Fish’s Crustacean Parasites: Types, Prevalence, Clinical signs, and Control

Document Type : Reviews

Authors

Department of Zoology, Faculty of Science, Sohag University, 82524, Sohag, Egypt

Abstract

Crustaceans during a parasitism relationship with fish cause biological disruption and diseases to the hosting fish that threaten their life. Several crustacean groups were reported to parasitize different fish species as definitive hosts. Copepods, Isopods, and Branchiura are the major fish parasitic groups under the crustacea. They are mainly ectoparasites and occasionally, the small and microscopic members can infest the internal organs of their fish hosts. The infected fish are suffering from serious clinical signs and the infested organs are usually suffering from severe pathological disruptions and lesions. Treatment is taking place by several chemical and biological facilities. Here in the current article, the major crustaceans that parasitize on fish are reviewed by describing their corresponding harms to the hosting fish. Factors affecting the prevalence of the crustacean parasites and some of their hazardous effects on the infected fish were considered.  In addition, trials for the chemical and biological control of the crustacean infestations are summarized.

Keywords

Main Subjects


[1]     Mansoor, N.T. & Al-Shaikh, S.M.J.; Isolate two crustaceans which infect Cyprinus carpio L. from Bab Al-Muatham fish markets, Baghdad City. Iraq. J. Vet. Med., 2011, 35: 52–59. https://doi.org/10.30539/iraqijvm.v35i1.603.
[2]     Faruk, A.R.; Fish parasite: Infectious diseases associated with fish parasite. Seaf. Saf. Qual., 2018, 154–176.
[3]     Rameshkumar, G. & Ravichandran, S.; Problems caused by isopod parasites in commercial fishes. J. Para. Dis.; 2014, 38: 138–141. https://doi.org/10.1007/s12639-012-0210-4.
[4]     Tavares-Dias, M.; Dias-Júnior, M.B.F.; Florentino, A.C.; Silva, L.M.A.; da Cunha, A.C.; Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Revi. Brasi. de Parasit. Veteri., 2015, 24: 136–147. https://doi.org/10.1590/s1984-29612015036.
[5]     Binning, S.A.; Roche, D.G.; Layton, C.; Ectoparasites increase swimming costs in a coral reef fish. Biol. Lett., 2013, 9. https://doi.org/10.1098/rsbl.2012.0927.
[6]     Soliman, F.M.; Abd El-Galil, M.A.A.; Mohamed, A.A.; Ahmed, F.-A.A.A.; Studies on trichodinosis of some cultured freshwater fishes at Sohag Governorate. Lif. Sci. J., 2013, 10(4): 1400–1409. http://dx.doi.org/10.1016/j.jsames.2011.03.003%0Ahttps://doi.org/10.1016/j.gr.2017.08.001%0Ahttp://dx.doi.org/10.1016/j.precamres.2014.12.018%0Ahttp://dx.doi.org/10.1016/j.precamres.2011.08.005%0Ahttp://dx.doi.org/10.1080/00206814.2014.902757%0Ahttp://dx.
[7]     Adly, A.M.; Abd El-Galil, M.A.A.; Soliman, F.M.; Ahmed, F.E.Z.A.A.; Histopathological studies on trichodinosis of farmed Oreochromis niloticus. Am. J. Lif. Sci., 2015, 3(6-1): 30-37. https://doi.org/10.11648/j.ajls.s.2015030601.15.
[8]     Waldman, J.; Grunwald, C.; Wirgin, I.; Sea lamprey Petromyzon marinus: An exception to the rule of homing in anadromous fishes. Biol. Lett., 2008, 4:659–662. https://doi.org/10.1098/rsbl.2008.0341.
[9]     Bullingham, O.M.N.; Firkus, T.J.; Goetz, F.W.; Murphy, C.A.; Alderman, S.L.; Lake charr (Salvelinus namaycush) clotting response may act as a plasma biomarker of sea lamprey (Petromyzon marinus) parasitism: Implications for management and wound assessment. J. Gre. Lak. Res., 2021, 22. https://doi.org/10.1016/j.jglr.2021.11.005.
[10]  Yuniar, A.T.; Palm, H.W.: Walter, T.; Crustacean fish parasites from Segara Anakan Lagoon, Java, Indonesia. Paras. Res., 2007, 100:1193–1204. https://doi.org/10.1007/s00436-006-0391-9.
