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Parasites of the grouper fish Epinephelus coioides (Serranidae) as potential environmental indicators in Indonesian coastal ecosystems

Published online by Cambridge University Press:  10 September 2013

S. Kleinertz  and
H.W. Palm
S. Kleinertz*
Affiliation:
Institute of Parasitology, Justus Liebig University Giessen, D-35392Giessen, Germany Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, D-18059Rostock, Germany
H.W. Palm
Affiliation:
Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, D-18059Rostock, Germany Faculty of Veterinary Medicine, UDAYANA University, Denpasar, Bali, Indonesia
*
*Fax: +49 (0)641 99 38469 E-mail: [email protected]
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Abstract

A total of 195 Epinephelus coioides (Hamilton, 1822) were studied for fish parasites from Javanese (Segara Anakan lagoon) and Balinese waters. Up to 25 different parasite species belonging to the following taxa: one Ciliata, one Microsporea, five Digenea, one Monogenea, four Cestoda, four Nematoda, one Acanthocephala, one Hirudinea and seven Crustacea were identified with four new host and locality records. The dominant parasites included the monogenean Pseudorhabdosynochus lantauensis (53.3–97.1%), the nematode Spirophilometra endangae (23.3–42.9%), the digenean Didymodiclinus sp. (2.9–40.0%), the nematodes Philometra sp. (22.6–34.3%) and Raphidascaris sp. (2.9–28.6%), and the isopod Alcirona sp. (6.7–31.4%). Regional differences for E. coioides were found in terms of endoparasite diversity, total diversity according to Shannon–Wiener, Simpson index and Evenness. A comparison with published data from Sumatera revealed highest endoparasite diversity (Shannon–Wiener: 1.86/1.67–2.04) and lowest ectoparasite/endoparasite ratio (0.73/0.57–0.88) off the Balinese coast, followed by Lampung Bay, Sumatera (1.84; 0.67), off the coast of Segara Anakan lagoon (1.71; 0.71), and in the lagoon (0.30/0.19–0.66; 0.85/0.67–1.00). The presented data demonstrate the natural range of these parameters and parasite prevalences according to habitat and region, allowing adjustment of the scale that has been used in the visual integration of the parasite parameters into a star graph. The parasite fauna of E. coioides in Segara Anakan lagoon ‘improved’ from 2004 until 2008/09, possibly related to earlier oil spill events in 2002 and 2004. The use of grouper fish parasites as an early warning system for environmental change in Indonesian coastal ecosystems is discussed.

Type
Research Papers
Information
Journal of Helminthology , Volume 89 , Issue 1 , January 2015 , pp. 86 - 99
Copyright
Copyright © Cambridge University Press 2013 

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References

Arthur, J.R. (1997) Recent advances in the use of parasites as biological tags for marine fish. pp. 141–154in Flegel, T.W. & MacRae, I.H. (Eds) Diseases in Asian aquaculture III. Fish Health Section. Manila, Asian Fisheries Society.Google Scholar
Bell, J.J. & Barnes, K.A. (2003) Effect of disturbance on assemblages: an example using Porifera. Biological Bulletin 205, 144–159.CrossRefGoogle ScholarPubMed
Bell, S. & Morse, S. (2003) Measuring sustainability: learning by doing. London, UK, Earthscan Publications.Google Scholar
Bray, R.A. & Palm, H.W. (2009) Bucephalids (Digenea: Bucephalidae) from marine fishes off the south-western coast of Java, Indonesia, including the description of two new species of Rhipidocotyle and comments on the marine fish digenean fauna of Indonesia. Zootaxa 2223, 1–24.Google Scholar
Bush, O., Lafferty, A.D., Lotz, J.M. & Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Carpenter, K.E. & Springer, V.G. (2005) The center of the center of marine shore fish biodiversity: the Philippine Islands. Environmental Biology of Fishes 72, 467–480.Google Scholar
