DISEASES OF AQUATIC ORGANISMS Published December 16 Dis. aquat. Org.

REVIEW

Pathology of in marine

Pilar Alvarez-Pellitero, Ariadna Sitja-Bobadilla

Institute de Acuicultura Torre de la Sal (C.S.I.C.), E-12595 Ribera de Cabanes, Castellon, Spain

ABSTRACT A revlew of the pathogenic impact of Myxosporea in marine fish culture is presented. At least 11 species of and 7 species of Multi\~alvulidahave been described in marine or brack- ish fish kept in different culture systems. The pathological importance of these myxosporoses is dis- cussed, and their potential importance with the growth of culture facilities is stressed.

KEYWORDS: Aquaculture - Myxosporea . Pathology

INTRODUCTION different culture systems, including ponds, intensive and semi-intensive fdrms, and cages in the sea Myxosporea is a controversial group of parasites af- fecting mainly fish. Its taxonomical status is still to be revised in view of recent findings on myxosporean life spp. cycles (Wolf & Markiw 1984, El-Matbouli & Hoffmann 1989). The most recent knowledge of Myxosporea Ceratomj/xa spp. have been reported from different important for freshwater fish was reviewed by El- cultivable fish of the families Serranidae, Sparidae, Matbouli et al. (1992). These authors pointed out the Mugilidae, etc. (Lubat et al. 1989, Paperna 1991, difficulty in assessing the pathogenicity of Myxosporea Alvarez-Pellitero & Sitja-Bobadilla 1993, Sitja- and the economic losses they incur This is particularly Bobadilla & Alvarez-Pellitero 1993a). Two of them, true in mariculture, partly due to the scarcity of para- C:'cratomjxa labracis and C. diplodae, parasitize sitological studies on cultured marine fish. Some infor- blediterranean sea bass Dicentrarchus labrax in wild mation can be found in the reviews of Lom (1984) and and culture conditions (Sitja-Bobadilla & Alvarez- Paperna (1991). Nevertheless, with the development of Pellitero 1993a). No external cl.inica1 signs were usu- marine aquaculture, outbreaks of diseases due to ally found, but histopathological damage was detected Myxosporea are reported frequently, and some species in the gall bladder by light and electron m.icroscopy, inay become a serious constraint for maricult.ure. mainly consisting of vacuolation, deformation or even In this review, we present much of what is known of necrosis of epithelia1 cells (Figs. 1 & 2). Thickening and Myxosporea actually or potentially harmful for marine inflammation of the subepithelial connective tissue fish under culture conditions. We compile our own (Fig. 3) and damage to the neighbouring pancreatic findings from a long-term parasitologlcal survey of ma- tissue (Fig. 4) were also observed. Trophozoites ap- rine fish in different culture systems, as well as other peared frequently lining the epithelium, closely at- reports from the . tached to the cell surface or even forming invagina- tions in it. As in other ceratomyxoses, spread of the parasite to MYXOSPOROSES CAUSED BY BIVALVULIDA other organs was observed in very intense infections. Prevalence of Ceratomyxa labracis reached 421; in Cases of Bivalvulida in cultured marine or brackish cultured fish and intensities were very high In some in- fish are listed in Table 1. They have been reported in dividuals. Stress situations, such as starvation, seem to

