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Parasite diversity as an indicator of environmental change? An example from tropical grouper (Epinephelus fuscoguttatus) mariculture in Indonesia

Published online by Cambridge University Press:  15 February 2011

H. W. PALM*
Affiliation:
Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, 18059 Rostock, Germany
S. KLEINERTZ
Affiliation:
Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, 18059 Rostock, Germany Leibniz Center for Tropical Marine Ecology (ZMT) GmbH, Fahrenheitstrasse 6, 28359 Bremen, Germany
S. RÜCKERT
Affiliation:
Leibniz Center for Tropical Marine Ecology (ZMT) GmbH, Fahrenheitstrasse 6, 28359 Bremen, Germany Shimoda Marine Research Center, University of Tsukuba, 5-10-1, Shimoda, Shizuoka 415-0025, Japan
*
*Author to whom correspondence should be addressed: Tel: +49-381-498-3730. Fax: +49 381-498-3732. E-mail: harry.palm@uni-rostock.de, hpalm@gmx.net

Summary

Fish parasites are used to monitor long-term change in finfish grouper mariculture in Indonesia. A total of 210 Epinephelus fuscoguttatus were sampled in six consecutive years between 2003/04 and 2008/09 and examined for parasites. The fish were obtained from floating net cages of a commercially run mariculture facility that opened in 2001. The fauna was species rich, consisting of ten ecto- and 18 endoparasite species. The ectoparasite diversity and composition was relatively stable, with the monogeneans Pseudorhabdosynochus spp. (83–100% prevalence, Berger-Parker Index of 0·82–0·97) being the predominant taxon. Tetraphyllidean larvae Scolex pleuronectis and the nematodes Terranova sp. and Raphidascaris sp. 1 were highly abundant in 2003/04–2005/06 (max. prevalence S. pleuronectis 40%, Terranova sp. 57%, Raphidascaris sp. 1 100%), and drastically reduced until 2008/09. These parasites together with the prevalence of Trichodina spp., ecto-/endoparasite ratio and endoparasite diversity illustrate a significant change in holding conditions over the years. This can be either referred to a definite change in management methods such as feed use and fish treatment, or a possible transition of a relatively undisturbed marine environment into a more affected habitat. By visualizing all parameters within a single diagram, we demonstrate that fish parasites are useful bioindicators to monitor long-term change in Indonesian grouper mariculture. This also indicates that groupers can be used to monitor environmental change in the wild. Further taxonomic and systematic efforts in less sampled regions significantly contributes to this new application, supporting fish culture and environmental impact monitoring also in other tropical marine habitats.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Bell, S. and Morse, S. (2003). Measuring Sustainability: Learning by Doing. Earthscan Publications Ltd., London, Sterling, VAGoogle Scholar
Bray, R. A. and Palm, H. W. (2009). Bucephalids (Digenea: Bucephalidae) from marine fishes off thesouth-western coast of Java, Indonesia, including the description of two new species of and comments of the marine fish digenean fauna of Indonesia. Zootaxa 2223, 124.CrossRefGoogle Scholar
Bush, A. O., Lafferty, K. H., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575583.CrossRefGoogle Scholar
Diamant, A., Banet, A., Paperna, I., von Westernhagen, H., Broeg, K., Kruener, G., Koerting, W. and Zander, S. (1999). The use of fish metabolic, pathological and parasitological indices in pollution monitoring. II The Red Sea and Mediterranean. Helgoland Marine Research 53, 195208.CrossRefGoogle Scholar
Galli, P., Crosa, G., Mariniello, L., Ortis, M. and D'Amelio, S. (2001). Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia 452, 173179.CrossRefGoogle Scholar
Graney, R. L. Jr., Cherry, D. S. and Cairns, J. Jr. (1983). Heavy metal indicator potential of the Asiatic clam (Corbicula fluminea) in artificial stream systems. Hydrobiologia 102, 8188.CrossRefGoogle Scholar
DJPB (2009). Kinerja 2008 dan rencana 2009 perikanan budidaya. Disampaikan oleh direktur produksi-DJPB sebagai bahan diskuksi satgas perikanan budidaya, Cisaura, 05. February 2009.Google Scholar