[11]  Eissa, I.A.M.; El-Lamie, M.; Zakai, M.; Studies on crustacean diseases of seabass, Morone labrax, in Suez Canal Isamailia Governorate. Li. Sci. J., 2012, 9: 512–518. http://www.lifesciencesite.com.
[12]  Praveenraj, J.; Saravanan, K.; Kumar, P. P.; Ravichandran, S.; Baruah, A.; Monalisha Devi, S.; Kiruba Sankar, R.; Dam Roy, S.; First record on the occurrence of Ryukyua circularis (Pillai, 1954), a parasitic cymothoid (Crustacean: Isopoda) infesting the clupeid fish Amblygaster sirm (Walbaum) from Andaman Islands, India. J. Para. Dis., 2017, 41: 593–595. https://doi.org/10.1007/s12639-016-0823-0.
[13]  Smit, N.J.; Bruce, N.L.; Hadfield, K.A.; Parasitic rustacea, 2019. http://link.springer.com/10.1007/978-3-030-17385-2.
[14]  Aneesh, P.T.: Sudha, K.: Helna, A.K.; Anilkumar, G.; Trilles, J.P.; Multiple parasitic crustacean infestation on belonid fish Strongylura strongylura. Zook., 2014, 353:339–353. https://doi.org/10.3897/zookeys.457.6817.
[15]  Overstreet, R.M.; Jovonovich, J.; Ma, H.; Parasitic crustaceans as vectors of viruses, with an emphasis on three penaeid viruses. Integr. & Comp. Biol., 2009, 49: 127–141. https://doi.org/10.1093/icb/icp033.
[16]  Chandra, K.: Fish parasitological studies in bangladesh: A Review. J. Agricul. & Rur. Devel., 2006, 4:9–18. https://doi.org/10.3329/jard.v4i1.762.
[17]  Jithendran, K.P.; Natarajan, M.; Azad, I.S.; Crustacean parasites and their management in brackishwater finfish culture. Mar. finf. Aquac. netw., 2008, 47–50.
[18]  Misganaw, K.; Getu, A.; Review on major parasitic crustacean in fish. Fish. & Aquac. J., 2016, 7:13–17. https://doi.org/10.4172/2150-3508.1000175.
[19]  Abowei, J.F.N.; Briyai, O.F.; Bassey, S.E.; A review of some basic parasite diseases in culture fisheries flagellids, dinoflagellides and ichthyophthriasis, ichtyobodiasis, coccidiosis trichodiniasis, heminthiasis, hirudinea infestation, crustacean parasite, and Ciliates. J. Pharm. & Toxic., 2011, 2: 213–226.
[20]  Bennett, M.B.; Heupel, M.R.; Bennett, S.M.; Parker, A.R.; Sheina orri (Myodocopa: Cypridinidae), an ostracod parasitic on the gills of the epaulette shark, Hemiscyllium ocellatum (Elasmobranchii: Hemiscyllidae). Inter. J. Paras., 1997, 27:275–281. https://doi.org/10.1016/S0020-7519(96)00201-9.
[21]  Bowker, J.D.; Carty, D.G.; Wandelear, N.; Schaffer, J.; Swee, W.; Lapatra, S.E.; Efficacy of slice premix (0.2% emamectin benzoate) for reducing infestations of Salmincola spp. on freshwater-reared rainbow trout. Nor. Amer. J. Aquacul., 2012, 74:428–437. https://doi.org/10.1080/15222055.2012.676019.
[22]  Tokşen, E.; Nemli, E.; Degirmenci, U.; Karacalar, U.; Parasitic diseases of trout and their controls in sustainable development of aquculture : crustaceans. (n.d.), 256–264.
[23]  Luque, J.L.; Vieira, F.M.; Takemoto, R.M.; Pavanelli, G.C.; Eiras, J.C.; Checklist of crustacea parasitizing fishes from Brazil. Che. Lis., 2013, 9:1449–1470. https://doi.org/10.15560/9.6.1449.
[24]  Smit, N.J. & Hadfield, K.A.; A systematic survey of parasites of freshwater fish in Africa–Crustacea. A gui. para. Afric. Freshw. fish., 2018, 333–355.
[25]  Maran, B.A.V.; Seng, L.T.; Ohtsuka, S.; Nagasawa, K.; 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. Zool. Stud., 2009, 48:797–807.