O Inter-Research 3.993 Dis. aquat. Org. 17: 229-238, 1993

Table l B~valvulidaparasites of cultured marine fish

Species Culture system Source

Ceratomyxa labracis Dicentrarchus la brax Open systems, farms & Alvarez-Pellltero & C. diplodae research facilities on the Sitja-Bobadilla (1993); Mediterranean coast of Spain Sitja-Bobadilla & Alvarez-Pellitero (1993a) Sphaerospora Dicentrarchus la brax Research facilities on the Sitja-Bobadilla & testrcularis Mediterranean coast of Spain Alvarez-Pellitero (1990, 199313, c) S. dicentrarchi Dicentrarchus la brax Open systems, farms & Sitja-Bobadilla & research facilities on the Alvarez-Pellitero (1992, 1993b, c) Mediterranean coast of Spain S. epinepheli Epinephelus Cages in estuarine waters Supamattaya et al. (1990, 1991) mala baricus of South Thdiland S. irl-egulalis Pleuronectes platessa Scottlsh waters Mackenzie et al. (19761 Sphaerosporidae Sparus aura ta Open semi-intensive systems Sltla-tlobadilla et ai. (19921 Mugilidae on South Atlantic coast & Ebro River delta in Mediterranean waters, Spain Zschokkella m ugilis Mugilidae Open semi intensive system Sitja-Bobadilla & in River Ebro delta, Spain Alvarez-Pellitero (1993d) sp. Sparus a urata Open farms in Southern Cyprus Diamant (1992) spp. Mugilidae Ponds in Israel Paperna (1991) Myxobolus buri Seriola quinqueradiata Japanese farms Egusa (1985)

favour the appearance of ceratomyxosis (Alvarez- site in the seminiferous tubules, and does not provoke Pellitero & Sitja-Bobadilla 1993). any cellular host reaction or any apparent harm in slight infections (Fig 9). In massive infections, the par- asite can invade neighboring testicular tissues, pro- Sphaerospora spp voking the destruction of testicular areas (Fig. 10). TEM observations (Fig. 13 ) showed myxosporean Different Sphaerospora spp. have been recently stages in the lumen of affected tubules, whereas sper- found in cultured marine fish, mainly in Mediterra- matogonia and Sertoli cells adjacent to destroyed nean waters. areas appeared vacuolated, with disorganized orga- Dicentrarchus labrax harbours 2 species, each of nelles and hypertrophic nuclei. Interstitial tissue was them giving an example of a different type of infec- enlarged due to the abundance of myoid ceUs. tion (Sitja-Bobadilla & Alvarez-Pellitero 1990, 1992, Moreover, in massive infections the parasite spreads 199313, c). beyond the lumen, towards neighbouring testicular tis- Sphaerospora dicentrarchi is a histozoic systemic sue and the serosa of adjacent organs, generating an parasite in almost every organ of the host, though its important cellular host reaction. The affected serosa preferred locations are the connective and muscular was hypertrophied (Fig. 12) and leucocytic infiltration, ti.ssues of the gall bladder (Fig. 5) and intestine. mainly consisting of granulocytes, was observed. In Prevalences reach 100 %in wild fish and 70.5 %in cul- these cases of massive infections, gross signs of disease tured fish (Sitja-Bobadilla & Alvarez-Pellitero 1993~). may be observed, consisting of abdominal swelling This Myxosporea seems to be harmless, except in mas- due to the accumulation of ascites and hypertrophy sive infections, in which extensive areas of the organs and hyalinization of testes, with subsequent rise of the appear invaded with th.e subsequent destruction of gonadosornatic index. At the end of the spawning sea- tissues, especially in kidney, pancreas (F~gs.6 to 8) son, the massively infected testes exhibited most of the and testes. Nevertheless, no serious cellular reaction tubular lumen being occluded by encapsulated para- was detected by light microscopy, apart from some sites, with a fibrotic host reaction (fibroblast-like cells, leucocytic proliferation or macrophages engulfing desmosomes, fibrocytes and colldgen fibers). Degene- spores. rated spores and vacuolated or necrotic deposits were Sphaerospora testicularis 1s usually a coel.ozoic para- observed (Figs. 13 & 14). Therefore, the infection Alvarez-Pellitero & Sitja-Bobadilla: Myxosporea in fish culture 23 1