Jakob, E. and Palm, H. W. (2006). Parasites of commercially important fish species from the southern Java coast, Indonesia, including the distribution pattern of trypanorhynch cestodes. Verhandlungen der Gesellschaft für Ichthyologie 5, 165191.Google Scholar
Khan, R. A. and Thulin, J. (1991). Influence of pollution on parasites of aquatic animals. Advances in Parasitology 30, 201238.CrossRefGoogle ScholarPubMed
Klein, B. (1926). Ergebnisse mit einer Silbermethode bei Ciliaten. Archiv für Protistenkunde. 56, 243279.Google Scholar
Klein, B. (1958). The “dry” silver method and its proper use. Journal of Protozoology 5, 99103.CrossRefGoogle Scholar
Klimpel, S. and Palm, H. W. (2011). Anisakid nematode (Ascaridoidea) life cycles and distribution: Increasing zoonotic potential in the time of climate change? In Progress in Parasitology (ed. Mehlhorn, H.), Düsseldorf University Press, Düsseldorf.Google Scholar
Klimpel, S., Rückert, S., Piatkowski, U., Palm, H. W. and Hanel, R. (2006). Diet and metazoan parasites of silver scabbard fish Lepidopus caudatus from the Great Meteor Seamount (North Atlantic). Marine Ecology Progress Series 315, 249257.CrossRefGoogle Scholar
Kuchta, R., Scholz, T., Vlčková, R., Říha, M., Walter, T. and Palm, H. W. (2009). Revision of tapeworms (Cestoda: Bothriocephalidea) from lizardfish (Saurida: Synodontidae) from the Indo-Pacific region. Zootaxa 1977, 5567.CrossRefGoogle Scholar
Lafferty, K. D. (1997). Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251255.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Allesina, S., Arim, M., Briggs, C. J., De Leo, G., Dobson, A. P., Dunne, J. A., Johnson, P. T. J., Kuris, A. M., Marcogliese, D. J., Martinez, N. D., Memmott, J., Marquet, P. A., McLaughlin, J. P., Mordecai, E. A., Pascual, M., Poulin, R. and Thieltges, D. W. (2008 a). Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533546.CrossRefGoogle ScholarPubMed
Lafferty, K. D., Shaw, J. C. and Kuris, A. M. (2008 b). Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. Ecohealth 5, 338345.CrossRefGoogle ScholarPubMed
Landsberg, J. H., Blakesley, B. A., Reese, R. O., McRae, G. and Forstchen, P. R. (1998). Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51, 211232.CrossRefGoogle Scholar
MacKenzie, K., Williams, H. H., Williams, B., McVicar, A. H. and Siddall, R. I. (1995). Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Advances in Parasitology 35, 86245.Google ScholarPubMed
Magurran, A. E. (1988). Ecological Diversity and its Measurement. Croom Helm, London.CrossRefGoogle Scholar
Marcogliese, D. J. (2005). Parasites of the superorganism: Are they indicators of ecosystem health? International Journal for Parasitology 35, 705716.CrossRefGoogle ScholarPubMed
Marcogliese, D. J. and Cone, D. K. (1997). Parasite communities as indicators of ecosystem stress. Parassitologia 39, 27232.Google ScholarPubMed
Mersch, J., Jeanjean, A., Spor, H. and Pihan, J.-C. (1992). The freshwater mussel Dreissena polymorpha as a bioindicator for trace metals, organochlorines, and radionuclides. Limnologia Akta 4, 227244.Google Scholar
Overstreet, R. M. (1997). Parasitological data as monitors of environmental health. Parassitologia 39, 169175.Google ScholarPubMed
Ogut, H. and Palm, H. W. (2005). Seasonal dynamics of Trichodina spp. on whiting (Merlangius merlangus) in relation to organic pollution on the eastern Black Sea coast of Turkey. Parasitology Research 96, 149153.CrossRefGoogle ScholarPubMed
Palm, H. W. (1999). Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitology Research 85, 638646.CrossRefGoogle ScholarPubMed
Palm, H. W. (2000). Trypanorhynch cestodes from Indonesian coastal waters (East Indian Ocean). Folia Parasitologica 47, 123134.CrossRefGoogle ScholarPubMed
Palm, H. W. (2004). The Trypanorhyncha Diesing, 1863. IPB-PKSPL-Press, Bogor.Google Scholar
Palm, H. W. (2008). Surface ultrastructure of the elasmobranchia parasitizing Grillotiella exilis and Pseudonybelinia odontacantha (Trypanorhyncha, Cestoda). Zoomorphology 127, 249258.CrossRefGoogle Scholar
Palm, H. W. (2011). Fish parasites as biological indicators in a changing world: Can we monitor environmental impact and climate change? In Progress in Parasitology (ed. Mehlhorn, H.), Düsseldorf University Press, Düsseldorf.Google Scholar
