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RESEARCH ARTICLE

Species composition and molecular phylogeny of the Indo-Pacific teatfish (Echinodermata : Holothuroidea) bêche-de-mer fishery

Sven Uthicke A D , Tim D. O’Hara B and Maria Byrne C
+ Author Affiliations
- Author Affiliations

A Australian Institute of Marine Science, PMB No 3, Townsville, Qld 4810, Australia.

B Museum Victoria, GPO Box 666E, Melbourne, Vic. 3001, Australia.

C Department of Anatomy and Histology, F13, University of Sydney, NSW 2006, Australia.

D Corresponding author. Email: s.uthicke@aims.gov.au

Marine and Freshwater Research 55(8) 837-848 https://doi.org/10.1071/MF04226
Submitted: 23 August 2004  Accepted: 25 October 2004   Published: 16 November 2004

Abstract

Using mtDNA sequences we found that the Indo-Pacific teatfish fishery comprises at least three species, clarifying confusion on the taxonomic status of these commercially important holothurians. Traditional taxonomic characters, including the morphology of skeletal structures, could not be used to differentiate the species. Sequences of the COI gene (529 bp) distinguished three haplotype clusters, corresponding to distinct colour forms and, to some extent, previously described species. The white teatfish, Holothuria fuscogilva, comprises a range of colour morphs and has a wide distribution over the tropical Indo-Pacific region. The large sequence divergence indicates potential for the presence of several cryptic species in the white teatfish complex. In contrast to current taxonomy, we identified two species of black teatfish that appear to be allopatric: H. whitmaei is entirely black and has a Pacific distribution; whereas H. nobilis has white ventro-lateral dots and only occurs in the Indian Ocean. There is evidence for allopatric speciation between the black teatfish species, possibly driven by separation of the oceans and altered current patterns during the Pliocene, resulting in relatively young species with low intraspecific sequence divergence. These results provide insight into speciation in these tropical holothurians and are crucial for their conservation management.

Extra keywords: Aspidochirotida, diversity and conservation, Holothuriidae, invertebrate fishing, sea cucumber, taxonomy.


Acknowledgments

This study was funded internally by Museum Victoria and by a grant (to MB) from the Raine Island Corporation. Drs C. Massin and F. Rowe provided very helpful comments on the manuscript. We are especially grateful for advice and comments from Prof. C. Conand. Dr P. Cisternas, Dr A. Hoggett, Ms I. Falkner, Ms A. Smoothey and Mr T. Schultz assisted with collection of specimens. We are very grateful to Dr N. Reichenbach (Liberty University, Lynchburg, USA), Mr R. Aumeeruddy (Seychelles Fishing Authority, Victoria, Seychelles), Dr K. Friedman (Secretariat of the Pacific Community, Noumea, New Caledonia), Mr M. I. Ahmed (Hull University, Egypt), Mr T. Skewes (CSIRO, Brisbane, Australia), Mr P. Bacchet and C. Monier (Tahiti) for providing photos of teatfish in different areas. Dr P. Bock (Deakin University, Australia) assisted with SEM. Special thanks go to Dr I. Eeckhaut (University of Mons-Hainaut, Belgium) for the provision of the sequences from Madagascar specimens.


References

Anon.  (1984). ‘Shallow Water Holothurians of Calatagan, Batangas, Philippines.’ (Filipinas Foundation, Inc., and the University of the Philippines: Manilla.)

Arndt, A. , Marquez, C. , Lampert, O. , and Smith, M. J. (1996). Molecular phylogeny of eastern Pacific sea cucumbers (Echinodermata: Holothuroidea) based on mitochondrial DNA sequence. Molecular Phylogenetics and Evolution 6, 425–437.
Crossref | GoogleScholarGoogle Scholar | Byrne M., Smoothey A., Hoggett A., and Uthicke S. (in press a). Population biology of shallow water holothuroids and ophiuroids from Raine Island and Moulter Cay, Northern Great Barrier Reef. In ‘Proceedings of 11th International Echinoderms Conference, Munich’. (Eds T. Heinzeller and J. H. Nebelsick.) (Balkema: Lisse.)

