Infestation and effect of parasitic isopod Epipenaeon ingens ingens Nobili, 1906 on commercial shrimp species in the eastern Mediterranean: a case study of the population of brown shrimp Penaeus aztecus Ives, 1891

Abstract: Monthly samples of seven species of penaeid shrimps, namely, Penaeus aztecus (Ives, 1891), Penaus hathor (Burkenroad, 1959) Penaus japonicus (Spence Bate,1888), Penaus kerathurus (Forskȧl,1775), Penaus semisulcatus (De Haan,1844), Metapenaeus monoceros (Fabricus, 1798) and Metapenaeopsis aegyptia (Galil & Golani, 1990) were collected from Antalya Bay in the Eastern Mediterranean Sea from March, 2019 through March, 2020. Except for P. aztecus and P. semisulcatus, no other shrimp species were infected with the parasitic isopod Epipenaeon ingens ingens. Of the 3043 P. aztecus shrimp inspected, 541 individuals were infected (17.8%) with the bopyrid parasite E. ingens ingens. However, the annual infestation rate in recruiting year class (28 mm ˂ CL: 5.7%) was much less than in larger and sexually mature (CL ≥ 34 mm: 36.2%) individuals. Monthly infestation rates varied from 0.86 to 84.8%, and the size of infested shrimps ranged from 20 mm to 44 mm CL. The left branchial chamber was more likely infected (43.1%) than the right one (39.8%), and 17.1% appeared to be doubly infected. The percentage of the ovigerous female E. ingens ingens fluctuated between 31.7% (August) and 90.0% (February). We report for the first time the size at first accompaniment (FAS50%) and at first maturity (FMS50%) for the female parasite E. ingens ingens, 11.0 mm TL and 13.0 mm TL, respectively. The gonad weight (0.779 ± 0.73 g) and GSI (0.223 ± 0.333) value of uninfected female P. aztecus were about eight times greater than it was for infected shrimps (0.094 ± 0.18 g and 2.006 ± 1.669, respectively).Key words: Bopyrid isopod, Epipenaeon ingens, brown shrimp, Penaeus aztecus, Penaeus semisulcatus, parasite

PDF

___

An J, Boyko CB, Li X.-Z (2014). Review of the parasitic genus Epipenaeon Nobili, 1906 (Crustacea: Isopoda: Bopyridae), with new records and redescription of four species from China. Journal of Natural History 48: 2027-2048. doi:10.1080/002229 33.2014.897768
Anderson G (1975). Larval metabolism of the epicaridean isopod parasite Probopyrus pandalicola and metabolic effects of P. pandalicola on its copepod intermediate host Acartia tonsa. Comparative Biochemistry and Physiology Part A: Physiology 50A: 747-751. doi: 10.1016/0300-9629(75)90140-1
Anderson G (1990). Postinfection mortality of Palaemonetes spp. (Decapoda: Palaemonidae) following experimental exposure to the bopyrid isopod Probopyrus pandalicola (Packard) (Isopoda: Epicaridea). Journal of Crustacean Biology 10: 284- 292. doi:10.1163/193724090X00096
Ayub Z, Ahmed M (2004). Study on the host-parasite relationship of Parapenaeopsis stylifera (H. Milne Edwards) (Decapoda: Penaeidae) and Parapenaeon japonica (Thielemann); (Isopoda: Bopyridae). Hydrobiologia 523: 225-228. doi:10.1023/ B:HYDR. 0000033140. 45174.ce
Beck JT (1980). Life history relationships between the bopyrid isopod Probopyrus pandicola and one of its freshwater shrimp hosts Palaemonetes paludosus. The American Midland Naturalist 104 (1): 135-154. doi:10.2307/2424966
Bourdon R (1968). Les Bopyridae des Mers Européennes. Mem. Mus. Natl. Hist. Nat. Paris Nouvelle série Série A Zoologie L (2 et dernier) 50: 75-424.
Bursey CR (1978). Histopathology of the parasitization of Munida iris (Decapoda: Galatheidae) by Munidion irritans (Isopoda: Bopyridae). Bulletin of Marine Science 28: 566-570
Chu KH, Leong FLS (1996). Occurrence and influence of Orbione halipori Nierstrasz and Brendera Brandis (Isopoda: Bopyridae) on Metapenaeus joyneri (Miers) (Decapoda: Penaeidae) from the Zhujiang Estuary, China. Journal of Natural History 30: 835-839. doi:10.1080/00222939600770461
ConStat (1995). CC selectivity, Granspaettevej 10, DK-9800 Hjjlarring, Denmark
Courtney AJ (1991). Occurrence and Influence of Bopyrid Parasites on Female Penaeid Prawns from Coastal Waters of Central Queensland (Australia), Aust. Australian Journal of Marine and Freshwater Research 42: 15-23. doi:10.1071/MF9910615
Dale WE, Anderson, G (1982). Comparison of morphologies of Probopyrus bithynis, P. floridensis, and P. pandalicola larvae reared in culture (Isopoda, Epicaridea). Journal of Crustacean Biology 2: 392-409. doi:10.2307/1548055
Deval MC, Kaya Y, Güven O, Gökoğlu M, Froglia, C (2010). An unexpected find of the western Atlantic shrimp, Farfantepenaeus aztecus (Ives, 1891) (Decapoda, Penaeidae) in Antalya Bay, eastern Mediterranean Sea. Crustaceana 83 (12): 1531-1537.
