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The ecological role of Holothuria scabra (Echinodermata: Holothuroidea) within subtropical seagrass beds

Published online by Cambridge University Press:  09 July 2009

Svea-Mara Wolkenhauer*
Affiliation:
Institute for Biodiversity Research, University of Rostock, Universitätsplatz 2, 18055 Rostock, Germany CSIRO Marine & Atmospheric Research, PO Box 120, Cleveland, Queensland 4163, Australia
Sven Uthicke
Affiliation:
Australian Institute of Marine Science, Townsville MC, Queensland 4810, Australia
Charis Burridge
Affiliation:
CSIRO Mathematical and Information Sciences, PO Box 120, Cleveland, Queensland 4163, Australia
Timothy Skewes
Affiliation:
CSIRO Marine & Atmospheric Research, PO Box 120, Cleveland, Queensland 4163, Australia
Roland Pitcher
Affiliation:
CSIRO Marine & Atmospheric Research, PO Box 120, Cleveland, Queensland 4163, Australia
*
Correspondence should be addressed to: S.-M. Wolkenhauer, Institute for Biodiversity Research, University of Rostock, Universitätsplatz 2, 18055 Rostock, Germany email: [email protected]

Abstract

Some sea cucumbers species are heavily exploited as bêche-de-mer for the Asian food industry and the global decline of certain highly sought after species has generated an interest in determining the ecological function of those animals within their ecosystem. This study investigated the ecological role of Holothuria scabra, a commercially valuable tropical species closely associated with seagrass beds. Seagrass productivity, seagrass and benthic microalgae (BMA) biomass and organic matter (OM) were measured during two exclusion experiments conducted using in situ cages deployed for two months both in 2003 and 2004. Density of H. scabra was manipulated in caged exclusions (near-zero density, ‘EX’), caged controls (natural densities, ‘CC’) and uncaged controls (natural density, ‘NC’). Seagrass growth was lower when holothurians were excluded (5% in 2003, 12% in 2004). Seagrass biomass decreased in all treatments, but reduction was greater in EX than in controls (18% in 2003, 21% in 2004). Both BMA biomass and OM increased in EX compared to NC/CC (in 2004). From a multivariate perspective, a principal component biplot separated EX from both types of controls in 2004, and multivariate tests based on four attributes supported this separation. These results indicate that seagrass systems may suffer in the absence of holothurians; however, the effect size varied between the two experiments, possibly because experiments were conducted at different times of the year. Nevertheless, our results suggest that holothurian over-fishing could have a negative impact on the productivity of seagrass systems.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Akamine, J. (2002) Trepang exploitation in the Philippines: updated information. South Pacific Commission Bêche-de-mer Information Bulletin 17, 1721.Google Scholar
Birch, W.R. and Birch, M. (1984) Succession and pattern of tropical intertidal seagrasses in Cockle Bay, Queensland, Australia: a decade of observations. Aquatic Botany 19, 343367.CrossRefGoogle Scholar
Boon, P.I. (1986) Nitrogen pools in seagrass beds of Cymodocea serrulata and Zostera capricorni of Moreton Bay. Aquatic Botany 25, 119.CrossRefGoogle Scholar
Coleman, F.C. and Williams, S.L. (2002) Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends in Ecology and Evolution 17, 4044.CrossRefGoogle Scholar
Conand, C. (2001) Sea cucumber retail market in Singapore. South Pacific Commission Bêche-de-mer Information Bulletin 14, 1214.Google Scholar
Conand, C. (2004) Present status of world sea cucumber resources and utilization: an international overview. In Lovatelli, A., Conand, C., Purcell, S., Uthicke, S., Hamel, J.F. and Mercier, A. (eds) Advances in sea cucumber aquaculture and management. Rome: FAO Fisheries Technical Paper 463, pp. 1323.Google Scholar
de Boer, W.F. (2000) Biomass dynamics of seagrasses and the role of mangrove and seagrass vegetation as different nutrient sources for an intertidal ecosystem. Aquatic Botany 66, 225239.CrossRefGoogle Scholar