Figs. l to 4. Sections of Dicentrarchus labrax tissues infected by Ceratornyxa spp. Figs. 1 to 3. Parasitized gall bladders, showing vacuolation (Fig. 1) necrosis, sloughing of epithelia] cells together with trophozoites of the myxosporean (Fig. 2),and thickening of the subepithelial connective tissue (Fig. 3).Fig.. Pancreatic tissue neighbouring gall bladder, showing cellular vacuolation and destruction; t: trophozoite. Staining: toluidine blue caused by S. testicularis is considered to represent par- from estuarine areas of Southern Thailand. Necrosis of asitic castration. renal tubular epithelium and peritubular fibrosis were During the spawning period, parasitic stages are re- observed in many tubules filled with masses of spores leased with the sperm. Intensity was usually low at the and developing stages of the parasite. Renal corpus- beginning of spermiation period, when early tropho- cles were also affected, and some of them were ne- zoites were the main stage observed, and increased crotic and shrunken (Supamattaya et al. 1990, 1991). progressively while the parasite gradually developed. Spaherospora irregularis (syn. of Ortholinea irregu- Infection prevalence also showed a progressive in- laris according to Arthur & Lom 1985) was reported in crease throughout the spawning period (Sitja- plaice Pleuronectes platessa from Scottlsh waters with Bobadilla & Alvarez-Pellitero 1993~). high infection rates (up to 70 %) (Mackenzie et al. The other Sphaerosporidae from marine or estuarine 1976). cultured fish are kidney parasites. Another renal member of the Sphaerosporidae, pre- Sphaerospora epinepheli produced heavy infections viously reported as Sphaer-ospora sp. (Sitja-Bobadilla in cage-cultured grouper Epinephelus malabaricus et al. 1992),1s now considered a probable new Dls aquat. Org 17 229-238. 1993

'I.A!

Figs. 5 to 8. Sections of Dicentrarchus~ir~raxtissuesinfected by Sphaerospura dicentrarchi. Fig. EMdetail d a bag-like group of spmes in the intestinal wall, with light host reaction. Figs.6 to 8. LM (Rg.6) andTEM (Figs.7 & 8) images of infected pancreas Note degenerarian and destruction of areasinvaded by the myxosporean. LM stairung: toluidlne blue

7 Figs.9 to 14. Sections of Dicentrarchus Iabrdx testes infected by Sphaerospura tesiicufans. Rg, 9. view of a Iighl InfecUon Note the presence of lrophomites (t) in the tubule lumen without apparent host reaction. Fiqs. 10 & 11. LM [Fig. 10) and TM (Fig l l)images of heavily infected testes. Note destruction of germinal tbsue and enlargement of interstitial tissue. sg: residual sper- motogonia: sp: spore of the myxosporean.Fig. 12. LM image of a massively infected testis with invasion of serosa, appearing hypertrophied, with an inflammatory reaction. Figs. 13 & 14. Host reaction against the myxosporean at the end of the spawnihg season, showing residual spores inside a fibrotic capsule under TEM [Fig. 13) and LM (Flg 14) LM stalnlng toluid~neblue

Dis. aquat. Org. 17: 229-238, 1993

Table 2. parasites of cultured marine fish

Species Host Culture system Source

Kudoa thyrsites Coryphaena hyppurus Sea cages in Albany, Western Australia Langdon (1991) Oncorhynchus spp. Hatcheries & farms in British Columbia, Kabata & Whitaker (1989) Canada Salmo salar Srnolts transferred to sea water in Harrell & Scott (1985) Washington, USA K, arnarniensis Seriola quinqueradiata Sea cages in Japan Egusa & Nakajirna (1978, 1980) K pericardialis Seriola quinqueradiata Sea cages in Japan Nakajima & Egusa (1978) K. iwatai Pagrus major Sea cages in Japan Egusa & Shiom~tsu(1983) Oplegnathus punctatus K shiomitsui Takifugu rubripes Sea cages in Japan Egusa & Shiomitsu (1983) sp Sparus aurata Mediterranean waters in Israel Paperna (1982) fil2~d~dl~~~idLdieoiaurdx jdponicus Fish iarm in japan Yasunaga et al. (1981) neothunni (?) Oplegnathus fascia tus Seriola quinqueradiata following TEM studies demonstrating the presence of serious damage to the kidney. Glomerular destruction, several sporoplasmic cells (unpubl. data). It parasitizes haemorrhagia and leucocytic infiltration were the gilthead sea bream Sparus aurata and mugilids cul- main histopathological effects (Figs. 15 & 16). An tured in semi-extensive conditions. Prevalence may outbreak was observed in gilthead sea bream, in reach 80 % and intensities were high enough to cause which dermal ulcers were seen i.n 20 % of 18 mo old

