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6 Infectious Diseases of Warmwater Fish in Marine and Brackish Waters

Leong Tak Seng1 and Angelo Colorni2 1School of Biological Sciences, Universiti Sains Malaysia, Penang, Malaysia; 2Israel Oceanographic and Limnological Research, National Center for Mariculture, PO Box 1212, Eilat 88112, Israel

Introduction two main geographic regions, namely West Asia and Southeast Asia. The West Asia The culture of marine finfish in cages that regions present wider fluctuations of envi- hang from floating rafts was successfully ronmental conditions, particularly water initiated in Japan in the 1950s and in South- temperature, whereas in Southeast Asia east Asia in the 1970s. In those early years, they are generally more stable. The species fish for culture were obtained from the of fish cultured in the various regions wild. While in many regions this is still the reflect these environmental differences. way culture is started, some species of fish Other warmwater areas where cage culture are today successfully hatchery-produced. is practised on a commercial scale are the The cage culture system is basically similar tropical islands of the Pacific Ocean. throughout the world wherever intensive The most common species of marine mariculture is practised. However, disease fish cultured in floating cages are summa- types and severity are greatly influenced by rized in Table 6.1. the species of fish, the conditions in which the animals are cultured and the husbandry management. Diseases Caused by Viruses Fish cultured in floating cages become particularly susceptible to disease when Viral diseases in cage-cultured fish have various environmental parameters such as been on the increase since the 1980s in East temperature, salinity, dissolved oxygen and Asia and the 1990s in Southeast Asia (Nakai suspended particles fluctuate suddenly or et al., 1995; Arthur and Ogawa, 1996; widely, or following rough, although often Muroga, 1997; Bondad-Reantaso, 2001; unavoidable, handling operations. Once Roongkamnertwongse et al., 2001; Zhang, conditions suitable for pathological changes 2001). Virological research received a new develop, progress to disease in the warm- impetus following the high mortality in water environment is rapid. Early detection hatchery-bred juvenile fish soon after being of behavioural changes and clinical signs in placed in sea cages (Fukuda et al., 1996; the cultured animals are critical for proper Park and Sohn, 2001). With the increasing diagnosis of the disease. awareness of virus-related diseases and The warmwater culture of marine with new species of fish being selected for finfish in floating cages is concentrated in culture, more reports of known and new

©CAB International 2002. Diseases and Disorders of Finfish in Cage Culture (eds P.T.K. Woo, D.W. Bruno and L.H.S. Lim) 193

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194 T.S. Leong and A. Colorni

Table 6.1. Species (common name) of marine fish cultured in cages in Asia. Species East Asia Southeast Asia West Asia

Serranidae (seabass and groupers) Dicentrarchus labrax (European seabass) − − + Epinephelus aeneus (white grouper) − − + E. coioides (greasy grouper) + + + E. malabaricus (black dot grouper) + + − E. bleekeri (brown grouper) + + − E. fuscoguttatus (tiger grouper) + + − Lutjanidae (snappers) Lutjanus argentimaculatus (mangrove snapper) + + − L. johni (golden snapper) − + − L. russellii (Russell’s snapper) + − − Chanidae (milkfish) Chanos chanos (milkfish) + + − Centropomidae (snooks) Lates calcarifer (Asian seabass) − + − Mugilidae (mullets) Mugil cephalus (mullet) − − + Scorpaenidae (scorpion fishes) Sebastes schlegeli (black rockfish) − − + Carangidae (jacks) Seriola quinqueradiata (yellowtail) + − − S. dumerili (yellowtail) + − − Caranx (Pseudocaranx) dentex (striped jack) + − − Trachurus japonicus (horse mackerel) + − − Tetraodontidae (puffers) Takifugu rubripes (tiger puffer) + − - Sparidae (seabream) Sparus aurata (silver seabream) − − + Rhabdosargus sarba (goldlined seabream) + − − Pagrus major (red seabream) + − − P. schlegeli (black seabream) − − + Acanthopagrus bifasciatusi (black seabream) − − + Sciaenidae (drumfish) Sciaenops ocellatus (red drum) − − + Pleuronectidae (flounders) Paralichthys olivaceus (Japanese flounder) + − -

viral diseases are to be expected. The displaying little or no scar tissue (Paperna viruses reported in cultured marine fish et al., 1982). Although the unsightly are summarized in Table 6.2. appearance of the typical lesions renders the infected fish unmarketable, juveniles are considerably more susceptible to the Lymphocystis infection than larger, market-sized stages.

Lymphocystis is a highly contagious Host range. Although known to infect 30 infection caused by a cytoplasmic DNA families of marine fish (Wolf, 1988), iridovirus. The disease follows a chronic lymphocystis is a host-specific disease course and, in general, mortalities are (Overstreet and Howse, 1977; Chao, 1984), limited. The infected fish recover within a therefore the disease is most probably few weeks of the onset of the outbreak, caused by a group of different viral strains.

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Table 6.2. Viral diseases of warmwater maricultured finfish. Disease Causative agent Species affected

DNA virus Lymphocystis (LCDV) Iridovirus Japanese flounder (Paralichthys olivaceus) Japanese seabass (Lateolabrax japonicus) Seabream (Sparus aurata) Red drum (Sciaenops ocellatus) Red seabream iridoviral RSIV Red seabream (Pagrus major) disease Grouper (Epinephelus malabaricus) RNA virus Viral nervous necrosis Nodavirus Striped jack (Pseudocaranx dentex) (SJNNV and VNN) Black spotted grouper (Epinephelus bleekeri) Greasy grouper (Epinephelus coioides) Black spotted grouper (Epinephelus malabaricus) Grouper (Epinephelus tauvina) Marbled leopard grouper (Plectropomus maculates) European seabass (Dicentrarchus labrax) Asian seabass (Lates calcarifer)

In Southeast Asia, only seabass (Lates Diagnosis. The disease is characterized by calcarifer) has been reported to be affected tumour-like masses of tissue on the body by this disease (Limsuwan et al., 1983; Chao, surface (Fig. 6.1). These growths are clusters 1984). In Israel, it was reported in seabream of extremely hypertrophic fibroblastic (Sparus aurata), a species reared in the Red dermal cells (Fig. 6.2). In yellowtail, the Sea but originally imported from the infected cells are dispersed, covered by a Mediterranean Sea (Paperna et al., 1982), layer of epithelium and surrounded by black and in the red drum (Sciaenops ocellatus), pigment cells, thus appearing as small black originally imported from the USA (Colorni dots (Matsusato, 1975). Occasionally inter- and Diamant, 1995). Lymphocystis has nal organs can become infected (Colorni and been listed as a major viral disease Diamant, 1995). of maricultured fish in Japan (Muroga, Lymphocystis-infected cells are mainly 1995). In East Asia, outbreaks of this spherical in shape with a thick elastic mem- disease have been reported for seabass brane, but may be distorted when in clusters, (Lateolabrax japonicus) (Miyazaki and due to pressure from adjacent cells. The Egusa, 1972; Chen, 1996; Park and Sohn, infected cells apparently stimulate prolifera- 1996), yellowtail (Seriola quinqueradiata) tion of the adjacent healthy tissue. After 2 (Matsusato, 1975), Japanese flounder weeks of infection, the cells enlarge signifi- (Paralichthys olivaceus) (Tanaka et al., cantly. Both nucleus and nucleolus present 1984; Park and Sohn, 1996), red seabream large basophilic cytoplasmic inclusion (Pagrus major) (Chen, 1996; Park and Sohn, bodies that react positively for DNA. 1996; Muroga, 1997) and rockfish (Sebastes Diagnosis of lymphocystis disease is schlegeli) (Chun, 1998). Matsuoka (1995) confirmed through histological sections and reported that the incidence of this disease appropriate staining of the tissue lesions. In has increased since the early 1990s, particu- fact, this is one of the few viral diseases that larly in Japanese flounder. can be identified histologically. The obser- vation of the typical icosahedral virions by electron microscopy offers further confirma- Geographic distribution. Lymphocystis tion. Horizontal transmission is the most disease is not restricted to warm seas, but is probable route, facilitated by high stocking widespread throughout the world in both density and unfavourable environmental marine and freshwater fish (Wolf, 1988). conditions. In Southeast Asia, trash fish

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Fig. 6.1. Lymphocystis in Asian seabass, Lates calcarifer.

Fig. 6.2. Hypertropic fibroblastic cells in caudal fin of Asian seabass, Lates calcarifer.

used as feed may be another source of infec- hexagonal in shape, with a diameter of tion (T.S. Leong, personal observation). 200–240 nm (in red seabream) and 140–160 nm (in brown-spotted grouper) Prevention and control. There is presently (Danayadol et al., 1997; Kasornchandra and no effective therapy for this disease. A Khongpradit, 1997). decrease in stocking density and culling of visibly infected individuals are the only Host range. Red seabream iridovirus known measures that can be adopted to (RSIV) was first diagnosed in Japan where it reduce the impact of the disease. caused a systemic infection in farmed red seabream (Inouye et al., 1992). This serious disease, however, affects other cultured Red seabream and brown-spotted marine fish species (Nakajima et al., 1995). grouper iridovirus In 1993/94, an iridovirus disease similar to RSIV was reported in cultured grouper The virus belongs to the family Iridoviridae. (Epinephelus malabaricus) in Thailand In electron microscopy, the particles appear (Danayadol et al., 1997). So far, RSIV has

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been found in more than 20 marine species nervous necrosis virus (SJNNV) (Mori et al., (Matsuoka et al., 1996; Nakajima, 1997). 1992). Juvenile and young red seabream cultured in Electron microscopy demonstrates that cages are highly susceptible to the disease. the virus particles are packed in the cyto- plasm of affected retinal and brain cells and Geographic distribution. Red seabream are non-enveloped, icosahedral in shape, iridovirus disease and similar iridoviral about 20 nm in grouper and 25–34 nm in diseases have been reported in Southeast striped jack (Danayadol et al., 1993; Nguyen, and East Asia. 1996).