de Jonge, V.N. and van den Bergs, J. (1987) Experiments on the resuspension of estuarine sediments containing benthic diatoms. Estuarine, Coastal and Shelf Science 24, 725740.CrossRefGoogle Scholar
Enriquez, S. (2005) Light absorption efficiency and the package effect in the leaves of the seagrass Thalassia testudinum. Marine Ecology Progress Series 289, 141150.CrossRefGoogle Scholar
Grall, J. and Chauvaud, L. (2002) Marine eutrophication and benthos: the need for new approaches and concepts. Global Change Biology 8, 813830.CrossRefGoogle Scholar
Hamel, J.-F., Conand, C., Paeson, D.L. and Mercier, A. (2001) The sea cucumber Holothuria scabra (Holothuroidea: Echinodermata): its biology and exploitation as bêche-de-mer. Advances in Marine Biology 41, 129223.CrossRefGoogle Scholar
Haywood, M.D.E., Vance, D.J. and Loneragan, N.R. (1995) Seagrass and algal beds as nursery habitats for tiger prawns (Penaeus semisulcatus and P. esculentus) in a tropical Australian estuary. Marine Biology 122, 213223.CrossRefGoogle Scholar
Heck, K.L. and Valentine, J.F. (2007) The primacy of top-down effects in shallow benthic ecosystems. Estuaries and Coasts 30, 371381.CrossRefGoogle Scholar
Hughes, A.R., Bando, K.J., Rodriguez, L.F. and Williams, S.L. (2004) Relative effects of grazers and nutrients on seagrasses: a meta-analysis approach. Marine Ecology Progress Series 282, 8799.CrossRefGoogle Scholar
Kamal, A., Misri, K., Japar, S., Hishamuddin, O. and Hidir, H. (1999) Leaf growth, production and ecological aspects of toothed seagrass Cymodocea serrulata (R. Br.) Aschers. et Magnus at Port Dickson, Negeri Sembilan, Malaysia. In International Conference on the International Oceanographic Data and Information Exchange in the Western Pacific (IODE–WESTPAC—ICIWP ’99), Langkawi (Malaysia), 1–4 November 1999. Paris, France: IOC, pp. 173184.Google Scholar
Kelly, M.S. (2005). Echinoderms: their culture and bioactive compounds. In Matranga, V. (ed.) Progress in molecular and subcellular biology, Volume 39. Berlin and Heidelberg: Springer-Verlag, pp. 139165.Google Scholar
Kitano, M., Kurata, K., Kozuki, Y., Murakami, H., Yamasaki, T., Yoshida, H. and Sasayama, H. (2003) Effects of deposit feeder Stichopus japonicus on algal bloom and organic matter contents of bottom sediments of the enclosed sea. Marine Pollution Bulletin 47, 118125.Google Scholar
Klumpp, D.W. and Kwak, S.N. (2005) Composition and abundance of benthic macrofauna of a tropical sea-grass bed in North Queensland, Australia. Pacific Science 59, 541560.CrossRefGoogle Scholar
Lanyon, J.M. and Marsh, H. (1995) Temporal changes in the abundance of some tropical intertidal seagrasses in North Queensland. Aquatic Botany 49, 217237.CrossRefGoogle Scholar
Lundberg, J. and Moberg, F. (2003) Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6, 8798.CrossRefGoogle Scholar
Marbà, N., Cebrián, J., Enríquez, S. and Duarte, C.M. (1996) Growth patterns of West Mediterranean seagrasses: species-specific responses to seasonal forcing. Marine Ecology Progress Series 133, 203215.CrossRefGoogle Scholar
Mercier, A., Battaglene, S.C. and Hamel, J.-F. (1999) Daily burrowing cycle and feeding activity of juvenile sea cucumbers Holothuria scabra in response to environmental factors. Journal of Experimental Marine Biology and Ecology 239, 125156.CrossRefGoogle Scholar
Mercier, A., Battaglene, S.C. and Hamel, J.-F. (2000a) Settlement preferences and early migration of the tropical sea cucumber Holothuria scabra. Journal of Experimental Marine Biology and Ecology 249, 89110.CrossRefGoogle ScholarPubMed
Mercier, A., Battaglene, S.C. and Hamel, J.-F. (2000b) Periodic movement, recruitment and size-related distribution of the sea cucumber Holothuria scabra in Solomon Islands. Hydrobiologia 440, 81100.CrossRefGoogle Scholar
Moriarty, D.J.W., Pollard, P.C., Hunt, W.G., Moriarty, C.M. and Wassenberg, T.J. (1985) Productivity of bacteria and microalgae and the effect of grazing by holothurians in sediments on a coral reef flat. Marine Biology 85, 293300.CrossRefGoogle Scholar
Mosher, C. (1980) Distribution of Holothuria arenicola Semper in the Bahamas with observations on habitat, behaviour and feeding activity (Echinodermata: Holothuroidea). Bulletin of Marine Science 30, 112.Google Scholar
