Abstract
Seasonal trends in the gonad index (GI) of two widely separated populations of black teatfish, Holothuria whitmaei (formerly included in Holothuria nobilis), were investigated between Pacific (Great Barrier Reef) and Indian Ocean (Ningaloo Reef) coral reefs of Australia. Reproductive activity followed a similar annual trend, with the GI of both populations peaking typically between April and June. Macroscopic and histological analysis of Ningaloo Reef specimens revealed that large germinal tubules, positioned centrally on the gonad basis, progressed through four maturity stages: growing (II); mature (III); partly spawned (IV); and spent (V). Growing tubules dominated the central region of the gonad basis between January and March, followed by an increase in the number of mature tubules throughout the GI peak (April–June). The progressive appearance of partly spawned and spent tubules between June and October suggests that spawning in H. whitmaei continues intermittently over an extended period throughout the austral winter. The examination of the gonad structure of sexually mature male and female specimens identified five tubule size classes in total (C1 to C5), each of differing physical and gametogenic status. In females, smaller C1 tubules located at the anterior edge of the gonad basis contained pre- to early vitellogenic oocytes. Larger C2 and C3 tubule cohorts, positioned centrally on the gonad basis, contained mid- to late-stage vitellogenic oocytes. Smaller C4 and C5 tubules, located at the posterior edge, contained only relict oocytes. Similar physical and gametogenic differences were apparent between tubule cohorts in male specimens. We propose that these results, together with evidence of incomplete gonad resorption over the austral summer, indicate that gonad development in H. whitmaei conforms to the predictions of the Tubule Recruitment Model (TRM). The TRM is reported rarely among tropical aspidochirotes, and results presented here (1) provide the first direct evidence of this model in H. whitmaei, and (2) confirm that this species is one of the few winter-spawning tropical invertebrates.
Similar content being viewed by others
References
Andrew NL (1986) The interaction between diet and density in influencing reproductive output in the echinoid Evechinus chloroticus. J Exp Mar Biol Ecol 97:63–79
Babcock RC, Bull GD, Harrison PL, Heyward AJ, Oliver JK, Wallace CC, Willis BL (1986) Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Mar Biol 90:379–394
Bakus GJ (1973) The biology and ecology of tropical holothurians. In: Jones OA, Endean R (eds) Biology and geology of coral reefs VII. Biology 1. Academic, New York, pp 325–367
Battaglene SC, Seymour JE, Ramofafia C, Lane I (2002) Spawning induction of three tropical sea cucumbers, Holothuria scabra,H. fuscogilva and Actinopyga mauritiana. Aquaculture 207:29–47
Benzie JAH, Uthicke S (2003) Stock size of bêche-de-mer, and recruitment patterns and gene flow in the black teatfish on the Great Barrier Reef. Report prepared for the Fisheries Research and Development Corporation. The Australian Institute of Marine Science, Townsville, 86 p
Birkeland C (1988) The influence of echinoderms on coral-reef communities. In: Jangoux M, Lawrence (eds) Echinoderm studies, vol 3. AA Balkema, Rotterdam, pp 1–79
Byrne M (1990) Annual reproductive cycles of the commercial sea urchin Paracentrotus lividus from an exposed intertidal and sheltered subtidal habitats on the west coast of Ireland. Mar Biol 104:275–289
Byrne M, Andrew NL, Worthington DG, Brett PA (1998) Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Mar Biol 132:305–318
Cameron JL, Fankboner PV (1986) Reproductive biology of the sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). I. Reproductive periodicity and spawning behaviour. Can J Zool 64:168–175
