DISEASES OF AQUATIC ORGANISMS Vol. 19: 157-159.1994 Published July 28 Dis. aquat. Org. 1 -p-

NOTE

Hyperparasitism of Amyloodinium ocellatum (Dinoflagellida: Oodinidae) on melleni (: )

Angelo Colorni

Israel Oceanographic and Limnological Research, National Center for Mariculture. PO Box 1212. Eilat 88112, Israel

ABSTRACT: During a simultaneous infestation of the gilt- 900 g were found to be heavily infested with A. ocella- head sea bream Sparus aurata by Amyloodinium oceLlatum [a tum and lightly infested with N. melleni. Water tem- blastodiniid dinoflagellate parasite on gills and skin) and perature in the tank was 25 "C and salinity 40%0. Neobenedenia melleni (a capsalid monogenean parasite on fish skin), A. ocellatum was found to parasitize not only the Fresh mounts were examined and photographed fish but the rnonogenean parasites as well. This observation using regular light microscopy. Infested worms were indicates that A. ocellatum is able to obtain the necessary fixed in 10% neutral buffered formalin and embedded nutrients for its development from a non-piscine host. in methacrylate blocks according to standard proce- dures (Clark 1981). Sections (2 pm thick) were stained KEY WORDS: Hyperparasitism . Amyloodinium . Neobene- denia . Sparus aurata . Dinoflagellate . Capsalidae with methylene blue - basic fuchsin, periodic acid Schiff, hematoxylin-eosin and hematoxylin - Biebrich scarlet - fast green. The last stain is recommended for determining the effects of parasitic protozoans on tis- Infestations of the gilt-head sea bream Sparus aurata sues of invertebrates. L. by the gill/skin parasite Amyloodinium ocellatum Amyloodinium ocellatum trophonts were firmly Brown, 1931, a blastodiniid dinoflagellate, and Neo- anchored to the dorsal sides of the opisthaptor (Fig. 1) benedenia melleni (MacCallum, 1927) Yamaguti, and the body proper (Figs. 2 & 3) of the worm. Up to a 1963, a capsalid monogenean of the skin, are frequent dozen were found on each worm. The trophonts were occurrences in the facilities of the National Center for of various sizes (35 X 45 to 64 X 80 pm) which, had they Manculture (NCM) in Eilat, Red Sea, particularly dur- been growing on fish epithelia, would correspond to ing the summer. The 2 parasites have occasionally about 2 to 4 d of 'age' (i.e. post-attachment). been seen sharing the same host during simultaneous From the characteristic digestive vacuoles and the infestations (Ellis & Watanabe 1993, Colorni unpubl.). fine, PAS positive, polysaccharide granules present in A. ocellatum is virtually non-specific in its fish host the cytoplasm of Amyloodinium ocellatum trophonts selection (Lawler 1980, Lauckner 1984) and N. melleni (Fig. 4), it is evident that the dinoflagellates actively has been similarly reported to infest several of fed on the worms. The damage the trophonts caused to commercial fish cultured in tropical seas (Gallet de their unusual host was difficult to evaluate, but seemed Saint Aurin et al. 1990, Ellis & Watanabe 1993). Previ- minimal and in any case limited to a focal structural ously known as Epibdella melleni, N. melleni has been disruption. reported to infest many species of tropical fish held in Amyloodinium ocellatum is a highly adaptable, marine aquarium systems (Jahn & Kuhn 1932, Nigrelli cosmopolitan parasite (Nigrelli 1936, Lawler 1980, 1943). At NCM, N. mefleni infested, besides S. aurata, Paperna 1980, Barbaro & Francescon 1985). Its toler- the cichlid Oreochromis mossambicus, which was ance to varying osmotic conditions (Paperna 1984) and adapted to full strength seawater, and the dolphin fish lack of fastidiousness in its host range (Lawler 1980, Coryphaena hippurus. Lauckner 1984) have rendered the parasite amenable The present report describes Neobenedenia melleni to propagation on fish cell cultures (Noga 1987). hyperparasitized by Amyloodinium ocellatum. The Once detached from their fish host, whether sponta- case was observed in July 1993 in a 17 000 1 concrete neously or as a result of having been dislodged, the tank in which over 100 adult Sparus aurata of about trophonts sink to the bottom and transform into divid-