Figs. 15 & 16. Sections of Liza aurata kidney infected by a sphaerosporid. Fig. 15. Detail of a glomeruli harboring disporobldsts, surrounded by a thin capsule and a sl~ghtleucocytic infiltration. Tubul~also appear damaged. Fig. 16. Parasitic stages inside a granuloma. Staining: toluidine blue Alvarez-Pell~tero& Sit]&-BobadillaMyxosporea In f~shculture

Figs. 17 & 18 Sections of Llza saliens gall bladders Infected by Zschokella mugills Fig 17 Gall bladder epithelium llned with parasitic stages. Fig. 18. Very affected epithelium shovvlng cellular vilcuolat~on,sloughing and destruction, together w~thpara- sit~cstdges (arrows).Stalnlng toluidine blue fish. All ulcerated fish necropsied harboured this ently healthy mullets (Paperna 1991) and Myxobolus Sphaerosporidae in the kidney and dermal ulcers Ouriin the brain of farmed Japanese yellowtails Seriola (Sitja-Bobadilla et al. 1992). quinqueradiata (Egus 19851.

Zschokkella sp. MYXOSPOROSES DUE TO MULTIVALVULIDA

Zschokkella mugilis was found in the gall bladder of Reported cases of Multivalvulida in cultured marine mugilids captured in the wild (River Ebro delta, Spain) f~share mainly from sea cage and are listed in and maintained in a semi-intensive open system. Table 2. Histopathological damage consisted of vacuolation, deformation, or even necrosis of epithelia1 cells. Trophozoites and sporoblasts appeared frequently lin- Kudoa spp. ing the epithelium, usually forming invaginations in it (Figs. 17 & 18). Prevalence was about 70 % and inten- Several members of Kudoa have been reported sity was very high in some fish, so the infection prob- amongst the main pathogens of ddferent cultured ma- ably contributed to the mortalities observed in some rine fish, particularly in cage cultures. They produce fish groups (Sitja-Bobadilla & Alvarez-Pellitero 1993dl. typical focal lesions (Fig. 191, which are often the cause of the myoliquefactive postmortem condition known as 'milky flesh'. , one of the species para- Other Bivalvulida sitizing Pacific hake Merluccius productus in the wild (Kabata & Whitaker 19861, has also been reported in Other occasional findings of myxosporeans in cul- different fish in culture conditions, such as mahi mahi tured marine fish are those of Myxidium sp. in the in- Coryphaena hippurus in sea cages at Albany, western testinal mucosa of Sparus aurata suffering moderate Australia (Langdon 19911, Pacific Oncorhyn- mortalities (Diamant 19921, Myxobolus sp. in appar- chus spp. in different hatcheries and farms of British Dis. aquat. Org. 17: 229-238, 1993

Fig 19. Section of muscle of hake h/lerluccius mer- luccius infected by Kudoa sp. Staining: H&E