Chao S-M, Chen C-P, Alexander PS (1995) Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Mar Biol 122:289–295
Conand C (1981) Sexual cycle of three commercially important holothurian species (Echinodermata) from the lagoon of New Caledonia. Bull Mar Sci 31:523–543
Conand C (1993) Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Mar Biol 116:439–450
Conand C (2004) Present status of world sea cucumber resources and utilization: an international overview. In: Lovatelli A (comp/ed), Conand C, Purcell S, Uthicke S, Hamel J-F, Mercier A (eds) Advances in sea cucumber aquaculture and management. Fisheries Technical Paper. Rome, FAO, 463:13–24
Conand C, Uthicke S, and Hoareau T (2002) Sexual and asexual reproduction of the holothurian Stichopus chloronotus (Echinodermata): a comparison between La Réunion (Indian Ocean) and east Australia (Pacific Ocean). Invertebr Reprod Dev 41:235–242
Hamel J-F, Mercier A (1996) Gonad morphology and the gametogenesis of the sea cucumber Cucumaria frondosa. SPC Inf Bull Bêche-de-mer 8:22–33
Harriott VJ (1982) Sexual and asexual reproduction of Holothuria atra Jäger at Heron Island Reef, Great Barrier Reef. In: Rowe FWE (ed) Papers from the Echinoderm Conference, Australian Museum Memoir, vol 16, pp 53–66
Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel J-F, Mercier A (2004) (eds) Advances in sea cucumber aquaculture and management. Fisheries Technical Paper No 463. Rome, FAO, 425 p
Massin C (1982a) Food and feeding mechanisms: Holothuroidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. AA Balkema, Rotterdam, pp 43–55
Massin C (1982b) Effects of feeding on the environment: Holothuroidea. In: Jangoux M, Lawrence JM (eds) Echinoderm nutrition. AA Balkema, Rotterdam, pp 493–497
Morgan A (2000) Aspects of the reproductive cycle of the sea cucumber Holothuria scabra (Echinodermata: Holothuroidea). Bull Mar Sci 66:47–57
Ong Che RG, Gomez ED (1985) Reproductive periodicity of Holothuria scabra Jaeger at Calatagan, Batangas, Philippines. Asian Mar Biol 2:21–30
Pearse JS, Cameron RA (1991) Echinodermata: Holothuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates, vol VI. Echinoderms and lophophorates, pp 514–662
Preston GL (1990) Bêche-de-mer resource management studies in Guam. SPC Inf Bull Bêche-de-mer 1:8–9
Ramofafia C, Battaglene SC, Bell JD, Byrne M (2000) Reproductive biology of the commercial sea cucumber Holothuria fuscogilva in the Solomon Islands. Mar Biol 136:1045–1056
Ramofafia C, Byrne M, Battaglene S (2001) Reproductive biology of the intertidal sea cucumber Actinopyga mauritiana in the Solomon Islands. J Mar Biol Assoc UK 81:523–531
Ramofafia C, Byrne M, Battaglene S (2003) Reproduction of the commercial sea cucumber Holothuria scabra (Echinodermata: Holothuroidea) in the Solomon Islands. Mar Biol 142:281–288
Rees M, Colquhoun J, Smith L, Heyward A (2003) Surveys of Trochus, Holothuria, Giant Clams and the Coral Communities at Ashmore Reef, Cartier Reef and Mermaid Reef, Northwestern Australia. Report produced for Australian Government Department of Environment and Heritage. Australian Institute of Marine Science, Townsville, 64 p
Reichenbach N (1999) Ecology and fishery biology of Holothuria fuscogilva (Echinodermata: Holothuroidea) in the Maldives, Indian Ocean. Bull Mar Sci 64:103–113
Sewell MA (1992) Reproduction of the temperate aspidochirote Stichopus mollis (Echinodermata: Holothuroidea) in New Zealand. Ophelia 35:103–121
Sewell MA, Bergquist PR (1990) Variability in the reproductive cycle of Stichopus mollis (Echinodermata: Holothuroidea). Invertebr Reprod Dev 17:1–7
Sewell MA, Tyler PA, Young CM, Conand C (1997) Ovarian development in the class Holothuroidea: A reassessment of the “Tubule Recruitment Model”. Biol Bull 192:17–26
