Journal of Fish Diseases 2003, 26, 187206

Review Diseases of tunas, Thunnus spp.

B L Munday1, Y Sawada2, T Cribb3 and C J Hayward3
1 School of Human Life Sciences, University of Tasmania, Launceston, Tasmania, Australia 2 Fisheries Laboratory, Kinki University, Kushimoto, Wakayama, Japan 3 Department of Microbiology and Parasitology, University of Queensland, Brisbane, Queensland, Australia

Abstract

Much is known about those aspects of tuna health which can be studied in wild populations, e.g. helminth parasites. However, because aquaculture of these species is in its infancy, knowledge of microbial, nutritional and environmental diseases is limited. This review is an attempt to bring together the available information on those diseases of Thunnus spp. which cause signicant morbidity, mortality or economic loss. In doing so it has become clear that much more research needs to be undertaken on the physiology of the species (southern, northern and Pacic bluen tuna) currently used in aquaculture in order for the pathogenesis of some conditions to be properly understood. Attempts at hatchery culture of Pacic bluen tuna has indicated that Thunnus spp. will be problematic to hatch and propagate. Keywords: diseases, parasites, pathology, pathophysiology, Thunnus spp., tuna.
Introduction

Tunas of the genusThunnus are very important commercial species which have, until recently, been exclusively wild-caught (Kailola, Williams, Stewart, Reichelt, McNee & Grieve 1993). However, the drastic reduction in stocks resulting from uncontrolled harvesting has led to the imposition of stringent quotas for certain species and concurrent
Correspondence B L Munday, School of Human Life Sciences, University of Tasmania, Locked Bag 1320, Launceston, Tasmania 7250, Australia (e-mail barry.munday@utas.edu.au)

establishment of aquaculture of some of these species (Lee 1998). There is little information on diseases of these sh and this review is an attempt to assemble this information in one place for the use of interested parties. Both pathological and pathophysiological conditions will be addressed. Tunas are superb athletes and a number of species maintain stable body temperatures by having relatively high metabolic rates complemented by the use of heat-exchange mechanisms. Some species have been extensively studied at the physiological level, despite the practical problems involved in working with such sh (reviewed by Brill 1996; Farrell 1996; Korsmeyer, Dewar, Lai & Graham 1996). These studies have provided a sound basis for understanding pathophysiological conditions encountered in these species but more work is required, especially in southern bluen tuna, Thunnus maccoyii Castlenau, which is the basis for the Australian tuna aquaculture industry. With regard to pathology, there is little published information available with the exception of parasitological studies which have mainly been undertaken for parasite taxonomical studies or identication of discrete stocks of Thunnus spp. (Yamaguti 1970; Jones 1991a; Williams & Bunkley-Williams 1996). It is notable that adult tunas appear to be relatively resistant to bacterial infections even when subjected to trauma and other factors likely to predispose to such infections. This review is based on the published literature supplemented with unpublished data from the authors and colleagues. The diseases are divided into those of infectious and non-infectious origins with appropriate sub-divisions.

2003 Blackwell Publishing Ltd

187

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Infectious diseases

Virus diseases Red sea bream iridoviral infection

Aetiology. The disease is caused by red sea bream iridovirus (RSIV) which is a member of a recently recognized group of very pathogenic viruses affecting marine species in the Asian region (Miyata, Matsuno, Jung, Danayadol & Miyazaki 1997). Whereas many sh iridoviruses belong to the genus Ranavirus (Hyatt, Gould, Zupanovic, Cunningham, Hengstberger, Whittington, Kattenbelt & Coupar 2000), RSIV does not. Young Pacic bluen tuna, Thunnus orientalis (Temminck & Schegel), are often infected with this virus, but the disease never appears in bluen tuna more than 1 year of age. Occurrence of the disease is restricted to periods of higher water temperature (>24 C). Sometimes the mortality reaches some tens of percent for young sh. Clinical signs. Infected sh have dark body colour and anorexia. If the sh do not die during the acute phase of the disease they become emaciated and die later. Pathology. As in other sh species, basophilic, hypertrophied cells (probably leucocytes) are observed in sections of spleen from diseased Pacic bluen tuna. Epidemiology. Among tunas, this infection has only been reported in Pacic bluen tuna (Kawakami & Nakajima 2002). Net cages for young wild-caught tuna are often sited near cages containing other sh which are susceptible to this virus. Therefore, it is likely that wild-caught young tuna for aquaculture, which are not infected at the time of capture, become infected by being caged alongside other cultured sh. Diagnosis. The histopathological picture of enlarged cells in the spleen, liver, kidney and gills which stain strongly with Giemsa is very characteristic of RSIV infection. Further conrmation can be obtained by demonstrating iridovirus virions by electron microscopy, culture of the virus in RTG-2, CHSE-214, FHM, BF-2 or KRE-3 cells at 2025 C, detection of specic antibody by immunouorescence using monoclonal antibodies and detection of specic genomic sequences by PCR (Inouye, Yamano, Maeno, Nakajima, Matsuoka, Wada & Sorimachi 1992;Nakajima, Maeno, Yokoyama, Kaji & Manabe 1998; Oshi 2003 Blackwell Publishing Ltd

