First Report of Caligus minimus Otto, 1821 (Copepoda: Siphonostomatoida: Caligidae) from Plankton Samples Collected from Türkiye

Year 2023, Volume: 7 Issue: 1, 50 - 57, 30.06.2023

Seyit Ali Kamanli

https://doi.org/10.31594/commagene.1261446

Cited By: 2

Abstract

During a plankton sampling conducted off the northeastern Mediterranean coast of Türkiye, a single female copepod, Caligus minimus Otto, 1821 was collected from a marine plankton sample. C. minimus is a well-known species of the genus Caligus O.F. Müller, 1785 which has been previously reported as a parasite from nine marine fish species belonging to eight different families. To date, however, C. minimus has never been reported from plankton samples. In this study, the general morphology based on the key diagnostic characters of the planktonic C. minimus is presented using confocal laser scanning microscope (CLSM) images. This is the first report of C. minimus from plankton samples off Turkish waters and global marine environments.

Keywords

Planktonic copepod, Plankton net, Mediterranean, CLSM

Thanks

Acknowledgement: I would like to thank Dr. Gürkan AKBULUT for his technical help during the ichtyoplancton sampling.

Türkiye’den Toplanan Plankton Örneklerinde Deniz Biti, Caligus minimus Otto, 1821 (Copepoda: Siphonostomatoida: Caligidae) İle ilgili İlk Rapor

Abstract

Türkiye’nin kuzeydoğu Akdeniz kıyılarında yürütülen bir plankton örneklemesi sırasında, deniz plankton örneklerinden tesadüfen tek bir dişi Caligid parazitik kopepod, Caligus minimus Otto, 1821 bireyi örneklendi. C. minimus, daha önce sekiz farklı familyaya ait dokuz deniz balığı türünden bildirilen Caligus O.F. Müller, 1985 cinsinin iyi bilinen bir türüdür. Ancak bugüne kadar plankton örneklerinden C. minimus hiç rapor edilmemiştir. Bu çalışmada, konfokal lazer taramalı mikroskobu (CLSM) görüntüleri kullanılarak planktonik C. minimus’un genel morfolojisi ve tür teşhisinde kullanılan belirgin karakterleri sunulmuştur. Bu çalışma, Türkiye ve dünya denizel ortamlarından C. minimus’un planktonik formunun ilk raporudur.

