Abstract
The present study reports metazoan fish parasites from Segara Anakan, a brackish water lagoon located at the southern Java coast, Indonesia. Seven economically important marine fish species (Mugil cephalus, Siganus javus, Scatophagus argus, Caranx sexfasciatus, Lutjanus johnii, Eleutheronema tetradactylum and Johnius coitor) were examined at two different sampling sites within the lagoon for the occurrence of metazoan parasites. A diverse parasite fauna was found, consisting of 43 species/taxa. Ectoparasites (31) were more abundant than endoparasites (12). The fish species J. coitor, M. cephalus and S. argus harboured the most diverse metazoan parasite fauna with 11, 13, and 16 different parasite species, respectively. Prevalence and intensity of infection for each parasite species/taxon is given, including short descriptions for rapid diagnosis. For the first time, we discuss the utilisation of the sampled fish parasites as biological indicator organisms for fish and environmental health within this tropical mangrove ecosystem. Ecto- versus endoparasite ratio and endoparasite diversity are suitable tools to describe the environmental health status at a tropical brackish water locality, and might be applied also for other tropical and possibly non-tropical marine ecosystems.
Similar content being viewed by others
References
Amin OM, Nahhas FM (1994) Acanthocephala of marine fishes off Fiji Island with description of Filosoma longcementglandatus n. sp., Neorhadinorhynchus macrospinosus n. sp. (Cavisomidae), and gravid females of Rhadinorhynchus johnstoni (Rhadinorhynchidae); and key to species of the genera Filisoma and Neorhadinorhynchus. J Parasitol 80:768–774. doi:10.2307/3283256
Anderson RC (2000) Nematode parasites of vertebrates their development and transmission, 2nd edn. CABI Publishing, UK
Arthur JR (1997) Recent advances in the use of parasites as biological tags for marine fish. In: Flegel TW, MacRae IH (eds) Diseases in Asian aquaculture III. Fish health section. Asian Fisheries Society, Manila, pp 141–154
Arthur JR, Lumanlan-Mayo S (1997) Checklist of the parasites of fishes of the Philippines. FAO Fish Tec Pap 369:102
Broeg K, Zander S, Diamant A, Körting W, Krüner G, Paperna I, von Westernhagen H (1999) The use of fish metabolic, pathological and parasitological indices in pollution monitoring I. North Sea. Helgol Mar Res 53:171–194. doi:10.1007/s101520050023
Boxshall GA, Halsey SH (2004) An introduction to copepod diversity, vol 1 and 2. The Ray Society, London
Bunkley-Williams L, Williams EH Jr (1998) Isopods associated with fishes: a synopsis and corrections. J Parasitol 84:893–896
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583. doi:10.2307/3284227
Collard SN (1970) Some aspects of host-parasite relationship in mesopelagic fishes. In: Snieszko SF (ed) A symposium on diseases of fishes and shellfishes, vol 5. Am Fish Soc Spec Publ pp 41–56
Cone DK, Marcogliese DJ, Watt WD (1993) Metazoan parasite communities of yellow eels (Anguilla rostrata) in acid and limed rivers of Nova Scotia. Can J Zool 71:177–184. doi:10.1139/z93-024
Cruz-Lacierda ER, Toledo JD, Tan-Fermin JD, Burreson EM (2000) Marine leech (Zeylanicobdella arugamensis) infestation in cultured orange-spotted grouper, Epinephelus coioides. Aquaculture 185:191–196. doi:10.1016/S0044-8486(99)00356-7