Palm, H. W., Damriyasa, I. M., Linda, and Oka, I. B. M. (2008). Molecular genotyping of Anisakis Dujardin, 1845 (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia. Helminthologia 45, 312.CrossRefGoogle Scholar
Palm, H. W. and Dobberstein, R. C. (1999). Occurrence of trichodinid ciliates (Peritricha: Urceolariidae) in the Kiel Fjord, Baltic Sea, and its possible use as a biological indicator. Parasitology Research 85, 726732.CrossRefGoogle ScholarPubMed
Palm, H. W., Klimpel, S. and Walter, T. (2007). Demersal fish parasite fauna around the South Shetland Islands: high species richness and low host specificity in deep Antarctic waters. Polar Biology 30, 15131522.CrossRefGoogle Scholar
Palm, H. W. and Overstreet, R. (2000). New records of trypanorhynchs from the Gulf of Mexico, including Kotorella pronosoma (Stossich, 1901) and Heteronybelinia palliata (Linton, 1924) nov. comb. Folia Parasitologica 47, 293302.CrossRefGoogle Scholar
Palm, H. W. and Rückert, S. (2009). A new approach to visualize ecosystem health by using parasites. Parasitology Research 105, 539553.CrossRefGoogle ScholarPubMed
Riemann, F. (1988). Nematoda. In Introduction to the Study of Meiofauna (eds. Higgins, R. P. and Thiel, H.), pp. 293301. Smithsonian Institution Press, Washington, DC.Google Scholar
Rückert, S., Hagen, W., Yuniar, A. T. and Palm, H. W. (2009 a). Metazoan parasites of fishes and their potential use as biological indicators in the Segara Anakan Lagoon, Indonesia. Regional and Environmental Change 9, 315328.CrossRefGoogle Scholar
Rückert, S., Klimpel, S., Al-Quraishy, S., Mehlhorn, H. and Palm, H. W. (2009 b). Transmission of fish parasites into grouper mariculture (Serranidae: Epinephelus coioides (Hamilton, 1822)) in Lampung Bay, Indonesia. Parasitology Research 104, 523532.CrossRefGoogle ScholarPubMed
Rückert, S., Klimpel, S. and Palm, H. W. (2009 c). Parasites of cultured and wild brown-marbled grouper Epinephelus fuscoguttatus (Forsskal, 1775) in Lampung Bay, Indonesia. Aquaculture Research, 112 doi:10.1111/j.1365-2109.2009.02403.xGoogle Scholar
Rückert, S., Palm, H. W. and Klimpel, S. (2008). Parasite fauna of seabass (Lates calcarifer) under mariculture conditions in Lampung Bay, Indonesia. Journal of Applied Ichthyology 24, 321327.CrossRefGoogle Scholar
Sasal, P., Mouillot, D., Fichez, R., Chifflet, S. and Kulbicki, M. (2007). The use of fish parasites as biological indicators of anthropogenic influences in coral-reef lagoons: A case study of Apogonidae parasites in New-Caledonia. Marine Pollution Bulletin 54, 16971706.CrossRefGoogle ScholarPubMed
Shuanglin, D., Kehou, P. and Brockmann, U. (2000). Review on effects of mariculture on coastal environment. Journal of the Ocean University Qingdao 30, 572582.Google Scholar
Sures, B. (2003). Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, 5360.CrossRefGoogle Scholar
Sures, B. and Reimann, N. (2003). Analysis of trace metals in the Antarctic host-parasite system Notothenia coriiceps and Aspersentis megarhynchus (Acanthocephala) caught at King George Island, South Shetland Islands. Polar Biology 26, 680686.CrossRefGoogle Scholar
Sures, B. and Siddall, R. (2003). Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) as an indicator of metal pollution. International Journal for Parasitology 33, 6570.CrossRefGoogle ScholarPubMed
Vidal-Martínez, V. M., Aguirre-Macedo, M. L., Vivas-Rodríguez, C. M. and Moravec, F. (1998). The macroparasite communities of the red grouper, Epinephelus morio, from the Yucatan Peninsula, Mexico. Proceedings of the 50th Annual meeting of The Gulf and Caribbean Fisheries Institute, November 9–14, Mérida, Yucatán. 764779.Google Scholar
Vidal-Martínez, V. M., Pech, D., Sures, B., Purucker, S. T. and Poulin, R. (2010). Can parasites really reveal environmental impact? Trends in Parasitology 26, 4451.CrossRefGoogle ScholarPubMed
Williams, H. H. and MacKenzie, K. (2003). Marine parasites as pollution indicators: an update. Parasitology 126 (Suppl.) S27S41.CrossRefGoogle ScholarPubMed
Yeomans, W. E., Chubb, J. C. and Sweeting, R. A. (1997). Use of protozoan communities for pollution monitoring. Parassitologia 39, 201212.Google ScholarPubMed
Yuniar, A. T., Palm, H. W. and Walter, T. (2007). Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia. Parasitology Research 100, 11931204.CrossRefGoogle ScholarPubMed