Pathology of Myxosporea in Marine Fish Culture
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DISEASES OF AQUATIC ORGANISMS Published December 16 Dis. aquat. Org. REVIEW Pathology of Myxosporea in marine fish culture 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 Bivalvulida 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. KEY WORDS: 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 Ceratomyxa 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 literature. 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 Host 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) Myxidium sp. Sparus a urata Open farms in Southern Cyprus Diamant (1992) Myxobolus 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 genus 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 areas