Columbia, Canada (Kabata & Whitaker 1989), and several clupeoid fish from Australian waters could be Atlantic salmon Salmo salar after transferring to sea the source of K. thyrsites for cultured Coryphaena hy- water in Washington, USA (Harrell & Scott 1985). purus (Langdon et al. 1992), and the usual hosts of Apart from dorsal musculature lesions, consisting of a Kudoa spp. could transmit the parasite to certain sal- characteristic multifocal intracellular infection with monids, with subsequent implica.tions for salmon associated inflammatory reaction, inflammatory foci stocks. were observed in pericardium and myocardium and foci of coagulative hepatocellular necrosis in the liver and renal intertubular tissue of C. hippurus. Some sal- Hexacapsula sp. monids also showed infection of cardiac muscle. Occasional infections by Kudoa sp. have also been A myxosporean reminiscent of Hexacapsula neo- recorded in cultured Sparus aurata from the thunni was reported by Yasunaga et al. (1981) as a Med~terranean Sea in France and Israel. The myxo- cause of rnortalities of cultured sea bass Lateolabrax sporean was located in glomeruli and mesentery or japonicus, and was also present in cultured knifejaw serosa, though damage was only evident in the former, Oplegnathus fasciatus and yellowtail Seriola quinque- whose capillaries could become obstructed or com- radia ta. pletely obliterated (Paperna 1982) Kudoases have also been reported from different fish cultured in sea cages on Japanese coasts. Kudoa arna- CONCLUSION miensis parasitizes of yellowtail Sedola quinqueradiata (Egusa & Nakajima 1978, The data summarized above on Myxosporea of cul- 1980). Kudoa pericardialis was found in the pericardial tured marine fish reveal the actual and potential threat cavity of the same host (Nakajima & Egusa 1978). Sea of these infections in aquaculture. Some species are a bream Pagrus major and Oplegnatus punctatus were real danger to cultured stocks, e.g. Sphaerospora testi- parasitized by Kudoa iwatai in the lateral musculature, cularis decreases the reproduction rate of sea bass whereas Kudoa shiornitsui parasitizes the pericardial either by destroying the germinative tissue (Sitja- cavity and ventricle of Takdugu rubripes (Egusa & Bobadilla & Alvarez-Pelli.tero 3.993b) or by feedin.g Shiomitsu 1983). on spermatozoa (Sitja-Bobadilla & Alvarez-Pellitero Infected wild fish from neighboring waters may act 1993e); some Kudoa infections can detract from the as reservoir hosts for cage-cultured fish. This has been marketability of fish products, altho.ugh there is n.o suggested for yellowtail infected with Kudoa ama- health risk (see Langdon et al. 1992); this could miensis, since coral fish from the same area were also also be the case for the Sphaerospora-like infection in found parasitized by trophozoltes of the parasite. Also sea bream. Other Myxosporea infections, with no clin- Al\iarez-Pellltero & Sitja-Bobs~dilla. h4yxosporea ~n flsh culture 237

