Abstract
During an extensive survey of fish parasites along the Malabar coast of India we observed exceptionally high or even massive infection of the narrow-barred Spanish mackerel, Scomberomorus commerson (Scombridae), with parasitic copepods Cybicola armatus. Such infection has not hitherto been reported. The copepods occurred on the gills of its host and the infection persisted for many years (the survey lasted from January 2010 to July 2014). The overall prevalence was very high (95%); out of a total of 981 fish studied, 933 were infected, and the maximum intensity reached 42. The highest rate of infection (prevalence 99.2%) was observed in medium sized fish (36.0–79.9 cm). We found this parasite only on S. commerson even though we examined 81 fish species, including five of the family Scombridae. Interestingly, the parasite exhibits strict site specificity and microhabitat preference. A significant proportion of them was seen attached to pseudobranchs rather than to main gill arches. Significantly, the body size of the parasite was positively correlated with that of the host fish. Our SEM micrographs contributed new facts to this copepod’s morphology by illustrating for the first time the ventral part of its cephalothorax, illustrating the nature of attachment, and by finding a new structure — a premaxillary pad. We demonstrated the haematophagous nature of C. armatus by finding and documenting the host’s blood cells in the parasite’s intestine.
Similar content being viewed by others
References
Abdel-Aal A.A., Soliman M.F. 2004. Microhabitat and surface ultrastructure of Neothoracocotyle commersoni and Priceamultae (Monogenea: Microcotyloidea) from gills of scombrid fish, Scomberomorus commerson. Journal of the Egyptian Society of Parasitology, 34, 117–130
Abdul Khalid N.Q., Shaharoum-Harrison F. 2014. The life cycle of the parasitic crustacean, Lernanthropus latis Yamaguti, 1954 (Copepoda: Lernanthropidae), on marine-cultured fish, Lates calcarifer, from Setiu Wetland, Terengganu. Journal of Parasitology Research, 697134, 6 pages. DOI: 10.1155/2014/697134
Adel M., Azizi H.R., Nematolahi A. 2013. Scomberomorus commerson, a new paratenic host of Contracaecum sp. and Anisakis sp. (Nematoda: Anisakidae) from Persian Gulf. World Journal of Fish and Marine Sciences, 5, 310–314
Adlard R.D., Bryant M.S., Whipps C.M., Kent M.L. 2005 Multivalvulid myxozoans from eastern Australia: Three new species of Kudoa from scombrid and labrid fishes of the Great Barrier Reef, Queensland, Australia. Journal of Parasitology, 91, 1138–1142. DOI: 10.1645/GE-368R.1
Aloo P.A., Anam R.O., Mwangi J.N. 2004. Metazoan parasites of some commercially important fish along the Kenyan coast. Western Indian Ocean Journal of Marine Science, 3, 71–78
Aneesh P.T. 2014. Studies on parasitic crustaceans infecting the fishes of Malabar Coast. PhD Thesis, Kannur University
Arthur J.R., Lumanlan-Mayo S. 1997. Checklist of the parasites of fishes of the Philippines. FAO Fisheries Technical Paper, 369, FAO, Rome. pp. 102
Baker T.G., Pante E., de Buron I. 2005. Co-occurrence of Naobranchia lizae (Copepoda) and Metamicrocotyla macracantha (Monogenea), gill parasites of the striped mullet Mugil cephalus. Parasitology Research, 97, 515–520. DOI: 10.1007/s00436-005-1485-5
Bassett-Smith P.W. 1898a. Some new parasitic copepods found on fish at Bombay. Annals and Magazine of Natural History, 1, 1–17
Bassett-Smith P.W. 1898b. Some new or rare parasitic copepods found on fish in the Indo-tropic region. Annals and Magazine of Natural History, 11, 359–372
Beveridge I., Bray R.A., Cribb T.H., Justine J.-L. 2014. Diversity of trypanorhynch metacestodes in teleost fishes from coral reefs off eastern Australia and New Caledonia. Parasite 21, 60. DOI: 10.1051/parasite/2014060
Boxshall G.A. 2005. Copepods. In: Rohde K. (Ed.), Marine Parasites. CSIRO Publishing, Collingwood, Vic., Australia, pp.123–138
Boxshall G.A., Halsey S.H. 2004. An introduction to copepod diversity. Ray Society, London. No. 166, pp. 966
Bray R.A., Cribb T.H., Barker S.C. 1993. Hemiuridae (Digenea) from marine fishes of the Great Barrier Reef, Queensland, Australia. Systematic Parasitology, 25, 37–62.
