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An environmental assessment of the parasite fauna of the reef-associated grouper Epinephelus areolatus from Indonesian waters

Published online by Cambridge University Press:  25 October 2012

S. Kleinertz ,
I.M. Damriyasa ,
W. Hagen ,
S. Theisen  and
H.W. Palm
S. Kleinertz*
Affiliation:
Aquaculture and Sea-Ranching, Faculty of Agricultural and Environmental Sciences, University of Rostock, Justus-von-Liebig-Weg 6, D-18059Rostock, Germany Leibniz Center for Tropical Marine Ecology GmbH, Fahrenheitstr. 6, D-28359Bremen, Germany
I.M. Damriyasa
Affiliation:
Center for Studies on Animal Disease, Faculty of Veterinary Medicine, Udayana University, Kampus Bukit Jimbaran, Bali80361, Indonesia
W. Hagen
Affiliation:
Marine Zoology, BreMarE Bremen Marine Ecology Centre for Research & Education, Bremen University, Leobener Straße, D-28359Bremen, Germany
S. Theisen
Affiliation:
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
*
*Fax: +49 (0)641 99 38469 E-mail: sonja.kleinertz@vetmed.uni-giessen.de
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Abstract

Sixty Epinephelus areolatus were examined for metazoan fish parasites in Indonesia, off Segara Anakan lagoon, Java and in Balinese waters. The study revealed 21 different parasite species, and 14 new host and locality records. The anisakid nematodes Anisakis typica and, for the first time in Indonesia, Anisakis sp. HC-2005 were identified by using molecular methods. Ecological parameters were calculated for both sites off the anthropogenically influenced Segara Anakan lagoon and the relatively undisturbed reference site at the southern Balinese coast. The fish from Segara Anakan demonstrated a significantly higher enzymatic activity (Hepatosomatic index) and a significantly reduced number of heteroxenous gut helminths (e.g. the digenean Didymodiclinus sp., the nematode Raphidascaris sp. and the acanthocephalan Serrasentis sagittifer). Other regional differences for E. areolatus included ecto-/endoparasite ratio, endoparasite diversity, the parasite species composition and prevalence of infection of the respective parasite species. We applied the stargraph method to visualize observed regional differences using grouper parasites as biological indicators for the sampled coastal ecosystems at both sampling sites.

Type
Research Papers
Information
Journal of Helminthology , Volume 88 , Issue 1 , March 2014 , pp. 50 - 63
Copyright
Copyright © Cambridge University Press 2012 

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References

Allen, G.R. & Werner, T. (2002) Coral reef fish assessment in the ‘coral triangle’ of southeastern Asia. Environmental Biology of Fishes 65, 209–214.Google Scholar
Asmanelli, , Yuliansyah, H. & Muchari, (1993) Penyakit ikan laut di lokasi Keramba Jaring Apung di Kepulauan Riau. [Marine fish diseases in floating net cages in Riau Archipelago.]. Prosiding Seminar hasil penelitian perikanan budidaya pantai, 16–19 July 1993, Maros, Indonesia vol. 11, pp. 13–24.Google Scholar
Bell, S. & Morse, S. (2003) Measuring sustainability: Learning by doing. London, 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 and comments on the marine fish digenean fauna of Indonesia. Zootaxa 2223, 1–24.Google Scholar
Bu, S.S.H., Leong, T.S., Wong, S.Y., Woo, Y.S.N. & Foo, R.W.T. (1999) Three diplectanid monogeneans from marine finfish (Epinephelus sp.) in the Far East. Journal of Helminthology 73, 301–312.Google Scholar
Burhanuddin, & Djamali, A. (1978) Parasit Anisakis sebagai petunjuk perbedaan populasi ikan laying, Decapterus russelli Ruppell, di laut Jawa. Osean. Indonesia 9, 1–11.Google Scholar
Burhanuddin, & Djamali, A. (1983) Pengamatan larva Anisakidae pada ikan laut di laut Jawa dan sekitarnya. Osean. Indonesia 16, 19–27.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.CrossRefGoogle Scholar
