Rapp. P.-v. Réun. Cons. int. Explor. Mer, 182: 44^48. 1983

Review of diseases of cultured warm-water marine fish1

Han Paperna H. Steinitz Marine Biologv Laboratory of the Hebrew University of Jerusalem P.O.B. 469, Eilat 88103, Israel

minant etiological agents are strains of the opportunistic Introduction species, Vibrio alginolyticus (V. parahaemolyticus, ac­ There is an increasing awareness of the importance of cording to some authors, Bergey’s Manual, 8th Edition, diseases in the developing mariculture of the warm- 1974; Colorni et al., 1981). Pathological changes water fishes gilthead seabream (Sparus aurata), seabass observed in moribund fish with confirmed septicemia (Dicentrarchus labrax), and grey mullets (Mugil cepha- were of a non-specific type: edematous and hemor­ lus, Liza ramanda, and other Mugilidae). rhagic changes apparently resulting primarily from the The etiology, epizootology, and the process of mechanical injuries and stress reaction (Colorni et al., pathogenesis of diseases of fish in warm-water envi­ 1981). Vibrio spp. are also involved in chronic bacterial ronments may differ considerably from those experi­ infections. However, to date adequate diagnosis of the enced in fish cultured in cold-water environments, even bacterial strains taking part in such infections has not when the same fish species or same type of pathogen is been accomplished. Pathological changes observed in involved. Gilthead seabream, seabass, and mullets (and such chronic infections are either non-specific — re­ also warm-water freshwater fish such as Tilapia spp. and miniscent of the acute type (chronic vibriosis in mullets silver carp, Hypophthalmichthys molitrix) are very sus­ cultured in Spain, ACUIGROUP, 1979) - or are of a ceptible to handling injuries (Paperna et al., 1977, Be- more specific nature and confined to the particular jerano et al., 1979). In a warm-water environment the organ: ulcerative changes in the lateral line canals reproduction level and the invasiveness of microbial (“White head” disease of the seabass at Eilat), cutane­ organisms and the parasites are intense and hyperinfec­ ous hemorrhagic necrosis of the head (“Red head” dis­ tion occurs readily. The pathological changes which re­ ease of juvenile seabass at Brest, Barahona-Fernandes, sult from injuries, infections, and metabolic disorders, 1977), and necrosis of the caudal peduncle (in seabass develop at a faster rate than in a cold-water environ­ at Sète, Tesseyre, 1979). ment (Hoffman, 1976; Roberts, 1975; Paperna, 1979 a, Bacterial infections resulting in focal subcutaneous and unpublished data). Overcrowding and inadequate granuloma and visceral granulomata, particularly in the feeding with consequent growth suppression place a kidneys and liver were sporadically seen in gilthead more immediate stress on the fish and thus increase seabream and mullets at Eilat. Granulomas in viscera their vulnerability to infection (Paperna, 1963, 1975; associated with mycobacteria have been reported in Paperna et al., 1977; Sarig, 1971). Moreover, in the seabass in Italy (Ghittino, 1970). Acute gill necrosis warm-water habitat extreme changes in the tempera­ (“gill rot”) consequent to handling injuries commonly ture and the oxygen levels which adversely affect fish affects gilthead seabream at Eilat while a chronic con­ seem to have less impact on the reproductive activity of dition of gill necrosis is common among cultured sea­ the various microbial and parasitic infectious agents bass with natally deformed opercula in France and Is­ associated with these fish (Paperna and Lahav, 1974; rael. Gill necrosis in both conditions was associated with Paperna, 1975; Paperna and Overstreet, 1981). the proliferative growth of myxobacteria. The causative agent of epitheliocystis is an intracel­ lular chlamydia-like organism, infecting the cells of the gill epithelium (Paperna et al., 1978; Paperna and Sab- Bacterial diseases nai, 1981). Epitheliocystis occurs either as a benign in­ In acute bacterial septicemia in marine fish at Eilat, fection, inducing only limited focal changes in the gill resulting from handling injuries and stress, the predo- epithelium, irrespective of the level of infection or as a proliferative infection which induces extensive hyper­ plasia of the gill epithelium. The latter type of infection 1 Research on diseases of cultured marine fish at Eilat is sup­ leads to massive mortalities of the fish affected ported by grants from the GKSS Geesthacht-Tesperhude, Germany and the U.S.-Israel Agricultural Research and De­ (Paperna, 1977). In fish surviving the proliferative velopment Fund. stage, tissue changes eventually (within 2 -7 days) re-