De Silva PHDH (1963) Zeylanicobdella arugamensis gen. nov. and sp. nov. from Arugam Kalapu, Eastern Province, Ceylon. Spolia Zeylan 30:47–53
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. Helgol Mar Res 53:195–208. doi:10.1007/s101520050024
Dudley RG (2000) Segara Anakan fisheries management plan. Segara Anakan conservation and development project components B & C, Consultant’s report, 33 p
Dzikowski R, Paperna I, Diamant A (2003) Use of fish parasite species richness indices in analyzing anthropogenically impacted coastal marine ecosystems. Helgol Mar Res 57:220–227. doi:10.1007/s10152-003-0138-2
El-Rashidy H, Boxshall GA (1999) Ergasilid copepods (Poecilostomatoida) from the gills of primitive Mugilidae (grey mullets). Syst Parasitol 42:161–186. doi:10.1023/A:1006075223683
FAO Inland Water Resources and Aquaculture Service (FIRI) (2006) National Aquaculture Sector Overview—Indonesia. National Aquaculture Sector Overview Fact Sheets. FAO, Rome. Available via FIGIS from: http://www.fao.org/figis/servlet/static?dom=countrysector&xml=naso_indonesia.xml
Froese R, Pauly D (eds) (2007) FishBase. World Wide Web electronic publication. http://www.fishbase.org
Froese R, Luna SM, Capuli EC (1996) Checklist of marine fishes of Indonesia, compiled from published literature. In: Pauly D, Martosubroto P (eds). Baseline studies of biodiversity: the fish resources of Western Indonesia. ICLARM Stud Rev 23:217–275
Galli P, Crosa G, Mariniello L, Ortis M, D’Amelio S (2001) Water quality as a determinant of the composition of fish parasite communities. Hydrobiologia 452:173–179. doi:10.1023/A:1011958422446
Golvan YJ (1969) Systématique des Acanthocéphales (Acanthocephala Rudolphi 1801). Première partie: l’orde des Palaeacanthocephala Meyer 1931, premier fascicule la superfamille des Echinorhynchoidea (Cobbold 1876) Golvan et Houin 1963. Mem Mus Nat Hist Nat Ser A 57:1–373
Grutter AS (1995) Comparison of methods for sampling ectoparasites from coral reef fishes. Mar Freshw Res 46:897–903. doi:10.1071/MF9950897
Hine PM, Kennedy CR (1974) Observations on the distribution, specificity and pathogenicity of the acanthocephalan Pomphorhynchus laevis (Müller). J Fish Biol 6:521–535. doi:10.1111/j.1095-8649.1974.tb04569.x
Ho J-S, Lin C-L (2001) Parapetalus occidentalis Wilson (Copepoda, Caligidae) parasitic on both wild and farmed cobia (Rachycentron canadum) in Taiwan. J Fish Soc Taiwan 28:305–316
Ho J-S, Lin C-L (2004) Sea lice of Taiwan (Copepoda: Siphonostomatoida: Caligidae). The Sueichan Press, Taiwan
Jakob E, Palm HW (2006) Parasites of commercially important fish species from the southern Java coast, Indonesia, including the distribution pattern of trypanorhynch cestodes. Verh Ges Ichthyo 5:165–191
Kabata Z (1979) Parasitic Copepoda of British fishes. The Ray Society, London
Kabata Z (1985) Parasites and diseases of fish cultured in the tropics. Taylor & Francis, London
Khan RA (1990) Parasitism in marine fish after chronic exposure to petroleum hydrocarbons in the laboratory and to the Exxon Valdez oil spill. Bull Environ Contam Toxicol 44:759–763. doi:10.1007/BF01701799
Khan RA, Thulin J (1991) Influence of pollution on parasites of aquatic animals. Adv Parasitol 30:201–238. doi:10.1016/S0065-308X(08)60309-7
Klimpel S, Palm HW, Busch MW, Kellermanns E, Rückert S (2006) Fish parasites in the Arctic deep-sea: poor diversity in pelagic fish species vs heavy parasite load in a demersal fish. Deep Sea Res Part I Oceanogr Res Pap 53:1167–1181. doi:10.1016/j.dsr.2006.05.009