Byrne M., Cisternas P., Hoggett A., O’Hara T., and Uthicke S. (in press b). Diversity of echinoderms at Raine Island, Great Barrier Reef. In ‘Proceedings of 11th International Echinoderms Conference, Munich’. (Eds T. Heinzeller and J. H. Nebelsick.) (Balkema: Lisse.)

Cherbonnier, G. (1952). Les Holothuries de Quoy et Gaimard. Mémoires de l’Institut Royal des Sciences Naturelles de Belgique 44, 1–50.
Cherbonnier G. (1988). ‘Faune de Madagascar. 70. Echinodermes: Holothurides.’ (Centre National de la Recherche Scientifique: Paris.)

Clark A. M., and Rowe F. W. E. (1971). ‘Monograph of Shallow-water Indo-west Pacific Echinoderms.’ (Trustees of the British Museum (Natural History): London.)

Clark, H.L. (1921). The echinoderm fauna of Torres Strait. Papers from the Department of Marine Biology of the Carnegie Institution of Washington 10, 1–224.
Conand C. (1989). ‘Les Holothuries Aspidochirotes du Lagon de Nouvelle-Calédonie: Biologie, Écologie et Exploitation. Etudes et These.’ (ORSTOM: Paris.)

Conand C. (1990). The fishery Resources of Pacific Island countries. Part 2. Holothurians. FAO Fisheries Technical Paper 272.2, Rome.

Conand, C. (1993). Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Marine Biology 116, 439–450.
Conand C. (1998a). Overexploitation in the present world sea cucumber fisheries and perspectives in aquaculture. In ‘Echinoderms: San Francisco. Proceedings of the 9th International Echinoderm Conference, San Francisco, California, USA, 5–9 August 1996’. (Eds R. Mooi and M. Telford.) pp. 449–454. (Balkema: Rotterdam.)

Conand C. (1998b). Holothurians. In ‘FAO Species Identification Guide. The Marine Living Resources of the Western Central Pacific. Vol 2 Cephalopods, Crustaceans, Holothurians and Sharks’. (Eds K. Carpenter and V. Niem.) pp. 1157–1190. (FAO: Rome.)

Conand C. (1999). Manuel de qualité des holothuries du sud-ouest de l’ocean indien. Commission Océan Indien, Paris.

Conand C. (2001). Overview over the last decade of sea cucumber fisheries – what possibilities for a durable management? In ‘Echinoderms 2000, Proceedings of the 10th International Conference, Dunedin, New Zealand’. (Ed. M. Barker.) pp. 339–344.

Conand, C. , and Byrne, M. (1993). A review of recent developments in the world sea cucumber fisheries. Marine Fisheries Review 55, 1–13.
Forbes R., and Baine M. (Eds) (1998). ‘A Field Guide to Sea Cucumbers of Malaysia.’ (Heriot-Watt University: Scotland.)

Gosliner T. M., Behrens D. W., and Williams G. C. (1996). ‘Coral Reef Animals of the Indo-Pacific.’ (Sea Challengers: Monterey, CA.)

Grant, W. S. , and Bowen, B. W. (1998). Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. The Journal of Heredity 89, 415–426.
Crossref | GoogleScholarGoogle Scholar | Lincoln Smith M. P., Bell J. D., Ramohia P., and Pitt K. A. (2000). Testing the use of marine protected areas to restore and manage tropical multispecies invertebrate fisheries at Arnavon Islands, Solomon Islands. Great Barrier Reef Marine Park Authority Research Publication 69, Townsville.

Lovatelli A., Conand C., Purcell S., Uthicke S., Hamel J. F., and Mercier A. (Eds) (2004). Advances in sea cucumber aquaculture and management. FAO Report no. 463, Rome.

Martinez P. C., and Richmond R. H. (1998). Effects of diet on growth and larval development of the sea cucumber Holothuria nobilis in Guam. In ‘Echinoderms: San Francisco. Proceedings of the 9th International Echinoderm Conference, San Francisco, California, USA, 5–9 August 1996’. (Eds R. Mooi and M. Telford.) p. 480. (Balkema: Rotterdam.) [Abstract]

Massin, C. (1996). The holothurians from Easter Island. Bulletin de l’Institut royal des Sciences naturelles de Belgique, Biologie 66, 151–178.
Quoy J. R. C., and Gaimard P. (1833). ‘Voyage de découvertes de l’Astrolabe: Zoologie: Zoophytes.’ (J. Tastu: Paris.)