Keywords

Planktonik kopepod, plankton ağı, Akdeniz, CLSM

References

• Abouzaid, A.A., Bazh, K.E., Desouky, A.Y., & Abo-Rawash, A.A. (2018). Metazoan parasite fauna of wild sea bass; Dicentrarchus labrax (Linnaeus, 1758) in Egypt. Life Science Journal, 15(6), 48-60. https://doi.org/10.7537/marslsj150618.06
• Bahri, L., Ben Hamida, J., & Ben Hassine, O.K. (2002). Use of parasitic copepod, Lernanthropus kroyeri (Van Beneden, 1851) (Lernanthropidae) as a bio-indicator of two fish populations, Dicentrarchus labrax Linnaeus (1758) and Diplodus punctatus (Bloch, 1792) (Moronidae) in Tunisian inshore areas. Crustaceana, 75, 253-267.
• Benmansour, B., & Ben Hassine, O.K. (1998). Preliminary analysis of parasitic copepod species richness among coastal fishes of Tunisia. Italian Journal of Zoology, 65, 341-344.
• Boxshall, G.A. (1974). Infections with parasitic copepods in North Sea marine fishes. Journal of the Marine Biological Association of the United Kingdom, 54, 355-372. https://doi.org/10.1017/S0025315400058598
• 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 of London. Series B, Biological Sciences. 328, 167-212. https://doi.org/10.1098/rstb.1990.0113
• Bragoni, G., Romestand, B., & Trilles, J.P. (1983). Parasitism by cymothoids among sea bass in rearing. Annales de Parasitologie Humaine et Comparée, 58(6), 593-609. https://doi.org/10.1051/parasite/1983586593
• Brian, A. (1906). Copepodi parassiti dei Pesci d’Italia. Stabilimento Tipo-Litografico Regio Istituto Sordomuti, Genova, 187 pp.
• Brian, A. (1935). I Caligus parassiti dei pesci del Mediterraneo (Copepodi). Annali del Museo Civico di Storia Naturale 'Giacomo Doria', Genova, 57, 152-211.
• Cabral, P. (1983). Morphologie, biologie et écologie des Copépodes parasites du Loup Dicentrarchus labrax (Linné, 1758) et du Sar rayé Diplodus sargus (Linné, 1758) de la région languedocienne. Thèse de 3ème cycle, Université Montpellier, Montpellier, 221 pp.
• Cabral, P., & Raibaut, A. (1986). Discovery of a new caligid copepod, parasite of the wolf's seed coat, Dicentrarchus labrax (L., 1758) (Pisces, Moronidae) in breeding and in a natural environment. Bulletin of the Zoological Society of France, 111(1-2), 123-130.
• Canlı, M. (2010). Ectoparasite research on economic fish species which is caught from Hurmabogazı Lagoon (Adana). Dissertation. Cukurova University (in Turkish with English abstract).
• Cengizler, İ., Erdem, Ü., Özak, A.A., Genç, E., & Şahan, A. (2001). Caligiosis in Sea Bass (Dicentrarchus labrax) cultured in coast of Yumurtalık (Adana). In: XI National Symposium on Aquatic Products, 4-6 September 2001, Hatay, Turkey (in Turkish).
• Czerniavski, V. (1868). Materialia ad zoographiam Ponticam comparatam. Travaux de la Societe des naturalistes de St. Petersbourg, 1, 19-136.
• Delamare-Deboutteville, C. (1950). Copépodes parasites des poissons de Banyuls (1ère série). Vie et Milieu, 3, 305-309.
• El-Deen, A.I.E.N., Mahmoud, A.E., & Hassan, H.M. (2013). Field studies of Caligus parasitic infections among cultured seabass (Dicentrarchus labrax) and mullet (Mugil cephalus) in marine fish farms with emphasis on treatment trials. Global Veterinaria, 11(5), 511-520. https://doi.org/10.5829/idosi.gv.2013.11.5.76168
• Er, A., & Kayış, Ş. (2015). Intensity and prevalence of some crustacean fish parasites in Turkey and their molecular identification. Turkish Journal of Zoology, 39, 1142-1150. https://doi.org/10.3906/zoo-1409-35
• Essafi, K., Cabral, P., & Raibaut, A. (1984). Parasitic copepods of fish from the Kerkennah Islands (southern Tunisia). Les Archives de l'Institut Pasteur Tunis, 61(4), 475-523.
