Advertisement

The re-discovery of Caligus lichiae Brian, 1906 (Copepoda: Caligidae) parasitic on two carangid fishes in the Mediterranean Sea, and the recognition of Caligus aesopus Wilson C. B., 1921 as a junior subjective synonym

  • Argun Akif ÖzakEmail author
  • Yetkin Sakarya
  • Alper Yanar
  • Uğur Özbilen
  • Geoffrey Allan Boxshall
Article

Abstract

The caligid copepod Caligus lichiae Brian, 1906 is redescribed based on new material collected from the type-host, Lichia amia (Linnaeus), and from a second carangid, Seriola dumerili (Risso), both caught in the Gulf of Iskenderun, Turkey. Key diagnostic characters of both sexes are reported, supported by drawings and scanning electron microscopy images. Despite the commercial importance of its type-host, L. amia, C. lichiae has not been reported since its original description. After detailed comparison with recent descriptions of Caligus aesopus Wilson C. B., 1921, commonly found on S. dumerili, we recognise these two species as conspecific and propose to relegate C. aesopus Wilson C. B., 1921 to a junior subjective synonym of C. lichiae Brian, 1906. Caligus lichiae is a member of the C. confusus group of species and an identification key to species in this group is provided.

Notes

Acknowledgements

We would also like to thank Associate Professor Dr Kasım Ocakoglu, former head of the Advanced Technologies Research & Application Center (MEITAM) of the University of Mersin, Turkey, and Professor Süphan Karaytuğ and Ms Seher Kuru from Mersin University for their administrative and technical support during the SEM.

Funding

This research was funded by the Çukurova University academic research projects unit (Project No. FBA-2017-7490)

