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Sexual Reproduction in a Fissiparous Holothurian Species, Holothuria

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Sexual Reproduction in a Fissiparous Holothurian Species, Holothuria SPC Beche-de-mer Information Bulletin #18 – May 2003 33 D’Silva, D. 2001. The Torres Strait beche-de-mer Skewes, T.D. Dennis, D.M. and Burridge, C. 2000. (sea cucumber) fishery. SPC Beche-de-Mer Survey of Holothuria scabra (sandfish) on Information Bulletin 15:2–4. Warrior Reef, Torres Strait, January 2000. CSIRO Division of Marine Research. Jaquemet, S. and Conand, C. 1999. The Beche-de- Mer trade in 1995/1996 and an assessment of TRAFFIC South America. 2000. Evaluation of the exchanges between main world markets. SPC trade of sea cucumber Isostichopus fuscus Beche-de-Mer Information Bulletin 12:11–14. (Echinodermata: Holothuroidea) in the Galapagos during 1999. Quito. 19 p. Lokani, P. 1990. Beche-de-mer research and devel- opment in Papua New Guinea. SPC Beche-de- Uthicke, S. and Benzie, J.A.H. 2001. Effect of beche- Mer Information Bulletin 2:1–18. de-mer fishing on densities and size structure of Holothuria nobilis (Echinodermata: Secretariat of the Pacific Community. 1994. Sea cu- Holothuridae) populations on the Great cumbers and beche-de-mer of the tropical Barrier Reef. Coral Reefs 19:271–276. Pacific. A handbook for fishers. Handbook no. 18. SPC, Noumea New Caledonia. 51 p. Sexual reproduction in a fissiparous holothurian species, Holothuria leucospilota Clark 1920 (Echinodermata: Holothuroidea) Pradina Purwati1,2 and Jim Thinh Luong-van2 Abstract Holothuria leucospilota Clark 1920 inhabiting tropical Darwin waters primarily undergo asexual reproduc- tion by fission throughout the year (Purwati 2001). However, there is also evidence of sexual reproduction. Monthly sampling from August 1998 to January 2000 revealed that the gonadal tubules within each indi- vidual of H. leucospilota grew simultaneously. Complete spawning, where the oocytes throughout the gonad have equal opportunity to be released in one spawning event, could therefore be expected. Post- spawning tubules were absorbed, resulting in the disappearance of gonads between reproductive cycles. The development of gonadal tubules in this holothurian does not conform to the “tubules recruitment model” proposed by Smiley (1988), as reassessed by Sewell et al. (1997). A seasonal reproductive cycle with a restricted spawning period was recognised in the population studied. The resting stage that occurred simultaneously amongst individuals in the population made it possible to estimate gametogenesis, which may take less than a year. It is likely that gamete release occured in the pe- riod between new moon and full moon of April, at the end of the wet season in Darwin. The continuous flooding of the reefs during this period is thought to be effective for fertilisation. Introduction basis, whereas the population in the South Island maintains its spent tubules (Sewell 1992). Variations occur in holothurian gonad structures Intraspecific variation in number of gonad tufts is and development (Conand 1981; Harriott 1985; also possible. One example is dendrochirote Tuwo and Conand 1992; Hamel et al. 1993; Conand Cucumaria frondosa, in which geographical and lati- et al. 1997). In a holothurian population where the tudinal factors are the suggested influencing fac- gonads develop simultaneously and spent tubules tors (Sewell 1992; Hamel and Mercier 1996). are absorbed after the reproductive season, the go- nads may not be visible for a certain period. In view of these variations occurring amongst However, intraspecific variation can occur, such as holothurian populations, it was of interest to study in Stichopus mollis of New Zealand, where the pop- the sexual reproduction of Holothuria leucospilota ulation from the east coast of the North Island ab- from Darwin harbours, northern Australia. The in- sorbs the after-spawned tubules and the gonadal vestigation aimed to elucidate the types of gonadal 1. Research Centre for Oceanography – LIPI. Jl. Pasir Putih 1, Ancol Timur, Jakarta Utara, Indonesia. Email: [email protected] 2. SITE Faculty, Northern Territory University, Casuarina Campus, Darwin, NT, Australia. 34 SPC Beche-de-mer Information Bulletin #18 – May 2003 tubule recruitment, and synchrony and seasonality ronmental conditions provided by the Bureau of of gonad development over the population. H. leu- Meteorology Darwin were used to identify possible cospilota has been observed to reproduce asexually clues to the factors leading to spawning. by fission throughout the year (Purwati 2001; Conand et al. 1997) and this fission may influence Results the sexual reproductive activities. Characteristics of the gonadal tubules Materials and methods Gonadal tubules of H. leucospilota hang freely in the Individuals of H. leucospilota were collected from body cavity from a transparent saddle-like gonadal East Point reef, Darwin, northern Australia basis located at the side of the anterior part of the (12°24.20'S and 