ma, Hata, Hirasawa, Ohtaka, Hirono, Aoki & Yamashita 1998). Treatment. There is no available treatment. Prevention. Apart from normal hygienic precautions, especially siting tuna cages well away from other aquaculture species such as red sea bream, Chrysophrys major (Temminck & Schlegel), and yellowtail, Seriola quinqueradiata Temminck & Schlegel, there are no current specic control measures for the disease. However, promising vaccination trials have been reported (Nakajima, Maeno, Honda, Yokoyama, Tooriyama & Manabe 1999; Nakai & Nakajima 2002).

Bacterial diseases Opportunistic bacterial infections

Aetiology. Aeromonas sp. infections have been reported in association with Caligus elongatus damage to the eyes of southern bluen tuna (Rough, Lester & Reuter 1999). Buchanan (2002) and R. Reuter (personal communication) have reported a variety of Aeromonas and Vibrio spp. in the kidney and other internal organs of southern bluen tuna, especially those which have suffered trauma. Clinical signs. Rough et al. (1999) reported dissolution of the lens and consequent loss of the eye in Caligus elongatus infections. In instances of external trauma there may be large wounds which do not heal and the sh eventually die, presumably from a combination of bacteraemia and osmoregulatory failure. Epidemiology. The organisms concerned are normal environmental inhabitants which are able to colonize wounds resulting from mechanical or parasitic trauma. Diagnosis. Isolation of the organisms from the orbit or kidney is regarded as diagnostic. However, isolation of such bacteria from supercial wounds may only indicate contamination from the water column. Treatment. It is difcult to treat captive tuna and it is doubtful if severely affected animals would respond to therapy. Prevention. The prevalence and severity of supercial wounds can be reduced by careful handling of the sh. At present, C. elongatus infections are not a sufcient problem to warrant treatment but this may be necessary in the future to reduce morbidity.

188

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Photobacterium spp. infections

Aetiology. Peric (2002) reported lesions consistent with Photobacterium damsela subsp. piscicida in a single northern bluen tuna, T. thynnus (Bonnaterre). Hamaguchi & Kusuda (1992) reported on experimental infections of Pacic bluen tuna with P. phosphoreum. Pathology. Peric (2002) described the spleen of the tuna as being enlarged with a rough surface. The cut surface showed multiple granulomas which, histologically, contained small numbers of short plump rods. He indicated that the lesions were similar to those seen in sparids with chronic pasteurellosis (P. damsela subsp. piscicida infection). Epidemiology. Pasteurellosis is essentially a warmwater (2025 C) disease and as the causative organism does not survive for long outside the host. Transmission is presumed to be lateral between sh (AQIS 1999). Diagnosis. The macroscopic lesions are not diagnostic as such granulomas can be caused by a variety of agents such as Mycobacterium or Nocardia spp. The detection of short, plump Gram-negative bacteria should enable a presumptive diagnosis but a denitive diagnosis requires isolation and identication of P. damsela subsp. piscicida. Hamaguchi & Kusuda (1992) conrmed experimental infections with P. phosphoreum by isolating the organism from the kidneys of diseased sh. Treatment and prevention. The reported very low prevalence of pasteurellosis in northern bluen tuna would not warrant attempts at treatment or specic prophylaxis.

Otherwise it most likely became infected from the environment as aquatic mycobacteria are capable of existing as environmental organisms. Diagnosis. There are a number of granulomatous diseases of marine sh which can be difcult to differentiate, e.g. mycobacteriosis and nocardiosis, pseudotuberculosis. The latter can be differentiated from the rst two on the basis that the organisms are Gram negative but the other two require isolation and identication of the causal bacteria. Treatment and prevention. Treatment is not practicable. As most cultured tuna are currently fed raw baitsh, care must be taken not to include sh with tuberculosis in the diet.