Diagnosis. Affected fish become lethargic Host range. Since it was first reported in and severely anaemic. The gills are haemor- Japanese parrotfish, VNN has been diag- rhagic. The spleen is hypertrophic and the nosed in more than ten fish species in Japan iridovirus appears in a crystalline array (Mori et al., 1991; Arimoto et al., 1993; in the enlarged, basophilic splenic cells Muroga, 1995; Nakai et al., 1995). Similar (Inouye et al., 1992). Presumptive diagnosis viral diseases have been reported in Asian based on Giemsa staining of histological seabass (see Glazebrook et al., 1990; Munday sections can be confirmed by immuno- et al., 1992; Comps et al., 1994), grouper fluorescence with a monoclonal antibody or (Epinephelus spp.) (Chong and Chao, 1986; a PCR assay (Inouye et al., 1992; Nakajima Danayadol et al., 1993, 1995; Chua et al., and Sorimachi, 1994; Nakajima et al., 1995, 1995; Boonyaratpalin et al., 1996; Tanaka 1997). RSIV can be isolated in several cell et al., 1998; Bondad-Reantaso et al., 2001), lines including RTG-2, CHSE-214 and FHM European seabass (Dicentrarchus labrax) (Inouye et al., 1992). Sensitivity was particu- (Breuil et al., 1991; Comps et al., 1994), larly high in KRE-3 and BF-2 (Nakajima and turbot (Scophtalmus maximus) (see Bloch Sorimachi, 1994). However, viral infectivity et al., 1991) and halibut (Hippoglossus decreased progressively with cell subcul- hippoglossus) (see Grotmol et al., 1995). A tures. The grouper iridovirus grew well in similar syndrome was reported in the Euro- epithelioma papulosum cyprini (EPC) and pean seabass cultured in Martinique, French grouper fin (GF) cell lines (Kasornchandra Caribbean Islands (Bellance and Gallet de and Khongpradit, 1997). Saint Aurin, 1988; Gallet de Saint Aurin et al., 1990). Prevention and control. An experimental vaccine prepared by Nakajima et al. (1997) Geographic distribution. VNN disease has produced a higher survival in treated red been found in all warmwater marine seabream than in the control group, suggest- environments where marine fish have been ing the possibility of controlling the disease cultured in cage environments, particularly through vaccination. in juvenile stages.

Diagnosis. Infected fish exhibit whirling Viral nervous necrosis (VNN) movements, lethargy, dark body coloration, loss of balance and hyper-excitability in The terms fish viral encephalitis and response to noise and light. Mortalities are encephalopathy have been used to describe usually high and occur within a week of the a number of infections with a similar syn- onset of first signs. Extensive spongiosis is drome. VNN was first reported in Japanese typically observed in the retina, brain and parrotfish (Oplegnathus fasciatus)ina central nervous system (Glazebrook et al., 1985–1987 disease outbreak (Yoshikoshi 1990; Yoshikoshi and Inoue, 1990; Arimoto and Inoue, 1990) and the causative agent et al., 1992, 1993; Munday et al., 1992; has since been identified as a member of Danayadol et al., 1995; Boonyaratpalin et al., the Nodaviridae and named striped jack 1996; Nguyen, 1996). SJNNV can be detected

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198 T.S. Leong and A. Colorni

by ELISA and PCR (Arimoto et al., 1992; epitheliocystis organisms (Lannan et al., Mushiake et al., 1992, 1994). A PCR method 1999). Two distinct developmental life based on the sequence of the virus coat cycles have been recently hypothesized for protein gene (RNA2) was used to diagnose a highly pleomorphic chlamydia-like organ- the virus in spawners, suggesting vertical ism that causes epitheliocystis infection in transmission of the infection (Arimoto et al., seabream (S. aurata) (Crespo et al., 1999). 1992; Mushiake et al., 1992; Nishizawa et al., 1994, 1995). Host range. Epitheliocystis infections have been reported from over 25 species of Prevention and control. At present there is fish, including Carangidae, Centrarchidae, no known method of therapy, but vaccina- Centropomidae, Mugilidae, Pleuronectidae, tion using recombinant coat protein of live Serranidae and Sparidae (see Crespo et al., piscine nodavirus in sevenband grouper, 1999). Epinephelus septemfasciatus, resulted in significantly lower mortality in the virus Geographic distribution. Epitheliocystis is challenge tests, indicating great potential for not limited to a warm marine environment protection against the virus. and has been reported worldwide (see Noga, 1996; Crespo et al., 1999; Lannan et al., 1999). Diseases Caused by Bacteria Diagnosis. Affected fish typically display Many clinical signs of bacterial diseases of flared opercula and fast, shallow respiration. cultured marine fish are similar. Definitive In histological sections, epithelial hyperpla- diagnosis requires the isolation and in vitro sia and fusion of adjacent gill lamellae are culture of the organisms involved. A great apparent. Infected cells (up to 220 × 100 µm number of aquatic bacteria are oppor- in size, depending on developmental stage) tunistic and under normal environmental are basophilic and appear either amorphous conditions do not cause disease, becoming or uniformly granular. pathogenic only when the balance of the host/environment is changed by elevated Prevention and control. At present, no stocking densities, inadequate nutrition, effective therapy for epitheliocystis is deteriorating water quality, rough handling known. (e.g. net changing, grading) and other stress factors. The bacteria reported in cultured marine fish are summarized in Table 6.3. Gram-negative bacteria

Vibriosis Epitheliocystis Vibriosis is the disease caused by a group The epitheliocystis organism is a chlamydia- of bacteria belonging to the family Vibrion- like, obligate, intracellular prokaryote that aceae. The infectious disease they cause is has not been cultured in vitro. Infection pri- one of the most significant in mariculture. marily involves epithelial cells of the gills Age and sex of fish are not relevant factors that become packed with a large mass of the in the disease (Sano and Fukuda, 1987; minute coccoid organisms. Transmission is Arthur and Ogawa, 1996; Leong, 1996; apparently horizontal and direct. Extensive Sako, 1996; Shariff and Arulampalam, infections occur in juveniles and are often 1996). In Southeast Asia, 4–6-week-old lethal. Epitheliocystis is highly infective caged grouper weighing approximately and host-specific, indicating that the 200 g often die overnight without any disease in different species of fish is most apparent signs of disease except that the probably caused by different strains of body darkens. This condition is referred to

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Table 6.3. Bacterial diseases of warmwater maricultured finfish. Causative agent Disease Species affected

Gram-negative pathogens Vibrionaceae Listonella anguillarum Vibriosis Yellowtail (Seriola quinqueradiata) Amberjack (Seriola dumerili) Horse mackerel (Trachurus japonicus) Red seabream (Pagrus major) Vibrio alginolyticus Vibriosis Greasy grouper (Epinephelus coioides) European seabass (Dicentrarchus labrax) Seabream (Sparus aurata) Vibrio parahaemolyticus Vibriosis Golden snapper (Lutjanus johni) Seabream (S. aurata) Photobacterium damsela ‘Pasteurellosis’ Yellowtail (S. quinqueradiata) Amberjack (S. dumerili) European seabass (D. labrax) Seabream (S. aurata) Red drum (Sciaenops ocellatus) Enterobacteriaceae Edwardsiella tarda Edwardsiellosis Japanese flounder (Paralichthys olivaceus) Cytophagaceae Flexibacter maritimus Saltwater Red seabream (P. major) myxobacteriosis Greasy grouper (E. coioides) Asian seabass (Lates calcarifer) Mangrove snapper (Lutjanus argentimaculatus) Japanese flounder (P. olivaceus) Gram-positive pathogens Streptococcus spp. Streptococcosis Greasy grouper (E. coioides) Yellowtail (S. quinqueradiata) Amberjack (S. dumerili) European seabass (D. labrax) Red drum (S. ocellatus) Tilapia (O. mossambicus) (adapted to seawater) Acid-fast pathogens Nocardiaceae Nocardia seriolae Nocardiosis Yellowtail (S. quinqueradiata) Mycobacteriaceae Amberjack (S. dumerili) Mycobacterium marinum Mycobacteriosis Seabream (S. aurata) European seabass (D. labrax)

as ‘sleepy-grouper syndrome’, but its aetiol- Host range. The majority of marine fish ogy is still controversial. In Singapore and cultured in cages are susceptible to vibriosis, Indonesia, cases of sleepy-grouper syn- with some fish species more sensitive to drome were originally attributed to a virus the infection than others. In East Asia, (Chua et al., 1994; Arthur and Ogawa, yellowtail, red seabream, horse mackerel 1996), with vibrios considered as secondary and flounder are particularly susceptible. invaders. In Malaysia, groupers with In Southeast Asia, grouper, seabass and sleepy-grouper syndrome were found with snapper have been frequently reported as high numbers of monogeneans as well as affected by vibriosis. The greasy grouper with gastroenteritis vibriosis (however, fish (Epinephelus coioides) (Fig. 6.3) is more were not examined for virus) (Leong and susceptible than black-spotted grouper (E. Wong, 1993). malabaricus) and brown-spotted grouper

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Fig. 6.3. Vibriosis in greasy grouper, Epinephelus coioides.

(Epinephelus bleekeri), even when all three appearing on the body surface and gradual species are cultured in the same cage. It darkening of the body. Initially, the haemor- occurs frequently during periods of fluctua- rhage usually enlarges into irregular and tions in salinity, increased organic load, deep lesions, which disintegrate the skin, or stress brought on by net changing and exposing the underlying muscle, which grading of fish. The period following initial becomes necrotic. Vibrios produce a wide stocking is particularly critical. Horizontal variety of proteases and extracellular transmission is the most probable route, enzymes that are responsible for the with bacteria being shed from open lesions. extensive tissue damage (Thune et al., 1993). In Israel, mortalities of seabream cul- Two forms of vibriosis are recognized. tured in the Red Sea were associated with The first form produces external haemor- isolation from the blood stream of Vibrio rhage and is referred to as the dermatitis alginolyticus, Vibrio parahaemolyticus and form of vibriosis. The second form is less Vibrio anguillarum or anguillarum-like. common and is referred to as gastroenteritis Infection by these microorganisms, how- vibriosis. The latter does not have external ever, was low (Colorni et al., 1981). signs (Muroga et al., 1990; Egusa, 1992). In the dermatitis form of vibriosis, internal Geographical distribution. Vibrios are ubiq- pathology occurs as the disease progresses, uitous in all marine environments and most with congestion and haemorrhage of the are facultative pathogens. The species of liver and enlargement and liquefaction of vibrios involved in diseases reflect regional spleen, liver and kidney. The histopatho- differences. In East and West Asia, the most logical changes are associated with intesti- commonly isolated species are Vibrio ord- nal haemorrhage and destruction of the alii, Vibrio ichithyoenteri, Vibrio trachuri, tunica mucosa. Groupers with sleepy- Vibrio damsela and Listonella (Vibrio) grouper syndrome tend to give out a charac- anguillarum (Kusuda and Kawai, 1997). In teristic strong, foul smell from the abdomen Southeast Asia, V. parahaemolyticus and V. when examined. Biochemical and immuno- alginolyticus are the main species involved logical methods are used for identification, (Wong and Leong, 1986, 1990). but most require culture and isolation of these pathogens. The organisms are Gram- Diagnosis. Vibriosis is characterized by negative rods with motile polar flagella, haemorrhagic septicaemia. The clinical non-capsulated and non-spore producing. signs are capillary congestion and ‘red boils’ They are positive for oxidase and catalase,

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Infectious Diseases of Warmwater Fish in Salt Water 201

and generally ferment a large number of and Salati, 1993; Park and Sohn, 1996; Sako, carbohydrates. 1996).