[26]  Vasconcelos, H.C.G. & Tavares-Dias, M.; Host-parasite interaction between crustaceans of six fish species from the Brazilian Amazon. Acta Scient. – Biol. Sci., 2016, 38:113–123. https://doi.org/10.4025/actascibiolsci.v38i1.29601.
[27]  Aly, S.M.; A Review of fish diseases in the Egyptian aquaculture. Research program on livestock and fish., 2013. www.livestockfish.cgiar.org.
[28]  Smit, N.J.; Bruce, N.L.; Hadfield, K.A.; Global diversity of fish parasitic isopod crustaceans of the family Cymothoidae. Inter. J. Parasitol.: Para. and Wildlif., 2014, 3: 188–197. https://doi.org/10.1016/j.ijppaw.2014.03.004.
[29]  Rajkumar, M.; Perumal, P.; Trilles, J.P.; Cymothoa indica (Crustacea, Isopoda, Cymothoidae) parasitizes the cultured larvae of the Asian seabass Lates calcarifer under laboratory conditions. Dis. Aqu. Org., 2005, 66:87–90. https://doi.org/10.3354/dao066087.
[30]  Hadfield, K.A.; Bruce, N.L.; Smit, N.J.; Review of the fish parasitic genus Ceratothoa Dana, 1852 (Crustacea, Isopoda, Cymothoidae) from South Africa, including the description of two new species. Zook., 2014 400:1–42. https://doi.org/10.3897/zookeys.400.6878.
[31]  Pasternak, A.F.; Mikheev, V.N.; Valtonen, E.T.; Adaptive significance of the sexual size dimorphism in the fish ectoparasite Argulus coregoni (Crustacea: Branchiura). Dok. Biol. Sci., 2004, 399:477–480. https://doi.org/10.1007/s10630-005-0017-x.
[32]  Steckler, N. & Yanong, R.P.; Argulus (fish louse) infections in fish. Edis., 2013, 2013:1–5. https://doi.org/10.32473/edis-fa184-2012.
[33]  Hakalahti, T. & Valtonen, E.T.; Population structure and recruitment of the ectoparasite Argulus coregoni Thorell (Crustacea: Branchiura) on a fish farm. Parasitol., 2003, 127:79–85. https://doi.org/10.1017/S0031182003003196.
[34]  Harrison, A.J.; Gault, N.F.S.; Dick, J.T.A.; Seasonal and vertical patterns of egg-laying by the freshwater fish louse Argulus foliaceus (Crustacea: Branchiura). Dis. Aquat. Organ., 2006, 68:167–173. https://doi.org/10.3354/dao068167.
[35]  Taylor, N.G.H.; Sommerville, C.; Wootten, R.; The epidemiology of Argulus spp. (Crustacea: Branchiura) infections in stillwater trout fisheries, J. Fish Dis., 2006, 29:193–200. https://doi.org/10.1111/j.1365-2761.2006.00704.x.
[36]  Öktener, A.; Ali, A.H.; Gustinelli, A.; Fioravanti, M.L.; New host records for fish louse, Argulus foliaceus L., 1758 (Crustacea, Branchiura) in Turkey. Ittiopatol., 2006, 3:161–167.
[37]  Everts, L.A.M. & Avenant-Oldewage, A.; First record of Argulus coregoni: A fish ectoparasite crustacean from Malaysia and additional notes on the morphology. Malays. Appl. Biol., 2009, 38:61–71.
[38]  Saha, M. & Bandyopadhyay, P.K.; First report of three species of Argulus (Crustacea: Branchiura) infesting on red- can Oranda gold fish (Carassius auratus auratus) in India. Biolif., 2015, 3:813–819. https://doi.org/10.17812/blj.2015.3411.
[39]  Wafer, L.N.; Whitney, J.C.; Jensen, V.B.; Fish lice (Argulus japonicus) in goldfish (Carassius auratus). Comp. Med., 2015 65:93–95.
[40]  Katahira, H.; Yamamoto, A.; Masubuchi, T.; Isshiki, T.; Watanabe, N.; Kanaiwa, M.; A report on potential effects of an ectoparasite Argulus coregoni (Crustacea: Branchiura) on ayu under rearing condition. Aquacul., 2021, 543:736980. https://doi.org/10.1016/j.aquaculture.2021.736980.