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

References

  1. Baeza-Kuroki, H., & Castro-Romero, R. (1982). Tres especies de Caligidae, nuevas para la fauna chilena (Copepoda, Siphonostomatoida). Noticiario Mensual del Museo Nacional de Historia Natural, Santiago, Chile, 25, 3–7.Google Scholar
  2. Boxshall, G. A. (1974). Lepeophtheirus pectoralis (O.F. Müller); a description, a review and some comparisons with the genus Caligus Müller, 1785. Journal of Natural History, 8, 445–468.CrossRefGoogle Scholar
  3. Boxshall, G. A. (1990). The skeletomusculature of siphonostomatoid copepods, with an analysis of adaptive radiation in structure of the oral cone. Philosophical Transactions of the Royal Society, London, Series B, 328, 167–212.CrossRefGoogle Scholar
  4. Boxshall, G. A. (2018). The sea lice (Copepoda: Caligidae) of Moreton Bay (Queensland, Australia) with descriptions of thirteen new species. Zootaxa, 4398, 1–172.CrossRefGoogle Scholar
  5. Boxshall, G. A., & El-Rashidy, H. H. (2009). A review of the Caligus productus species group, with the description of a new species, new synonymies and supplementary descriptions. Zootaxa, 2271, 1–26.Google Scholar
  6. Brian, A. (1898). Catalogo di copepodi parassiti dei Pesci della Liguria. Bollettino dei Musei e Laboratorii di Zoologia e Anatomia Comparata della Royale Università di Genova, 61, 1–27.Google Scholar
  7. Brian, A. (1906) Copepodi parassiti dei Pesci d’Italia. Genova: Tipo-Litografico R. Istituto Sordomuti, 187 pp.Google Scholar
  8. Capart, A. (1959). Copépodes parasites. Résultats Scientifiques de lʼExpédition Océanographique Belge dans les Eaux Côtieres Africaines de lʼAtlantique Sud (1948-1949). Institut Royale des Sciences Naturelles de Belgique, 3, 55–126.Google Scholar
  9. Causey, D. L. (1955). Parasitic Copepoda from Gulf of Mexico fish. Occasional Papers of the Marine Laboratory of Louisiana State University, 9, 1–19.Google Scholar
  10. Choe, M. K., & Kim, I. H. (2010). Redescriptions of two morphologically confusing sea lice Caligus aesopus Wilson, 1921 and C. spinosus Yamaguti, 1939 (Copepoda: Siphonostomatoida: Caligidae) parasitic on amberjacks (Seriola spp.) from Korea. Zootaxa, 2483, 23–34.CrossRefGoogle Scholar
  11. Cordeiro, A. S., & Luque, J. L. (2004). Community ecology of the metazoan parasites of Atlantic moonfish Selene setapinnis (Osteichthyes: Carangidae) from the coastal zone of the State of Rio de Janeiro, Brazil. Brazilian Journal of Biology, 64, 399–406.CrossRefGoogle Scholar
  12. Cressey, R. F., & Cressey, H. B. (1980). Parasitic copepods of mackerel and tuna-like fishes (Scombridae) of the world. Smithsonian Contributions to Zoology, 311, 1–186.Google Scholar
  13. Cressey, R. F. (1991). Parasitic copepods from the Gulf of Mexico and Caribbean Sea, III: Caligus. Smithsonian Contributions to Zoology, 497, 1–53.CrossRefGoogle Scholar
  14. Dippenaar, S. M. (2005). Reported siphonostomatoid copepods parasitic on marine fishes of southern Africa. Crustaceana, 77, 1281–1328.CrossRefGoogle Scholar
  15. Felgenhauer, B. (1987). Techniques for preparing crustaceans for scanning electron microscopy. Journal of Crustacean Biology, 7, 71–76.CrossRefGoogle Scholar
  16. Fernández, J., & Villalba, C. (1986). Contribución al conocimiento del género Caligus Müller, 1785 (Copepoda: Siphonostomatoida) en Chile. Gayana Zoología, 50, 37–62.Google Scholar
  17. Froese, R., & Pauly, D. (Eds) (2018). FishBase. World Wide Web electronic publication. Retrieved June, 2018 from, http://www.fishbase.org.
  18. Grobler, N. J. (2004). A review of the genus Caligus (Copepoda: Caligidae) from South Africa. Dissertation, University of the Free State Bloemfontein, South Africa.Google Scholar
  19. Grobler, N. J., Van As, J. G., & Olivier, P. A. S. (2003). Additional morphological information on two species of Caligus (Copepoda: Caligidae) parasitic on South African marine and estuarine fish. African Zoology, 38, 139–143.CrossRefGoogle Scholar
  20. Hameed, M. S., & Pillai, N. K. S. (1986). A new species of Caligus (Copepoda: Caligidae) from Kerala. Indian Journal of Fisheries, 33, 487–492.Google Scholar
  21. Hewitt, G. C. (1963). Some New Zealand parasitic Copepoda of the family Caligidae. Transactions of the Royal Society of New Zealand, 4, 61–115.Google Scholar
  22. Hewitt, G. C., & Hine, P. M. (1972). Checklist of parasites of New Zealand fishes and of their hosts. New Zealand Journal of Marine and Freshwater Research, 6, 69–114.CrossRefGoogle Scholar