Prevention and control. Leong et al. (1997) Geographical distribution. The majority of reported that groupers vaccinated against disease outbreaks involving this bacterium vibriosis do not show any sign of sleepy- have been reported in both Mediterranean grouper syndrome. The vaccinated groupers and Red Sea Israeli fish farms (Colorni, 1998), were healthier and grew faster, suggesting as well as in Japan, America and Mediter- that the sleepy-grouper syndrome in grouper ranean countries. This bacterium is affected could in fact be gastroenteric vibriosis. Good by water temperature and the disease tends husbandry practice and adequate nutrition to occur in the summer months with water are essential to prevent the development of temperature between 20 and 25°C. vibriosis. The initial stage of the disease can be treated with a number of sulphur drugs in Diagnosis. Pasteurellosis is a septicaemic feed with good results. The dosage varies − disease with no external signs except between 50 and 200 mg kg 1 fish weight − occasional darkened spots on the body day 1 for 10–20 days (Sano and Fukuda, surface in yellowtail (Kubota et al., 1970a; 1987). Intraperitoneal injection has been Fukuda and Kusuda, 1981). A large number most effective for the treatment of vibriosis of white spots of 0.5–3.5 mm corresponding in adult grouper. to foci of bacterial colonization engulfed by phagocytes is found in the spleen and ‘Pasteurellosis’ kidney, and to a lesser extent in the liver (Kubota et al., 1970a,b, 1972; Egusa, 1992). ‘Pasteurellosis’ is the second most impor- The numbers of macrophages increase in the tant infectious disease in cultured yellow- spleen, kidney, gill and liver, which often tail in Japan. It causes the loss of thousands appear necrotic and enlarged (Figs 6.4 and of tonnes of cultured yellowtail (Sano 6.5). Many bacteria are able to survive in the and Fukuda 1987; Sako, 1996). The route macrophage (Nelson et al., 1989). The dis- of infection is probably oral. Stress is an eased fish rapidly lose their vigour, sink to important predisposing factor to infection. the bottom of the cage and die. Although the aetiological agent was first P. damsela is Gram-negative, non- described by Janssen and Surgalla (1968) motile, usually short (0.5–0.7 × 0.7–2.6 µm), as a member of the Pasteurella genus, its bipolar and pleomorphic (from coccoidal to taxonomic position was later questioned rod-like, depending on the culture and envi- by Gauthier et al. (1995) who placed it in ronmental conditions). A variety of media, the genus Photobacterium and renamed it including yeast peptone agar, brain and Photobacterium damsela subsp. piscicida. heart infusion agar and blood agar contain- However, while confirming that the ing 1.5–2.0% NaCl can be used to isolate the pathogen should be included in the genus bacterium. Colonies are small (1–2 mm in Photobacterium, Thyssen et al. (1998) found diameter) and translucent. no evidence, morphological or biochemical, to justify its classification as a subspecies of Prevention and control. Ampicillin (Aoki Photobacterium damselae. and Kitao, 1985) and florfenicol (Yasunaga and Yasumoto, 1988) have been reported Host range. The seabream in Israel to be effective when administered in feed. (Colorni, 1998) and yellowtail, black This bacterium is known, however, readily seabream, horse mackerel and Japanese to become resistant to antibiotics. Vaccine flounder in Japan and Korea have been preparations also gave satisfactory results reported to be seriously affected by the (Fukuda and Kusuda, 1985; Kusuda and bacterium (Sano and Fukuda, 1987; Kusuda Hamaguchi, 1988; Kusuda et al., 1988).

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202 T.S. Leong and A. Colorni

Fig. 6.4. Enlarged spleen with white spots in seabream, Sparus aurata, typical of ‘pasteurellosis’ by Photobacterium damsela.

Fig. 6.5. Splenic foci of Photobacterium damsela, typical of ‘pasteurellosis’ in seabream, Sparus aurata.

Edwardsiellosis cephalus) (Kusuda et al., 1976a), crimson seabream (Evynnis japonica) (Kusuda et al., Edwardsiellosis, caused by bacteria of 1977), yellowtail (S. quinqueradiata), red the genus Edwardsiella (family Enterobac- seabream (Chrysophrys major) (Yasunaga teriaceae), is a systemic bacterial disease, et al., 1982) and Japanese flounder (P. reported in warm freshwater and marine olivaceus) (Nakatsugawa, 1983). fish. The pathogenesis in cultured marine fish has not been well documented. Two species are involved, Edwardsiella tarda Geographic distribution. E. tarda has a (infecting a variety of both freshwater and worldwide distribution, occurring in both marine fish) and Edwardsiella ictaluri freshwater and marine environments. It (infecting mainly cultured catfish of the causes severe disease problems in a variety genus Ictalurus) (see Chapter 7). of cultured marine fish, mainly in Southeast Asia (see Plumb, 1999). Host range. This bacterial disease has been reported from a large variety of cultured Diagnosis. Edwardsiellosis is characterized marine fish including mullet (Mugil by cutaneous haemorrhagic ulcers, which

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gradually deepen into the muscle forming identified as a Flexibacter sp. (Ruangpan, large necrotic abscesses. Internally, greyish- 1985; Ruangpan et al., 1987). Since 1988, white spots develop in the spleen and disease epizootics have been observed kidney (Kusuda et al., 1977). E. tarda is whenever the seabass fingerlings have been an enteric, Gram-negative motile rod with introduced for culture in netcages through- peritrichous flagella. It grows on media out Southeast Asia (Chong and Chao, 1986; with 0.5–4% NaCl, a temperature range Perngmark, 1992; Leong, 1994). of 15–41°C and a pH level of 5.5–9.0, A disease associated with gliding with small circular transparent colonies bacteria was described in red seabream and (Wakabayashi and Egusa, 1973; Kusuda black seabream in Japan by Masumura and et al., 1976a, 1977; Amandi et al., 1982; Wakabayashi (1977). This disease is similar Yasunaga et al., 1982; Nakatsugawa, 1983; in appearance to columnaris disease of Farmer and McWhorter, 1984; Waltman freshwater fish and the aetiological agent et al., 1986). Little variation in the biochemi- also belongs to the genus Flexibacter. cal and biophysical characteristics existed Wakabayashi et al. (1986) proposed the in 116 isolates from Taiwan and the USA name Flexibacter maritimus for the organ- (Waltman et al., 1986). Traditional diagnosis ism, which has an obligate requirement for of edwardsiellosis involves isolation of the seawater irreplaceable by NaCl alone for bacterium and identification by biochemical growth (Hikida et al., 1979). In Southeast tests. A fluorescent antibody (FA) method Asia, gliding bacteria were reported as and an ELISA have been developed (Kusuda Flexibacter sp. (Danayadol et al., 1984; and Salati, 1993). Ruangpan, 1985; Baxa et al., 1986; Chong and Chao, 1986: Wakabayashi et al., 1986; Prevention and control. Infection of E. tarda Ruangpan et al., 1987; Leong, 1994). can be treated by application of antibiotic Two species of Flexibacter have been medicated feed. Salati (1988) reported that described, F. maritimus from seabream (P. the most effective drug is oxolinic acid, major) (see Wakabayashi et al., 1986) and followed by trimethoprim, oxytetracycline, Flexibacter ovolyticus from Atlantic halibut furazolidone and piromidic acid. Although (H. hippoglossus L.) (see Hansen et al., the bacterium is sensitive to a wide variety 1992). The flexibacter-like bacteria that of antibiotics, strains resistant to chloram- cause tail rot syndrome in cultured marine phenicol, furazolidone and sodium nifur- fish, particularly Asian seabass, have not styrenate have been detected (Aoki et al., been characterized. 1977, 1989; Waltman and Shotts, 1986). Most studies on vaccination against E. Host range. A variety of marine fish tarda have been carried out on eel in Taiwan cultured in cages has been reported to be and Japan (Song and Kou, 1979; Song et al., affected by gliding bacteria. In East Asia, 1982; Salati et al., 1983; Salati, 1985; Salati yellowtail, red seabream, black seabream, and Kusuda, 1985a,b), but overall little Japanese flounder, tiger puffer, grouper research has been carried out on the vac- and grey mullet are susceptible to this cination of cultured marine fish. Salati et al. gliding bacterial disease (Masumura and (1987) showed that vaccination of red Wakabayashi, 1977; Baxa et al., 1986, seabream with formalin-killed cells and 1987a,b; Arthur and Ogawa, 1996; crude lipopolysaccharide (LPS) preparation Lavilla-Pitogo et al., 1996; Liao et al., 1996; of E. tarda enhanced phagocytosis and Park and Sohn, 1996; Sako, 1996; Kusuda increased antibody titres. and Kawai, 1997). In Southeast Asia, caged Asian seabass Gliding bacterial disease/tail rot disease (Fig. 6.6) are most susceptible to tail rot, followed by the mangrove snapper, golden A columnaris disease in Asian seabass was snapper and grouper, though to a lesser reported in Thailand in 1983 (Danayadol extent (Danayadol et al., 1984; Ruangpan, et al., 1984) and the bacterium involved was 1985; Chong and Chao, 1986; Ruangpan

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204 T.S. Leong and A. Colorni