O Inter-Research 1994 u~d02 = leq aless urels msoa-ur[Axoleuraq 'uo!pas ~eurpn~r6uo~ueaua6 -ouour aql jo eurhqsuaied 6mKliapun aql pue (a~oqe)slaKel leluaurn6al uaamlaq laploq aql yleur sal6ueu~alrqM 'luaurm jo airs :* :ruay[aur 'N 6urzr1rsexd (salnuel6 ap~~~ssesrilod.sMorle 'salonse~pool nj 'snapnu U) luoydo~lurnje[[aJo v p .61d urri08 = sleq apss ,pau!elsun 'lunour law luaurqselle jo al!s .~011v ruallaur 'N 10 aprs ~eslopaql oi payselle sluoydo.~lurn1 -e[[aso v .cp .s6!.~ .urd 002 = leq aless paurelsun 'lunour laM (pa~olie)saqs lualajjrp jo s~uoqdoqurnlefla2o v jo laqurnu e qlr~palsajur (aprs lesiop) ~oldeqlsrdonrallaw N ruanaur eruapauaqoaN 6urlsajur uIn)ellaJo wnrurpoolAury p 01 1 s6rd Colorni: Hyperparasitism of Amyloodinium ocellatum 159

ing tomonts (Paperna 1984). There is no evidence that Ellis, E. P., Watanabe, W. 0. (1993). The effects of hypo- an established trophont can detach from its original salinity on eggs, juveniles and adults of the marine attachment site and re-attach to a different site. Evi- monogenean, Neobenedenia melleni. Treatment of ecto- parasitosis in seawater-cultured tilapia. Aquaculture 117. dently, Amyloodinium ocellatum attached to the mono- 15-27 genean at the stage of dinospore. Although the break- Gallet de Saint Aurin, D., Raymond, J. C., Vianas, V. (1990). ing down of A. ocellatum specificity for fish was Marine finfish pathology: specific problems and research probably determined by the unnatural conditions of in the French West Indies. In: Barret, J., Calvas. J., Cuzon, G., Fuchs, J., Weppe, M. (ed.) Advances in tropical aqua- intensive mariculture, it is nevertheless remarkable culture, Tahiti. French Polynesia, Feb. 20 - March 4. 1989. that A. ocellatum was able to obtain the necessary AQUACOP, Institut Franqais de Recherche pour nutrients for its growth and development from a non- 1'Exploitation de la Mer (IFREMER), Actes de Colloque piscine substrate. No. 9. IFREMER, Plouzane, p. 143-160 The versatility and resilience of Amyloodinium ocel- Jahn, T L., Kuhn, L. R. (1932). The life history of Epibdella melleni Maccallurn, 1927, a monogenetic trematode para- latum should be taken into account in the logistics for sitic on marine . Biol. Bull. 62: 89-111 the control of this parasite, as attempts to eradicate it, Lauckner, G. (1984). Diseases caused by protophytans for example by means of temporary fish exclusion (algae). In: Kinne, 0. (ed.) Diseases of marine , (Bower 1987), may be frustrated by this organism's Vol. IV, Part 1, Pisces. Biologische Anstalt Helgoland, Hamburg, p 169-179 ability to exploit alternative host phyla. Lawler, A. R. (1980). Studies on Amyloodinium ocellatum (Dinoflagellata) in Mississippi sound: natural and experi- Acknowledgements. I am indebted to Prof. I. Paperna of the mental hosts. Gulf Res. Rep. 6(4): 403-413 Dept of Sciences, Faculty of Agriculture, Hebrew Nigrelli, R. F. (1936). The morphology, cytology and life University of Jerusalem, Rehovot, for positive identification of history of Oodinium ocellatum Brown, a dinoflagellate Neobenedenia melleni and critical review of the manuscript. parasite on marine fishes. Zoologica, N.Y. 21: 129-164 The techical assistance of E. Berger and H. Kruglish is grate- Nigrelli, R. F. (1943). Causes of diseases and death of fishes in fully acknowledged. captivity. Zoologica, N.Y. 28: 203-216 Noga, E. J. (1987). Propagation in cell culture of the dinofla- LITERATURE CITED gellate Amyloodinium, an ectoparasite of marine fishes. Science 236: 1302-1304 Barbaro, A., Francescon, A. (1985). Parassitosi da Amylo- Paperna, I. (1980). Amyloodinium ocellatu~n(Brown, 1931) odinium oceuatum (Dinophyceae) su larve di Sparus [Dinoflasellidal infestations in cultured marine fish at aurata allevate in un impianto di nproduzione artificiale. ~ilat,~ei Sea: kpizootiology and pathology. J. Fish Dls 3: CEbalia XI-2: 745-752 363-372 Bower, C. E. (1987).Update on Amyloodinlum ocellatum. Sea Paperna, 1. (1984). Reproduction cycle and tolerance to tem- Scope, Aquarium Systems, Inc., Mentor, OH perature and salinity of Amyloodinium ocellatum (Brown, Clark, G. (1981).Staining procedures. Wdliams and Wilkins, 1931) (Dinoflagelhda). Annls Parasit. hum. comp. 59(1): Baltimore 7-30

Responsible Subject Editor: A. K. Sparks, Seattle, Washington, Manuscript first received: November 30, 1993 USA Revised version accepted: March 18, 1994