44 gress, infection declines to a sporadic level or is elimi­ recognized thus far in cultured gilthead seabream, sea­ nated altogether. Epitheliocystis infections occur in bass, and mullets in the Mediterranean region and at gilthead seabream, seabass, and mullets (in Israel and Eilat on the Red Sea. Available data already suggest France, Paperna, 1977; Paperna and Baudin-Lauren- that all of these parasites are widely distributed in the cin, 1979). Epitheliocystis organisms in each of these Mediterranean region and, thus, follow the distribution hosts appear to form a distinct species. Epitheliocystis range of their respective hosts (Paperna and Baudin- infections occur in nature predominantly in wild fry and Laurencin, 1979; Paperna and Overstreet, 1981). are introduced into culture systems utilizing wild fry as Fish in sea cages are threatened with the highest risk culture seed. of infection, particularly if placed in the natural habitat of the fish species. Cage-cultured seabass on the Mediterranean coast of France were reported to be Parastic infection heavily infected by their specific species of monogenean The potential pathogenicity to fish has already been (Diplectanum aequans) and copepod (Caligus minimus) demonstrated in 14 of 25 parasitic species (Table 2) (Oliver, 1977; Paperna and Baudin-Laurencin, 1979).

Table 2. List of parasites reported from cultured gilthead seabream (Spams aurata, SA), seabass (Dicentrarchus labrax, DL), and grey mullets (Mugilidae, MG). P, pathogenic, B, benign.

Parasite Hosts Effect Site of infection References

Protozoa Trichodina spp. MG P skin and gills 1, 4, 6 Tripartiella spp. SA DL MG P skin and gills 1, 3, 4, 8 Colponema sp. SA DL MG B gills 1,4, 6 Chloromyxum sp. SA P gut 8 Kudoa sp. SA ? kidneys, mesenteries 12 MG B gut wall 8 M yxobolus sp. MG P-B gills, gut wall other visceral organs 1, 4, 6, 8 M yxobolus sp. DL B liver, gall bladder wall and gut wall 4, 8 Ceratomyxa spp. DL MG B gall bladder 4, 8 Amyloodinium ocellatum SA DL MG P skin and gills 4, 8 Cryptocaryon irritons SA P skin and gills 8 Haemogregaria sp. SA B kidney, liver, gut wall 11 (cystozoites only) MG B muscles 13

Monogenea Ligophorus spp. MG B gills 6 Furnestia echeneis SA P gills, opercular folds 3 Diplectanum aequans DL P gills 4, 8 Benedenia monticelli MG (DL) P mouth, skin 1 ,4 , 8 Metamicrocotyle cephalus MG B? gills 8 Gyrodactylus sp. SA MG P skin 8

Copepoda Caligus pageti MG P skin 5, 9 Caligus mugilis MG P skin, mouth 8 Caligus minimus DL P mouth 4, 8 Pseudocaligus apodus MG P opercular region, gills, skin 5, 9 Ergasilus lizae MG P gills 1, 6, 10

Isopoda Nerocila orbignyi MG P skin, operculum, gills 6 (and other spp.) Gnathia elatica & Gnathia piscivora MG SA P skin 7