• Fernández, J.P., Muñoz, M.V., Orts, M.E., & Carbonell, E. (1989). Prevalencia e intensidad de parasitación por crustáceos en peces del Mar Mediterráneo, Revista Ibérica de Parasitología, 49(1), 75-76.
• Fioravanti, M.L., Caffara, M., Florio, D., Gustinelli, A., & Marcer, F. (2006). A parasitological survey of European Sea Bass (Dicentrarchus labrax) and Gilthead Sea Bream (Sparus aurata) cultured in Italy. Veterinary Research Communications, 30(1), 249-252. https://doi.org/10.1007/s11259-006-0053-5
• Froese, R., & Pauly, D. (2023). FishBase. Retreived from http://www.fishbase.org
• Grabda, J. (1977). Crustaceans-parasites of marine fishes, Wiadomosci Parazytologiczne. 23(1-3), 171-176.
• Hayward, C.J., Aiken, H.M., & Nowak, B.F. (2008). An epizootic of Caligus chiastos on farmed southern bluefin tuna Thunnus maccoyii off South Australia. Diseases of Aquatic Organisms, 79, 57-63. https://doi.org/10.3354/dao01890
• Hayward, C.J., Svane, I., Lachimpadi, S.K., Itoh, N., Bott, N.J., & Nowak, B.F. (2011). Sea lice infections of wild fishes near ranched southern bluefin tuna (Thunnaus maccoyi) in South Australia. Aquaculture, 320, 178-182. https://doi.org/10.1016/j.aquaculture.2010.10.039
• Heegaard, P. (1966). Parasitic copepods from Texas. Videnskabelige Meddelelser fra Dansk naturhistoriske Forening, Copenhagen, 129, 187-197.
• Heegaard, P. (1972). Caliginae and Euryphorinae of the Dana Expedition (Crustacea, Copepoda, Caligidae). Steenstrupia, 2, 295-317.
• Heller, C. (1865). Crustaceen. Reise der Oesterreichischen Fregatte Novara um die Erde in den Jahren 1857, 1858, 1859. Zoologischer Theil, 2, 1-280.
• Hemmingsen, W., & MacKenzie, K. (2001). The parasite fauna of the Atlantic cod, Gadus morhua L. Advances in Marine Biology, 40, 1-80.
• Hewitt, G.C. (1971). Two species of Caligus (Copepoda, Caligidae) from Australian waters, with a description of some developmental stages. Pacific Science, 25, 145-164.
• 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(1-2), 69-114. https://doi.org/10.1080/00288330.1977.9515410
• Ho, J.S., & Lin, C.L. (2004). Sea Lice of Taiwan (Copepoda: Siphonostomatoida: Caligidae). The Sueichan Press, Keelung, 388 pp.
• Holmes, J.M.C. (1998) A checklist of the Siphonostomatoida (Crustacea: Copepoda) of Ireland. Bulletin of the Irish Biogeographical Society, Dublin, 22(2), 194-228.
• Huys R., & Boxshall, G.A. (1991). Copepod Evolution, The Ray Society, London.
• Kabata, Z. (1979). Parasitic Copepoda of British Fishes, The Ray Society, London, 468 pp.
• Kabata, Z. (2003). Copepods Parasitic on Fishes. 2nd, revised edition. Synopses of the British Fauna, 2nd revised edition. Backhuys. No. 47, 1-274.
• Kamanli, S.A., Kihara, T.C., Ball, A.D., Morritt, D., & Clark, P.F. (2017). A 3D imaging and visualisation workflow, using confocal microscopy and advanced image processing for brachyuran crab larvae. Journal of Microscopy, 266, 307-323. https://doi.org/10.1111/jmi.12540
• Kim, I., Suárez-Morales, E., & Márquez-Rojas, B. (2019). Caligid copepods (Copepoda: Siphonostomatoida: Caligidae) as zooplankters off the Venezuelan coast, western Caribbean Sea. Thalassas: An International Journal of Marine Sciences, 35(2), 607‑618. https://doi.org/10.1007/s41208-019-00130-w
• Limaye, A. (2012). Drishti: a volume exploration and presentation tool, in: Stock SR (ed), Proceedings of SPIE Vol. 8506 SPIE. Developments in X-ray Tomography VIII Bellingham, Washington.
