activity with a To characterise the reproductive cycle of T. peak spawning period in late winter (Maharavo, gratilla, the gonad index (GI) and the maturity 1993). In some tropical echinoid species, the index (MI) were calculated for each month studied. breeding season is spread throughout the year when The ratio of gonad fresh weight to total fresh the population is located near the equator, but weight was used to calculate the gonad index (GI): farther away, spawning occurs over a restricted FW g period (Pearse & Cameron, 1991). We report on GI = x100 (1) an investigation of the reproductive cycle of a TW population of T. gratilla located in the southwestern where FWg is the weight of the gonads in gram coast of Madagascar. The study covers two and TW is the weight of the whole animal in gram. breeding seasons and reproductive patterns were The MI was determined after histological analysis determined by means of gonad and maturity indices of the fixed gonad.. A preliminary study confirmed and attempt to relate these to environmental factors the homogeneous gametogenic state in T. gratilla and to the known seasonal variability in the feeding which is in agreement with previous echinoids activity of the population (Vaïtilingon et al., 2003). studies (Byrne, 1990; King et al., 1994; Spirlet et REPRODUCTIVE CYCLE OF EDIBLE ECHINODERMS FROM INDIAN OCEAN (I) 49 al., 1998). Hence histology was performed only where the direction of the vector points to on the middle portion of one of the five gonads corresponding gonadal stage and the vector length from each sampled individual. The fixed gonad was represents the homogeneity of the sample. rinsed, dehydrated, embedded in paraffin wax and To assess the possible relationship between the sectioned at 7 µm. Serial sections were placed on reproductive cycle and the variation in gut content, glass slides, dewaxed and stained with Masson’s the repletion index (RI), was calculated each month trichrome. All slides of gonad sections were as follows: examined under light microscope for sex determination, and photographed using a Q- FW dt RI = x100 (2) imaging Micropublisher digital camera. Maturity TW stages were classified according to previous studies where FW is the fresh weight of the digestive tract of echinoid gametogenesis (Byrne, 1990; Spirlet dt (including contents) in gram. The variation in the et al., 1998) based on oocyte size (females), RI was compared to that of the reproductive cycle thickness of peripheral spermatocyte layer (males) (GI and MI) in order to detect any correlation. and the amount of nongerminal nutritive tissues Some basic environmental parameters such as, (males and females). For each monthly sample, seawater temperature and salinity were recorded measurements of at least 100 oocyte diameters and at time of sampling using a combined salinometer- the widths of at least 30 spermatocyte layers were thermometer apparatus (WTW LF 330, Bioblock performed using Scion Image analysis software. Scientific). Photoperiod was also considered and The maturity index (MI) represents the monthly its value on the sampling date was calculated from mean gonadal stage calculated after transforming the Online-Photoperiod Calculator V 1.94 (http:// the maturity stage of every individual to a circular www.sci.fi/~benefon/sol.html) and expressed as scale (Zar, 1996; Spirlet et al., 1998). Each monthly day length in hours. mean value is represented as a vector in a circle Table 1. Synopsis of monthly measurements taken from Tripneustes gratilla individuals throughout the two-year study period (n = 30). Test diameter expressed in cm and fresh weight in gram. Sampling month Mean (±sd) test diameter Mean (±sd) total fresh weight (TW) Oct.-99 7.92±0.31 213.01±23.14 Nov.-99 8.18±0.53 212.67±40.02 Dec.-99 8.13±0.44 220.86±38.97 Jan.-00 8.10±0.62 214.36±48.69 Feb.-00 8.58±0.57 250.76±49.35 Mar.-00 8.10±0.42 203.60±36.47 Apr.-00 8.47±0.59 250.78±49.35 May-00 8.40±0.62 246.34±50.88 Jun.-00 8.26±0.60 229.84±44.00 Jul.-00 8.62±0.51 255.19±43.98 Aug.-00 8.00±0.45 206.06±34.33 Sep.-00 8.56±0.56 248.71±41.58 Oct.-00 8.43±0.41 235.42±42.05 Dec.-00 8.24±0.45 223.86±40.14 Jan.-01 8.61±0.55 248.54±41.70 Mar.-01 7.89±0.50 218.84±34.66 Apr.-01 7.98±0.48 212.77±37.65 May-01 8.73±0.42 248.88±36.66 Jun.-01 8.05±0.55 210.59±40.82 Jul.-01 8.13±0.41 232.41±35.43 Aug.-01 8.32±0.32 234.09±26.35 Sep.-01 8.16±0.30 225.90±33.79 Oct.-01 8.52±0.52 233.93±39.43 50 D.
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