  23. Hirunraks, W., Sittiphuprasert, U., & Sontirat, S. (1977). A checklist of parasitic copepods from marine fishes of Thailand and the adjacent areas including their hosts. In: A checklist of cartilagenous fishes (subclass Selachii) found in Thai-waters and the adjacent areas. Notes of the Faculty of Fisheries, Kasetsart University, Bangkok, 8, 6–9.Google Scholar
  24. Ho, J.-S., & Lin, C.-L. (2001). Parapetalus occidentalis Wilson (Copepoda, Caligidae) parasitic on both wild and farmed cobia (Rachycentron canadum) in Taiwan. Journal of the Fisheries Society of Taiwan, 28, 305–316.Google Scholar
  25. Ho, J.-S., & Lin, C.-L. (2003). Solution to the taxonomic confusion surrounding Caligus epinepheli Yamaguti, a caligid copepod (Siphonostomatoida) parasitic on marine fishes. Zoological Studies, 42, 268–283.Google Scholar
  26. Ho, J.-S., & Lin, C.-L. (2004). Sea Lice of Taiwan (Copepoda: Siphonostomatoida: Caligidae). Keelung: The Sueichan Press, 388 pp.Google Scholar
  27. Ho, J.-S., & Lin, C.-L. (2007). Three species of Caligus Müller, 1785 (Copepoda, Siphonostomatoida, Caligidae) parasitic on Caranx spp. (Teleostei: Carangidae) off Taiwan. Systematic Parasitology, 68, 33–43.CrossRefGoogle Scholar
  28. Ho, J.-S., Nagasawa, K., Kim, I. H., & Ogawa, K. (2001). Occurrence of Caligus lalandei Barnard, 1948 (Copepoda, Siphonostomatoida) on amberjacks (Seriola spp.) in the western North Pacific. Zoological Science, 18, 423–431.CrossRefGoogle Scholar
  29. Huys, R., & Boxshall, G. A. (1991). Copepod Evolution. London: The Ray Society.Google Scholar
  30. 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.Google Scholar
  31. Kabata, Z. (1965). Copepoda parasitic on Australian fishes. IV. Genus Caligus (Caligidae). Annals and Magazine of Natural History, 13, 109–126.CrossRefGoogle Scholar
  32. Kazachenko, V. N. (1975). A new species of the genus Caligus Müller, 1785 (Copepoda Parasitica, Caligidae) from Usacaranx georgianus (Cuvier et Valenciennes) of the Great Australian Bight. Parazitologiya, 9, 425–431.Google Scholar
  33. Kensley, B., & Grindley, J. R. (1973). South African parasitic Copepoda. Annals of the South African Museum, 62, 69–130.Google Scholar
  34. Kirtisinghe, P. (1964). A review of the parasitic copepods of fish recorded from Ceylon, with descriptions of additional forms. Bulletin Fisheries Research Station, Department of Fisheries, Ceylon, 17, 45–132.Google Scholar
  35. Lagarde, P. G. (1991). Crustáceos parásitos en peces marinos de la zona central de Venezuela. Boletín del Instituto Oceanográfico de Venezuela, Universidad de Oriente, 28, 135–144.Google Scholar
  36. Lewis, A. G. (1967). Copepod crustaceans parasitic on teleost fishes of the Hawaiian Islands. Proceedings of the United States National Museum, 121, 1–204.CrossRefGoogle Scholar
  37. Lewis, A. G. (1968). Copepod crustaceans parasitic on fishes of Eniwetok Atoll. Proceedings of the United States National Museum, 125, 1–78.CrossRefGoogle Scholar
  38. Lin, C.-L., & Ho, J.-S. (2003). Two species of rare sea lice (Copepoda, Caligidae) parasitic on marine fishes of Taiwan. Journal of the Fisheries Society of Taiwan, 29, 313–332.Google Scholar
  39. Lin, C.-L., & Ho, J.-S. (2007). Six species of Sea Lice (Copepoda, Caligidae) new to Taiwan. Journal of the Fisheries Society of Taiwan, 34, 41–67.Google Scholar
  40. Luque, J. L., & Cezar, A. D. (2004). Metazoários ectoparasitos do pampo-galhudo, Trachinotus goodei Jordan & Evermann, 1896 (Osteichthyes: Carangidae), do litoral do Estado do Rio de Janeiro, Brasil. Acta Scientiarum Biological Sciences, 26, 19–24.CrossRefGoogle Scholar
  41. MacKenzie, K., Campbell, N., Mattiucci, S., Ramos, P., Pereira, A., & Abaunza, P. (2004). A checklist of the protozoan and metazoan parasites reported from the Atlantic horse mackerel, Trachurus trachurus (L.). Bulletin of the European Association of Fish Pathologists, 24, 180–184.Google Scholar
  42. Margolis, L., Kabata, Z., & Parker, R. R. (1975). Catalogue and synopsis of Caligus, a genus of Copepoda (Crustacea) parasitic on fishes. Journal of the Fisheries Research Board of Canada, 192, 1–117.Google Scholar
  43. Marques, E. (1965). Copépodes parasitas de peixes marinhos de S. Tomé. Garcia de Orta, Lisbon, 13, 185–192.Google Scholar
  44. Morales-Serna, F. N., Hernández-Inda, Z. L., Gómez, S., & Pérez-Ponce de León, G. (2013). Redescription of Caligus serratus Shiino, 1965 (Copepoda: Caligidae) parasitic on eleven fish species from Chamela Bay in the Mexican Pacific. Acta Parasitologica, 58, 367–375.CrossRefGoogle Scholar
  45. Oldewage, W. H., & van As, J. G. (1989). Occurrence and distribution of Caligus (Copepoda: Siphonostomatoida) in African coastal waters. Revue de Zoologie Africaine, 103, 91–98.Google Scholar