[41]  Ogawa, K. & Yokoyama, H.; Parasitic diseases of cultured marine fish in Japan, Fish Pathol., 1998, 33:303–309. https://doi.org/10.3147/jsfp.33.303.
[42]  Scholz, T.; Parasites in cultured and feral fish. Vet. Parasitol., 1999, 84:317–335. https://doi.org/10.1016/S0304-4017(99)00039-4.
[43]  Oguz, M.C. & Oktener, A.; Four parasitic crustacean species from marine fishes of Turkey. Turk. Parazitol. Derg., 2007, 31:79–83.
[44]  Grant, B.; Huchzermeyer, D.; Hohls, B.; Manual for fish kill investigations in South Africa. 2014. https://doi.org/10.13140/RG.2.1.1338.4080
[45]  Bandilla, M.; Hakalahti, T.; Hudson, P.J.; Valtonen, E.T.; Aggregation of Argulus coregoni (Crustacea: Branchiura) on rainbow trout (Oncorhynchus mykiss): A consequence of host susceptibility or exposure?. Parasitol., 2005, 130:169–176. https://doi.org/10.1017/S0031182004006407.
[46]  Quattrini, A.M. & Demopoulos, A.W.J.; Ectoparasitism on deep-sea fishes in the western North Atlantic: In situ observations from ROV surveys. Int. J. Parasitol. Parasites Wildl., 2016, 5:217–228. https://doi.org/10.1016/j.ijppaw.2016.07.004.
[47]  Mikheev, V.N.; Mikheev, A.V.; Pasternak, A.F.; Valtonen, E.T.; Light-mediated host searching strategies in a fish ectoparasite, Argulus foliaceus L. (Crustacea: Branchiura). Parasitol., 2000, 120:409–416. https://doi.org/10.1017/S0031182099005569.
[48]  Mikheev, V.N.; Pasternak, A.F.; Valtonen, E.T.; Lankinen, Y.; Spatial distribution and hatching of overwintered eggs of a fish ectoparasite, Argulus coregoni (Crustacea: Branchiura). Dis. Aquat. Organ., 2001, 46: 123–128.
[49]  Ravichandran, S.; Rameshkumar, G.; Kumaravel, K.; Variation in the morphological features of Isopod fish parasites. World J. Fish Mar. Sci., 2009, 1: 137–140.
[50]  Koyun, M., The Effect of water temperature on Argulus foliaceus L. 1758 (Crustacea; Branchiura) on different fish species. Not. Sci. Biol., 2011, 3:16–19. https://doi.org/10.15835/nsb325893.
[51]  Avenant-Oldewage, A.; Integumental damage caused by Dolops ranarum (Stuhlmann, 1891) (Crustacea: Branchiura) to Clarias gariepinus (Burchell), with reference to normal histology and wound‐inflicting structures. J. Fish Dis., 1994, 17: 641–647. https://doi.org/10.1111/j.1365-2761.1994.tb00262.x.
[52]  Mikheev, V.N.; Pasternak, A.F.; Valtonen, E.T.; Behavioural adaptations of argulid parasites (Crustacea: Branchiura) to major challenges in their life cycle. Paras. & Vect. 2015, 8:1–10. https://doi.org/10.1186/s13071-015-1005-0.
[53]  Kashinskaya, E.N.; Simonov, E.P.; Andree, K.B.; Vlasenko, P.G.; Polenogova, O.V.; Kiriukhin, B.A.; Solovyev, M.M.; Microbial community structure in a host–parasite system: the case of Prussian carp and its parasitic crustaceans. J. Appl. Microbiol., 2021, 131:1722–1741. https://doi.org/10.1111/jam.15071.
[54]  Ahmed, F.; Kumar, G.; Soliman, F.M.; Adly, M.A.; Soliman, H.A.M.; El-Matbouli, M.; Saleh, M.; Proteomics for understanding pathogenesis, immune modulation and host pathogen interactions in aquaculture. Comp. Biochem. Physiol. - Part D Genomics Proteomics., 2019, 32:100625. https://doi.org/10.1016/j.cbd.2019.100625.
[55]  Sudhagar, A.; Kumar, G.; El-Matbouli, M.; Transcriptome analysis based on RNA-Seq in understanding pathogenic mechanisms of diseases and the immune system of fish: A comprehensive review. Int. J. Mol. Sci., 2018, 19:245. https://doi.org/10.3390/ijms19010245.