References. Paperna, 1975(1), 1979 a (2); Paperna et al., 1977(3); Paperna and Baudin-Laurencin, 1979(4); Paperna and Lahav, 1974(5); Paperna and Overstreet, 1981(6); Paperna and Por, 1977(7); Paperna et al., unpublished data (8); Russell, 1924(9); Sarig, 1971(10). Since the Symposium the following data have been published, Paperna, 1979 b (11); Paperna, 1982(12); Paperna and Sabnai, 1982(13). 45 However, since culture conditions in cages are usually may also be introduced with fry), and the copepod maintained at optimal levels morbid epizootics are on Caligus minimus in seabass (Paperna and Baudin- the whole, infrequent. Contamination of inshore Laurencin, 1979; A. Raibaut, personal communica­ mariculture systems by parasites occurs either when tion). Ergasilus lizae, an euryhaline copepod adaptable wild-caught fry of fingerlings are utilized as culture seed to fresh water, after being introduced into freshwater or when wild-caught mature fish are utilized as spaw- farms in Israel by mullets, expanded its distribution to ners. Once infection is established in the farm as was many inland freshwater farms throughout the country experienced at Eilat, Sète, and Brest (C.O.B.) the entire and extended its host range to cultured tilapia and carp system including the hatchery runs the risk of contami­ (Sarig, 1971). Microcotylid monogeneans were re­ nation. Though it is highly unlikely in most situations, ported to cause mortalities in cage-cultured fish in Ja­ pumped unfiltered seawater was suggested as a possible pan (Kubota and Takakua, 1963). Microcotylids intro­ route for the infiltration of parasites into the culture duced with rabbitfish (Siganus luridus and S. rivulatus) system (Wilkie and Gordin, 1969). to the culture system at Eilat caused severe mortalities In wild populations of seabream, seabass, and mul­ in these fish held in ponds and tanks. To date even at lets, most ectoparasitic metazoan elements of their relatively high infection levels microcotylids are tole­ parasitofauna - caspaloid and polyopistocotylid mono- rated by cultured mullets. Microcotylids were also re­ geneans and parasitic copepods - are absent in the fry ported in wild gilthead seabream and seabass, but so far arriving from the offshore spawning grounds in littoral are unknown in the cultured monogeneans. Epizootics waters. These parasites gradually become established in mullets cultured in seawater earth ponds by caligiid on the fish at a later stage, after the fourth month of life copepods have been reported from Egypt and Israel when they come in closer contact with fish older than a (Russell, 1924; Paperna and Lahav, 1974). Epizootics year (Paperna, 1964, 1975; Paperna et al., 1977; with mortalities were also reported from wild popula­ Paperna and Overstreet, 1981). The parasitofauna of tions of mullets by monogeneans (Benedenia monticelli) the fry consists predominantly of parasitic protozoans — in the Gulf of Suez (Paperna, 1975) and copepods Trichodina and Tripartiella spp., Colponema sp., and (Caligus epidemicus) in a river in Australia (Hewitt, more rarely also dactylogyroid monogeneans - Gyro- 1971). dactyliis spp., Furnestia echeneis in gilthead seabream, Of all the parasites introduced into