Fig. 6.6. Trail rot syndrome in juveniles of Asian seabass, Lates calcarifer.

et al., 1987; Leong et al., 1992; Perngmark, Prevention and control. It is difficult to 1992). Histopathological study of the tail rot prevent and control the disease in the cage syndrome in Asian seabass has indicated environment. The standard treatment is feed that the onset of the disease is through the medicated with oxytetracycline or a bath in pathogen infection in the tail region and sodium nifurstyrenate. However, the results proliferation in the epidermis and dermis are usually unsatisfactory. A combination of (Perngmark, 1992). freshwater treatment and reduction of stocking density helps to reduce mortality in Geographic distribution. Gliding bacteria of affected seabass (T.S. Leong, unpublished the genus Flexibacter appear to have a data). worldwide distribution. Only F. maritimus has been reported in East Asia. Gram-positive bacteria Diagnosis. In seabream and yellowtail in East Asia, the gliding bacteria first gain entry Two Gram-positive bacteria are of through the damaged caudal fin, where major importance in maricultured fish: the tissues are gradually eroded away by Enterococcus seriolicida and Streptococcus the action of the bacteria. The bacteria then iniae (Kusuda and Salati, 1999). invade the muscular region, the muscles disintegrate and typical tail rot occurs. Streptococcosis No pathological changes are normally observed in the internal organs. The disease The taxonomy of fish streptococci is still usually affects seabream and Asian seabass controversial, but more than one species fry, 2–3 weeks after their introduction into causing a similar syndrome is involved. sea cages. The disease is most severe when farmed F. maritimus is a long slender fish are stressed and water temperature is Gram-negative rod, which exhibits gliding high. The onset of the disease is related to movements on a wet surface. Culture (on the rapid growth of the bacterium in the cytophaga medium) requires at least 30% intestine where both extracellular and intra- seawater, which cannot be replaced by NaCl. cellular toxins are produced (Kusuda et al., Colonies are pale yellow. 1978; Kimura and Kusuda, 1979, 1982).

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Infectious Diseases of Warmwater Fish in Salt Water 205

Kusuda and Hamaguchi (1989) showed that Diagnosis. The clinical signs vary depend- the former have haemolytic activity and ing on the fish species affected. In tilapia, the latter leucocidal activity. The disease S. iniae infection produces panophthalmitis is transmitted by contact (Robinson and and meningitis with only minor pathologi- Meyer, 1966), but feed may also be a source cal changes in other organs (Eldar et al., of infection (Taniguchi, 1983). 1995). In red drum, clinical signs include lethargy, loss of orientation, protrusion of the eye with clouding of the cornea and Host range. A large variety of freshwater erosion of the skin (Eldar et al., 1999). Other and marine fish species has been reported to common signs are darkening of the body, be susceptible to Streptococcus spp. The erratic swimming, haemorrhage in the intes- farmed species affected by streptococci are tine, liver, spleen and kidney, and abdomi- grouper and rabbitfish in Southeast Asia nal distention. Necrosis in the heart, gill, (Chong and Chao, 1986; Leong, 1994), and skin, spleen and eye have also been reported yellowtail, red seabream, Japanese flounder, (Egusa, 1992). Japanese seaperch, rockfish and horse Confirmation of the diagnosis requires mackerel in East Asia. culturing the pathogen, preferably on a In Israel, Streptococcus spp. have been blood-enriched medium. Pathogen presence isolated from European seabass, tilapia can also be confirmed through direct or indi- (Oreochromis mossambicus) adapted to sea- rect fluorescent antibody methods (Kusuda water and red drum. This last isolate was and Kawahara, 1987; Kawahara et al., 1989). identified as S. iniae (Eldar et al., 1999). Recent studies have placed some isolates in the genus Enterococcus (Kusuda et al., 1991; Geographic distribution. Streptococcosis is Kusuda and Salati, 1999). Streptococcus spp. not confined to warm water, and both fresh- (Fig. 6.7) are non-motile, Gram-positive, water and marine species can be affected. spherical to ovoid-shape cells, less than µ Heavy losses have been reported in 2 m in diameter. When grown in liquid yellowtail, horse mackerel and Japanese media, they occur in pairs or form short flounder in Japan (Kusuda et al., 1976b; chains (Kusuda and Kawai, 1982; Kusuda Kitao et al., 1979; Sako, 1996) but this et al., 1991). Most are facultative anaerobes, disease has been known to occur in a without endospores, while some form cap- variety of fish in Australia, Italy, Israel, sules. Streptococci can be isolated from South Africa and the USA (see Austin and diseased fish using brain heart infusion Austin, 1993). In Israel, severe mortalities agar with or without 1.5–2% NaCl. were recorded among the red drum cultured in cages on the Mediterranean coast (Eldar Prevention and control. Control is mainly et al., 1999). by chemotherapy. Antibiotic treatment with

Fig. 6.7. Streptococcus iniae from seabass, Dicentrarchus labrax.

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206 T.S. Leong and A. Colorni

erythromycin, spiramycin and josamycin S. aurata), grouper (Epinephelus aeneus) has proved effective (Kashiwagi et al., and tilapia (O. mossambicus). Of these, only 1977a,b; Shiomitsu et al., 1980; Kusuda and S. rivulatus and M. cephalus are native to the Onizaki, 1985; Kusuda and Takemaru, 1987; Red Sea. Takemaru and Kusuda, 1988a,b,c, 1990). Geographic distribution. Fish mycobacter- iosis is not restricted to warm seas, but is Acid-fast bacteria widespread throughout the world in both marine and freshwater environments. Differ- Mycobacteriosis ent endemic strains of M. marinum exist, specific to geographic regions (Colorni et al., The aetiological agents of mycobacteriosis, 1996). Mycobacterium marinum and other Myco- bacterium spp., cause systemic, chronic Diagnosis. The disease follows a chronic infections in fish and other aquatic animals, course and remains asymptomatic for a long and can occasionally cause skin ulcers in time. Superficial ulcers and exophthalmia humans. are often the only external signs. Spleen and kidney, however, are severely affected and Host range. Since its first isolation from are enlarged with granulomatous lesions the European seabass in 1990 in Eilat (Red that appear macroscopically as whitish Sea, Israel) (Colorni, 1992), M. marinum has nodules (Fig. 6.8). In advanced cases these been detected in at least 18 other species of lesions spread to liver, heart, mesentery, etc. local fish and may have spread from sea Special media (such as Löwenstein–Jensen cages to other farmed and native species or Middlebrook) are required for the culture in the Gulf of Eilat (Diamant and Colorni, of these mycobacteria, whose growth is usu- 1995). The commercial species found to be ally slow (2–3 weeks for the first colonies to infected are seabream (S. aurata), striped become visible). A Ziehl–Nielsen stain bass (Morone saxatilis), sheepshead (sharp- reveals the typical slender acid-fast rods snout) (Puntazzo puntazzo), red drum (Fig. 6.9). (S. ocellatus), rabbitfish (Siganus rivulatus), mullet (M. cephalus), red seabream (P. Prevention and control. There is no effec- major), hybrid red seabream (P. major × tive control.

Fig. 6.8. Extremely enlarged granulomatous spleen of seabass, Dicentrachus labrax, infected with Mycrobacterium maritimus.

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Infectious Diseases of Warmwater Fish in Salt Water 207

(Kusuda and Taki, 1973; Kusuda et al., 1974). It produces flat, wrinkled colonies after 10 days at 25°C. N. kampachi does not grow at 37°C.

Prevention and control. There is no effective therapy for this disease. The route of infec- tion in fish is not known, but is probably through direct contact or contaminated food. A clean environment is an important factor in preventing the occurrence of the disease. Fig. 6.9. Mycobacterium marinum in seabass, Kusuda and Nakagawa (1978) showed that N. kampachi can survive for more than Dicentrachus labrax (Ziehl–Neelsen stain). − 90 days in the presence of 100 mg l 1 fish extracts, but only 2 days in open seawater. Nocardiosis

Nocardiosis is a chronic bacterial disease that affects both freshwater and marine fish. Diseases Caused by Protistans In Japanese yellowtail, amberjack and striped jack it is caused by Nocardia A large, heterogeneous group of pathogenic kampachi (Kariya et al., 1968; Kawatsu one-cell organisms are associated with fish. et al., 1976; Sako, 1996). Some are ectoparasites while others are endoparasites. Many of these organisms are Host range. N. kampachi appears to be not selective in their host preferences and restricted to yellowtail, amberjack and can cause severe damage to any marine fish striped jack (Kariya et al., 1968; Kubota in intensive culture. Others may coexist et al., 1968). with their host as epicommensals or as facultative parasites. The obligate parasitic Geographic distribution. Norcadiosis species are host-specific, thus better adapted caused by N. kampachi is restricted to to coexist with their host causing limited East Asia, primarily where yellowtails are harm (Lom, 1984). The endoparasites may cultured. considerably alter the appearance, taste and odour in the affected fish. Diagnosis. Many clinical characteristics of nocardiosis are similar to mycobacteriosis. The disease occurs sporadically during Myxosporean infections autumn but outbreaks can extend from July to February. Early signs of infection include Myxosporeans are endoparasites that can anorexia, inactivity, skin discoloration and reside either in visceral cavities such as emaciation. In the late stages, nodular skin the gallbladder, swimbladder and urinary lesions may ulcerate or extend to skeletal tract (coelozoic species), or settle as inter- muscle and visceral organs, causing abdomi- or intracellular parasites in blood, muscle nal distension. or connective tissue (histozoic species). The morphology of Nocardia varies, but Spores with four polar bodies in the stellate cells are generally filamentous, branched or arrangement typical of the genus Kudoa beaded. The bacterium is acid-fast and can (6.4–13.6 µm in length) have been found grow on a variety of media containing carbon in the viscera of seabream cultured in the and nitrogen sources. It can be isolated on Red Sea (Paperna, 1982). This histozoic brain heart infusion agar (BHIA), tryptone myxosporean may have originated in the soya agar (TSA) and nutrient agar (NA), with Mediterranean Sea and been introduced optimum growth temperature at 20–30°C into the Red Sea with infected seabream.

