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Reproduction of the Commercial Sea Cucumber Holothuria Scabra (Echinodermata: Holothuroidea) in the Solomon Islands

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Reproduction of the Commercial Sea Cucumber Holothuria Scabra (Echinodermata: Holothuroidea) in the Solomon Islands Marine Biology (2003) 142: 281–288 DOI 10.1007/s00227-002-0947-x C. Ramofafia Æ M. Byrne Æ C.S. Battaglene Reproduction of the commercial sea cucumber Holothuria scabra (Echinodermata: Holothuroidea) in the Solomon Islands Received: 26 September 2001 / Accepted: 18 January 2002 / Published online: 12 November 2002 Ó Springer-Verlag 2002 Abstract Over a 3-year period (1996–1998), reproduc- tubule recruitment model described for holothurian tion of the commercial sea cucumber Holothuria scabra oogenesis. Continuous reproduction in H. scabra and (Jaeger, 1833) was investigated in the Solomon Islands prolonged availability of mature gametes would facili- to determine the spawning pattern and whether ga- tate use of this species for aquaculture. metogenesis is continuous or seasonal. The gonad con- sisted of a single cohort of tubules that developed uniformly. Macroscopic examination of the gonads re- vealed that mature gametes were present throughout the Introduction year. Individuals with gonads at different stages of ma- turity were present in most samples. Partly spawned Holothuria scabra (commonly known as sandfish) is an gonads were prevalent in females, whereas mature go- aspidochirote holothurian widely distributed in coastal nads were prevalent in males. The time at which the regions throughout the Indo-Pacific region (Conand peak gonad index was recorded differed among years. 1998). H. scabra is often found on inner reef flats and Although gametogenesis was continuous, with a poten- near estuaries, half buried in the silty sand during the tial for prolonged gamete release, a period of enhanced day and emerging at night to feed (Mercier et al. 1999). spawning occurred during the dry season, from Sep- Two colour morphs, black and grey, are known, and tember to December. Maximum gonad indices were genetic data have shown that these are a single species reached prior to and during this period of enhanced (Uthicke and Benzie 1999). H. scabra is among ap- spawning. Histology revealed that gametogenesis reini- proximately 20 aspidochirote species that constitute the tiated in partly spawned gonads, resulting in the pres- beˆ che-de-mer fishery in the Indo-Pacific and is among ence of gametes at different stages of development in the the most valuable species in the trade (Conand and gonad. The uniform growth of gonad tubules indicated Byrne 1993; SPC 1994). that H. scabra does not conform to the progressive A biannual spawning pattern for H. scabra is re- ported in India, the Philippines, New Caledonia and Communicated by G.F. Humphrey, Sydney Indonesia (Table 1). These studies also reported that mature H. scabra can be found year-round, raising the C. Ramofafia (&) Æ M. Byrne possibility that reproduction may be continuous. In Department of Anatomy and Histology F13, subtropical regions of Australia, by contrast, annual University of Sydney, NSW 2006, Australia reproduction is reported for H. scabra (Harriot 1980; E-mail: chris.ramofafia@ffa.int Morgan 2000a). A recent review of the biology of Tel.: +677-25090 H. scabra concluded that, despite the investigations Fax: +677-23296 conducted over its geographic range, further research is C.S. Battaglene required to gain a better understanding of the repro- ICLARM–The World Fish Center, P.O. Box 438, Honiara, Solomon Islands ductive cycle and spawning cues (Hamel et al. 2002). In particular, the suggestion that tropical H. scabra popu- Present address: C.S. Battaglene lations have continuous gametogenesis has to be as- University of Tasmania, Tasmanian Aquaculture and Fisheries Institute, sessed by histological examination of gonad condition Taroona, TAS 7053, Australia throughout the year: most other studies have relied on Present address: C. Ramofafia the gonad index method (Hamel et al. 2002). ICLARM–The World Fish Center, In this study, we investigated the reproduction of P.O. Box 438, Honiara, Solomon Islands H. scabra in the Solomon Islands. Our aims were to 282 Table 1 Holothuria scabra. Reproduction of Holothuria scabra in the Indo-Pacific. – not documented Latitude Location Methods used Study duration GI max Reproductive pattern Spawning period Reference years 27°N Red Sea Field spawning – – – Includes June Mortensen observation 1937 13°N Philippines GI and 2NoContinuous mature Increased activity Ong Che and histology obvious specimens year in June and Gomez 1985 peaks round October (biannual peaks assumed) 09°N India GI 1 July and Biannual July–August (main) Krishnaswamy October October–November and Krishnan 1967 05°S Indonesia GI and 1 April and Biannual mature April and November Tuwo 1999 histology November specimens year round 09°S Solomon GI and 3 August and Continuous mature Enhanced activity Present Islands histology October specimens year from