Koesharyani I, Roza D, Mahardika K, Johnny F, Zafran, Yuasa K (2001) Manual for fish disease diagnosis. II Marine fish and crustacean diseases in Indonesia. Gondol Research Institute for Mariculture. Central Research Institute for Sea Exploration and Fisheries, pp 1–57
Køie M, Lester RJG (1985) Larval didymozoid (Trematoda) in fishes from Moreton Bay, Australia. Proc Helminthol Soc Wash 52:196–203
Lafferty KD (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitol Today 13(7):251–255. doi:10.1016/S0169-4758(97)01072-7
Landsberg JH, Blakesley BA, Reese RO, McRae G, Forstchen PR (1998) Parasites of fish as indicators of environmental stress. Environ Monit Assess 51:211–232. doi:10.1023/A:1005991420265
Leong TS (1992) Diseases of brackishwater and marine fish cultured in some Asian countries. In: Shariff M, Subasinghe RP, Arthur JR (eds) Diseases in Asian aquaculture I. Proceedings of the first symposium on diseases in Asian aquaculture, 26–29 November 1990, Bali, Indonesia. Fish Health Section, Asian Fisheries Society, Manila, Philippines, pp 223–236
Leong TS, Wong S-Y (1989) Parasites of wild and cultured golden snapper, Lutjanus johnii (Bloch), in Malaysia. Trop Biomed 6:73–76
Leong TS, Tan Z, Enright WJ (2006) Important parasitic diseases in cultured marine fish in the Asia-Pacific region. AQUA Cult Asia Pac Mag 2:14–16
Lin C-L, Ho J-S (1998) Two new species of ergasilid copepods parasitic on fishes cultured in brackish water in Taiwan. Proc Biol Soc Wash 111:15–27
Machida M (1996) Digenean trematodes from mullets in Japanese and adjacent waters. Jpn J Parasitol 2:123–133
MacKenzie K, Williams HH, Williams B, McVicar AH, Siddall RI (1995) Parasites as indicators of water quality and the potential use of helminth transmission in marine pollution studies. Adv Parasitol 35:86–245
Magurran AE (1988) Ecological diversity and its measurement. Croom Helm, London
Marcogliese DJ, Cone DK (1997) Parasite communities as indicators of ecosystem stress. Parassitol 39:227–232
Margolis L, Esch GW, Holmes JCM, Kuris AM, Schad GA (1982) The use of ecological terms in parasitology (report of an AD HOC Committee of the American Society of Parasitologists). J Parasitol 68:131–133. doi:10.2307/3281335
Möller H, Anders K (1986) Diseases and parasites of marine fishes. Verlag Möller, Germany
Moravec F (1987) Revision of capillariid nematodes (subfamily Capillarinae) parasitic in fish. Academia Praha, Czech Republic
Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Academia Praha, Czech Republic
Moravec F (1998) Nematodes of freshwater fishes of the neotropical region. Academia Praha, Czech Republic
Moser M (1991) Parasites as biological tags. Parasitol Today 7(7):1–4. doi:10.1016/0169-4758(91)90128-B
Naamin N (1991) The ecological and economic roles of Segara Anakan, Indonesia, as a nursery ground of shrimp. In: Chou LM, Chua TE, Khoo HW, Lim PE, Paw JN, Silvestre GT, Valencia MJ, White AT, Wong PK (eds) Towards an integrated management of tropical coastal resources. ICLARM Conf Proc 22:119-130
Overstreet RM (1971) Some adult digenetic trematodes in striped mullet from the northern gulf of Mexico. J Parasitol 57:967–974. doi:10.2307/3277846
Palm HW (1999) Ecology of Pseudoterranova decipiens (Krabbe, 1878) (Nematoda: Anisakidae) from Antarctic waters. Parasitol Res 85:638–646. doi:10.1007/s004360050608