ical signs or serious mortalities, but clear h~stopatho- Harrell, L W, Scott, T h4 (1985) Kudoa thyrsites (Gilchr~st) logical damage, can become a potential threat under (Myxosporea: Mult~valvulida)In Atlantic salmon (Salmo stress conditions or may immunodepress the host, salal- L.) J F~shDis 8. 329-332 Kabata, Z., Wh~taker,D J. (1986) Distr~but~onof two species hence favouring the entrance and establishment of of Kudoa ( h4ult1val\~ul1da)In offshore popula- other pathogens. t~onof the Pacific hake, A4eri~1cc1~1sprod~ict~js (Ayl-es, In addition, other Myxosporea hitherto found in dif- 1855).Cdn. J. Zool 64. 2103-2110 ferent wild fish may become of concern with the Kabatil, Z.,Whitdker, D. J (1989) Kudod thyrsites (Gilchr~st, 1924) (hlyxozoa) in the cardiac muscle of Pacific salmon growth in culture facilities. In sea cages, where the (Oncorhynchus spp ) and steelhead trout (Salmo gall-d- transmission of Myxosporea from the same or other neri). Can. J Zool 67: 341-342 host fish species cannot be ignored, wild fish may be a Langdou, J S. (1991). h4yoliquefaction post-mortem ('milky direct source 01- alternate reservoir host of infections. flesh') due to Kudoa thyrsltes (Gllchr~st)(h,lyxosporea. Although the pathogenic effects of some myxospor- Multivalvul~da)In mahi rnah~,Coryphaena hippur-us L. J. Fish Dls. 14. 45-54 ean species have been extensively described, little is Langdon, J. S., Thorne, T., Fletcher, W. J. (1992). Reservoir known about the transmission and pathogenic mecha- hosts and new clupeoid host records for the myol~quefac- nlslns of these organisms, or how they challenge the tive myxosporean parasite Kudoa thyrsltes (Gllchrlst). J. fish immune system. Such knowledge might help in Flsh. DIS 15: 459-471 Lom, J. (1984). Diseases caused by Protistans. In. Kinne, determining more rational and effective prophylactic 0. (ed) Dlseases of marine , Vol. IV, Part I. measures, which the current fish culture industry is so Biologische Anstalt Helgoland, Hamburg, p. 114-168 devoid of. Lubat, J., Radujkovic, B., Marques, A., Bonix, G. (1989) Prasltes des poissons marins du Montenegro Myxosporidies Acta Adnat~ca30. 31-50 Acknowledgements Th~swork was suppoited in part by a MacKenzie, K.,McVicar, A. H , Waddell, I. F (1976). Some grant (FPI) from the M~n~stenode Educaclon Clencia of parasites of plaice, Pleuronectesplatessa L in three differ- Spain to A Sitja-Bobadilld and the project MAR/89/0557 from ent farm environments Scott Fish Res Rep. 4: 1-14 the Comislon lntermln~sterial de Cienc~a y Tecnologia Nakajlma, K, Egusa, S. (1978) Kudoa perlcardialis n. sp (CICYT) ot Spaln (Myxosporidea: Chloromyxidae) from cultured yellowtail, Senola quinqueradiata Temminck et Schlegel. Bull. Jap Soc scient Fish. 44: 117-120 Paperna, I. (1982) Kudoa infection in the glomeruli, mesent- LITER.\TURE CITED ery and peritoneum of cultured Sparus aurata L. J F~sh DIS 5 539-543 Alvarez-Pellitei-o, P., Sitjd-Bobadilla, A. (1993) Population dy- Paperna, 1. (1991). Dlseases caused by parasites in the aqua- namlcs of Ceratomyxa spp ( %lysosporea) ~nfec- culture of warn1 water fish. Ann. Rev. Fish Dis. 1: 155-194 tlon In wild and cultured sea bass, Dlcentl-archus labrax Sitja-Bobadilla, A , Alvarez-Pellitero, P. (1990).Sphaerospora (L.)from the Spanish h,Icd~teri-aneanarea J Fish Biol. 42: testiculans sp. nov. (Myxosporea. Sphaerosporidae) In 889-901 w~ldand cultured sea bass, Dicentrarchus labrax (L ), from Arthur, J. R., Lom. J (1985) Sphaerospora araii n sp. (hdyxo- the Spanish Mediterranean area. J. F~shDis. 13. 193-203 spored. Sphaerospor~dae)from the kidney of a longnose Sitja-Bobadilla, A., Alvarez-Pellitero, P. (1992). Light and skate (Rala rhlna Jordan and Gilbert) from the Pacif~c electron microscopic description of Sphaerospora dlcen- Ocean off Canada. Can J. Zool.63: 2902-2906 trarchi n. sp. (Myxosporea: Sphaerosporidae) from wild Dldmant, A. (1992) A new pathogenic h~stozoicMyxidlum and cultured sea bass (Dlcentrarchus labrax L.). J. (Myxosporea) in cultured gllt-head sea bream Sparus au- Protozool 39: 273-281 rata Bull. Eur. Ass. Flsh Pathol 12: 64-66 Sitja-Bobadilla, A , Alvarez-Pellitero. P (1993a). Light and Egusa, S. (1985) Myxobolus bun sp. n. (Myxosporea: electron mlcroscoplc description of Ceratomyxa labraris B~valvulida)parasitic in the brain of Senola qulnqueradl- n sp. and redescription of C. diplodae (Myxosporea ata Temmick et Schlegel. Fish Pathol. 19: 239-244 B~valvulida)from w11d and cultured Mediterranean sea Egusa, S., Nakajima, K. (1978). Kudoasis of cultured yellow- bass (Dlcentrarchus labrax L ) (Teleostei: Seri-anidae) tall. Fish Pathol. 13: 1-7 System. Parasitol (in press) Egusa, S., Nakajima, K. (1980). Kudoa amamiemsis n. sp Sitjh-Bobadilla, A., Alvarez-Pellitero, P. (1993b). Pathologic (Myxosporea: Multivalvulida) found In cultured yellow- effects of Sphael-ospora dicentrarchi Sitja-Bobadilla et tails and wild damselfishes from Amami-Ohshima and Alvarez-Pell~tero,1990 (Myxosporea: Bivalvulida), para- Okinawa, Japan. Bull Jap Soc scient. Fish. 46 sitic of Mediterranean sea bass (Dlcentrarchus labrax L ) 1193-1198 (Teleostei Serranidae), and the cell mediated iinlnune re- Egusa. S., Shiomitsu, T (1983).Two new species of the genus action: a light and electron mlcroscoplc study. Parasitol. Kudoa (Myxosporea: Muyltivalvulida) from marlne cul- Res. 79: 119-129 tured In Japan Fish Pathol. 18 163-171 Sitja-Bobadilla, A., Alvarez-Pellitero, P. (1993~)Populat~on El-Matbouli, M , Fischer-Scherl, Th., Hoffmann, R.W. (1992). dynamics of Sphaerospora dicentrarchi Sitja-Bobadilla et Present knowledge of the l~fecycle, , pathology Alvarez-Pellitero, 1992 and S. testjcular~sSitja-Bobadilla and therapy of some Myxospol-ea ~mportantfor freshwdter et Alvarez-Pellitero, 1990 (Myxosporea. B~valvulida)in- fish. Ann. Rev. Fish Dis 2: 367-402 fections in wild and cultured Med~terranean sea bass El-Matbouli, M., Hoffmann, R.W (1989).Experimental trans- (Dicentrarchus labrax L.).Parasitology 106: 39-45 mission of two ~Vyxobolusspp developing bisporogeny Sitja-Bobadilla, A., Alvarez-Pellltero, P. (1993d). Zschokkella v1a tubificid worms Parasitol. Res 75. 461-464 n~ug~llsn. sp. (Myxosporea: Bivalvulida) from mullets 238 Dis. aquat. Org. 11: 229-238, 1993