Protozoan diseases Coccidiosis

Aetiology. Only Goussia auxidis has been reported

from tunas.
Clinical signs. No clinical signs have been reported. Pathology. Jones (1990) reported that oocysts

occurred in both the liver and spleen where they produced minimal host response. Epidemiology. The method of transmission of infection is unknown. Jones (1990) found 98% (140 of 143) of albacore, T. alalunga (Bonnaterre), and an individual yellown tuna, T. albacares (Bonnaterre), from the South Pacic were infected. He found no infection in 11 southern bluen tuna although R. Reuter (personal communication) has noted coccidial bodies in the liver of this species. Treatment and prevention. Not required. Scuticociliate infection
Aetiology. Munday, ODonoghue, Watts, Rough & Hawkesford (1997) reported an encephalitis in young adult southern bluen tuna caused by Uronema nigricans. Williams & Bunkley-Williams (1996) reported an apparently similar condition in northern bluen tuna in the Pacic. As their record was not their own work, and such a report has not appeared in the mainstream scientic literature, it is possible that their citation actually applies to U. nigricans in southern bluen tuna. Unidentied scuticociliates have caused signicant mortalities of larval Pacic bluen tuna at 1418 days post-hatch in hatcheries in Japan (Miyashita & Kumai 2002; Y. Sawada, unpublished data).

Mycobacteriosis or piscine tuberculosis

Aetiology. The cause of putative tuberculosis reported in a single northern bluen tuna (Biavati & Manera 1991) is not known. However, most isolates from marine species are Mycobacterium marinum (Austin & Austin 1987). Clinical and pathological ndings. Biavati & Manera (1991) reported a granulomatous peritonitis. Histologically, there were granulomas composed predominantly of epithelioid cells and broblasts. Bacilli within the granulomas were Gram positive and stained with modied ZiehlNeelsen stain. The authors believed that the diagnosis was more likely to be mycobacteriosis than nocardiosis. Epidemiology. It is possible that the tuna could have eaten a sh which itself had mycobacteriosis.
2003 Blackwell Publishing Ltd

189

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Clinical signs. Adult southern bluen tuna with Uronema encephalitis suffer from the so-called swimmer syndrome. Typically, such sh come to the surface, turn light blue and swim vigorously around the cage. Eventually, they cease compulsive swimming and tend to alternately sink and rise to the surface until they nally sink and die (Munday et al. 1997). Morbidity and mortality rates are comparable (B.L. Munday & K.M. Rough, unpublished data) and have decreased from about 5% in captive sh in 1993 to 1.34% in 1995 and <1% in 2001. In the case of infection of 14-day post-hatch Pacic bluen tuna larvae, approximately half of the larvae died within 3 days (Y. Sawada, unpublished data). The smaller larvae showed the heaviest mortality and signs of infection ceased at 18 days post-hatch. Pathology. In adult southern bluen tuna pathology is restricted to the olfactory system and brain. Although parasites containing food vacuoles can be found in the brain (Fig. 1) there is no host response except where the meninges are involved. However, lymphocytic responses are frequent in the olfactory nerves and rosettes. The parasites preferentially invade the epidermis and muscle of tuna larvae. Epidemiology. In the case of the swimmer syndrome it is believed that the scuticociliates proliferate in the undercage sediment and invade the olfactory rosette of the sh when water passes through the nares during olfaction. The reduction in prevalence of the disease in recent years appears to be associated with improved undercage environmental conditions. It is not known what predisposes the olfactory rosette to colonization by Uronema, but water temperature appears to be an important variable because the