Palm HW (2000) Trypanorhynch cestodes from Indonesian coastal waters (East Indian Ocean). Folia Parasitol (Praha) 47:123–134
Palm HW (2004) The Trypanorhyncha Diesing, 1863. PKSPL-IPB Press, Bogor
Palm HW, Walter T (1999) Nybelinia southwelli sp. nov. (Cestoda: Trypanorhyncha) with re-description of N. perideraeus (Shipley & Hornell, 1906) and synonymy of N. herdmani (Shipley & Hornell, 1906) with Kotorella pronosoma (Stossich, 1901). Bull Brit Mus Nat Hist Zool 65:123–131
Palm HW, Reimann N, Spindler M, Plötz J (1998) The role of the rock cod Notothenia coriiceps Richardson, 1844 in the life cycle of Antarctic parasites. Polar Biol 19:399–406. doi:10.1007/s003000050265
Palm HW, Klimpel S, Bucher C (1999) Checklist of metazoan fish parasites of German coastal waters. Ber Inst Meereskd Christian-Albrechts-Univ Kiel 307:148
Palm HW, Damriyasa IM, Linda, Oka IBM (2008) Molecular genotyping of Anisakis Dujardin, 1845. (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia. Helminthologia 45:3–12. doi:10.2478/s11687-008-0001-8
Paperna I (1975) Parasites and diseases of grey mullet (Mugilidae) with spezial reference to the seas of the Near East. Aquaculture 5:65–80. doi:10.1016/0044-8486(75)90018-6
Paperna I, Overstreet RM (1981) Parasites and diseases of mullets (Mugilidae). Aquaculture of grey mullets. In: Oren OH (ed) International Biological Programm 26. Cambridge University Press, USA, pp 411–493
Piasecki W, Hayward CJ (2002) Redescription of the fish parasite Lernanthropus polynemi Richiardi, 1881 (Copepoda: Siphonostomatoida) and relegation of two congeners to synonymy. Syst Parasitol 52:137–144. doi:10.1023/A:1015636300605
Pillai NK (1962) A revision of the genera Parapetalus Steenstrup and Lütken and Pseudopetalus nov. Crustaceana 3:285–303. doi:10.1163/156854062X00526
Rasheed S (1963) A revision of the genus Philometra Costa, 1845. J Helminthol 37:89–130
Riemann F (1988) Nematoda. In: Higgins RP, Thiel H (eds) Introduction to the study of meiofauna. Smithsonian Institution Press, Washington, DC, pp 293–301
Robinson DG, Ehlers U, Herken R, Hermann B, Mayer F, Schürmann FW (1985) Präparationsmethodik in der Elektronenmikroskopie. Springer, Berlin
Rohde K, Hayward C, Heap M (1995) Aspects of the ecology of metazoan ectoparasites of marine fishes. Int J Parasitol 25:945–970. doi:10.1016/0020-7519(95)00015-T
Romimohtarto K, Hutagalung H, Razak H (1991) Water quality of Segara Anakan—Cilacap (Central Java, Indonesia) with a note on lagoon fishery. In: Chou LM, Chua TE, Khoo HW, Lim PE, Paw JN, Silvestre GT, Valencia MJ, White AT, Wong PK (eds) Towards an integrated management of tropical coastal resources. ICLARM Conf Proc 22:131–141
Roubal FR (1997) Survival and development of Caligus epidemicus Hewitt in sea water of different salinity. Bull Eur Assoc Fish Pathol 17:78–80
Rückert S, Klimpel S, Palm HW (2008a) Parasite fauna of seabass (Lates calcarifer) under mariculture conditions in Lampung Bay, Indonesia. J Appl Ichthyology 24:321–327. doi:10.1111/j.1439-0426.2008.01064.x
Rückert S, Klimpel S, Al-Quraishy S, Mehlhorn H, Palm HW (2008b) Transmission of fish parasites into grouper mariculture (Serranidae: Epinephelus coioides) (Hamilton, 1822) in Lampung Bay, Indonesia. Parasitol Res. doi:10.1007/s00436-008-1226-7
Santos CP, Mourao ED, Cárdenas MQ (2001) Pseudempleurosoma gibsoni n.sp., a new ancyrocephalid monogenean from Paralonchurus brasiliensis (Sciaenidae) from off the southeastern coast of Brazil. Mem Inst Oswaldo Cruz 96:215–219