mariculture sys­ and Diplectanum aequans in seabass. Also common in tems the dinoflagellate, Amyloodinium ocellatum and wild fry of these fish species is the microbial agent for the ciliate, Cryptocaryon irritans (the marine analogue epitheliocystis, as discussed above. of the freshwater Ichthophthirius multifilis) appear to In sea culture systems the parasites listed above affect be the most morbid pathogens to fish. Both made their mainly nursery fish, particularly wild fry during their first devastating appearance in tropical marine aquaria acclimation period in holding tanks. Trichodina spp. (Brown, 1931, 1934; Nigrelli and Ruggieri, 1966) and and Tripartiella spp. will endanger fish larvae if intro­ have only recently spread to cultured marine fish. duced into a hatchery — as happened in Sète (M. G. These parasites are apparently widely distributed in Barnabe, personal communication). In large fish ponds the tropical Indo-Pacific and Atlantic waters. There are and on larger fish these parasites have a limited effect. also increasing reports of their occurrence in subtropical Stocks of wild fry are often infected, occasionally and temperate waters. Epizootics of A. ocellatum were heavily by the trematode metacercaria, Acanthocephala reported in cultured fish in Fiji (in Siganus spp.) and at (Golvanacanthus blenii) as well as by larval cestodes Eilat (in gilthead seabream and seabass), (Paperna, and nematodes (Schmidt and Paperna, 1978; Paperna 1980), in the Gulf of Mexico in pompano (Trachinotus et al., 1977; and unpublished data). However, in the carolinus) (Lawler, 1972) as well as in seabass cultured absence of suitable hosts to perpetuate their cycle, in Italy and Yugoslavia (P. Ghittino, personal com­ neither of these helminth forms were capable of be­ munication). Infection was also found in gilthead sea­ coming established in the system. The likelihood of in­ bream cultured at Sète (Paperna and Baudin-Lauren­ troducing additional species of monogeneans as well as cin, 1979). To date C. irritans has been reported in parasitic crustaceans increases when “larger” wild fish pompano in Florida (Sindermann, 1977), in gilthead (fingerlings and yearlings) are utilized as culture seed. seabream fry at Eilat (unpublished data), and from These fish as well as the spawners were the apparent holding tanks (in a wide variety of fishes) in California route for introducing metazoan parasitic infections, (Wilkie and Gordin, 1969). Both of the parasites are some of which developed into morbid epizootics in the extremely prolific. The A. ocellatum produces 128 to culture systems - the monogenean Benedenia mon- 256 progeny every 6 to 12 days, i.e. and instantaneous ticelli, and the copepods Ergasilus lizae, Pseudocaligus rate of increase of 0 5 per day (Paperna, unpublished apodus, Caligus paged, and Caligus mugilis in mullets data). The C. irritans produces up to 200 progeny every (Russell, 1924; Sarig, 1971; Paperna and Lahav, 1974; 11 to 14 days (Nigrelli and Ruggieri, 1966). Both para­ Paperna, 1975; Paperna and Overstreet, 1981), the sites tolerate a wide range of temperatures (15°-30°C monogenean Diplectanum aequans (which more rarely for A. ocellatum and 19°-37°C for C. irritans) and