disease does not occur when the water temperature is above 18 C (Munday et al. 1997). The build-up of organic matter which occurs in hatcheries is conducive to the development of high concentrations of scuticociliates and outbreaks of disease. Diagnosis. Cases of swimmer syndrome can be diagnosed by demonstrating Uronema in wet preparations or sections of brain from affected sh. Watts, Burke & Munday (1996) developed a uorescent antibody stain for specic identication of U. nigricans. Scuticociliate infection of larval/juvenile tuna is diagnosed by demonstrating the parasites in wet preparations or tissue sections. Treatment. Treatment is not practicable for adult tuna reared in open sea cages. Copper treatment has been found to be effective for scuticociliate infections of many sh which are reared in tanks in Japan. Usually, copper ions in the range of 5080 ppb concentration are effective. In Japan, this concentration of copper ions is achieved by the use of a simple electrolytic apparatus which consists of copper electrodes installed in the pipework carrying the inuent water. However, larval and juvenile sh are less tolerant to copper ions than adult sh (S. Miyashita, personal communication) and the tolerance of larval and juvenile tuna to copper is unknown. It is helpful to increase the water exchange rate in larval rearing tanks and, of course, the removal of dead sh is necessary. In the case of larval Pacic bluen tuna, a higher water temperature of 28 C has been found to be effective in reducing losses. It is not clear whether the higher temperature prevents proliferation of the parasite or if higher temperatures

Figure 1 Brain of southern bluen tuna showing presence of Uronema nigricans (arrows) containing food vacuoles. Note lack of host response (PAS, bar 50 lm).
2003 Blackwell Publishing Ltd

190

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

accelerate the shs development to the juvenile stage at which they develop higher tolerance toUronema spp. However, it may be pertinent that Crosbie (1996) found that the maximum U. nigricans densities, which were achieved during the exponential phase of cultured organisms, were lower at 30 C than at 1025 C. This suggests that the effect of high water temperatures on the organisms may be the more important mechanism. Prevention. Prevention is by improved hygiene/ husbandry. Metazoan infections As given in Table 1, many metazoans infect Thunnus spp. but only a few are of health and/or economic importance. These will be discussed here. Additionally, the reader needs to be aware that, while an effort has been made to identify errors in records of parasites of tunas, Table 1 may still contain contentious citations. Postmortem liquefaction of muscle due to myxosporean infections
Aetiology. Hexacapsula neothunni in albacore, yel-

measure 6.2 11.0 lm and have six shell valves each containing one polar capsule (Lom & Dykova 1992). Kudoa nova spores measure 5.36.5 8.5 9.8 lm and have four shell valves each containing one polar capsule. Treatment and prevention. Neither treatment nor prevention is practicable. Kudoa sp. infection of northern and southern bluen tuna producing lesions in the musculature
Aetiology. Kent et al. (2001) reported K. crumena in a yellown tuna. Similar lesions because of an unidentied Kudoa sp. have been reported in southern bluen tuna and Langdon (1990) suggested that the parasite could be K. nova, but as it does not produce myoliquefaction, this seems unlikely. Clinical signs. None reported. Pathology. The infection in southern bluen tuna produces white cysts 110 mm in diameter which are apparently in the muscle (J.C. Harshbarger, personal communication; Rough 2000) although Langdon (1990) produced evidence to suggest that most, if not all, cysts in southern bluen tuna were in peripheral nerves, especially the intercostal nerves. Histologically the cysts are found to consist of numerous Kudoa spores surrounded by a brous capsule (Fig. 2). Epidemiology. The infections described by Langdon (1990) were in southern bluen tuna caught off southwestern Western Australia when the sh would have been 13 years of age and feeding on cephalopods, crustaceans and salps (Kailola et al. 1993). Infections have also been reported in southern bluen tuna in South Australia (Rough 2000) and wild sh caught off the New South Wales coast where the prevalence of about 1% affected sh was a cause of commercial loss (B.L. Munday, unpublished data). The prevalence of K. crumena in albacore was reported as 5% (J.C. Harshbarger, personal communication). Diagnosis. Typical Kudoa spores measuring 7.5 9.9 (K. crumena) and 4.45.6 7.810.0 lm (Kudoa sp.) can be seen in wet preparations or histological sections. Treatment and prevention. Neither treatment nor prevention are practicable.

lown tuna and bigeye tuna, T. obesus (Lowe), Kudoa nova in bigeye tuna and, possibly, K. clupeidae in poorly identied Thunnus spp. (Williams & Bunkley-Williams 1996). Clinical signs and pathology. The parasites produce no clinical signs and, while with heavy infections cysts may be visible in the musculature, it is the postmortem liquefaction of the muscle caused by the release of proteases from the parasites that is the most dramatic result of the infection (Ogawa 1996). Histologically, the myxosporean spores are found aggregated in the cystic structures and usually produce minimal host response. Epidemiology. Most myxosporeans, for which life cycles are known, have a two-host cycle with the myxosporean in a sh and an actinosporean in an invertebrate (Kent, Andree, Bartholomew, El-Matbouli, Desser, Devlin, Feist, Hedrick, Hoffman, Khattra, Hallett, Lester, Longshaw, Palenzeula, Siddall & Xiao 2001). As most juvenile tuna consume invertebrates such as squid and crustaceans (Kailola et al. 1993), it is conceivable that these prey species could be alternative hosts. Diagnosis. Typical myxosporean spores can be easily found in wet preparations or histological sections of affected muscles. Hexacapsula neothunni spores
2003 Blackwell Publishing Ltd