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208 T.S. Leong and A. Colorni

The parasite causes relatively benign infec- Infections by ciliates tions, usually limited to a few individuals. A debilitating myxosporean disease was Brooklynellosis described in S. aurata by Diamant (1992) and Diamant et al. (1994). The aetiological Brooklynella hostilis is a ciliate protozoan agent, Myxidium leei, is a histozoic species that was first described in aquarium fish by that settles in the intestinal mucosa. In heavy Lom and Nigrelli (1970) as a gill pathogen. infections, fish present an enlarged abdo- However, B. hostilis can also cause serious men, with the intestinal tract filled with skin lesions (Noga, 1996). In heavy infec- purulent, foul-smelling liquid. Histologi- tions the ciliates destroy the host’s surface cally, small plasmodia (22 µm average size), tissue with their cytopharyngeal armature, which each give rise to two spores, are feeding on tissue debris, ingesting blood detected between the epithelial cells of the cells and causing haemorrhage in the gills mucosa along the entire intestinal tract. (Lom and Dyková, 1992). As the same parasite was later discovered in other Mediterranean sparids and grey Host and geographic distribution. European mullets (Lom and Bouix, 1995), M. leei too seabass (D. labrax) and lutjanids cultured was probably imported with its host into the in Martinique suffered heavy infestations Red Sea. Recently, Diamant (1997) demon- of this parasite (Gallet de Saint Aurin strated that transmission of this organism et al., 1990). B. hostilis has been detected does not require an intermediate host. repeatedly in mariculture facilities in Another histozoic myxosporean, S. Kuwait and Singapore (Lom and Dyková, epinepheli, was described in the urinary 1992). Recently, it was diagnosed in cage- system of adult groupers (E. malabaricus) cultured seabream (S. aurata) in the Red Sea from Southeast Asia (Supamattaya et al., (Diamant, 1998). 1990, 1993). Presporogonic stages, round to oval in shape (1.98–10.75 µm), carried Diagnosis. B. hostilis is recognizable by in the blood stream, settle in the kidney its oval, dorsoventrally flattened shape, tubules where sporogenesis occurs. Mature notched oral area and size, measuring spores, subspherical to spherical in shape 36–86 × 32–50 µm (Lom and Dyková, 1992). (7.8–10 µm in length, 12.3–14.5 µmin µ thickness, 7–9.5 m in width) present two Prevention and control. There are no repor- round polar capsules. The epithelium of ted methods for caged fish. the renal tubules harbouring the parasites appears highly vacuolated. The life cycle Cryptocaryonosis of myxosporean parasites from marine hosts is unknown, but as Diamant (1997) Cryptocaryonosis is a disease caused by demonstrated for M. leei, the notion that an the holotrich ciliate, Cryptocaryon irritans, intermediate host is indispensable for the a parasite belonging to the class Colpodea completion of the myxosporeans’ life cycle (order Colpodida) (Diggles and Adlard, needs to be revised. 1995). Only one species, C. irritans,is A Sphaerospora-like myxosporidean reported for the genus. However, intra- was reported to have caused a high cumu- specific variants exist (Diamant et al., 1991; lative mortality (90%) in cultured cobia, Colorni and Diamant, 1993; Diggles and Rachycentron canadian (L.), in Taiwan Lester, 1996b; Diggles and Adlard, 1997). (Chen et al., 2001). The extrasporogonic The ciliate invades the skin, eyes and gills and/or sporogonic stages appeared in the of a suitable host, impairing the physio- blood, glomerulus, renal tubules and renal logical functions of these organs. Its life interstitium. Matured spores with polar cycle is quadriphasic and includes a para- filaments were elongated or spherical, sitic phase on the fish (trophont), during with numerous refractile granules in the which Cryptocaryon feeds and can be cytoplasm. observed continuously revolving in the

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Infectious Diseases of Warmwater Fish in Salt Water 209

fish epithelia. After growing for 3–7 days logistically feasible, the cages should be to a maximum size of 300–400 µm, the moved into an area where sufficient depth parasite spontaneously leaves its host and currents prevent the theronts from rein- (as a protomont) and within several hours fecting the fish (Colorni, 1987). encysts and starts dividing (tomont), even- tually producing up to 200 free-swimming infective stages (theronts). Sizes and num- Diseases Caused by Metazoans bers of theronts vary with the geographic locations, fish host species and water Monogenea temperature (Colorni and Burgess, 1997). The theront life span is approximately 24 h, The monogeneans are gill and skin flukes but its infectivity rapidly decreases after the frequently encountered in mariculture sys- first 6–8 h post-excystment (Yoshinaga and tems. Most monogeneans are host-specific, Dickerson, 1994; Diggles and Lester, 1996a). but some species have a wide host range. Monogeneans are hermaphroditic. Their Host range. This ciliate protozoan shows direct life cycle, together with the availabil- low host specificity and is capable of infect- ity of constantly stressed fish hosts in high ing most marine teleosts. Host susceptibil- stocking density environments, facilitates ity, however, may vary (Nigrelli and fish-to-fish infestation (Paperna et al., 1984; Ruggieri, 1966; Wilkie and Gordin, 1969; Leong and Wong, 1987; Cone, 1995). Colorni, 1985). Grouper cultured in marine cages in Hong Kong were susceptible to the Capsalid monogeneans protozoan infection; other fish species were not (ADB/NACA, 1991). Cultured grouper, Capsalid monogeneans are generally found snapper and Asian seabass fingerling are on the fish skin and under the scales, while susceptible to this protozoan during the a few are found on the gills. They can move early stage of cage culture (Chong and Chao, actively on the body surface, feeding on 1986; Glazebrook and Campbell, 1987; epithelial cells and mucus. The body of Leong, 1994). these parasites is relatively large and flat, with a conspicuous muscular disc haptor at Geographic distribution. Although typical the posterior end (Fig. 6.10). The haptor of tropical seas, this parasite has a world- may be subdivided by septa. At the anterior wide distribution that extends well into tem- end is a pair of large disc-like adhesive perate environments (Diamant et al., 1991). organs. The intestinal caeca are diverticular and end blindly. Three genera, Benedenia, Diagnosis. The parasite burrows into the Neobenedenia and Megalocotyloides, are fish epithelia and appears macroscopically commonly found infecting marine fish as pinhead-size whitish ‘blisters’, more con- cultured in floating net cages (Table 6.4). spicuous on coloured fish and on the trans- lucent parts of the fins. Heavily infested fish Host range. The capsalid monogeneans may frequently come to the surface, gasping have been reported from a wide host range in for oxygen. Mucus production increases. A the wild (Yamaguti, 1963; Paperna et al., definitive diagnosis of cryptocaryonosis can 1984), in cultured marine fish and in marine be made from the examination of a gill clip aquarium fish (Nigrelli, 1943; Paperna and or a wet mount of fin or skin scraping for Overstreet, 1981; Leong and Wong, 1987; the presence of the large, revolving ciliate Ogawa et al., 1995a,b; Hla Bu et al., 1998). protozoans. High mortalities associated with heavy infestation of Benedenia epinepheli (Ogawa Prevention and control. The presence of et al., 1995a) were reported in Japanese floun- C. irritans in cage-cultured fish means that der (P. olivaceus) in Shimane Prefecture and the cages are kept in too shallow waters. If in black rockfish (Sebastes schlegeli) (with

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210 T.S. Leong and A. Colorni

Fig. 6.10. Capsalid monogenean commonly found on cultured marine fish.

an intensity of 900–1500 worms per fish) in B. epinpheli and Neobenedenia girellae). Yamaguchi Prefecture. Ogawa et al. (1995b) Both B. epinpheli and N. girellae were reported that 100% mortality of juvenile found to be equally distributed on the amberjack (Seriola rivoliana) in Okinawa greasy grouper (E. coioides) and the Asian was associated with N. girellae. seabass (L. calcarifer). In general, serranid, Some capsalid monogeneans appear sparid and lutjanid fish appear to be more to have low host specificity. For example, susceptible than other species. In the golden Ogawa et al. (1995a) reported that B. snapper (Lutjanus johni)upto60B. lutjani epinepheli was found in 25 fish host species, per infected host were counted. Tilapia cul- with tetraodontid fish being most sus- tured in cages in the marine environment ceptible, as up to 3000 individuals of B. were heavily infested by Neobenedenia epinepheli were recovered from a single melleni in Hawaii and in the West Indies individual in Japan. In Malaysia, 13 species (Kaneko et al., 1988; Robinson et al., 1989; of cultured marine fish were found with Gallet de Saint Aurin et al., 1990; Hall, capsalid monogeneans (Benedenia lutjani, 1992).

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Infectious Diseases of Warmwater Fish in Salt Water 211

Geographic distribution. The capsalid The active feeding of the monogeneans monogeneans have a wide distribution pat- on mucus and epithelial cells leads to tern (Table 6.5). More benedenid species haemorrhage, inflammation and mucus have been reported from the East Asia region hyperproduction (Paperna, 1991; Egusa, than from other regions. This is probably due 1992). The monogeneans often settle on not only to a greater variety of fish species and around the eyes, damaging the cornea cultured, but also to the availability there of and causing blindness (Egusa, 1992; Ogawa more diagnostic facilities. et al., 1995a; Colorni, 1998). Cultured fish infested with capsalid monogeneans gradually withdraw from Prevention and control. The capsalid mono- the group, quit eating and their bodies geneans are found on a large variety of wild gradually darken. Heavily infected fish fish and it is difficult to prevent and control swim erratically and rub against the net, them in the cage environment. Despite their which results in dermal ulceration and size (up to a few mm) the monogeneans subsequent bacterial invasion. may go unnoticed. Whenever logistically

Table 6.4. Capsalid monogeneans found in various cultured marine finfish.* Fish species

Capsalid species 1 2 3 4 5 6 7 8 9 10 11

Benedenia epinepheli + + + + + + + + + − − B. hoslinai − − − − − − − − − − + B. lutjani + + + + + + + − − − − B. monticelli − − − − − − − − + − − B. seriolae − − − − − − − − − − + Benedenia spp. + + − + + + + − − − − Neobenedenia girellae + + + + − − − − − + + N. melleni − − − − − − − − + + − Neobenedenia sp. + + − + + + + − − − − Megalocotyhoides + + − − − − − − − − − epinepheli M. convoluta + − − − − − − − − − −

(1) Epinephelus coioides; (2) E. malabaricus; (3) E. bleekeri; (4) Lutjanus johni; (5) L. argentimaculatus; (6) Lates calcarifer; (7) Pinjalo-pinjalo; (8) Pagrus major; (9) Liza and Mugil spp.; (10) Prepchromis spp.; (11) Oplegnathus fasciatus. *Many more cultured marine finfish susceptible to capsalids are not listed here.