Nakaoka, M. (2005) Plant–animal interaction in seagrass beds: ongoing and future challenges for understanding population and community dynamics. Population Ecology 47, 167177.CrossRefGoogle Scholar
Parsons, T.R., Maita, Y. and Lalli, C.M. (1984) A manual of chemical and biological methods for seawater analysis. Oxford: Pergamon Press.Google Scholar
Pollard, P.C. and Greenway, M. (1993) Photosynthetic characteristics of seagrasses (Cymodocea serrulata, Thalassia hemprichii and Zostera capricorni) in a low-light environment, with a comparison of leaf-marking and lacunal–gas measurements of productivity. Australian Journal of Marine and Freshwater Research 44, 127139.CrossRefGoogle Scholar
Purcell, S. (2004) Rapid growth and bioturbation activity of the sea cucumber Holothuria scabra in earthen ponds. In Proceedings of Australasian Aquaculture, Sydney, p. 244.Google Scholar
Skewes, T., Dennis, D., Wassenberg, T.J., Austin, M., Moeseneder, C., Koutsoukos, A., Haywood, M., Pendrey, R. and Bustamante, R. (2002) Surveying the distribution and abundance of Holothuria scabra (sandfish) in Moreton Bay. Brisbane: CSIRO Division of Marine Research Final Report.Google Scholar
Skewes, T.D., Taylor, S., Dennis, D.M., Haywood, M.E.D. and Donovan, A. (2006) Sustainability assessment of the Torres Strait sea cucumber fishery. Brisbane: CSIRO Marine & Atmospheric Research, pp. 50.Google Scholar
Tegner, M.J. and Dayton, P.K. (1999) Ecosystem effects of fishing. Trends in Ecology and Evolution 14, 261262.CrossRefGoogle ScholarPubMed
Udy, J.W. and Dennison, W.C. (1997) Growth and physiological response of three seagrass species to elevated sediment nutrients in Moreton Bay, Australia. Journal of Experimental Marine Biology and Ecology 217, 253277.CrossRefGoogle Scholar
Uthicke, S. (1999) Sediment bioturbation and impact of feeding activity of Holothuria (Halodeima) atra and Stichopus chloronotus, two sediment feeding holothurians, at Lizard Island, Great Barrier Reef. Bulletin of Marine Science 64, 129141.Google Scholar
Uthicke, S. (2001a) Interactions between sediment-feeders and microalgae on coral reefs: grazing losses versus production enhancement. Marine Ecology Progress Series 210, 125138.CrossRefGoogle Scholar
Uthicke, S. (2001b) Nutrient regeneration by abundant coral reef holothurians. Journal of Experimental Marine Biology and Ecology 265, 153170.CrossRefGoogle Scholar
Uthicke, S. (2004) Overfishing of holothurians: lesson from the Great Barrier Reef. South Pacific Commission Bêche-de-mer Information Bulletin 19, 9.Google Scholar
Uthicke, S. and Klumpp, D.W. (1998) Microphytobenthos community production at a near-shore coral reef: seasonal variation and response to ammonium recycled by holothurians. Marine Ecology Progress Series 169, 111.CrossRefGoogle Scholar
Uthicke, S. and Benzie, J.A.H. (2000) Allozyme electrophoresis indicates high gene flow between populations of Holothuria (Microthele) nobilis (Holothuroidea: Aspidochirotida) on the Great Barrier Reef. Marine Biology 137, 819825.CrossRefGoogle Scholar
van Eys, S. (1986) The international market for sea cucumber. Infofish Marketing Digest 5, 4144.Google Scholar
Wiedemeyer, W.L. (1992) Feeding behaviour of two tropical holothurians, Holothuria (Metriatyla) scabra (Jaeger 1833) and H. (Halodeima) atra (Jaeger 1833), from Okinawa, Japan. In Richmond, R.H. (ed.) Proceedings of the 7th International Coral Reef Symposium, Volume 2. Mangilao, Guam: University of Guam Press, pp. 853860.Google Scholar
Wolkenhauer, S.-M. (2008) Burying and feeding activity of adult Holothuria scabra (Echinodermata: Holothuroidea) in a controlled environment. South Pacific Commission Bêche-de-mer Information Bulletin 27, 2528.Google Scholar
Zavodnik, N., Travizi, A. and De Rosa, S. (1998) Seasonal variations in the rate of photosynthetic activity and chemical composition of the seagrass Cymodocea nodosa (Ucr.) Asch. Scientia Marina 62, 301309.CrossRefGoogle Scholar
Zieman, J.C. (1974) Methods for the study of the growth and production of turtle grass, Thalassia testudinum König. Aquaculture 4, 139143.CrossRefGoogle Scholar