September study (females) round to December August (males) 20°S New GI 2 or more years’ August and Biannual August–September Conand Caledonia data, annual December December–January 1993 cycle presented 27°S Australia GI and histology 1.5 December Annual November–January Harriott 1980 27°S Australia GI and histology 1.5 November Annual mature November–December Morgan 2000a specimens seasonal determine the breeding pattern of H. scabra, to identify H. scabra in each of these stages was determined for all samples the timing of gamete availability, and to determine collected from May 1996 to December 1998. To determine whether GI differed among months and years, the whether gametogenesis is continuous or seasonal. GI data of both sexes were combined and compared by analysis of variance (ANOVA). Factors were year (Y) and month nested in year [M(Y)]; sample size n=17, the minimum monthly sample size Materials and methods was recorded. Where monthly sample size was greater than 17, specimens were picked at random to achieve n=17. A second ANOVA was also carried out to determine whether Samples of Holothuria scabra were collected from Kogu Halingi the GI data of females and males differed. For this ANOVA, fac- Bay on Kohinggo Island, Vona Vona Lagoon, Western Province of tors were sex (S), year (Y) and months nested in year [M(Y)]; the Solomon Islands (8°10’S, 157°11’E). Samples were collected by sample size was n=6. For the ANOVA models to be balanced, the snorkelling or by SCUBA diving from May 1996 to December data obtained in 1996 were excluded from the analyses, since only 1998. Each specimen was placed in a plastic bag containing sea six monthly samples were collected. The 1997 and 1998 November water, sealed and packed in a fish box (60 l capacity), for trans- data were also excluded from the second ANOVA, since the male portation to the ICLARM Coastal Aquaculture Centre (CAC) on sample size in 1998 was lower than n=6. Homogeneity of variance Guadalcanal Island (09°18’S, 159°47’E). was tested using Cochran’s test and the data were transformed to In the laboratory, a longitudinal incision was made along the log (X+1) to achieve homogeneity of variance. Student–Newman– dorsal surface of each specimen and the coelomic fluid and gonad Keuls (SNK) multiple-range tests were used for a posterori com- were removed. Drained body weight (dwt) and gonad weight (gwt) parisons of monthly GI results that differed. were measured to 0.01 g and the gonads were fixed in 7% formalin in sea water. Gonad index (GI) was determined for each animal as (wet gwt/wet dwt)·100. Gonad indices were determined for each monthly sample and a mean GI was calculated for females and for males. Results The five-stage maturity scale, based on tubule morphology (Ramofafia et al. 2000), was used to describe gonad development. A total of 845 Holothuria scabra were collected, The maturity stages, based on macroscopic examination of the tubules, included: stage I, indeterminate; stage II, growing; stage 414 females (x dwt=644.94 g, SE=11.28) and 428 males III, mature; stage IV, partly spawned; and stage V, spent. Each (xmacr; dwt=655.49 g, SE=11.87). Two specimens gonad was assigned to one of these stages. Tubule size was also with indeterminate gonads (x dwt=384.95 g, SE= measured to determine whether tubule biopsies would provide a 105.05) were collected in July 1996 and April 1998 and meaningful assessment of reproductive condition. For each gonad, 15 tubules were removed, and their length and diameter measured one specimen that lacked a gonad (=396.50 g; dwt) was to the nearest millimetre. collected in December 1996. The sex ratio did not differ The histology of gametogenesis was also documented for each significantly from unity (v=0.85; P>0.05). specimen. For histology, gonad tubules were dehydrated through graded ethanols, rinsed in histoclear and embedded in paraffin. The sections (6 lm thick) were stained with haemotoxylin and eosin. Gonad morphology Based on the staining response, the gonads were assigned a gametogenic stage. Five gametogenic stages were defined: recovery, growing, mature, partly spawned, and spent, similar to the stages The gonad of H. scabra was a single tuft of numerous used in other studies of sea cucumbers (Sewell and Bergquist 1990; branched tubules on the right side of the dorsal mesen- Tuwo and Conand 1992; Ramofafia et al. 2000). The percentage of tery. All the tubules developed uniformly through the 283 gametic maturity stages. The size, colour and shape of tubules were reduced in size and appeared flaccid. The tubules and numbers of branches of each tubule de- unspawned tubules were similar in appearance to that pended on the stage of gonad development. Gonad described for mature tubules. Phagocytes were evident in maturity stages are compared in Table 2. All stages, with the lumen of both tubule types and were particularly the exception of indeterminate stage I, were present in abundant in the unspawned tubules, indicating that the samples throughout the year. gametes present were being resorbed.
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