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
Farjallah, S., Ben Slimane, B., Busi, M., Paggi, L., Amor, N., Blel, H., Said, K. & D'Amelio, S. (2008) Occurrence and molecular identification of Anisakis spp. from the North African coasts of Mediterranean Sea. Parasitology Research 102, 371–379.Google Scholar
Froese, R. & Pauly, D. (2010) Fish Base. World Wide Web electronic publication Available at websitewww.fishbase.org . version (accessed March 2010).Google Scholar
Gray, J.S. (1997) Marine biodiversity: patterns, threats and conservation needs. Biodiversity and Conservation 6, 153–175.CrossRefGoogle Scholar
Hadidjaja, P., Ilahude, H.D., Mahfudin, B. & Malikusworo, H. (1978) Larvae of Anisakidae in marine fish of coastal waters near Jakarta, Indonesia. American Journal of Tropical Medical Hygiene 27, 51–54.CrossRefGoogle ScholarPubMed
Hafeezullah, M. & Siddiqi, A.H. (1970) Digenetic trematodes of marine fishes of India. Part I. Bucephalidae and Cryptogonimidae. Indian Journal of Helminthology 22, 1–22.Google Scholar
Harris, E. (2001) Status of Indonesian fisheries today and the research needed Proceedings of the JSPS DGHE International Symposium on Fisheries Science in tropical area. Faculty of Fisheries and Marine Science-IPB Bogor-Indonesia, 21–25 August 2000, pp. 62–66.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
Heemstra, P.C. & Randall, J.E. (1993) FAO species catalogue. Vol. 16. Groupers of the world. (Family Serranidae, Subfamily Epinephelinae). An annotated and illustrated catalogue of the grouper, rockcod hind, coral grouper and lyretail species known to date. FAO Fisheries Synopses 125 (16), 382 pp.Google Scholar
Holtermann, P., Burchard, H. & Jennerjahn, T. (2009) Hydrodynamics of the Segara Anakan lagoon. Regional Environmental Change 9, 245–258.Google Scholar
Hutomo, M., Burhanuddin, & Hadidjaja, P. (1978) Observations on the incidence and intensity of infection of nematode larvae (Fam. Anisakidae) in certain marine fishes of waters around Panggang Island, Seribu Islands. Marine Research in Indonesia 21, 49–60.Google Scholar
Ilahude, H.D. (1980) Anisakid larvae in marine fish in Indonesia (a review). Asian Meeting on parasitic infections, 26–28 February, Bangkok, Thailand.Google Scholar
Ilahude, H.D., Hadidjaja, P. & Mahfudin, B. (1978) Survey on anisakid larvae in marine fish from markets in Jakarta. SE Asian Journal of Tropical Medical Public Health 9, 48–50.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-fringes Segara Anakan Lagoon, Java Indonesia. Regional Environmental Change 9, 259–274.Google Scholar
Justine, J.L., Beveridge, I., Boxhall, 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 Parasitologia 57, 237–262.Google Scholar
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
Kiceniuk, J.W. & Khan, R.A. (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
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. 263 pp.Google Scholar
Klimpel, S. & Palm, H.W. (2011) Anisakid nematode (Ascaridoidea) life cycles and distribution: increasing zoonotic potential in the time of climate change? pp. 201–222in Mehlhorn, H. (Ed.) Progress in parasitology, Parasitology Research Monographs, vol. 2. doi:10.1007/978-3-642-21396-0_11Google 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., Vlčková, R., Říha, M., Walter, T. & Palm, H.W. (2009) Revision of tapeworms (Cestoda: Bothriocephalidea) from lizardfish (Saurida: Synodontidae) from the Indo-Pacific region. Zootaxa 1977, 55–67.Google Scholar
Lafferty, K.D. (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.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.Google Scholar
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