Table 6.5. Geographical distribution of various benedenid species in cultured marine fish. Benedenid species East Asia Southeast Asia West Asia

Benedenia epinepheli + + − B. monticelli − − + B. seriolae + − − B. lutjani − + − B. hoshinai + − − Benedenia spp. − + − Neobenedenia girellae + − − N. melleni + − + Neobenedenia sp. − + − Megalocotyloides epinepheli + + + M. convoluta + + −

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212 T.S. Leong and A. Colorni

feasible, a freshwater dip of 3–5 min should Host range. The diplectanid monogeneans be made to dislodge the parasites from have been reported from a wide variety the host (Leong, 1997; Zafran et al., of fish hosts (Beverly-Burton and Suraino, 2000). The treatment kills the parasites, 1981; Kritksy and Beverly-Burton, 1986; which turn white and become more visi- Leong and Wong, 1987; Hla Bu et al., 1999). ble. Ellis and Watanabe (1993) reported In the tropical environment, they are com- that the egg, juvenile and adult stage of monly found on cultured serranids, sparids N. melleni in cultured tilapia could be and centropomids (Table 6.6). − eliminated in a 5 day hyposalinity (15 g l 1 ) Diplectanid species are very host- treatment. Tropical cleaner-fish, such as specific and do not infect other fish species. the wrasse (Thalassoma bifasciatum) and Pseudorhabdosynochus epinepheli, Pseudo- gobies (Gobiosonia genie, G. ocenops have rhabdosynochus lanteuensis, Pseudorhab- been used to control N. melleni infecting dosynochus coioidesis and Diplectanum seawater-cultured tilapia (Cowell et al., grouperi are found only in serranids, whereas 1993). Pseudorhabdosynochus lateis, Pseudorhab- dosynochus monosquamodisci and Diplec- Diplectanid monogeneans tanum penangi (Fig. 6.11) are found only in centropomids. Diplectanids are not known Diplectanid monogeneans are found only to infect cultured lutjanid fish. on the gills of fish hosts, feeding on mucus. Two genera of diplectanids are found to Geographic distribution. The geographic infest cultured marine finfish: Diplectanum distribution of diplectanid monogeneans in and Pseudorhabdosynochus. cultured marine fish is shown in Table 6.7.

Table 6.6. Diplectanid monogeneans found in various cultured marine finfish. Fish species

Dicentrarchus Epinephelus E. E. Lates Diplectanid species labrax coioides malabaricus bleekeri calcarifer

Pseudorhabdosynochus − + + + − epinepheli P. lanteuensis − + + − − P. lateis − − − − + P. monosquamodisci − − − − + P. coioidesis − + + + − Diplectanum penangi − − − − + D. grouperi − + + + − D. aequans + − − − − D. laubieri + − − − −

Table 6.7. Diplectanid monogeneans found in various culture locations. Diplectanid species East Asia Southeast Asia West Asia

Pseudorhabdosynochus epinepheli + + − P. lanteuensis + + − P. lateis − + − P. monosquamodisci − + − P. coioidesis + + − Diplectanum penangi − + − D. grouperi − + − D. aequans − − + D. laubieri − − +

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More diplectanids are reported in cultured Diagnosis. Fish infected with diplectanid marine fish from Southeast Asia but due to monogeneans do not show conspicuous the numerous transfers of live fish from one signs; haemorrhage, hyperplasia and fusion region to another, similar reports are to be of lamellae at the points of attachment expected from East Asian regions, where are commonly observed (Oliver, 1977; many exotic marine finfish were recently Giavenni, 1983; Hla Bu and Leong, 1997). imported by fish farmers. The body of diplectanid monogeneans is elongated and characterized by a large flat haptor with squamodiscs at the posterior end.

Prevention and control. It is difficult to prevent the introduction of diplectanids into the culture system, especially when fingerling and juvenile fish are obtained from the wild. Freshwater treatment, which works effectively on benedenids, is not effective against diplectanids. The popula- tion size of diplectanids may be controlled in culture systems through appropriate stocking density of the fish in each cage.

Dactylogyrid monogeneans

Dactylogyrid monogeneans are parasites on the gills of cultured snapper. They are mucus feeders. One genus, Haliotrema, has been reported from cultured lutjanids (Leong and Wong, 1987, 1989; Liang and Leong, 1992; Leong, 1994).

Host range. The monogeneans found in various cultured marine finfish are shown in Table 6.8. They show restricted infectivity of Fig. 6.11. Diplectanum penangi, a monogenean fish host and are found mainly on lutjanid worm infecting the Asian seabass, Lates calcarifer. fish, with the exception of Haliotrema

Table 6.8. Dactylogyrid monogeneans found in various cultured marine finfish. Fish species

Dactylogyrid species 1 2 3 4 5

Haliotrema johni + + + − − H. noncalcaris − + − − − Haliotrema sp. A + + − − − Haliotrema sp. B + + − − − Haliotrema sp. C − + − − − Haliotrema sp. E − + − − − Haliotrema sp. F + − − − − Haliotrema sp. − − + − − Haliotrema epinepheli − − − − +

(1) Lutjanus johni; (2) L. argentimaculatus; (3) L. russelli; (4) Pinjalo-pinjalo; (5) Epinephelus coioides.

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214 T.S. Leong and A. Colorni

epinepheli, which is found on serranids as Geographic distribution. The dactylogyrids well. are commonly found in golden and man- There are nine known species of grove snapper cultured in Southeast Asia dactylogyrids found in various species of and in East Asia (Hong Kong). cultured marine snappers, all belonging to the genus Haliotrema (Table 6.8). The mean Disease signs and pathology. Moderate intensity of infection of Haliotrema johni infection of dactylogyrids in cultured finfish (Fig. 6.12) in cultured golden snapper (L. does not show significant clinical signs. johni) (mean range of 162–409 per fish) was In heavy infection, however, the forehead found to be an order of magnitude higher of the golden snapper is often devoid of than that in wild snapper (33 per infected scales and with epidermal lesions from the fish) (Leong and Wong, 1989). Furthermore, repeated rubbing against the net in response the prevalence and mean intensity of infec- to the irritative action of the parasite (Chong tion of H. johni in cultured disease finger- and Chao, 1986). The histopathology of ling golden snapper (90–97%; 107–314 per dactylogyrids on cultured marine finfish infected fish) were much higher than those has not been reported. in wild golden snapper (8–60%; 13–29 per infected fish) (Leong and Wong, 1987). In Prevention and control. It is not possible to Penang, Malaysia, Haliotrema noncalcaris prevent fish from being infected by these was found in all cultured mangrove snapper monogeneans. Reducing stocking density (Lutjanus argentimaculatus), with a mean of juveniles in the cage would probably range intensity of 45–58 per infected fish. reduce the build-up of population size of Both Haliotrema sp. A and Haliotrema sp. B monogeneans in the fish. In heavily infected were also dominant numerically in both golden snapper, a formalin treatment of golden and mangrove snappers (Liang and 300 ppm for 30 min significantly reduces Leong, 1992). H. johni (48%) and Haliotrema sp. (78%), while treatment with fresh water reduced Haliotrema sp. by 91% (Liang and Leong, 1992). Dipterex and malachite green were found to be ineffective in reducing the popu- lation size of these monogeneans (Liang and Leong, 1992).

Microcotylid monogeneans

Microcotylid monogeneans are gill para- sites in which the haptor has numerous clamps that are important for taxonomic identification. Some clamps are situated on long stalks, while others are found on the body surface at the posterior end. The mouth of microcotylids is adapted for blood sucking.

Host range. The microcotylid monogen- eans have been reported on a wide range of hosts in the wild (Yamaguti, 1963) and on cultured marine fish (Paperna, 1991; Egusa, 1992). The microcotylids reported in cul- Fig. 6.12. Haliotrema johni, a monogenean infect- tured marine fish are shown in Table 6.9. ing cultured golden snapper (Lutjanus johni). Only a few of the many species of cultured

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Infectious Diseases of Warmwater Fish in Salt Water 215

Table 6.9. Microcotylid monogeneans found in various cultured marine finfish. Microcotylid species Fish host Culture sites

Bivagina tai Pagrus major East Asia Choricotyle elongata Pagrus major East Asia Heterobothrium okamotoi Pagrus major East Asia H. tetradonis Takifugu rubripes East Asia Heteraxine heterocerca Seriola quiqueradiata East Asia Metamicrocotyle cephalus Mugil spp. West Asia Microcotyle mugilis Mugil spp. West Asia Microcotyle sp. Lutjanus russelli East Asia M. chrysophryei Sparus aurata West Asia M. labrachis Dicentrarchus labrax West Asia Polylabris sp. Siganus spp. West Asia

fish have been reported to be infected by induce hatching between 10 and 28°C the microcotylids, which display a certain (Matsusato, 1968). The spawning period of degree of host specificity. Bivagina tai extends from November to January and eggs hatch in approximately ° Geographic distribution. The geographic 8.5 days at 18.5–19.5 C (Fujita et al., 1969). distribution of microcotylid monogeneans is shown in Table 6.9. None of them has been Prevention and control. Preventing the found in Southeast Asia. introduction of microcotylid monogeneans into cage culture systems is difficult when- Disease signs and pathology. Cultured ever wild juvenile marine finfish are used marine finfish infected by microcotylids do for stocking. Finfish infected with microco- not always show clinical signs. There were tylids have been successfully removed with few or no pathological changes in grey immersion in hyposaline water (Okamoto, mullets, European seabass and gilthead sea- 1963; Akazaki et al., 1965; Fujita et al., bream infected with microcotylids (Paperna, 1969), sodium pyrophosphate–hydrogen 1991). Conversely, in other cultured fish, peroxide but not by oral administration of such as yellowtail and red seabream, mortal- bithionol (Okamoto, 1963; Akazaki et al., ity in the cages has been directly attributed 1965; Fujita et al., 1969). In addition, to the heavy infestation of these flukes. freshwater immersion was successful in An average of 85 Heteraxine heterocerca removing Choricotyle sp. in seabream were counted per infected yellowtail (Egusa, (Egusa, 1992). 1992). A large amount of mucus is secreted when the parasite is present in high num- bers, gill filaments are destroyed, and haem- Sanguinicolid digeneans orrhage due to parasite feeding activity can cause severe anaemia (Egusa, 1992). Par- Digenean species are endoparasitic and asitized fish often suffer from a concurrent require one or more intermediate hosts bacterial infection. (mostly snails) for the completion of their The microcotylids have a flat body life cycle. The first larval stage emerging and are relatively large, reaching 17 mm in from an egg (miracidium) is ciliated and H. heterocerca on yellowtail and 20 mm free-swimming and develops into the sporo- in Heterobothrium tetradonis on puffer fish cyst and redia stages, eventually producing (Egusa, 1992). Very little is known about cercariae and metacercariae. The parasite is their development. The optimum tempera- most lethal, particularly to juveniles, when ture for eggs of H. heterocerca to hatch is the metacercariae migrate within the fish 18–25°C. At 25°C, approximately 4 days are body. The adult digeneans live in piscivore necessary but it was found possible to birds.