(Teleostei: Mugilidae) of Mediterranean waters: light tured grouper Ephinephelus rnalabaricus. Dis. aquat. Org. and electron microscopic descript~on. J. eukaryot. 8: 35-38 Microb~ol.40: In press Suparnattaya, K., Flscher-Scherl, Th., Hoffrnann, R. W., Sitjd-Bobadilla, A., Alvarez-Pellitero, P. (1993e). Ultrastrur- Boonyaratpalin, S. (1991). Sphaerospora epinepheli n. sp. tural and cytochernical observations on the sporogenesis (blyxosporea: Sphaerosporidae) observed in grouper of Sphaerospora testicularis (Protozoa: Myxosporea) from (Ep~nephelusrnalabaricus) J. Protozool. 38: 448-454 Mediterranean sea bass. Dicentrarchus Iabrax (L.).Eur. J. Wolf, K.. Markiw. M. E. (1984). Biology contravenes taxonomy Protistol. 29: 219-229 in the Myxozoa: new discoveries show alternation of in- Sitja-Bobadllla, A., Franco-Sierra, A., Alvarez-Pellitero. P. and vertebrate hosts. Sc~ence225: 1449-1452 (1992). Sphaerospora (blyxosporea: Bivalvulida) infection Yasunaga, N., Hatei, K., Ogawa, S., Yasumoto, S. (1981). An in cultured gilt head sea bream, Sparus aurata L.. a pre- unknown rnyxozoa found in brain of cultured sea bass, liminary report J. Fish Dis. 15: 339-343 Lateolobrax japonicus and cultured Japanese striped Supamattaya, K., Fischer-Scherl, Th., Hoffrnann. R. W., knifejaw, Oplegnatus fasciatus (Japan.). Fish Pathol. 16: Boonyaratpalin, S. (1990). Renal sphaerosporosis in cul- 51-54

Responsible Subject Editor: W. Korting, Hannover, Germany Manuscript first received: February 23, 1993 Revised version accepted: July 22, 1993