Schell SC (1970) How to know the trematodes. M. C. Brown Company Publishers, Dubuque
Sures B, 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 Biol 26(10):680–686. doi:10.1007/s00300-003-0538-4
Sures B, Taraschewski H, Jackwerth E (1994) Lead accumulation in Pomphorhynchus laevis and its host. J Parasitol 80:355–357. doi:10.2307/3283403
Te BQ (1998) Parasitic fauna of the freshwater fish of the Cuulong River delta (lower Mekong River delta) and methods for prevention and treatment. AAHRI Newsl 7:2–7
Tomascik T, Mah AJ, Nontji A, Moosa MK (1997) The ecology of the Indonesian seas Part II. Periplus Editions (HK) Ltd, Singapore
Walter T, Palm HW, Piepiorka S, Rückert S (2002) Parasites of the Antarctic rattail Macrourus whitsoni (Regan, 1913) (Macrouridae, Gadiformes). Polar Biol 25:633–640
White AT, Martosubroto P, Sadorra MSM (1989) The coastal environment profile of Segara Anakan—Cilacap, South Java, Indonesia. ICLARM. Association of Southeast Asian Nations. United States coastal resources management project. ICLARM Tech Rep 25:82
Williams EJ, Bunkley-Williams L (2000) Multicellular parasite (Macroparasite) problems in aquaculture. In: Stickney RR (ed) Encyclopedia of aquaculture. Wiley, New York, pp 562–579
Williams HH, MacKenzie K, McCarthy AM (1992) Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Rev Fish Biol Fish 2:144–176. doi:10.1007/BF00042882
Yamaguti S (1952) Parasitic worms mainly from Celebes. Part 1. New digenetic trematodes of fishes. Acta Med Okayama 8:146–198
Yamaguti S (1953) Parasitic worms mainly from Celebes. Part 2. Monogenetic trematodes of fishes. Acta Med Okayama 8:203–256
Yamaguti S (1963) Systema Helminthum, vol I: Monogenea and Aspidocotylea. Interscience Publisher, London
Yuasa K, Zafran, Koesharyani I, Roza D, Johnny F (1998) Diseases in marine fishes reared at Gondol Research Station for coastal fisheries. Prosiding Seminar Teknologi Perikanan Pantai, Bali 6–7 August 1998, pp 94–98
Yuniar AT, Palm HW, Walter T (2007) Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia. Parasitol Res 100:1193–1204. doi:10.1007/s00436-006-0391-9
Zafran, Roza D, Koesharyani I, Johnny F, Yuasa K (1998) Manual for fish diseases diagnosis. Marine fish and crustacean diseases in Indonesia. Gondol Research Station for Coastal Fisheries. Central research Institute for Fisheries, pp 1–44
Acknowledgments
We would like to thank Prof. R.M. Overstreet (Department of Coastal Sciences, The University of Southern Mississippi, USA) and Prof. H. Mehlhorn (Department of Zoomorphology, Cell Biology and Parasitology, Düsseldorf University, Germany) for help with the digenean identification and access to the SEM, respectively. The study was supported by the German Academic Exchange Service (DAAD), the German Federal Ministry for Education and Science (BMBF Grant No. 03F0391A) within the framework of the joint Indonesian-German research programme SPICE (Science for the Protection of Indonesian Coastal Marine Ecosystems), and the German Research Council (DFG PA 664/4-1).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Rueckert, S., Hagen, W., Yuniar, A.T. et al. Metazoan fish parasites of Segara Anakan Lagoon, Indonesia, and their potential use as biological indicators. Reg Environ Change 9, 315–328 (2009). https://doi.org/10.1007/s10113-008-0076-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10113-008-0076-2