Clarke, K.R. & Warwick, R.M. (1994) Change in marine communities: an approach to statistical analysis and interpretation. 144 pp. Plymouth, Plymouth Marine Laboratory.Google Scholar
Cooper, T.F., Gilmour, J.P. & Fabricius, K.E. (2009) Bioindicators of changes in water quality on coral reefs: review and recommendations for monitoring programmes. Coral Reefs 28, 589–606.Google Scholar
Dewi, K. & Palm, H.W. (2013) Two new species of philometrid nematodes (Nematoda: Philometridae) in Epinephelus coioides (Hamilton, 1822) from the South Bali Sea, Indonesia. Zootaxa 3609, 49–59.Google Scholar
Diamant, A., Banet, A., Paperna, I., von Westernhagen, H., Broeg, K., Kruener, G., Koerting, W. & 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, 195–208.CrossRefGoogle Scholar
DJPB, (2009) Kinerja 2008 dan rencana 2009 perikanan budidaya. Cisaura, Disampaikan oleh direktur produksi-DJPB sebagai bahan diskuksi satgas perikanan budidaya, 5 February.Google Scholar
Downs, C.A., Woodley, C.M., Richmond, R.H., Lanning, L.L. & Owen, R. (2005) Shifting the paradigm of coral-reef ‘health’ assessment. Marine Pollution Bulletin 51, 486–494.CrossRefGoogle ScholarPubMed
Dsikowitzky, L., Nordhaus, I., Jennerjahn, T., Khrycheva, P., Sivatharshan, Y., Yuwono, E. & Schwarzbauer, J. (2011) Anthropogenic organic contaminants in water, sediments and benthic organisms of the mangrove-fringed Segara Anakan Lagoon, Java, Indonesia. Marine Pollution Bulletin 62, 851–862.Google Scholar
Dzikowski, R., Paperna, I. & Diamant, A. (2003) Use of fish parasite species richness indices in analyzing anthropogenically impacted coastal marine ecosystems. Helgoland Marine Research 57, 220–227.Google Scholar
Grosser, C., Heidecke, D. & Moritz, G. (2001) Untersuchungen zur Eignung heimischer Hirudineen als Bioindikatoren für Fließgewässer. Hercynia N.F. 34, 101–127.Google Scholar
Hechinger, R.F., Lafferty, K.D., Huspeni, T.C., Andrew, J.B. & Armand, M.K. (2007) Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151, 82–92.Google Scholar
Holtermann, P., Burchard, H. & Jennerjahn, T. (2009) Hydrodynamics of the Segara Anakan lagoon. Regional Environmental Change 9, 245–258.Google Scholar
Jakob, E. & 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, 165–191.Google Scholar
Jennerjahn, T.C., Nasir, B. & Pohlenga, I. (2009) Spatio-temporal variation of dissolved inorganic nutrients related to hydrodynamics and land use in the mangrove-fringed Segara Anakan Lagoon, Java Indonesia. Regional Environmental Change 9, 259–274.Google Scholar
Justine, J.L., Beveridge, J., Boxshall, G.A., Bray, R.A., Moravec, F., Trilles, J.P. & Whittington, I.D. (2010) An annotated list of parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda and Nematoda) collected in groupers (Serranidae, Epinephelinae) in New Caledonia emphasizes parasite biodiversity in coral reef fish. Folia Parasitologica 57, 237–262.CrossRefGoogle ScholarPubMed
Khan, R.A. (1990) Parasitism in marine fish after chronic exposure to petroleum hydrocarbons in the laboratory and to the Exxon Valdez oil spill. Bulletin of Environmental Contamination and Toxicology 44, 759–763.Google Scholar
Khan, R.A. & Kiceniuk, J.W. (1988) Effects of petroleum aromatic hydrocarbons on monogeneids parasitizing Atlantic cod, Gadus morhua L. Bulletin of Environmental Contamination and Toxicology 41, 94–100.Google Scholar
Khrycheva, P. (2009) Anthropogenic contaminants in water and sediments from the Segara Anakan lagoon, Indonesia. Master of Science thesis in Marine Biology, University of Bremen.Google Scholar