[56]  Shivam, S.; El-Matbouli, M.; Kumar, G.; Development of fish parasite vaccines in the omics Era: Progress and opportunities. Vaccin., 2021, 9:1–23. https://doi.org/10.3390/vaccines9020179.
[57]  Roth, M.; The availability and use of chemotherapeutic sea lice control products. Contrib. to Zool., 2000, 69:109–118.
[58]  Madrid, R.R.M.; Mertins, O.; Tavares-Dias, M.; Flores-Gonzales, A.P.; Patta, A. C.M.F.; Ramirez, C.A.B.; Rigoni, V.L.S.; Mathews, P.D.; High compliance and effective treatment of fish endoparasitic infections with oral drug delivery nanobioparticles: Safety of intestinal tissue and blood parameters. J. Fish Dis., 2021 44:1819–1829. https://doi.org/10.1111/jfd.13501.
[59]  Ahmed, F.; Soliman, F.M.; Adly, M.A.; Soliman, H.A.M.; Recent progress in biomedical applications of chitosan and its nanocomposites in aquaculture : A review. Res. Vet. Sci., 2019, 126:68–82. https://doi.org/10.1016/j.rvsc.2019.08.005.
[60]  Ahmed, F.; Soliman, F.M.; Adly, M.A.; Soliman, H.A.M.; El-Matbouli, M.; Saleh, M.; In vitro assessment of the antimicrobial efficacy of chitosan nanoparticles against major fish pathogens and their cytotoxicity to fish cell lines. J. Fish Dis., 2020 43:1049–1063. https://doi.org/10.1111/jfd.13212.
[61]  Ahmed, F.; Soliman, F.M.; Adly, M.A.; Soliman, H.A.M.; El-Matbouli, M.; Saleh, M.; Dietary chitosan nanoparticles: Potential role in modulation of rainbow trout (Oncorhynchus mykiss) antibacterial defense and intestinal immunity against enteric redmouth disease. Mar. Drugs., 2021, 19:72. https://doi.org/10.3390/md19020072.
[62]  Treasurer, J.W.; A review of potential pathogens of sea lice and the application of cleaner fish in biological control. Pest Manag. Sci., 2002, 58:546–558. https://doi.org/10.1002/ps.509.
[63]  Leclercq, E.; Davie, A.; Migaud, H.; Delousing efficiency of farmed ballan wrasse (Labrus bergylta) against Lepeophtheirus salmonis infecting Atlantic salmon (Salmo salar) post-smolts. Pest Manag. Sci., 2014, 70:1274–1282. https://doi.org/10.1002/ps.3692.
[64]  Treasurer, J.W.; Parasites of wrasse (Labridae) in inshore waters of west Scotland stocked as cleaner fish of sea lice (Caligidae) on farmed Atlantic salmon. J. Fish Biol., 1997, 50:895–899. https://doi.org/10.1006/jfbi.1996.0342.
[65]  Bjordal, A.; Sea lice infestation on farmed salmon: Possible use of cleaner-fish as an alternative method of de-lousing. Can. Tech. Rep. Fish. Aquat. Sci., 1990, 176185–89.
[66]  Tully, O.; Daly, P.; Lysaght, S.; Deady, S.; Varian, S.J.A.; Use of cleaner-wrasse (Centrolubrus exoletus (L.) and Ctenolabrus rupestris (L.)) to control infestations of Caligus elongatus Nordmann on farmed Atlantic salmon. Aquacul., 1996, 142:11–24.
[67]  Skiftesvik, A.B.; Bjelland, R.M.; Durif, C.M.F.; Johansen, I.S.; Browman, H.I.; Delousing of Atlantic salmon (Salmo salar) by cultured vs. wild ballan wrasse (Labrus bergylta). Aquacul., 2013, 402–403: 113–118. https://doi.org/10.1016/j.aquaculture.2013.03.032.
[68]  Imsland, A.K.; Reynolds, P.; Eliassen, G.; Hangstad, T.A.; Foss, A.; Vikingstad, E.; Elvegård, T.A.; The use of lumpfish (Cyclopterus lumpus L.) to control sea lice (Lepeophtheirus salmonis Krøyer) infestations in intensively farmed Atlantic salmon (Salmo salar L.). Aquacul., 2014, 424–425:18–23. https://doi.org/10.1016/j.aquaculture.2013.12.033.