46 salinities (10—70 %ofor A. ocellatum and 16—31 %o2 for dium, and the eyes (Paperna et al., 1980). The disease C. irritans, Cheung et al., 1979; Paperna, unpublished appears principally among the young fish. Losses among data). Both parasites are indiscriminate in their host affected 0-class fish may amount to 50 % or more. Fish preference and therefore most species of teleostean fish may succomb within 3 weeks to 2 months after the onset run the risk of becoming infected (Nigrelli and Ruggieri, of feeding on test diets. Surviving fish may maintain a 1966; Lawler, 1972). The life cycle of both organisms granulomatous condition for a year or two. In some consists of intermittent phases of active feeding (tro­ cases, the granulomata completely regress while in phozoite) and an encapsulated non-parasitic dividing others prolonged chronic inflammation eventually re­ stage (sporont or tomonts). The encapsulated tomont is sults in either extensive necrosis or in advanced fibrosis resistant to most conventional parasite-killing agents; and atrophy of the visceral organs. This process finally division within the tomont of A. ocellatum was not inhi­ leads to emaciation and death of the affected fish. The bited even when tomonts were incubated with 100 ppm damage in the eyes usually causes irreversible blindness. formalin and 4 ppm copper sulfate. Immersion in 200 Bilateral blindness further enhances the starvation of ppm formalin for up to 24 hours only temporarily inhi­ the fish. bited the division within the tomont; division resumed Occasionally the prevalence of body deformities and upon transfer to fresh sea water (Paperna, unpublished tumors occurs at high levels in hatchery-spawned sea­ data). bass and to a lesser extent in gilthead seabream. Fish The greatest losses inflicted by A. ocellatum at Eilat with cranial deformations do not survive beyond the was on gilthead seabream larvae in the hatchery. larval stage or past the second month of life (Barahona- Among larvae 50 to 80 days old, losses due to oor- Fernandes, 1979). On the other hand opercular defor­ diniasis in the 1979 season amounted to 50 % of the mation, scoliosis, and swimbladder abnormalities be­ entire stock. By repeated treatments with formalin (200 come apparent only in the fish which are beyond the ppm/6 hours) or copper sulfate (2 ppm/6 hours) larval stages; affected fish are capable of surviving hyperinfection could be suppressed.3 Meanwhile mor­ beyond their first year of life (Paperna, 1978; Bara- talities were prevented and eventually infection was also hona-Fernandes, 1979; Tesseyre, 1979). However, suppressed and eliminated. This eventual suppression of such fish demonstrate growth retardation and are very infection suggests the development of a form of resist­ susceptible to bacterial diseases and parasitic infections. ance to infection in the fish.3 In gilthead seabream the swimbladder is displaced by epithelial tumors derived from the gas gland non-differ- entiated epithelium. This phenomenon was linked to Metabolic disorders. Abnormalities and the occurrence of scoliosis (Paperna, 1978). Spinal de­ formation in gilthead seabream may also occur inde­ deformities pendently of the swimbladder deformities (Tesseyre, Feeding on diets containing fish meal or unprocessed 1979, and personal communication). In seabass with trash fish is suspected to be the primary cause of the dysfunction of the swimbladder discrete histological development of a metabolic disorder coupled with sys­ changes which might lead to this condition have so far temic chronic inflammation in cultured Sparus aurata in not been demonstrated. Swimbladder deformation and Israel and Spain. Experiments to elucidate the etiology skeletal deformations occurred in seabass indepen­ of this condition named “systemic granuloma” have so dently of each other. To date only a partial correlation far yielded inconclusive results. Tests made to isolate could be demonstrated experimentally between the ad­ primary viral, bacterial, or fungal agents yielded nega­ verse effects of abiotic factors during the prenatal or tive results. At the same time environmental factors postnatal larval stages or between inadequate nutrition were excluded as a possible primary cause since the and the occurrence of abnormalities in hatchery- disease occurs in fish reared in diverse culture condi­ spawned fish (Barahona-Fernandes, 1979). The role of tions (Paperna, 1979 a). hereditary factors still remains to be examined. The early pathological process is localized in the renal uriniferous ducts, where degenerative changes in the epithelium, obstruction of the lumen by crystals, and References calculi of tyrosine occur. Subsequently, granulomata ACUIGRUP (Acuicultura Bioter, Bioter Biona S. A., Mad­ and necrotic foci developing in the hematopoietic tis­ rid). 1979. Vibriosis in Spain. Its importance for marine polyculture. Report submitted to 4th session FAO/ sues of the kidney and the spleen lead to hypertrophy of COPRAQ Barcelona 16-19 Oct. 1979. these organs. Granulomata and necrotic lesions spread Barahona-Fernandes, M. H. 1977. Bacterial disease of seabass to other organs: liver, gut wall, mesenteries, pericar­ (.Dicentrarchus labrax (L.)) reared in the laboratory: an ap­ proach to treatment. Aquaculture, 10: 317-322. 2Hypersaline range not studied. Barahona-Fernandes, M. H. 1979. L’élévage intensif des 3The problem of infection in hatcheries was eventually solved larves et des juvenils du bar (Dicentrarchus labrax (L.)), by continuous application of 0 • 75 ppm CuS04 x 5 H20 for 5 donnés biologiques, zootechniques et pathologigues. Thèse to 6 days to the holding tanks (Paperna, unpublished data). d’Etat de l’Université d’Aix Marseille II.