Bruce N.L. 1990. Redescription of the ascaridoid nematode Hysterothylacium scomberomori (Yamaguti) from Australian Spanish mackerel Scomberomorus commerson (Lacepède). Memoirs of the Queensland Museum, 28, 427–434
Bush A.O., Lafferty K.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. DOI: 10.2307/3284227
Cabral P., Coste F., Raibaut A. 1984. Cycle évolutif de Lernanthropus kroyerii Van Beneden, 1851, Copépode branchial hématophage du loup Dicentrarchus labrax (Linné, 1758) dans des populations naturelles et en élevage. Annales de Parasitologie Humaine et Comparee, 59, 189–207 (In French)
Castro R., Santos M.J. 2013. Metazoan ectoparasites of Atlantic mackerel, Scomber scombrus (Teleostei: Scombridae): macroand microhabitat distribution. Parasitology Research, 112, 3579–3586. DOI: 10.1007/s00436-013-3543-8
Cavaleiro F.I., Santos M.J. 2011. Site selection of Acanthochondria cornuta (Copepoda: Chondracanthidae) in Platichthys flesus (Teleostei: Pleuronectidae). Parasitology, 138, 1061–1067. DOI: 10.1017/S1368980008002541
Cressey R.F., Cressey H.B. 1979. The parasitic copepods of Indo-West Pacific lizardfishes (Synodontidae). Smithsonian Contributions to Zoology, 196, 1–71. DOI: 10.5479/si.00810282.296
Cressey R.F., Cressey H.B. 1980. The parasitic copepods of mackerel and tuna-like fishes (Scombridae) of the world. Smithsonian Contributions to Zoology, 311, 1–186. DOI: 10.5479/si.00 810282.311.i
Cressey R.F., Collette B.B., Russo L. 1983. Copepods and scombrid fishes: A study in host-parasite relationships. Fishery Bulletin, 81, 227–265
de Meeûs T., Marin R., Renaud F. 1992. Genetic heterogeneity within populations of Lepeophtheirus europaensis (Copepoda, Caligidae) parasite on to host species. International Journal of Parasitology, 8, 1179–1181. DOI: 10.1016/0020-7519(92) 90039-N
Froese R., Pauly D. 2016. FishBase. World Wide Web electronic publication. Available from: http://www.Fishbase.org, Version (January 2016). Accessed 4 July 2016.
Gnanamuthu C.P. 1950. Two dichelesthiid copepods from Madras fish. Parasitology, 40, 276–282. DOI: 10.1017/S0031182000018138
Heegaard P.E. 1962. Parasitic Copepoda from Australian waters. Records of the Australian Museum, 25, 149–234
Hermida M., Cruz C., Saraiva A. 2012. Distribution of Hatschekia pagellibogneravei (Copepoda: Hatschekiidae) on the gills of Pagellus bogaraveo (Teleostei: Sparidae) from Madeira, Portugal. FoliaParasitologica, 59, 148–152. DOI: 10.14411/fp.2012.020
Huys R., Boxshall G.A. 1991. Copepod evolution. Ray Society, London. No. 159, pp. 468
Johnson S.C., Treasurer J.W., Bravo S., Nagasawa K., Kabata Z. 2004. A review of the impact of parasitic copepods on marine aquaculture. Zoological Studies, 43, 229–243
Kabata Z. 1979. Parasitic Copepoda of British fishes. Ray Society, London. No. 152, pp. 468
Kabata Z. 1982. Copepoda (Crustacea) parasitic on fishes: Problems and perspectives. Advances in Parasitology, 19, 1–71. DOI: 10.1016/S0065-308X(08)60265-1
Kensley B., Grindley J.R. 1973. South African parasitic Copepoda. Annals of the South African Museum, 62, 69–130
Kirtisinghe P. 1935. Parasitic copepods of fish from Ceylon. Parasitology, 27, 332–344. DOI: 10.1017/S0031182000015249
Kirtisinghe P. 1937. On the genus Cybicola Basett-Smith (1898). Parasitology, 29, 453–456. DOI: 10.1017/S0031182000024987
Kirtisinghe P. 1964. A review of the parasitic copepods of fish recorded from Ceylon with description of additional forms. Bulletin of the Fisheries Research Station, Ceylon 17, 45–132
Kurian C.V. 1965. Parasitic copepods of fishes from Kerala — No. 3. Bulletin of the Research Institute, University of Kerala, 8, 63–66