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216 T.S. Leong and A. Colorni

Only digenean species belonging to the corventum, with a mean intensity of eight family Sanguinicolidae have been reported per fish (Harisson, 1995). to cause mortality in cultured marine finfish (Ogawa and Egusa, 1986; Herbert et al., 1994; Geographic distribution. The few sanguini- Ogawa and Fukudome, 1994; Harisson, colids are reported to show a limited geo- 1995). Heterophyiid metacercariae have also graphical distribution, in accordance with been reported in the muscles of marine fish, that of their host (Table 6.10). Paradeonta- particularly in the mullets (Liza spp. and cylix spp. are found in East Asia, whereas Mugil spp.) (Egusa, 1992). Cruoricola sp., Pearsonellum sp. and Car- The infective stage of sanguinicolids dicola sp. are found in Southeast Asia. penetrates the fish host eventually gaining Without any doubt, however, increased entry and settling into the vascular system. awareness will widen the geographic distri- The flukes as well as their eggs are normally bution as well as the variety of hosts in found obstructing the blood flow in the gill which these worms have been detected. arteries, ventral aorta and the heart.

Diagnosis. Host range. The sanguinicolids reported in No particular signs are observed various cultured marine finfish are shown in in fish infected with sanguinicolids, except Table 6.10. So far, only cultured carangid that the fish die with open mouth and flared (Seriola sp.), seabass, grouper and snapper opercula (Ogawa and Fukudome, 1994). have been reported to be infected with four Field observations indicate that affected fish genera of sanguinicolids, comprising five gasp for oxygen and die soon after being fed, species. Surveys by Ogawa et al. (1989, suggesting that they require more oxygen 1993) and Ogawa and Fukudome (1994) when actively competing for food (Ogawa revealed that nearly all the cultured et al., 1989). Heart and gills are the main Seriola spp. examined were infected by organs affected by the sanguinicolids. In the Paradeontacylix spp. All seabass from Pulau gills, hyperplasia is extensive, especially in Ketam, Selangor, Malaysia, larger than 10 g the area around encapsulated eggs, resulting were found to be infected by Cruoricola lates in lamellar fusion. Eggs lodged in the heart (Herbert et al., 1994), while 63% of 19 tissue may form nodules, most of them in the examined seabass weighing between 18 and ventricle, where muscle cells atrophied, but 1073 g in Penang were infected (Harisson, did not become necrotic (Ogawa et al., 1989). 1995). According to Herbert et al. (1994), the majority of C. lates are found in the venules Prevention and control. There are no known around the stomach, pyloric caeca, intestine methods for controlling sanguinicolids in and excretory bladder. In Penang, 70% of fish cultured in cages. Fish caught in the cultured greasy grouper (E. coioides), with a wild become infected in their natural weight range between 52 and 364 g, were habitat. As all seabass fingerlings cultured infected by the sanguinicolid, Pearsonellum in Southeast Asia are hatchery-produced,

Table 6.10. Sanguinicolid blood flukes in cultured marine fish according to geographical location. Fish host

Seriola Lates Epinephelus Lutjanus Cultured Parasite quinqeradia calcarifer coioides spp. site

Paradeontacylix grandispinnis + − − − East Asia P. kampachi + − − − East Asia Cruoricola lates − + − − Southeast Asia Pearsonellum corventum − − + − Southeast Asia Cardicola sp. − − − + Southeast Asia

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Infectious Diseases of Warmwater Fish in Salt Water 217

C. lates infects the fish once they are moved 6.11. The only branchiuran reported is into the cages. Argulus sp. infecting grey mullet (M. cephalus), milkfish (C. chanos) and Asian seabass (L. calcarifer) (Paperna and Over- street, 1981; Chong and Chao, 1986; Arthur Diseases Caused by Crustaceans and Ogawa, 1996). A. scutiformis was reported from Takifugu rubripes (Egusa, Crustaceans belonging to the Branchiura, 1992). The life history of marine argulids Copepoda, Isopoda and Amphipoda are has not been reported. frequently found on the body surface Most of the copepods reported are and/or gills of caged marine fish. Some, like caligids, which could cause epizootics in Argulus spp., glide freely on the body sur- the farms. A large population of yellowtail face, while others anchor themselves to the was infected with Caligus spinosus, which host. caused serious injuries to the fish host They do not require an intermediate in Japan (Fujita et al., 1968), and Caligus host for their transmission. The mature patulus in milkfish cultured in the Philip- female lays eggs, which develop into free- pines (Lavina, 1977; Jones, 1980; Lin, 1989). living nauplii and copepodid larval stages. In Malaysia, cultured groupers (E. coioides All larval stages undergo several moultings and E. malabaricus) are often infested by from one stage to another before metamor- Caligus spp., which are also found in cul- phosing into adults in a suitable fish host. tured snapper and seabass, and by Ergasilus borneoensis (see Leong and Wong, 1988; Host range. The number of parasitic crusta- T.S. Leong, unpublished data). Izawa (1969) ceans reported from cultured marine finfish reported that the developmental stages of are relatively few and are shown in Table C. spinosus in cultured yellowtail included

Table 6.11. Parasitic crustaceans found in cultured marine finfish. Parasite crustacean Fish host Cultured site

Alcirona insularis Epinephelus sp. Caribbean Aega sp. Lates calcarifer Southeast Asia L. calcarifer Southeast Asia Chanos chanos Southeast Asia Argulus scutiformis Mugil cephalus Caribbean Takifugu rubripes East Asia Caligus spinosus Seriola quinqueradiata East Asia C. patulus Chanos chanos Southeast Asia Caligus sp. Epinephelus coioides, L. calcarifer, Lutjanus johni Southeast Asia Ergasilus borneoensis E. coioides Southeast Asia Elaphognathia sp. M. cephalus West Asia Gnathia sp. L. calcarifer Southeast Asia C. chanos Southeast Asia L. johni Southeast Asia Gnathia piscivora M. cephalus West Asia Lemathropus latis L. calcarifer Southeast Asia Lernaea cyprinacea C. chanos Southeast Asia Nerocila sp. E. coioides, L. calcarifer, L. johni Southeast Asia Pseudocaligus apodus M. cephalus West Asia P. fugus T. rubripes East Asia Jassa sp. E. coioides, L. calcarifer, L. johni Southeast Asia Microjassa sp. E. coioides, L. calcarifer, L. johni Southeast Asia Lembos sp. E. coioides, L. calcarifer, L.johni Southeast Asia Stenothole sp. E. coioides, L. calcarifer, L. johni Southeast Asia

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218 T.S. Leong and A. Colorni

two nauplius stages, one copepodid stage, borneoensis and Asian seabass infested with three chalimus stages and two juvenile Lernathropus latis. stages before the copepod metamorphosed Mortalities caused by copepods have into an adult. been reported for Caligus spineus on yellow- The isopod, Nerocila sp., has been tail in Japan (Fujita et al., 1968), Pseudo- found in grouper, seabass and snapper in caligus apodus on grey mullets in Israel Singapore and Malaysia, whereas Aega sp. (Paperna and Lahav, 1974), Caligus patulus has been detected in seabass in Thailand in milkfish in the Philippines (Lavina, 1977) (Chong and Chao, 1986; Ruangpan, 1988) and Pseudocaligus fugus in puffer fish in Larval stages of gnathiid isopods were also Japan (Arthur and Ogawa, 1996). frequently encountered in grouper, seabass, The isopod, Aega sp., caused mortality milkfish and mullets (Paperna and Por, in juvenile Asian seabass L. calcarifer in 1977; Leong and Wong, 1988). Thailand (Ruangpan, 1988) and an unidenti- The amphipods, Lembos sp., Microjassa fied isopod on yellowtail in Japan (Kubota sp., Jassa sp. and Stenothol sp., are found in and Takakuwa, 1963). The larval stages of grouper, seabass and snapper cultured in gnathiid isopods have been found in Asian Malaysia (Leong et al., 1998). seabass, snapper and milkfish in Malaysia and Thailand (Leong and Wong, 1988) and Geographic distribution. As indicated in Gnathia piscivora in mullets in Israel Table 6.11, parasitic crustaceans, particu- (Paperna and Por, 1977). The gnathiids feed larly the caligids and isopods, are widely on fish blood and can cause severe anaemia distributed especially in Southeast Asia. when present in large numbers. Fish mortality has been attributed to the presence of large numbers of these Prevention and control. Parasitic crusta- crustaceans. ceans are generally introduced along with fish caught in the wild for culture, but Diagnosis. The nature and severity of several of them are transmitted by wild pathogenic effects depend on the interaction fish around the cages. Prevention, therefore, between the host and the parasite. Some of is difficult. Organophosphate insecticides these parasites are mobile and cause less are commonly used for treatment. Fujita damage than those that are stationary, as et al., (1968) successfully treated yellowtail the latter firmly anchor themselves to the infected with Caligus elongatus by means host. of 50 s immersion in 100 ppm solution Argulids, however, though motile, of Dipterex. Freshwater dip proved to be do cause considerable injury to the host effective for Caligus sp. in cultured grouper because they tend to remain in one spot for a and snappers in Malaysia, and C. elongata in long period of time. The pointed styles of red drum (Landsberg et al., 1991). Other argulids pierce the skin while feeding on chemicals that have been used include mucus. Furthermore, acting as a cephalo- formaldehyde, hydrogen peroxide and thoracic suction cup, they exert a great pres- ivermectin. sure with their body. The presence of large numbers of argulids results in haemorrhage as well as thinning of the epithelial cells. Concluding Remarks and Current Many parasitic crustaceans on the gills Perspectives attach themselves by grasping or anchoring. The epithelial cells are generally reduced Like other aquaculture systems, cage aqua- or lost, resulting in the inflammation and culture uses resources and produces wastes. thickening of the local epithelial layer, Certain types of site habitats are particularly haemorrhage, haemolysis, hyperaemia and sensitive to cage aquaculture development hyperplasia. These signs are evident in and the impacts of cage fish farming on the the gills of grouper infested with E. aquatic environment can exert with time a