130°49.20'E). The population occu- intestine. A simple gonoduct emerges from the go- pied an area of approximately 500 x 700 m with a nadal basis and ends at the gonopore, approxi- relatively low density (0.077–0.29 individuals m-2) mately 2–3 cm from the oral end. Tubules were ob- and was composed of small animals, mostly less served to protrude from the gonadal basis in two than 350 g in fresh body weight. rows. Each tubule was straight and bifurcated twice or three times, rarely exceeding four times. The di- Tubule fractions of 170 gonads in total, sampled mension, colour and number of the tubules were from individuals weighing 200 g or more in fresh correlated with the stages of development (Fig. 1). body weight, were examined. This size was deter- mined after a preliminary study revealed that indi- Male tubules were always creamy white in colour. viduals weighing at least 200 g in fresh condition Female tubules were more transparent, with the in- carried gonads. Collections were conducted once terior having a granulated appearance. The female every month from August 1998 to January 2000, tubules became reddish-orange with the develop- except in April 1999 when sampling was carried ment of fecund ovaries. After spawning, the out twice (15 and 29 April). Sample size ranged tubules deteriorated and turned brown; un- from 5 to 18 individuals per month, the inconsis- spawned oocytes were likely to be reabsorbed. Of tency being due to the conservation policy prac- the individuals sectioned, 59 were males, 64 were tised on the study sites. females and 47 either carried unidentified gonads or had no visible gonads. The number of males was Asmall incision was made on the antero-dorsal in- calculated to be similar to the number of females, tegument of each individual to remove fractions of in which x observed (0.2030) was smaller than x ex- gonadal tubules from the body cavities. This was pected (3.841) (d.f. +1; p = 0.05). made on the site and the dissected bodies were re- turned to the reef. Chao et al. 1994 utilised this Table 1 gives the dimensions of the ovarian tubules method and reported that the scar on the dorsal and oocytes at various stages. The smallest ovaries part of Holothuria atra caused by incision disap- were in the early development stage. They con- peared within six months. During our study, two sisted of 7 transparent tubules, less than 8 mm long individuals with scar at the point of incision were and 0.01 g fresh weight. The largest ovary in fe- observed on the reef of East Point approximately cund condition consisted of more than 14 large or- 8–11 months after the first sampling. ange tubules weighing 81.92 g fresh weight. Gonads collected were clas- sified into four stages: early, Ta b l e 1. Size of ovarian tubules and oocytes at different stages growing, fecund and post- of development spawning stage, based on morphology and histology Ovarian stage Ovarian tubules Oocyte of the gonads. Tubule frac- of development tions were prepared for mi- Length Diameter Diameter croscope slides by applying 10 per cent buffered formal- Early developing ≤70 mm ≤0.9 mm 5–60 mm dehyde fixation, paraffin Growing 22–25 cm <2.5 mm, but 5–110 mm procedures and hema- may reach 4 mm toxylen-eosin staining. A Fecund 20–30 cm, may 4–5 mm 120–140 mm camera lucida was set up reach 40–45 cm on a compound microscope Post-spawning Varied Shrinking Large oocytes to enable diagrams of the remained ovarian histology to be drawn. Data on the envi- SPC Beche-de-mer Information Bulletin #18 – May 2003 35 Advanced ovaries were heavier as a consequence Stage of development of increased gamete number and volume. Tubules protruding from the anterior part of the basis were Figure 2 illustrates the pattern of development ob- frequently shorter but diameter, coloration and in- served between August 1998 and January 2000. ternal appearance were similar to the others. The early stage of development was mainly found in October–November 1998 and again in August– All tubules within each individual gonad were al- September 1999. Growing gonads were gathered ways at the same stage of maturity. Furthermore, go- among samples collected in December 1998– nads collected in one sampling event tended to be in January 1999 and December 1999. From January to a similar state of maturity, indicating synchronous early April 1999 and in January 2000, collected go- progression throughout the population (Fig. 2). A nads were mostly in fecund condition. In the last seasonal pattern can therefore be expected. week of April through June 1999, post-spawning Figure 1. Ovarian tubules of H. leucospilota under dissecting (above line) and compound microscope (below line). A: early stage; B: growing stage; C: fecund; D: post spawning. gb: gonadal base; gd: gonoduct; gt: gonadal tubules; l: lumen; o: pre- vitellogenic oocytes; od: degenerated oocytes; op: postvitellogenic oocyte; ov: vitellogenic oocyte; t: tubule; tl: tubule lining. Scale bars in A, B, C, and D: 20, 40, 50 and 50 µm 1998 1999 2000 Aug.
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