47 Bejerano, Y., Sarig, S., Horne, M. T., and Roberts, R. J. 1979. Paperna, I. 1980. Amyloodinium ocellatum (Brown, 1931), Mass mortalities in silver carp Hypophthalmichthys molitrix (Dinoflagellata) infestations in cultured marine fish at Eilat, (Valenciennes) associated with bacterial infections following Red Sea: epizootology and pathology. J. Fish Dis., 3: handling. J. Fish Dis., 2: 49-56. 363-372. Bergey’s manual of determinative bacteriology. 1974. 8th Paperna, I. 1982. Kudoa infection in the glomeruli, mesentery, edition. Ed by R. E. Buchanan and N. E. Gibbons. Williams and peritoneum of cultured Sparus aurata L. J. Fish Dis., 5: and Wilkins Co., Baltimore, Maryland. 539-543. Brown, E. M. 1931. Note on a new species of dinoflagellate Paperna, I., and Baudin-Laurencin, F. 1979. Parasitic infec­ from the gills and epidermis of marine fishes. Proc. Zool. tions of seabass, Dicentrarchus labras, and gilthead sea­ Soc. London, Part I: 345-346. bream, Sparus aurata in mariculture facilities in France. Cheung, P. J., Nigrelli, R. F., and Ruggieri, G. D. 1979. Aquaculture, 16: 173-175. Studies on cryptocaryoniasis in marine fish. Effect of tem­ Paperna, I., Colorni, A., Gordin, H., and Kissil, G. W. 1977. perature and salinity on the reproductive cycle of Cryp- Diseases of Sparus aurata in marine culture at Eilat. tocaryon irritans Brown, 1951. J. Fish Dis., 2: 93-97. Aquaculture, 10: 195-213. Colorni, A., Paperna, I., and Gordin, H. 1981. Bacterial infec­ Paperna, I., Harrison, J. G., and Kissil, G. W. 1980. Pathology tions in gilthead seabream Sparus aurata cultured at Eilat. and histopathology of a systemic granuloma in Sparus aurata Aquaculture, 23: 257-267. L. cultured in the Gulf of Eilat. J. Fish Dis., 3: 213-221. Ghittino, P. 1970. Piscicoltura e ittiopatologia. Vol. 2, it- Paperna, I., and Lahav, M. 1974. Mortality among grey mul­ tiopatologia. Edizione Rivista di Zootecnia. lets in a seawater pond due to caligiid parasitic copepod Hewitt, G. C. 1971. Two species of Caligus (Copepoda, epizooty. Bamidgeh, Bull. Fish Cult. Israel, 26: 12-15. Caligidae) from Australian waters, with a description of de­ Paperna, I., and Overstreet, R. M. 1981. Parasites and diseases velopmental stages. Pacific Sei., 25(2): 145-164. of mullets (Mugilidae). Cambridge University Press. IBP Hoffman, G. L. 1976. Fish diseases and parasites in relation to 26(13): 411-493. the environment. J. Fish Pathol., 10(2): 123-128. Paperna, I., and Por, D. 1977. Preliminary data on the Kubota, S. S., and Takakua, M. 1963. Studies on the diseases Gnathiidae (Isopoda) of the northern Red Sea, the Bitter of marine culture fishes. 1. General description and prelimi­ Lakes, and eastern Mediterranean and the biology of nary discussion of fish diseases in Mie Prefecture. J. Fac. Gnathia piscivora n. sp. Rapp. P.-v. Réun. Commn int. Fish. pref. Univ. Mie-Tsu, 6: 107-124. Explor. scient. Mer Méditerr., 24: 195-197. Lawler, A. R. 1972. Preliminary studies on Amyloodinium Paperna, I., and Sabnai, I. 1981. Epitheliocystis disease in ocellatum (Brown, 1931) in the Gulf of Mexico: natural fishes. In Fish diseases, third COPRAQ-Session, pp. hosts, experimental hosts, and control. Gulf Coast Res. Lab. 228-234. Ed. by W. Ahne. Springer-Verlag, Berlin, National Marine Fisheries Service. Compl. Report., 2-85-R, Heidelberg. 