Monogenean infection of gills

Aetiology. An unidentied, capsalid monogenean (Rough 2000, type 3) infecting southern bluen tuna.

191

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Table 1 Metazoan parasites of Thunnus spp.

Parasite Myxosporea Hexacapsula neothunni Kudoa Kudoa Kudoa Kudoa clupeidae crumena nova sp. Species infected Reference

Alb, BET, YFT NBT Alb BET SBT YFT Alb, BET,YFT PBT, SBT YFT NBT BET, SBT,YFT LTT, NBT NBT PBT BET BET,YFT NBT, SBT LTT BET,YFT YFT Alb, YFT BET, NBT NBT NBT BET, PBT Alb, BET,YFT BET, NBT, YFT BET, YFT NBT LTT, NBT NBT BET,BFT, NBT,YFT YFT NBT BET NBT SBT, YFT BET, NBT, YFT NBT Alb, BET, NBT,YFT BET, NBT YFT YFT PBT YFT PBT SBT,YFT BET YFT PBT BET, YFT SBT SBT Alb, PBT, YFT SBT YFT BET BET, YFT BET, YFT

Arai & Matsumoto (1953), Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Harshbarger pers. comm. Williams & Bunkley-Williams (1996) Langdon (1990) Pozdnyakov (1990) Pozdnyakov (1990) Kohn & Cohen (1998) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Murugesh (1995) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990), Rough (2000) Young (1970) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Williams & Bunkley-Williams (1996) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Murugesh (1995) Wheeler & Beverley-Burton (1987) Walters (1980), Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Williams & Bunkley-Williams (1996) Pozdnyakov (1990), Rough (2000) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Williams & Bunkley-Williams (1996) Payne (1990) Srivastava & Sahai (1978) Nikolaeva & Parukhin (1968) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996), Rough (2000) Williams & Bunkley-Williams (1996) Nikolaeva & Parukhin (1968) Williams & Bunkley-Williams (1996) Yamaguti (1970) Cribb et al. (2000) Manter (1970) Yamaguti (1938), Pozdnyakov (1990) Rough (2000) Ahmad (1983) Nikolaeva & Dubina (1978) Yamaguti (1970) Yamaguti (1970)

Monogenea Allopseudaxine sp. Areotestis sibi Benedenia seriolae Caballerocotyla abidjani Caballerocotyla albsmithi Caballerocotyla biparasitica Caballerocotyla goueri Caballerocotyla magronum Caballerocotyla paucispinosa Caballerocotyla pseudomagronum Caballerocotyla verrucosa Caballerocotyla sp. Capsala foliacea Capsala gotoi Capsala neothunni Capsala thynni Hexostoma acutum Hexostoma albsmithi Hexostoma dissimile Hexostoma grossum Hexostoma sibi Hexostoma thynni Hexostoma sp. Kuhnia thunni Metapseudaxine ventrosicula Nasicola hogansi Nasicola klawei Neohexostoma euthynni Neohexostoma extensicaudatum Neohexostoma robustum Neohexostoma thunninae Neohexostoma sp. Sibitrema poonui Tristomella interrupta Tristomella nozawae Tristomella onchidiocotyle Udonella caligorum Zeuxapta taylori Digenea Anaplerurus thynnusi Angionematoborium cephalodomus Aponurus lagunculus Atalostroppion sardae Botulus microporus Brachyphallus parvus Bucephalopsis sibi Cardicola ahi Cardicola forsteri Cetiotrema crassum Coeliotrema thynni Colocyntotrema sp. Decemtestis dollfusi Dermatodidymocystis indicus Dermatodidymocystis vivipira Dermatodidymocystis viviparoides