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Infectious Diseases of Warmwater Fish in Salt Water 219

negative feedback effect on cage operations ‘foreign’ antigenic proteins can be produced (Beveridge, 1996). in bulk. The food is the most practical deliv- Many species of wild fish are attracted ery system of these products to caged fish, by the cage structures, for shelter and abun- requiring no extra labour and no handling dant supply of food. They often gain access stress. However, oral vaccines have so far into the cages through the mesh, while proved disappointing, providing protection farmed species manage to escape into the that is generally weak and of short duration, surrounding environment. The mingling of presumably because protective antigenic fish populations creates new opportunities determinants are destroyed in the fish for disease transfer (Diamant and Colorni, foregut. Encapsulation of vaccines is needed 1995; Colorni, 1998) and the interactions to ensure that the essential antigenic deter- between cultured and feral fish may minants reach the second gut segment in have important ecological implications. a non-degraded and immuno-stimulatory Translocated species may carry exotic form (van Muiswinkel, 1995). diseases that could spread and devastate indigenous wild populations or may be themselves extremely sensitive to a local References pathogen. In any case, the introduction of large numbers of caged fish to a system tends Adams, A., Thompson, K.D. and Roberts, R.J. to have dramatic effects on disease agents. It (1997) Fish vaccines. In: Mowat, N. and has become increasingly apparent that high Rweyemamu, M. (eds) Vaccine Manual. The stocking densities of caged fish cause ‘patho- Production and Quality Control of Veterinary gen loading’ in the surrounding area, where Vaccines for Use in Developing Countries. patterns of occurrence, prevalence and Food and Agriculture Organization, UN, Rome, pp. 127–142. pathogenicity change greatly. ADB/NACA (1991) Fish Health Management in Only a limited number of therapeutic Asia-Pacific. Report on a Regional Study and drugs are licensed for use in fish. When Workshop on Fish Disease and Fish Health drugs are used, costs are usually high and Management. ADB Agriculture Department residues may remain in the fish flesh after Report Series No. 1, Network of Aquaculture treatment, which means a long withdrawal Centres in Asia-Pacific, Bangkok. period before the fish can be marketed. Also, Akazaki, M., Harada, T., Umeda, S. and Kumai, T. accumulation of therapeutics in waste prod- (1965) Death and extermination test on the ucts can compromise water quality. Use of gill trematode, Heteraxine heterocerca of the antibiotics, in particular, may not only yellowtail. Memo, Faculty of Agriculture, Kinki University 75–83. enhance the development of resistant strains Amandi, A., Hiu, S.F., Rohovec, J.S. and Fryer, J.L. of bacterial populations but may also sup- (1982) Isolation and characterization of press the immune system of the fish (Adams Edwardsiella tarda from Chinook salmon et al., 1997). (Oncorhynchus tshawytscha). Applied Envi- Considerable effort has been made in ronmental Microbiology 43, 1380–1384. recent years to develop effective, safe and Aoki, T. and Kitao, T. (1985) Detection of trans- economical vaccines for numerous bacterial ferable R plasmids in strains of the fish- and viral diseases. Since in vitro culture pathogenic bacterium Pasteurella piscicida. of the causative agent or its inactivation is Journal of Fish Diseases 8, 345–350. not always feasible, subunit vaccines have Aoki, T., Arai, T. and Egusa, S. (1977) Detection of R plasmids in naturally occurring been prepared using recombinant technol- fish-pathogenic bacteria, Edwardsiella tarda. ogy. Here, the pathogens’ antigenic determi- Microbiology and Immunology 21, 77–83. nants that elicit a protective host response Aoki, T., Kitao, T. and Fukudome, M. (1989) Che- have been identified and isolated, molecu- motherapy against infection with multiple larly cloned and expressed in the bacterium drug resistant strains of Edwardsiella tarda Escherichia coli or the yeast Saccharomyces antigens. Fish Pathology 22, 93–98. cerevisiae. Using biotechnology for the Arimoto, M., Muskiake, K., Mizuta, Y., Nakai, T., growth of these organisms, expressed Muroga, K. and Furusawa, I. (1992) Detection

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of striped jack nervous necrosis virus Transmission and Vaccine Development’, (SJNNV) by enzyme-linked immunosorbent 18–20 October 2000, Bangkok, Thailand. assay (ELISA). Fish Pathology 27, 191–195. APEC, AAHRI, FHS/AFS, NACA, Bangkok, Arimoto, M., Mori, K., Nakai, T., Muroga, K. and pp. 121–146. Furusawa, I. (1993) Pathogenicity of the caus- Boonyaratpalin, S., Supamattaya, K., Kasorn- ative agent of viral nervous necrosis disease chandra, J. and Hoffmann, R.W. (1996) in striped jack, Pseudocaranx dentex (Bloch Picorna-like virus associated with mortality & Schneider). Journal of Fish Diseases 16, and a spongious encephalopathy in grouper 461–469. Epinephelus malabaricus. Diseases of Arthur, J.R. and Ogawa, K. (1996) A brief review of Aquatic Organisms 26, 75–80. disease problems in the culture of marine Breuil, G., Bonami, J.R., Pepin, J.F. and Pichot, Y. finfishes in East and Southeast. In: Main, K.L. (1991) Viral infection (picorna-like virus) and Rosenfeld, C. (eds) Aquaculture Health associated with mass mortalities in Management Strategies for Marine Fish. The hatchery-reared sea-bass (Dicentrarchus Oceanic Institute, Hawaii, 280 pp. labrax) larvae and juveniles. Aquaculture Austin, B. and Austin, D.A. (1993) Bacterial Fish 97, 109–116. Pathogens, Diseases in Farmed and Wild Chao, T.M. (1984) Studies on the transmissibility Fish, 2nd edn. E. Horwood Publications, New of lymphocystis disease occurring in seabass York, 384 pp. (Lates calcarifer Bloch). Singapore Journal of Baxa, D.V., Kawai, K. and Kusuda, R. (1986) Primary Industries 12, 11–16. Characteristics of gliding bacteria isolated Chen, B.S. (1996) An overview of the disease from diseased cultured flounder, Paralich- situation, diagnostic technique, preventives thys olivaceus. Fish Pathology 21, 251–258. and treatments for cage-cultured, high value Baxa, D.V., Kawai, K. and Kusuda, R. (1987a) marine fishes in China. In: Main, K.L. Molecular taxonomic classification of glid- and Rosenfeld, C. (eds) Aquaculture Health ing bacteria isolated from diseased cultured Management Strategies for Marine Fishes. flounder. Fish Pathology 22, 11–14. The Oceanic Institute, Hawaii, pp. 109–116. Baxa, D.V., Kawai, K. and Kusuda, R. (1987b) Chong, Y.C. and Chao, T.M. (1986) Common Experimental infection of Flexibacter Diseases of Marine Foodfish. Fish Handbook maximus in black seabream (Acanthopagrus No. 2, Primary Production Department, Min- schlegeli) fry. Fish Pathology 22, 105–109. istry of National Development, Republic of Bellance, R. and Gallet de Saint Aurin, D. (1988) Singapore, 34 pp. L’encéphalite virale du loup de mer. Caraïbes Chua, F.H.C., Ng, M.L., Ng, K.L., Loo, J.J. and Medical 105–114. Wee, J.Y. (1994) Investigation of outbreaks of Beveridge, M. (1996) Cage Aquaculture, 2nd edn. a novel disease, ‘Sleepy Grouper Disease’, Fishing News Books, Blackwell Science Ltd, affecting the brown-spotted grouper, Oxford, 346 pp. Epinephelus tauvina Forskal. Journal of Fish Beverley-Burton, M. and Suraino, D.M. (1981) Diseases 17, 417–427. A revision of Cyclopectanum Oliver, 1968 Chua, F.H.C., Loo, J.J. and Wee, J.Y. (1995) Mass (Monogenea: Diplectanidae) and description mortality in juvenile greasy grouper, Epine- of C. hongkongenese n. sp. and C. lantanensis phelus tauvina, associated with vacuolating n. sp. from Epinephelus spp. in South China encephalopathy and retinopathy. In: Shariff, Sea. Canadian Journal of Zoology 59, M., Arthur, J.R. and Subasinghe, R.P. (eds) 1276–1285. Diseases in Asian Aquaculture, II. Fish Bloch, B., Gravningen, K. and Larsen, J.L. (1991) Health Section, Asian Fisheries Society, Encephalomyelitis among turbot associated Manila, pp. 235–241. with a picornavirus-like agent. Diseases of Chun, S.K. (1998) Studies on lymphocystis Aquatic Organisms 10, 65–70. diseases in Sebastes schlegeli. Journal of Fish Bondad-Reantaso, M.G., Kanchanakhan, S. and Pathology 1, 73–76. Chinabut, S. (2001) Review of grouper dis- Colorni, A. (1985) Aspects of the biology of eases and health management strategies for Cryptocaryon irritans, and hyposalinity groupers and other marine finfishes. In: as a control measure in cultured gilt-head Bondad-Reantaso, M.G., Humphrey, J., seabream Sparus aurata. Diseases of Aquatic Kanchanakan, S. and Chinabut, S. (eds) Organisms 1, 19–22. Report and Proceedings of APEC FWG Project Colorni, A. (1987) Biology of Cryptocaryon 02/2000 ‘Development of a Regional irritans and strategies for its control. Research Programme on Grouper Virus Aquaculture 67, 236–237.

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