Kudoa Sp. (Myxozoa) Causing a Post-Mortem Myoliquefaction of North-Pacific Giant Octopus Paroctopus Dofleini (Cephalopoda: Octopodidae)
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Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 266 Kudoa sp. (Myxozoa) causing a post-mortem myoliquefaction of North-Pacific giant octopus Paroctopus dofleini (Cephalopoda: Octopodidae) H. Yokoyama1 and K. Masuda2 1Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo, Tokyo 113-8657, Japan, 2Hyogo Prefectural Tajima Fisheries Research Institute, Kasumi 1852-1, Kinosaki, Hyogo 669-6541, Japan. Abstract A myxosporean belonging to the genus Kudoa was found from a North-Pacific giant octopus Paroctopus dofleini (Cephalopoda) exhibiting the muscle degeneration, often referred to as “a post-mortem myoliquefaction”, in the arm. The spores were 6-8 µm in diameter and possessed 4 pyriform polar capsules. This is the first report of a myxosporean infection in octopus. The octopus fishery is economically impor- gladius), K. cruciformum in Japanese seaperch tant in Japan. One commercially valuable spe- (Lateolabrax japonicus), K. funduli in cies, the North-Pacific giant octopus, mummichog (Fundulus heteroclitus), K. Paroctopus dofleini, is relatively large, reach- histolytica in Atlantic mackerel (Scomber ing several meters. Recently, an unusual para- scombrus), K. paniformis in Pacific hake site that is suspected to be a Kudoa sp. (Merluccius productus), K. peruvianus in Chil- (Myxozoa), was identified in a boiled North- ean hake (Merluccius gayi) and K. rosenbuschi Pacific giant octopus exhibiting a post- in Argentine hake (Merluccius hubbsi). This mortem myoliquefaction in one arm. muscle degeneration is probably the results of proteolytic enzymes released by the para- The genus Kudoa is comprised of more than site, and it has been believed that the enzymes 40 identified species (Moran et al., 1999; are used by the parasite to breakdown host Sweare & Robertson, 1999), which manifest tissues for its growth and development as 2 types of clinical disease (Yokoyama et al., (Moran et al., 1999). To date, however, there is 2000): one type results in macroscopic no information on a myoliquefaction of shell- pseudocysts and the other is associated with fishes. post-mortem myoliquefaction, often refered to ‘soft flesh’, ‘milky condition’ or ‘jelly meat’. In May 1997, North-Pacific giant octopus Among the latter, the following species have Paroctopus dofleini were caught by a fishing been reported from feral and farmed fishes; trawl net on the coast of Japan Sea, Kasumi- K. thyrsites in farmed Atlantic salmon (Salmo cho, Hyogo Prefecture, Japan (35º 40´ N, 134º salar) and other marine fishes, K. 40´ E), and transported to an octopus-process- musculoliquefaciens in swordfish (Xiphias ing company. During the boiling of octopus, Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 267 merous refractile granules were also found in the muscle lesion (Fig. 3). This is the first record of a myxosporean in- fection in octopus. The phylum Myxozoa Grasse, 1970 is comprised of more than 1200 species, reported mainly from teleost fishes, and rarely from amphibian, crustacea and mammmals (Friedrich et al., 2000). To date, there have been no reports of myxozoan from shellfishes. Recently, a new genus Tetracapsula possessing 4 polar capsules was established in bryozoan hosts (Canning et al., 1996), and T. bryosalmonae was subsequently identified as the PKX organism, a parasite of salmonid fish (Canning et al., 1999). However, Tetracapsula is coelozoic and develops in a sac- like compartment. The histozoic character in Figure 1. Slices of arm of North-Pacific giant the musculature and the morphology of po- octopus Paroctopus dofleini. Right: healthy arm. Left: Affected arm. Note a large hole caused by the lar capsules of the parasite observed here vali- muscle breakdown in the central region. Figure 2. date