Devi SL (1982). Bopyrid parasites of prawns at Kakinada. Journal of Marine Biological Association of India, 24 (1&2): 23-32.
Gopalakrishnan A, Rajkumar M, Ravichandran S, Trilles JP, Vasanthan TM (2009). Identification of Parapenaeopsis stylifera, a new host for Epipenaeon ingens. Journal of Environmental Biology 30 (6): 1063-1064.
Gopalakrishnan A, Kulanthaivel R, Trilles J, Mayalagu R, Rahman M et al. (2017). Bopyrid isopods parasitizing on the cultured fresh water prawn, Macrobrachium malcolmsonii in South India. Journal of Parasitic Diseases, 41 (1): 93-96. doi:10.1007/ s12639-016-0756-7
Gökoğlu M, Teker S, Karun J (2020). Infestation rate and impacts of Epipenaeon ingens on growth and reproduction of brown shrimp (Penaeus aztecus), Acta Aquatica: Aquatic Sciences Journal, 7:1, 50-53.
Gönülal O, Türetken PSÇ (2019). One of the most invasive alien species, Penaeus aztecus Ives, 1891 reached the Black Sea coasts. BioInvasions Records 8 (4): 871-875. doi: 10.3391/ bir.2019.8.4.15
Jay C (1989). Prevalence, size and fecundity of the parasitic isopod Argeia pugettensis on its host shrimp Crangon francisorum. The American Midland Naturalist, 121 (1): 68- 77. doi:10.2307/2425657.
Klompmaker AA, Robins CM, Portell RW, De Angeli A (2018). Crustaceans as hosts of parasites throughout the Phanerozoic. bioRxiv, 505495. doi:10.1101/505495
Korun J, Gökoğlu M, Balcı BA, Özvarol Y (2013). Infestation of brown shrimp, Farfantepenaeus aztecus, Ives (1891) (Penaeidae) by Epipenaeon ingens, Nobili (1906) (Isopoda, Bopyridae) from the Antalya Bay, Turkey. Revue de Médecine Vétérinaire 164: 559-563.
Larson SC, Van Den Avyle MJ, Bozeman EL (1989). Species profiles: life histories and environmental requirements of coastal fishes and in vertebrates (South Atlantic)--brown shrimp. U.S. Fish Wildl. Serv. Biol. Rep. 82(11.90). U.S. Army Corps of Engineers TR EL-82-4. 14 pp.
Nobili G (1906). Nuovi Bopiridi. Atti. R. Acad.Sci.Torino, 41: 1098
Nierstrasz HF, Brender GA, Brandis À (1931). Papers from Dr. Th. Mortensen’s Pacific Expedition 1914–16. LVII. Epicaridea II. Videnskabelige Meddedelser fra den Dansk Naturhistoriske Forening i København 91: 147-226.
O’Brien J, Van Wyk P (1985). Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. In: Wenner AM (editor). Crustacean Issues 3: Factors in Adult Growth. A. A. Balkema. 191-218.
Owens L (1983). Bopyrid parasite Epipenaeon ingens Nobili as a biological marker for the banana prawn, Penaeus merguiensis de Man. Australian Journal of Marine and Freshwater Research 34, 477-81. doi:10.1071/MF9830477
Owens L, Glazebrook JS (1985). The biology of bopyrid isopods parasitic on commercial penaeid prawns in northern Australia, p. 105-113. In: P. C. Rothlisberg, B. J. Hill and D. J. Staples (eds.). Second Australian National Prawn Seminar, Kooralbyn (Australia). 22 Oct. 1984.