Marcogliese, D.J. (2003) Food webs and biodiversity: are parasites the missing link? Journal of Parasitology 89, 106–113.Google Scholar
Marcogliese, D.J. (2005) Parasites of the superorganism: are they indicators of ecosystem health? International Journal for Parasitology 35, 705–716.Google Scholar
Marcogliese, D.J. & Cone, D.K. (1997) Parasite communities as indicators of ecosystem stress. Parassitologia 39, 27–232.Google Scholar
Mattiucci, S., Paggi, L., Nascetti, G., Portes Santos, C., Costa, G., Di Beneditto, A.P., Ramos, R., Argyrou, M., Cianchi, R. & Bullini, L. (2002) Genetic markers in the study of Anisakis typica (Diesing, 1860): larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Systematic Parasitology 51, 159–170.Google Scholar
Mattiucci, S., Nascetti, G., Dailey, M., Webb, S.C., Barros, N.B., Cianchi, R. & Bullini, L. (2005) Evidence for a new species of Anisakis (Dujardin, 1845): morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Systematic Parasitology 61, 157–171.Google Scholar
MoMAF (2009) Coral Triangle Initiative Indonesia National Plan of Actions. Jakarta, Indonesia, National Secretariat of CTI-CFF Indonesia, Ministry of Marine Affairs and Fisheries (MoMAF). 52 pp.Google Scholar
Moravec, F. & Justine, J.L. (2008) Some philometroid nematodes (Philometridae), including four new species of Philometra, from marine fishes off New Caledonia. Acta Parasitologica 53, 369–381.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
Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fronesca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853–858.Google Scholar
Nadler, S., D'Amelio, S., Dailey, M.D., Paggi, L., Siu, S. & Sakanari, J. (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from the northern Pacific marine mammals. Journal of Parasitology 91, 1413–1429.Google Scholar
Nordhaus, I., Hadipudjana, F.A., Janssen, R. & Pamungkas, J. (2009) Spatio-temporal variation of macrobenthic communities in the mangrove-fringed Segara 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. (2004) The Trypanorhyncha Diesing, 1863. Bogor, PKSPL-IPB Press.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, vol. 2. doi:10.1007/978-3-642-21396-0_12.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., Klimpel, S. & 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, 1513–1522.Google Scholar
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
Parukhin, A.M. (1970) Study of the trematode fauna of fish in the Red Sea and Gulf of Aden. Biologiya Morya, Kiev 20, 187–213.Google Scholar
Parukhin, A.M. (1976) Parasitic worms of food fishes of the Southern Seas. Kiev, Naukova Dumka.Google Scholar
Petersen, F., Palm, H.W., Möller, H. & Cuzi, M.A. (1993) Flesh parasites of fish from central Philippine waters. Diseases of Aquatic Organisms 15, 81–86.Google Scholar
Purivirojkul, W. & Areechon, N. (2008) A survey of parasitic copepods in marine fishes from the Gulf of Thailand, Chon Buri Province. Kasetsart Journal (Natural Sciences) 42, 40–48.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. Canberra, Australian Centre for International Agricultural Research Monograph.Google Scholar
Roberts, C.M., McClean, C.J., Veron, J.E.N., Hawkins, J.P., Allen, G.R., McAllister, D.E., Mittermeier, C.G., Schueler, F.W., Spalding, M., Wells, F., Vynne, C. & Werner, T.B. (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295, 1280–1284.Google Scholar
Romimohtarto, K., Hutagalung, H. & Razak, H. (1991) Water quality of Segara Anakan-Cilacap (Central Java, Indonesia) with a note on lagoon fishery. pp. 131–141in Chou, L.M., Chua, T.E., Khoo, H.W., Lim, P.E., Paw, J.N., Silvestre, G.T., Valencia, M.J., White, A.T. & Wong, P.K. (Eds) Towards an integrated management of tropical coastal resources. International Center for Living Aquatic Resources Management Conference Proceedings, vol. 22, .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. 181 pp.Google Scholar