• Montú, M. (1982). Alguns copépodos parasites de peixes do sul do Brasil. Arquivos de Biologia e Tecnologia, 5, 329-339.
• Möller, H. (1975). Bibliography on parasites and diseases of marine fishes from North Sea and Baltic Sea. 15. Berichte aus dem Institut für Meereskunde an der Christian-Albrechts-Universität Kiel, 015. Institut für Meereskunde Kiel. 1-35. https://doi.org/10.3289/IFM_BER_15
• Ocaña-Luna, A., & Álvarez-Silva, C. (2001). Range extension of Caligus chelifer (Copepoda: Siphonostomatoida) to coastal lagoons. Revista de Biología Tropical, 49, 1277-1277.
• Ohtsuka, S., Ho, J., Nagasawa, K. (2004). Ergasilid copepods (Poecilostomatoida) in plankton samples from Hokkaido, Japan, with reconsideration of the taxonomic status of Limnoncaea Kokubo, 1914. Journal of Natural History, 38, 471-498. https://doi.org/10.1080/0022293021000034778
• Ohtsuka, S., Madinabeitia, I., Yamashita, H., Venmathi Maran, B.A., Suárez-Morales, E., & Ho, J.S. (2018). Planktonic phases in symbiotic copepods: a review. Bulletin of the Southern California Academy of Sciences, 117(2),104-19.
• Ohtsuka, S., & Boxshall, G.A. (2019). Two new species of the genus Caligus (Crustacea, Copepoda, Siphonostomatoida) from the Sea of Japan, with a note on the establishment of a new species group. ZooKeys, 893, 91‑113. https://doi.org/10.3897/zookeys.893.46923
• Ohtsuka, S., Nawata, M., Nishida, Y., Nitta, M., Hirano K, Adachi K, ..., & Suárez-Morales, E. (2020). Discovery of the fish host of the ‘planktonic’ caligid Caligus undulatus Shen & Li, 1959 (Crustacea: Copepoda: Siphonostomatoida). Biodiversity Data Journal, 8, e52271. https://doi.org/10.3897/BDJ.8.e52271
• Ortega, I., Scott-Frías, J., & Martin, A. (2017). Diversity and composition of copepods assemblage associated with hyperbenthic zone of the Venezuelan central coast sandy beaches. Juan Antonio Bolaños Curvelo, In Memoriam, Publicación Especial del Boletín del Instituto Oceanográfico de Venezuela, 123‑132.
• Öktener, A., Türker, D., & Alaş, A. (2017). The Sea of Marmara: new locality for two caligids and one lernanthropid in Turkey. Journal of Wetland Biodiversity,7, 109-130.
• Özak, A.A. (2007). Studies on the biology of parasitic copepod, Caligus minimus Otto, 1821 on European Sea Bass, Dicentrarchus labrax L. 1758. Dissertation, Çukurova University 110 pp (in Turkish with English abstract).
• Özak, A.A. (2020). Sea lice (Copepoda: Caligidae) of Turkey, with the discovery of Caligus quadratus Shiino, 1954 in the Mediterranean Sea and the re-description of a rare caligid copepod, Caligus scribae Essafi, Cabral & Raibaut, 1984. Systematic Parasitology, 97, 779-808. https://doi.org/10.1007/s11230-020-09953-1
• Özer, A., & Öztürk, T. (2011). First report of Ceratomyxa sp. (Myxozoa) and Caligus minimus (Copepoda) on sea bass (Dicentrarchus labrax) from Turkey. In: 16th Symposiyum on National Aquatic Products 25–27 October 2011, Antalya, Turkey.
• 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.
• Paperna, I. (1977). Copepod infection in fish in euryhaline environments. Wiadomosci Warazytologiczne, 23, 183‒188.
• Paperna, I., & Baudin Laurencin, P. (1979). Parasitic infections of sea bass, Dicentrarchus labrax, and gilt head sea bream, Sparus aurata, in mariculture facilities in France, Aquaculture, 16,173-175.
• Paperna, I. (1980). Study of Caligus minimus (Otto, 1821) (Caligidae Copepoda) infections of the Sea bass Dicentrarchus labrax (L.) in Bardawil Lagoon. Annales des Sciences Naturelles Zoologie, 55(6), 687-706. https://doi.org/10.1051/parasite/1980556687