Ramofafia, C. , Battaglene, S. C. , Bell, J. D. , and Byrne, M. (2000). Reproductive biology of the commercial sea cucumber, Holothuria fuscogilva in the Solomon Islands. Marine Biology 136, 1045–1056.
Crossref | GoogleScholarGoogle Scholar | Rowe F. W. E., and Gates J. (1995). ‘Zoological Catalogue of Australia. Vol. 33. Echinodermata.’ (CSIRO Publishing: Melbourne.)

Russell B. C., and Vail L. L. (1988). ‘Field Guide to Marine Fauna and Flora collected by Indonesian Fishermen at Ashmore Reef Northwestern Australia.’ (Australian National Parks and Wildlife Service: Canberra.)

Samyn Y. (2003). Towards an understanding of the shallow-water holothuroid fauna (Echinodermata: Holothuroidea) of the western Indian Ocean. Ph.D. thesis, University of Brussels.

Saville-Kent W. (1890). ‘Bêche-de-mer and Pearl-shell Fisheries of Northern Queensland.’ (Queensland Government Publisher: Brisbane.)

Selenka, E. (1867). Beiträge zur Anatomie und Systematik der Holothurien. Zeitschrift der Wissenschaftlichen Zoologie 17, 291–374.
Schneider S., Roessli D., and Excoffier L. (2000). ‘Arlequin ver. 2.000: A software for Population Genetic Data Analysis.’ (Genetics and Biometry Laboratory, University of Geneva: Switzerland.) Available at http://anthro.unige.ch/arlequin [Verified 10 November 2004]

Schoppe S. (2000). ‘Echinoderms of the Philippines.’ (Times Editions: Singapore.)

Trianni, M. S. (2002). Summary of data collected from the sea cucumber fishery on Rota, Commonwealth of the Northern Mariana Islands. SPC Bêche-de-mer Information Bulletin 16, 5–11.
Uthicke S. (2004). Over fishing of holothurians: lessons from the Great Barrier Reef. In ‘Advances in sea cucumber aquaculture and management. Fao Report No. 463’. (Eds A. Lovatelli, C. Conand, S. Purcell, S. Uthicke, J. F. Hamel and A. Mercier.) pp. 163–171. (FAO: Rome.)

Uthicke, S. , and Benzie, J. A. H. (2000a). The effect of bêche-de-mer fishing on densities and size structure of Holothuria nobilis (Echinodermata: Holothurioidea) populations on the Great Barrier Reef. Coral Reefs 19, 271–276.


Uthicke, S. , and Benzie, J. A. H. (2000b). Allozyme electrophoresis indicates high gene flow between populations of Holothuria nobilis (Holothuroidea: Aspidochirotida) on the Great Barrier Reef. Marine Biology 137, 819–825.
Crossref | GoogleScholarGoogle Scholar |

Uthicke, S. , and Benzie, J. A. H. (2002). A genetic fingerprint recapture technique for measuring growth in ‘unmarkable’ invertebrates: negative growth in commercially fished holothurians (Holothuria nobilis). Marine Ecology Progress Series 241, 221–226.


Uthicke, S. , and Benzie, J. A. H. (2003). Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific. Molecular Ecology 12, 2635–2648.
Crossref | GoogleScholarGoogle Scholar |

Uthicke, S. , Welch, D. , and Benzie, J. A. H. (2004). Slow growth and lack of recovery in overfished holothurians on the Great Barrier Reef: Evidence from DNA fingerprints and repeated large-scale surveys. Conservation Biology 18, 1395–1404.


Vanden Spiegel, D. , Jangoux, M. , and Flammang, P. (2000). Maintaining the line of defense: regeneration of cuverian tubules in the sea cucumber Holothuria forskali (Echinodermata, Holothurioidea). Biological Bullutin 198, 34–49.


Williams, T. S. , and Benzie, J. A. H. (1998). Evidence of a biogeographical break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by colour morphs, mtDNA and allozyme data. Evolution 52, 87–99.