Kiceniuk, J.W. (1983) Toxicology of chronic crude oil exposure: sublethal effects on aquatic organisms. pp. 425–536in Nraigu, J.O. (Ed.) Aquatic toxicology. New York, John Wiley.Google Scholar
Klein, B. (1926) Ergebnisse mit einer Silbermethode bei Ciliaten. Archiv für Protistenkunde 56, 243–279.Google Scholar
Klein, B. (1958) The ‘dry’ silver method and its proper use. Journal of Protozoology 5, 99–103.Google Scholar
Kleinertz, S. (2010) Fish parasites as bioindicators: Environmental status of coastal marine ecosystems and a grouper mariculture farm in Indonesia. PhD thesis of natural sciences, Faculty 2 (Biology/Chemistry), University of Bremen.Google Scholar
Kleinertz, S., Damriyasa, M., Hagen, W., Theisen, S. & Palm, H.W. (2012) An environmental assessment of the parasite fauna of the reef-associated grouper Epinephelus areolatus from Indonesian waters. Journal of Helminthology doi:10.1017/S0022149X12000715.Google Scholar
Klimpel, S., Rückert, S., Piatkowski, U., Palm, H.W. & 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, 249–257.Google Scholar
Kuchta, R., Scholz, T., Vlcková, R., Ríha, M., Walter, T., Yuniar, A.T. & Palm, H.W. (2009) Revision of tapeworms (Cestoda: Bothriocephalidea) from lizardfish (Saurida: Synodontidae) from the Indo-Pacific region. Zootaxa 1977, 55–67.CrossRefGoogle Scholar
Kuhn, T., Hailer, F., Palm, H.W. & Klimpel, S. (2013) Global assessment of molecular identified Anisakis spp. (Nematoda: Anisakidae) in the teleost intermediate host. Folia Parasitologica 4826, 1–29.Google Scholar
Kurtz, J.C., Jackson, L.E. & Fisher, W.S. (2001) Strategies for evaluating indicators based on guidelines from the Environmental Protection Agency's Office of Research and Development. Ecological Indicators 1, 49–60.Google Scholar
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. & Thieltges, D.W. (2008a) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Lafferty, K.D., Shaw, J.C. & Kuris, A.M. (2008b) Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kiritimati Island. Ecohealth 5, 338–345.Google Scholar
Landsberg, J.H., Blakesley, B.A., Reese, R.O., McRae, G. & Forstchen, P.R. (1998) Parasites of fish as indicators of environmental stress. Environmental Monitoring and Assessment 51, 211–232.Google Scholar
Magurran, A.E. (1988) Ecological diversity and its measurement. London, Croom Helm.Google Scholar
Munkittrik, K.R., Van der Kraak, G.J., McMaster, M.E., Portt, D.C.B., Van den Heuval, M.R. & Servos, M.R. (1994) Survey of receiving-water environmental impacts associated with discharges from pulp mills. II. Gonad size, liver size, hepatic EROD activity and plasma sex steroid levels in white sucker. Environmental Toxicology and Chemistry 13, 1089–1101.Google Scholar
Nordhaus, I., Hadipudjana, F.A., Janssen, R. & Pamungkas, J. (2009) Spatio-temporal variation of macrobenthic communities in the mangrove-fringed Seagara Anakan lagoon. Indonesia, affected by anthropogenic activities. Regional Environmental Change 9, 291–313.Google Scholar
Ogut, H. & 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, 149–153.Google Scholar
Overstreet, R.M. (1997) Parasitological data as monitors of environmental health. Parassitologia 39, 169–175.Google Scholar
Palm, H.W. (1999) Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitology Research 85, 638–646.Google Scholar
Palm, H.W. (2000) Trypanorhynch cestodes from Indonesian coastal waters (East Indian Ocean). Folia Parasitologica 47, 123–134.Google Scholar
Palm, H.W. (2008) Surface ultrastructure of the elasmobranchia parasitizing Grillotiella exilis and Pseudonybelinia odontacantha (Trypanorhyncha, Cestoda). Zoomorphology 127, 249–258.Google Scholar