Lester R.J.G., Thompson C., Moss H., Barker S.C. 2001. Movement and stock structure of narrow-barred Spanish mackerel as indicated by parasites. Journal of Fish Biology, 59, 833–842. DOI: 10.1111/j.1095-8649.2001.tb00154.x
Lin C.L., Ho J.S. 2006. Four species of Unicolax Cressey and Cressey, 1980 (Copepoda: Bomolochidae) parasitic on marine fishes of Taiwan. Zoological Studies, 45, 339–356
Lo C.M., Morand S. 2001. Gill parasites of Cephalopholis argus (Teleostei: Serranidae) from Morrea (French Polynesia): Site selection and coexistence. Folia Parasitologica, 48, 30–36. DOI: 10.14411/fp.2001.006
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
Moore B.R., Buckworth R.C., Moss H., Lester R.J.G. 2003. Stock discrimination and movements of narrow-barred Spanish mackerel across northern Australia as indicated by parasites. Journal of Fish Biology, 63, 765–779. DOI: 10.1046/j.1095- 8649.2003.00190.x
Morton A.B., Routledge R. 2005. Mortality rates for juvenile pink Oncorhynchus gorbuscha and chum O. keta salmon infested with sea lice Lepeophtheirus salmonis in the Broughton Archipelago. Alaska Fishery Research Bulletin 11, 146–152
Natarajan P., Balakrishnan Nair N. 1972. Observations on Pseudocycnus armatus (Bassett-Smith) parasitic on Indocybium guttatum (Bloch and Schn.). Hydrobiologia, 40, 69–76. DOI: 10.1007/BF00123593
Nolan M.J., Cribb T.H. 2006. Cardicola Short, 1953 and Braya n. gen. (Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa, 1265, 1–80
Piasecki W. 1989. Life cycle of Tracheliastes maculatus Kollar, 1835 (Copepoda, Siphonostomatoida, Lernaeopodidae). Wiadomosci Parazytologiczne, 35, 187–245
Piasecki W. 1994. Infection seasonality of Tracheliastes maculatus Kollar, 1835 (Copepoda, Siphonostomatoida, Lernaeopodidae) in the warm-water canal of the “Dolna Odra” power plant. Wiadomosci Parazytologiczne, 40, 187–192
Piasecki W., Avenant-Oldewage A. 2008. Diseases caused by Crustacea. pp. 1113–1198. In: Eiras J., Segner H., Wahli T., Kapoor B.G. (Eds.) Fish diseases. Science Publishers, Enfield, NH, USA, pp. 1200
Piasecki W., Goodwin A.E., Eiras J.C., Nowak B.F. 2004. Importance of Copepoda in freshwater aquaculture. Zoological Studies, 43, 193–205
Piasecki W., MacKinnon B.M. 1995. Life cycle of a sea louse, Caligus elongatus von Nordmann, 1832 (Copepoda, Siphonostomatoida, Caligidae). Canadian Journal of Zoology, 73, 74–82. DOI: 10.1139/z95-009
Pillai N.K. 1964. A miscellaneous collection of copepods parasitic on South Indian fishes. Journal of the Marine Biological Association of India, 6, 61–83
Pillai N.K. 1985. The fauna of India: Copepod parasites of marine fishes. Zoological Survey of India, Calcutta, pp. 900
Ramasamy P., Ramalinga M.K., Hanna R.E.B., Halton D.W. 1985. Microhabitats of gill parasites (Monogenea and Copepoda) of teleosts (Scomberoides spp.). International Journal of Parasitology, 15, 385–397. DOI: 10.1016/0020-7519(85)90023-2
Rohde K. 1980. Host specificity indices of parasites and their application. Experientia, 36, 1369–1371. DOI: 10.1007/BF01960103
Rohde K. 1993. Ecology of marine parasites, 2nd edn. CAB International, Wallingford, pp. 298
Rohde K. 1994. Niche restriction in parasites: proximate and ultimate causes. Parasitology, 109: S69–S84. DOI: 10.1017/ s0031182000085097
Samotylova N.N. 2011. Representatives of Cyclopoida and Siphonostomatoida (Crustacea: Copepoda) in Vietnamese fauna. Izvestja Samarskogo nauchnogo centra Rosijskoj akademii nauk, 13, 1146–1148. (In Russian)
Scott-Holland T.B., Bennett S.M., Bennett M.B. 2006. Distribution of an asymmetrical copepod, Hatschekia plectropomi, on the gills of Plectropomus leopardus. Journal of Fish Biology, 68, 222–235. DOI: 10.1111/j.0022-1112.2006.00895.x.