the assignment of the current A fresh spore (arrow) of Kudoa sp. from the octopus. Figure 3. Putative presporogonic plasmodium myxosporean to the genus Kudoa. A distinct (arrow) of Kudoa sp. in the muscle lesion. Scale bars host difference suggests that the octopus are 10 µm. myxosporean is a new species of Kudoa, but one of them showed an abnormal texture in further morphological characterization is re- the basal arm. The octopus was brought to quired to identify this parasite at the species Hyogo Prefectural Tajima Fisheries Office for level. parasitological examinations. Recent findings on the life-cycle of myxozoan The muscle tissue in the central region of the have revealed the alternation of myxosporean affected octopus arm was pale and liquefied stage in the vertebrate host and actinosporean (Fig. 1). Microscopic observation of wet mount stage in the invertebrate (mainly oligochaete) preparations revealed the presence of Kudoa host (Yokoyama, 1997). The possibility of ac- spores characterized by 4 polar capsules ar- cidental infection of an originally fish-para- ranged tetrahedrally with their anterior ends sitic Kudoa cannot be excluded, but the find- close together (Fig. 2). Spores were 6-8 µm in ings of myoliquefaction and developmental diameter, but the morphology of spore valves stages indicate that the parasite established (stellate or quadrate) could not be discerned. the infection and developed in the octopus Four polar capsules were pyriform in shape tissue. If octopus is a natural host for this para- and almost equal in size (2.5 x 1.5 µm). Puta- site, it is of great interest to see whether the tive presporogonic plasmodia containing nu- octopus myxosporean has an alternate (fish Bull. Eur. Ass. Fish Pathol., 21(6) 2001, 268 or other invertebrate) host in the life cycle. It Friedrich, C., Ingolic, E., Freitag, B., Kastberger, G., Hohmann, V., Skofitsch, G., is presumed that transmission of this Kudoa Neumeister, U. and Kepka, O. (2000) A may occur without a fish host. myxozoan-like parasite causing xenomas in the brain of the mole, Talpa europaea L., 1758 The octopus fisheries industry is growing (Vertebrata, Mammalia). Parasitology, 121: worldwide, and large numbers of octopus 483-492. have been imported into Japan from all over Moran, J.D.W., Whitaker, D.J. and Kent, M.L. the world. Although the prevalence of (1999) A review of the myxosporean genus myoliquefaction in the octopus catch is un- Kudoa Meglitsch, 1947, and its impact on the known, the Kudoa infection first discovered international aquaculture industry and com- in this study is a potential threat to the octo- mercial fisheries. Aquaculture 172: 163-193. pus fisheries and should be recognised as an Swearer, S.E. and Robertson, D.R. (1999) Life important emerging diseases of octopus. history, pathology, and description of Kudoa ovivora n. sp. (Myxozoa, Myxosporea): an We thank Dr. Jerri Bartholomew, Oregon State ovarian parasite of Caribbean labroid fishes. University, for reviewing this manuscript. J. Parasitol. 85: 337-353. Yokoyama, H. (1997) Transmission of References Thelohanellus hovorkai Achmerov, 1960 (Myxosporea: Myxozoa) to common carp Canning, E.U., Curry, A., Feist, S.W., Cyprinus carpio through the alternate Longshaw, M. and Okamura, B. (1999) oligochaete host. Syst. Parasitol., 36: 79-84. Tetracapsula bryosalmonae n. sp. for PKX organ- ism, the cause of PKD in salmonid fish. Bull. Yokoyama, H., Inoue, D., Sugiyama, A. and Eur. Ass. Fish Pathol., 19: 203-206. Wakabayashi, H. (2000) Polymerase chain re- action and indirect fluorescent antibody tech- Canning, E.U., Okamura, B. and Curry, A. nique for the detection of Kudoa amamiensis (1996) Development of a myxozoan parasite (Multivalvulida: Myxozoa) in yellowtail Tetracapsula bryozoides gen. n. et sp. n. in Seriola quinqueradiata. Fish Pathol. 35: 157-162. Cristatella mucedo (Bryozoa: Phylactolaemata). Folia Parasitol. 43: 249-261..