Owens L, Rothlisberg PC (1995). Vertical migration and advection of bopyrid isopod cryptoniscid larvae in the Gulf of Carpentaria, Australia. Journal of Plankton Research, 13: 779-787. doi:10.1093/plankt/13.4.779
Overstreet RM (1987). Solving parasite-related problems in cultured crustacea. International Journal for Parasitology, 17 (2): 309- 318. doi:10.1016/0020-7519(87)90105-6
Özcan T, Ateş AS, Özcan G (2019). The distribution of the alien species Penaeus aztecus Ives, 1891 (Decapoda, Penaidae) in the Mediterranean Sea, Transylvanian Review of Systematical and Ecological Research, 21 (2): 41-48. doi:10.2478/trser-2019-0011
Palisoc FJr (1987). Observation on the host-parasite relationship of Epipenaeon ingens Nobili (Epicaridea: Bopyridae) and Penaeus semisulcatus De Haan. Philippine Journal of Science, 116 (3): 281-293.
Pazir MK, Jamshid KA, Akbarpour E, Zendehboudi AA (2016). Identification of Bopyridae, Isopoda in green tiger prawn (Penaeus semisulcatus) and Jinga shrimp (Metapenaes affinis) from coastal area of Buoshehr Persian Gulf. Journal of Marine Science and Technology, 15 (3): 21-34 (In Persian).
Ravichandran S, Soundarapandian P, Kannupandi T (2000). Infestation of isopod Epipenaeon ingens Nobili parasitized on Penaeus monodon from Parangipettai coastal environment. Advances in Biosciences, 19: 55-62.
Rajkumar M, Manokaran S, Jun S, Trilles JP (2011). A review of Epipenaeon ingens Nobili, 1906 (Isopoda: Bopyridae) host species and documentation of a new host, Metapenaeopsis stridulans (Alcock, 1905) (Decapoda: Penaeidae). Chinese Journal of Oceanology and Limnology 29 (1): 136-140. doi:10.1007/s00343-011-9923-y
Reinhard EG (1949). Experiments on the determination and differentiation of sex in the bopyrid Stegophryxus hyptius Thompson. The Biological Bullettin 96: 17-31.
Reverberi G (1947). Ulterior annotazione biolgiche sulla “Callianassa laticauda” parassitata della “Ione thoracica”. Atti della Accademia Nazionale dei Lincei, Rendiconti Classe di Scienze fisica mat. nat. (8) 2: 345-347.
Sivasubramanian K, Ravichandran S, Rameshkumar G, Veerappan N (2016). Occurrence, morphology and molecular characterisation of Bopyrid parasite Epipenaeon ingens Nobili, 1906 (Isopoda: Bopyridae). Journal of Parasitic Diseases 40 (4) : 1301-1306. doi:10.1007/s12639-015-0675-z
Smith AE, Chapman JW, Dumbauld BR (2008). Population structure and energetics of the bopyrid isopod parasite Orthione griffenis in mud shrimp Upogebia pugettensis. Journal of Crustacean Biology 28: 228-233. doi:10.1163/20021975-99990368
Somers IF, Kirkwood GP (1991). Population ecology of the grooved tiger prawn, Penaeus sernisulcatus in the north-western Gulf of Carpentaria: growth movement, age structure and infestation by the bopyrid parasite Epipenaeon ingens. Australian Journal of Marine and Freshwater Research 42: 349-367. doi:10.1071/ MF9910349
Teker S (2016). Determine some reproductive characterises of Brown shrimp Farfantepenaus aztecus Ives, 1891 which originated from Atlantic in the gulf of Antalya. Akdeniz University, Antalya, Turkey (in Turkish).
Thirumilu P (2011). Bopyrid parasite Epipenaeon ingens (Nobili, 1906) (Bopyridae, Isopoda) infestation in penaeid shrimps of Cuddalore coast, Tamil Nadu. Marine Fisheries Information Service TandE Series. 209: 11-12.
Thomas MM (1977). A new record of Epipenaeon ingens Nobili (Bopyridae, Isopoda) parasitic on Penaeus semisulcatus De Haan from Palk Bay and Gulf of Mannar. Indian Journal of Fisheries 24: 258-261.
Warren PJ (1974). Some observations on the relationship of the bopyrid parasite Hemiarthrus abdominalis (Krøyer) with Pandalus montagui Leach and Pandalus borealis Krøyer. Crustaceana 27:21-26. doi:10.1163/156854074X00181
Whitaker JD (1981). Description of the stock comprising the management unit. Pages 5-1 to 5-54 in M.D. McKenzie (ed.). Profile of the penaeid shrimp fishery in the South Atlantic. South Atlantic Fishery Management Council. Charleston, S.C.
Williams AB (1964). A postlarval shrimp survey in North Carolina. North Carolina Department of Conservation and Development, Division of Commercial and Sports Fisheries Special Scientific Report 3: 5 pp
Williams JD, Boyko CB (2012). The Global Diversity of Parasitic Isopods Associated with Crustacean Hosts (Isopoda: Bopyroidea and Cryptoniscoidea). PLoS ONE 7 (4): e35350. doi.org/10.1371/journal.pone.0035350