Sethi S. 2012. Occurence [sic] of parasitic copepods, Lernaeenicus sprattae on king mackerel (Scomberomorus commerson), along south-east of India. e-planet 10, 36–38
Shaharom F.M., Lester R.J.G. 1982. Description of and observations on Grillotia branchi n.sp., a larval trypanorhynch from the branchial arches of the Spanish mackerel, Scomberomorus commerson. Systematic Parasitology, 4, 1–6. DOI: 10.1007/BF00012227
Shinn A.P., Pratoomyot J., Bron J.E., Paladini G., Brooker E.E., Brooker A.J. 2015. Economic costs of protistan and metazoan parasites to global mariculture. Parasitology, 142, si1, 196–270. DOI: 10.1017/S0031182014001437
Silas E.G., Ummerkutty A.N.P. 1967. Parasites of scombroid fishes. Part II. Parasitic Copepoda. Proceedings of the Symposium on scombroid fishes held at Mandapam Camp from January 12–15, 1962. Part III. Symposium Series I, Marine Biological Association of India, Mandapam Camp, S. India, pp. 876–993
Sasidharan Pillai N.K. 1984. Studies on the copepod fish parasites of Kerala coast. PhD Thesis. Department of Industrial Fisheries, University of Cochin, Cohin, India
Székely C., Láng M., Molnár K. 2010. Role of the copepod parasite Tracheliastes maculatus Kollar, 1836 (Lernaeopodidae) in the common bream (Abramis brama) mortality occurring in Lake Balaton, Hungary. Bulletin of the European Association of Fish Pathologists, 30, 170–176
Whipps C.M., Adlard R.D., Bryant M.S., Kent M.L. 2003. Two unusual myxozoans, Kudoa quadricornis n. sp. (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp. (Multivalvulida) from the muscle of Spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. Journal of Parasitology, 89, 168–173. DOI: 10.1645/0022-3395 (2003)089[0168:TUMKQN]2.0.CO;2
Williams R.E., Lester R.J.G. 2006. Stock structure of Spanish mackerel Scomberomorus commerson along the Australian east coast deduced from parasite data. Journal of Fish Biology, 68, 1707–1712. DOI: 10.1111/j.1095-8649.2006.01026.x
Wilson C.B. 1922. North American parasitic copepods belonging to the family Dichelesthiidae. Proceedings of the United States National Museum, 60, 1–98
Wilson J.M., Laurent P. 2002. Fish gill morphology: Inside out. Journal of Experimental Zoology, 293, 192–213. DOI: 10.1002/jez.10124
Yamaguti S. (Ed.) 1963. Parasitic Copepoda and Branchiura of fishes. Interscience Publishers, New York, pp. 1104
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Helna, A.K., Sudha, K., Aneesh, P.T. et al. A case of persisting massive infection of Scomberomorus commerson, a commercially exploited scombrid fish, with Cybicola armatus (Copepoda: Siphonostomatoida: Pseudocycnidae). Acta Parasit. 61, 836–848 (2016). https://doi.org/10.1515/ap-2016-0116
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1515/ap-2016-0116