  46. Palm, H.W., Klimpel, S., & Bucher, C. (1999). Checklist of metazoan fish parasites of German coastal waters. Berichte aus dem Institut für Meereskunde an der Christian-Albrechts-Universität Kiel, 307, 148 pp.Google Scholar
  47. Parker, R. R., Kabata, Z., Margolis, L., & Dean, M. D. (1968). A review and description of Caligus curtus Müller, 1785 (Caligidae: Copepoda), type species of its genus. Journal of the Fisheries Research Board of Canada, 25, 1923–1969.CrossRefGoogle Scholar
  48. Pearse, A. S. (1952). Parasitic Crustacea from the Texas coast. Publications of the Institute of Marine Science, University of Texas, 2, 5–42.Google Scholar
  49. Pillai, N. K. (1963). Copepods parasitic on south Indian fishes - family Caligidae. Journal of the Marine Biological Association of India, 5, 68–96.Google Scholar
  50. Pillai, N. K. (1967). Copepods parasitic on Indian marine fishes. A review. Proceedings of Symposium on Crustacea, Cochin, 5, 1556–1680.Google Scholar
  51. Prabha, C., & Pillai, N. K. (1983). Additions to the copepods parasitic on the marine fishes of India. 4. On twenty-six species of Caligids. Records of the Zoological Survey of India Occasional Paper, 46, 1–49.Google Scholar
  52. Raibaut, A., Combes, C., & Benoit, F. (1998). Analysis of the parasitic copepod species richness among Mediterranean fish. In: Dahms, H. U., Glatzel, T., Hirche, H. J., Schiel, S., & Schminke, H. K. (Eds). Proceedings of the 6th International Conference on Copepoda, Journal of Marine Systems, 15, 185–206.Google Scholar
  53. Rangnekar, M. P. (1956). Parasitic copepods from the marine fishes of Bombay. Journal of the University of Bombay, 24, 42–65.Google Scholar
  54. Rangnekar, M. P. (1959). Parasitic copepods from fishes of the western coast of India with description of one new and redescription of four known species. Journal of the University of Bombay, 28, 43–58.Google Scholar
  55. Rohde, K. (1980). Comparative studies on microhabitat utilization by ectoparasites of some marine fishes from the North Sea and Papua New Guinea. Zoologischer Anzeiger, 204, 27–63.Google Scholar
  56. Sharp, N. J., Poortenaar, C. W., Diggles, B. K., & Willis, T. J. (2003). Metazoan parasites of yellowtail kingfish, Seriola lalandi lalandi in New Zealand: Prevalence, intensity, and site preference. New Zealand Journal of Marine and Freshwater Research, 37, 273–282.CrossRefGoogle Scholar
  57. Shiino, S. M. (1960). Copepods parasitic on the fishes collected on the coast of Province Shima, Japan. Report of the Faculty of Fisheries, Prefectural University of Mie, 3, 471–500.Google Scholar
  58. Shiino, S. M. (1965). Parasitic copepods of the eastern Pacific fishes. 5. Caligus. Report of the Faculty of Fisheries, Prefectural University of Mie, 5, 391–420.Google Scholar
  59. Song, D. X., & Chen, G. X. (1976). Some parasitic copepods from marine fishes of China. Acta Zoologica Sinica, 22, 406–424.Google Scholar
  60. Takemoto, R. M., & Luque, J. L. (2002). Parasitic copepods on Oligoplites spp. (Osteichthyes, Carangidae) from the Brazilian coastal zone, with the redescription of Tuxophorus caligodes Wilson, 1908 (Siphonostomatoida, Tuxophoridae). Acta Scientiarum, 24, 481–487.Google Scholar
  61. Venmathi Maran, B. A., Seng, L. T., Ohtsuka, S., & Nagasawa, K. (2009). Records of Caligus (Crustacea: Copepoda: Caligidae) from marine fish cultured in floating cages in Malaysia with a redescription of the male of Caligus longipedis Bassett-Smith, 1898. Zoological Studies, 48, 797–807.Google Scholar
  62. Walter, T. C., & Boxshall, G. A. (2018). World of Copepods database. Accessed through: World Register of Marine Species. Retrieved July 9, 2018, from http://marinespecies.org/aphia.php?p=taxdetails&id=135765.
  63. Wilson, C. B. (1921). Report on the parasitic Copepoda collected during the survey of the Juan Fernandez Islands, 1916–1917. Natural History of the Juan Fernandez & Easter Islands, 3, 69–74.Google Scholar
  64. Yamaguti, S. (1936) Parasitic copepods from fishes of Japan. Part 2. Caligoida I, Kyoto Imperial University (published by the author), 1–22.Google Scholar
  65. Yamaguti, S. (1939). Parasitic copepods from fishes of Japan. Part 5. Caligoida, III. Volume. Jubilare pro Prof. Sadao Yoshida, 2, 443–487.Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Fish Diseases and Aquaculture, Faculty of FisheriesUniversity of CukurovaAdanaTurkey
  2. 2.Department of Marine Sciences, Faculty of Marine Sciences and TechnologyIskenderun Technical UniversityIskenderun/HatayTurkey
  3. 3.Life Sciences DepartmentNatural History MuseumLondonUK

Personalised recommendations