• Papoutsoglou, S., Costello, M.J., Stamou, E., & Tziha, G. (1996). Environmental conditions at sea-cages and ectoparasites on farmed European sea-bass. Dicentrarchus labrax (L.), and gilt-head sea-bream, Sparus aurata L., at two farms in Greece. Aquaculture Research, 27, 25-34.
• Pavoletti, E., Fioravanti, M.L., Prearo, M., & Ghittino, C. (1999). Osservazioni sulla Caligosi in spigole dallevamento. Bollettino della Società Paleontologica Italiana, 11, 2-9.
• Pillai, N.K. (1985). The Fauna of India. Copepod Parasites of marine Fishes. Zoological Society of India, Calcutta, 900 pp.
• Poquet, M. (1979). Aportaciones al estudio morfologico de algunas especies de copepodos parasitos de peces del litoral mediterraneo. Miscellaneous publications (University of Michigan) Museum of Zoology, 5, 161-171.
• Radujković, B.M., & Raibaut, A. (1989). Copepodes parasites des poissons des cotes du Montenegro (Adriatique Sud). Parassitologia, 31(1), 1-24.
• Ragias, V., Tontis, D., & Athanassopoulou, F. (2004). Incidence of an intense Caligus minimus Otto 1821, C. pageti Russell, 1925, C. mugilis Brian, 1935 and C. apodus Brian, 1924 infection in lagoon cultured sea bass (Dicentrarchus labrax L.) in Greece. Aquaculture, 242, 727-733. https://doi.org/10.1016/j.aquaculture.2004.08.019
• Raibaut, A. & Ben Hassine, O.K. (1977). Les copépodes parasites des muges en Méditeranée. Bulletin du Museum National d'histoire Naturelle. Ser. 3, 329, 833-848.
• 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, Spec, 15(1-4), 185-206.
• Salama, S.S.A., & Yousef, N.S.I. (2020). The impact of co-infection of sea lice and its concurrent some bacterial diseases with field treatment trials in some marine cultured fishes. Egyptian Journal of Aquatic Biology and Fisheries, 24(7-Special issue), 363-381. https://doi.org/10.21608/ejabf.2020.120412
• Santos, M.J. (1996). Observations on the parasitofauna of wild sea bass (Dicentrarchus labrax L.) from Portugal. Bulletin of the European Association of Fish Pathologists, 16, 77-79.
• Saraiva, A., Costa, J., Serrão, J., Eiras, J.C., & Cruz, C. (2015). Study of the gill health status of farmed sea bass (Dicentrarchus labrax L., 1758) using different tools. Aquaculture, 441, 16-20. https://doi.org/10.1016/j.aquaculture.2015.02.004
• Schneider, C.A., Rasband, W.S., & Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671-675. https://doi.org/10.1038/nmeth.2089
• Shen, C.-j., & Li, H.-l. (1959). Parasitic copepods from fishes of China, IV. Caligoida. Caligidae (3). Acta Zoologica Sinica, 11, 12-20 (In Chinese with English summary).
• Sterud, E. (2002). Parasites of wild sea bass Dicentrarchus labrax from Norway. Diseases of Aquatic Organisms, 48, 209-212. http://dx.doi.org/10.3354/dao048209
• Sterud, E. (2002). Parasites of wild sea bass Dicentrarchus labrax from Norway. Diseases of Aquatic Organisms, 48, 209-212. https://doi.org/10.3354/dao048209
• Suárez-Morales, E., Camisotti, H., & Martín, A. (2012a). A new species of Caligus (Copepoda, Siphonostomatoida) from the plankton of the Caribbean coast of Venezuela with a key to species. Zookeys, 201, 59-71. http://dx.doi.org/10.3897/zookeys.201.3099
• Suárez-Morales, E., Kim, I.-H., & Escamilla, B.J. (2012b). On some caligids (Copepoda: Caligidae) from plankton of a coastal lagoon in the Gulf of Mexico with a description of a new species of Metacaligus. Zoological Studies, 51, 804-818.
• Suárez-Morales, E., & Gasca, R. (2012). A new Lepeophtheirus (Copepoda: Siphonostomatoida: Caligidae) from Isla del Coco National Park, Costa Rica, Eastern Tropical Pacific. Revista de Biología Tropical, 60 (Suppl.3), 235-242.