41 pp. Paperna, I., ^nd Sabnai, 1. 1982. A coccidian cyst stage in the Nigrelli, R. F., and Ruggieri, G. D. 1966. Enzootic in the New musculature of Liza subviridis (Mugilidae). Z. Parasitenk., York aquarium caused by Cryptocaryon irritans (Ichthyop- 68: 161-170. thirius marinus Sikama, 1961) a histophagous ciliate in the Paperna, I., Sabnai, I., and Castel, M. 1978. Ultrastructural skin, eyes and gills of marine fishes. Zoologica, 51: 97-102. study of epitheliocystis organisms from gill epithelium of the Oliver, G. 1977. Pathogenic effect of fixation of Diplectanum fish Sparus aurata L. and Liza ramada (Risso), and their aequans Wagener, 1857, Diesing, 1858 (Monogenea, Mo- relationship to the host. J. Fish Dis., 1(2): 181-189. nopisthocotylea, Diplectanidae) on the gills of Dicentrar- Roberts, R. J. 1975. The effect of temperature on diseases and chus labrax (Linnaeus, 1758) (Pisces, Serranidae). Z. their histological manifestations in fish. In The pathology of Parasit Kde., 53: 7—11. fishes, pp. 477-496. Ed. by W. E. Ribelin and G. Migaki. Paperna, I. 1963. Dynamics of Dactylogyrus vastator Nybelin Univ. Wis. Press, Madison. 1004 pp. (Monogenea) population on the gill of carp fry in fish ponds. Russell, F. S. 1924. A new species of Caligus from Egypt, Bamidgeh, Bull. Fish Cult. Israel, 15: 31-50. Caligus pageti sp. n. Ann. Mag. nat. Hist., 15(9): 611-618. Paperna, I. 1964. The metazoan parasite fauna of Israel inland Sarig, S. 1971. The prevention and treatment of diseases of water fishes. Bamidgeh, Bull. Fish Cult. Israel, 16: 3—66. warm-water fish under subtropical conditions with special Paperna, I. 1975. Parasites and diseases of the grey mullet emphasis on intensive fish farming. Diseases of Fishes Book (Mugilidae) with special reference to the seas of the Near 3, TFH Publications, New Jersey. East. Aquaculture, 5: 65-80. Schmidt, G. D., and Paperna, I. 1978. Sclerocollum rubrimaris Paperna, I. 1977. Epitheliocystis infection in wild cultured gen. et. sp. n. (Rhadinorhynchidae, Gorgorhynchinae) and seabream Sparus aurata (Sparidae), and grey mullets (Mu­ other acanthocephala of marine fishes from Israel. J. gilidae). Aquaculture, 10: 169—176. Parasit., 64(5): 846—850. Paperna, I. 1978. Swimbladder and skeletal deformations in Sindermann, C. J. (Ed.) 1977. Disease diagnosis and control in hatchery-bred Sparus aurata. J. Fish Biol., 12: 109-114. North American marine aquaculture. Elsevier, New York. Paperna, I. 1979 a. Systematic granuloma, a diet-related dis­ Tesseyre, C. 1979. Etude des conditions d’élévage intensif du ease in gilthead bream Sparus aurata L. in marine culture. loup (Dicentrarchus labrax L.). Thèse d’Etat de l’Université Proc. world Symp. Finfish Nutrition Fish Feed Techn., des Science et Technique du Languedoc. Hamburg, 20-23 June, 1978, 2: 370-376. Wilkie, D. W., and Gordin, H. 1969. Outbread of cryp­ Paperna, I. 1979 b. Sporozoa infection in cultured Sparus au­ tocaryoniasis in marine aquaria at Scripps Institution of rata L. and wild Siganus luridus. Ann. Parasitol., 54: Oceanography. Calif. Fish Game, 55(3): 227-236. 386-392.

48