Simpson CJ (1991) Mass spawning of corals on Western Australian reefs and comparisons with the Great Barrier Reef. J R Soc West Aust 74:85–91
Smiley S (1988) The dynamics of oogenesis and the annual ovarian cycle of Stichopus californicus (Echinodermata: Holothuroidea). Biol Bull 175:79–93
Smiley S, Cloney RA (1985) Ovulation and fine structure of the Stichopus californicus (Echinodermata: Holothuroidea) fecund ovarian tubules. Biol Bull 169:342–364
Smiley S, McEuan F-S, Chaffee C, Krishan S (1991) Echinodermata: Holothuroidea. In: Giese AC, Pearse JS, Pearse VB (eds) Reproduction of marine invertebrates. Echinoderms and lophophorates, vol VI, The Boxwood Press, Pacific Grove, pp 663–750
Tuwo A, Conand C (1992) Reproductive biology of the holothurian Holothuria forskali (Echinodermata). J Mar Biolog Assoc UK 72:745–758
Underwood AJ (1997) Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, New York, 504 p
Uthicke S, Benzie JAH (2000a) Effect of bêche-de-mer fishing on densities and size structure of Holothuria nobilis (Echinodermata: Holothuroidea) populations on the Great Barrier Reef. Coral Reefs 19:271–276
Uthicke S, Benzie JAH (2000b) Allozyme electrophoresis indicates high gene flow between populations of Holothuria nobilis (Holothuroidea: Aspidochirotida) on the Great Barrier Reef. Mar Biol 137:819–825
Uthicke S, Karez R (1999) Sediment patch selectivity in tropical sea cucumbers (Holothuroidea: Aspidochirotida) analysed with multiple choice experiments. J Exp Mar Biol Ecol 236:69–87
Uthicke S, Klumpp DW (1998) Microbenthos community production in sediments of a near shore coral reef: seasonal variation and response to ammonium recycled by holothurians. Mar Ecol Prog Ser 169:1–11
Uthicke S, Benzie JAH, Ballment E (1998) Genetic structure of fissiparous populations of Holothuria (Halodeima) atra on the Great Barrier Reef. Mar Biol 132:141–151
Uthicke S, Benzie JAH, Ballment E (1999) Population genetics of the fissiparous holothurian Stichopus chloronotus (Aspidochirotida) on the Great Barrier Reef, Australia. Coral Reefs 18:123–132
Uthicke S, O’Hara TD, Byrne M (2004) Species composition and molecular phylogeny of the Indo-Pacific teatfish (Echinodermata: Holothuroidea) bêche-de-mer fishery. Mar Freshw Res 55:837–848
Yanigasawa T (1998) Aspects of the biology and culture if the sea cucumber. In: De Silva DD (ed) Tropical mariculture. Academic Press, London, pp 292–308
Acknowledgements
For the provision of funding and research infrastructure, we thank Oceanwest Fisheries, Exmouth, R Hall of the Bawinanga Aboriginal Corporation, and Glass Bottom Boats Ecology Cruises, Coral Bay. We are grateful to B Knott for assistance with earlier drafts of the manuscript and provision of laboratory facilities. GS is particularly grateful to N Malo, H Maitland and M Wolkenhauer for assistance in the field. We are also indebted to T Stewart for assistance with histology. The final manuscript benefited greatly from suggestions by Maria Byrne and two anonymous reviewers. This research was funded by an ARC SPIRT linkage grant to Brenton Knott and by a Fisheries Research Development Corporation (Project 98/133) grant to SU. Research was conducted in accordance with Conservation and Land Management (permit numbers NE002561, SF003283, SF003678) and Great Barrier Reef Marine Park Authority regulations (permit numbers G98/335, G99/281).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M.S. Johnson, Crawley
Rights and permissions
About this article
Cite this article
Shiell, G.R., Uthicke, S. Reproduction of the commercial sea cucumber Holothuria whitmaei [Holothuroidea: Aspidochirotida] in the Indian and Pacific Ocean regions of Australia. Marine Biology 148, 973–986 (2006). https://doi.org/10.1007/s00227-005-0113-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-005-0113-3