• Suárez-Morales, E., & Gasca, R. (2016). A new species of Caligus Müller, 1785 (Copepoda: Siphonostomatoida) from the coral reef plankton in the Mexican Caribbean. Zootaxa, 4174(1), 424-436. https://doi.org/10.11646/zootaxa.4174.1.26 Tanrikul, T.T., & Percin, F. (2012). Ectoparasitic sea lice, Caligus minimus (Otto 1821, Copepoda: Caligidae) on Brawn wrasse, Labrus merula L., in Izmir Bay, Aegean Sea. Italian Journal of Animal Science, 11, 38-41.
• Tokşen, E. (1999). Metazoan gill parasites of culture gilthead sea bream (Sparus aurata L.) and sea bass (Dicentrarchus labrax L.) in the Aegean Sea Coast and their treatment. PhD thesis, Ege University, İzmir, Turkey.
• Uluköy, G., & Kubilay, A. (2005). Ege sea lice (Caligus minimus Otto, 1821, Copepoda: Caligidae) infestation in cultured seabass (Dicentrarchus labrax, L 1758). Turkish Journal of Aquatic Life, 4, 256.
• Uluköy, G., & Kubilay, A. (2007). Caligus minimus infestation on cultured European sea bass, (Dicentrarchus labrax L., 1758). XIV National Symposium on Aquatic Products, 4-7 September 2007, Mugla, Turkey.
• Vagianou, S., Athanassopoulou, F., Ragias, V., Di Cave, D., Leontides, L., & Golomazou, E. (2006). Prevalence and pathology of ectoparasites of Mediterranean Sea bream and sea bass reared under different environmental and aquaculture conditions. The Israeli Journal of Aquaculture – Bamidgeh, 58, 78-88.
• Venmathi Maran, B.A., & Ohtsuka, S. (2008). Description of caligiform copepods in plankton samples collected from East Asia: Accidental occurrences or a new mode of life cycle? Plankton Benthos Research, 3, 202-215. https://doi.org/10.3800/pbr.3.202
• Venmathi Maran, B.A., Ohtsuka, S., & Jitchum, P. (2012a). Occurrence of caligid copepods (Crustacea) in plankton samples collected from Japan and Thailand, with the description of a new species. Species Diversity, 17, 87-95. https://doi.org/10.12782/sd.17.1.087
• Venmathi Maran, B.A., Ohtsuka, S., & Shang, X. (2012b). Records of adult caligiform copepods (Crustacea: Copepoda: Siphonostomatoida) in marine plankton from East Asia, including descriptions of two new species of Caligus (Caligidae). Species Diversity, 17, 201-219. http://dx.doi.org/10.12782/sd.17.2.201
• Venmathi Maran, B.A., Suárez-Morales, E., Ohtsuka, S., Soh, H.Y., & Hwang, U.W. (2016). On the occurrence of caligids (Copepoda: Siphonostomatoida) in the marine plankton: a review and checklist. Zootaxa, 4174(1), 437‑447. https://doi.org/10.11646/zootaxa.4174.1.27
• Venmathi Maran, B.A., Suárez-Morales, E., Ohtsuka, S., Soh, H.Y., & Hwang, U.W. (2018). Planktonic phase of symbiotic copepods: a brief review. Bulletin of the Southern California Academy of Sciences, 117,1-16.
• Yalım, F.B., Emre, N., Emre, Y., Yazmen, H., Öztürk, M.O., Akmirza, A., & Aydoğdu, A. (2014). Caligus minimus (Copepoda, Caligidae) infestation of European sea bass (Dicentrarchus labrax) from Beymelek Lagoon Lake (Antalya, Turkey): Effects of host sex, age, size and season. Journal of Academic Documents for Fisheries and Aquaculture, 1, 9-16.
• Yamak, S., & Ben Hassine, O.K. (2002). Impact of a fish farm on ichthyofauna and ichthyoparasitofauna of a Tunisian lagoon. In: Proceedings of the International Conference on the Environmental Problems of the Mediterranean Region, 12–15 April 2002, Nicosia, Turkish Republic of Northern Cyprus.
• Walter, T.C. & Boxshall, G.A. (2023). World of Copepods Database. Retreived from http://www.marinespecies.org/copepoda