Rückert, S., Palm, H.W. & Klimpel, S. (2008) Parasite fauna of seabass (Lates calcarifer) under mariculture conditions in Lampung Bay, Indonesia. Journal of Applied Ichthyology 25, 321–327.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.Google Scholar
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
Saoud, M.F.A., Ramadan, M.M. & Kawari, K.S.R.A. (1986) Helminth parasites of fishes from the Arabian Gulf. 2. The digenean trematode genera Hamacraedium Linton, 1919 and Cainocraedium Nicol, 1909. Qatar University Science Bulletin 6, 231–245.Google 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.Google Scholar
Sey, O., Nahhas, F.M., Uch, S. & Vang, C. (2003) Digenetic trematodes from marine fishes off the coast of Kuwait, Arabian Gulf: Fellodistomidae and some smaller families, new host geographic records. Acta Zoologica Academiae Scientiarum Hungaricae 49, 179–200.Google Scholar
Shih, H.H. (2004) Parasitic helminth fauna of the cutlass fish, Trichiurus lepturus L., and the differentiation of four anisakid nematode third-stage larvae by nuclear ribosomal DNA sequences. Parasitology Research 93, 188–195.Google Scholar
Sures, B. & Siddall, R. (2003) Pomphorhynchus laevis (Palaeacanthocephala) in the intestine of chub (Leuciscus cephalus) as an indicator of metal pollution. International Journal for Parasitology 33, 65–70.Google Scholar
Theisen, S. (2009) Fischparasiten von der Südküste Javas, Indonesien. Diplomarbeit, Mathematisch-Naturwissenschaftliche Fakultät, Heinrich-Heine-Universität Düsseldorf. 199 pp.Google Scholar
Thompson, J.D., Higgins, D.G. & Gibson, D.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google Scholar
Verweyen, L., Klimpel, K. & Palm, H.W. (2011) Molecular phylogeny of the Acanthocephala (Class Palaeacanthocephala) with a paraphyletic assemblage of the orders Polymorphida and Echinorhynchida. PLoS ONE 6 (12), e28285. doi:10.1371/journal.pone.0028285.Google Scholar
Vidal-Martínez, V.M., Aguirre-Macedo, M.L., Vivas-Rodríguez, C.M. & 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, 9–14 November, Mérida, Yucatán, pp. 764–779.Google Scholar
Vidal-Martínez, V.M., Pech, D., Sures, B., Purucker, S.T. & Poulin, R. (2010) Can parasites really reveal environmental impact? Trends in Parasitology 26, 44–51.Google Scholar
White, A.T., Marosubroto, P. & Sadorra, M.S.M. (1989) The coastal environment profile of Segara Anakan Cilacap, South Java, Indonesia. ICLARM. Technical report 25, 82 pp. Manila, Philippines, International Center for Living Aquatic Resources Management.Google Scholar
Williams, H.H. & MacKenzie, K. (2003) Marine parasites as pollution indicators: an update. Parasitology 126, 27–41.CrossRefGoogle ScholarPubMed
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. 118 pp.Google Scholar
Yuniar, A., Palm, H.W. & Walter, T. (2007) Crustacean fish parasites from Segara Anakan Lagoon, Java Indonesia. Parasitology Research 100, 1193–1204.Google Scholar
Zhu, X., Gasser, R.B., Podolska, M. & Chilton, N.B. (1998) Characterisation of anisakid nematodes with zoonotic potential by nuclear ribosomal DNA sequences. International Journal of Parasitology 28, 1911–1921.Google Scholar
Zhu, X., D'Amelio, S., Paggi, L. & Gasser, R.B. (2000a) Assessing sequence variation in the internal transcribed spacers of ribosomal DNA within and among members of the Contracaecum osculatum complex (Nematoda: Ascaridoidea: Anisakidae). Parasitology Research 86, 677–683.Google Scholar
Zhu, X., Gasser, R.B., Jacobs, D.E., Hung, G.C. & Chilton, N.B. (2000b) Relationship among some ascaridoid nematodes based on ribosomal DNA sequence data. Parasitology Research 86, 738–744.Google Scholar