Palm, H.W. (2011) Fish parasites as biological indicators in a changing world: Can we monitor environmental impact and climate change? pp. 223–250in Mehlhorn, H. (Ed.) Progress in parasitology. Parasitology Research Monographs 2, 223–250. Berlin, Springer-Verlag.Google Scholar
Palm, H.W. & 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, 726–732.Google Scholar
Palm, H.W. & Rückert, S. (2009) A new approach to visualize fish and ecosystem health by using parasites. Parasitology Research 105, 539–553.Google Scholar
Palm, H.W., Waeschenbach, A. & Littlewood, D.T.J. (2007) Genetic diversity in the trypanorhynch cestode Tentacularia coryphaenae Bosc, 1797: evidence for a cosmopolitan distribution and low host specificity in the teleost intermediate host. Parasitology Research 101, 153–159.CrossRefGoogle ScholarPubMed
Palm, H.W., Damriyasa, I.M., Linda, & 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, 3–12.Google Scholar
Palm, H.W., Kleinertz, S. & Rückert, S. (2011) Parasite diversity as an indicator of environmental change – an example from tropical grouper (Epinephelus fuscoguttatus) mariculture in Indonesia. Parasitology 138, 1–11.Google Scholar
Riemann, F. (1988) Nematoda. pp. 293–301in Higgins, R.P. & Thiel, H. (Eds) Introduction to the study of meiofauna. Washington, DC, Smithsonian Institution Press.Google Scholar
Rimmer, M.A., McBride, S. & Williams, K.C. (2004) Advances in grouper aquaculture. Australian Centre for International Agricultural Research Monograph, Canberra, ACIAR.Google Scholar
Rückert, S. (2006) Marine fish parasites in Indonesia: state of infestation and importance for grouper mariculture. PhD thesis, Heinrich-Heine University of Düsseldorf, Germany.Google Scholar
Rückert, S., Hagen, W., Yuniar, A.T. & Palm, H.W. (2009a) Metazoan parasites of Segara Anakan Lagoon, Indonesia, and their potential use as biological indicators. Regional Environmental Change 9, 315–328.Google Scholar
Rückert, S., Klimpel, S., Mehlhorn, H. & Palm, H.W. (2009b) Transmission of fish parasites into grouper mariculture (Serranidae: Epinephelus coioides (Hamilton, 1822)) in Lampung Bay, Indonesia. Parasitology Research 104, 523–532.CrossRefGoogle ScholarPubMed
Rückert, S., Klimpel, S. & Palm, H.W. (2010) Parasites of cultured and wild brown-marbled grouper Epinephelus fuscoguttatus (Forsskål, 1775) in Lampung Bay, Indonesia. Aquaculture Research 41, 1158–1169.CrossRefGoogle Scholar
Sasal, P., Mouillot, D., Fichez, R., Chifflet, S. & 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, 1697–1706.CrossRefGoogle ScholarPubMed
Sures, B. (2001) The use of fish parasites as bioindicators of heavy metals in aquatic ecosystems: a review. Aquatic Ecology 35, 245–255.CrossRefGoogle Scholar
Sures, B. (2003) Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology 126, 53–60.Google Scholar
White, A.T., Marosubroto, P. & Sadorra, M.S.M. (1989) The coastal environment profile of Segara Anakan Cilacap, South Java, Indonesia. ICLARM, Association of Southeast Asian Nations, United States coastal resources management project. Technical report 25. 82 pp. Manila, Philippines, International Center for Living Aquatic Resources Management.Google Scholar
Williams, H.H., MacKenzie, K. & McCarthy, A.M. (1992) Parasites as biological indicators of the population biology, migrations, diet and phylogenetics of fish. Reviews in Fish Biology and Fisheries 2, 144–176.CrossRefGoogle Scholar
Yuniar, A. (2005) Parasites of marine fish from Segara Anakan, Java, Indonesia and their potential use as biological indicators. Master of Science thesis in International Studies in Aquatic Tropical Ecology (ISATEC), University of Bremen.Google Scholar
Yuniar, A.T., Palm, H.W. & Walter, T. (2007) Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia. Parasitology Research 100, 1193–1204.Google Scholar