2003 Blackwell Publishing Ltd

192

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Table 1 Continued
Parasite Didymocylindrus liformis Didymocystis acanthocybii Didymocystis alalongae Didymocystis bifurcata Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis Didymocystis crassa dissimilis guernei irregularis katsuwonicola lanceolata macrorchis nasalis oesophagicola opercularis orbitalis ovata palati philobranchia philobranchiarca poonui reniformis rotunditestis semiglobularis soleiformis spirocauda superpalati Species infected PBT YFT Alb,BET Alb, BET, LTT, YFT PBT NBT Alb YFT PBT Alb Alb BET LTT, YFT Alb YFT, BET LTT, PBT YFT Alb, BET, YFT Alb, BET, YFT BET NBT Alb, BET, YFT PBT PBT YFT Alb, BET,LTT, YFT Alb, NBT, PBT, SBT Alb, LTT, NBT, PBT, SBT, YFT Reference Ishii (1935) Williams & Bunkley-Williams (1996) Yamaguti (1970) Yamaguti (1970), Nikolaeva & Dubina (1985), Murugesh & Madhavi (1995) Ishii (1935) Yamaguti (1971) Dollfus (1952) Yamaguti (1970) Ishii (1935) Dollfus (1952) Dollfus (1952) Yamaguti (1970) Yamaguti (1970), Murugesh & Madhavi (1995) Yamaguti (1938) Yamaguti (1970) Ishii (1935), Ku & Shen (1965) Yamaguti (1970) Yamaguti (1970), Williams & Bunkley-Williams (1996) Yamaguti (1970), Nikolaeva & Dubina (1985) Yamaguti (1970) Ariola (1902) Nikolaeva & Dubina (1985), Williams & Bunkley-Williams (1996) Ishii (1935) Williams & Bunkley-Williams (1996) Yamaguti (1970) Yamaguti (1970), Nikolaeva & Dubina (1985), Murugesh & Madhavi (1995) Dollfus (1952), Yamaguti (1971), Williams & Bunkley-Williams (1996), Rough (2000) Ariola (1902), Yamaguti (1934), Ishii (1935), Dollfus (1952), Murugesh & Madhavi (1995), Rough (2000) Yamaguti (1938), Murugesh & Madhavi (1995) Williams & Bunkley-Williams (1996) Yamaguti (1970) Williams & Bunkley-Williams (1996) Yamaguti (1971) Yamaguti (1970) Yamaguti (1971) Williams & Bunkley-Williams (1996) Pozdnyakov (1987a) Ishii (1935) Ariola (1902) Pozdnyakov (1990) Pozdnyakov (1990) Pozdnyakov (1990) Ishii (1935) Ishii (1935), Yamaguti (1970), Williams & Bunkley-Williams (1996) Ariola (1902), Williams & Bunkley-Williams (1996) Taschenberg (1879) Korotaeva & Korjakovtzeva (1983) Linton (1901) Korotaeva & Korjakovtzeva (1983) Yamaguti (1970) Yamaguti (1971) Linton (1940), Dollfus (1952) Yamaguti (1971) Dollfus (1952) Dollfus (1952) Yamaguti (1938)

Didymocystis thynni Didymocystis wedli

Didymocystoides alalongae Didymocystoides bifasciatus Didymocystoides buccalis Didymocystoides oesophagicola Didymocystoides opercularis Didymocystoides pectoralis Didymocystoides semiglobularis Didymocystoides superpalati Didymonaja branchialis Didymoproblema fusiforme Didymostoma bipartitum Didymosulcus aahi Didymosulcus dimidiatus Didymosulcus katsuwonicola Didymozoon licolle Didymozoon longicolle Didymozoon pretiosus Didymozoon thynni Dinurus breviductus Distomum clavatum Ectenurus lepidocybii Hirudinella ahi Hirudinella clavata Hirudinella fusca Hirudinella marina Hirudinella oxysoma Hirudinella poirieri Hirudinella spinulosa

Alb, LTT BET, YFT Alb YFT Alb BET PBT Alb, BET, YFT Alb PBT NBT Alb, YFT Alb BET, YFT PBT BET, NBT, PBT, YFT PBT, NBT NBT BET NBT YFT YFT NBT Alb, NBT YFT Alb Alb Alb

2003 Blackwell Publishing Ltd

193

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Table 1 Continued
Parasite Hirudinella ventricosa Koellikerioides apicalis Koellikerioides externogastricus Koellikerioides internogastricus Koellikerioides intestinalis Koellikerioides orientalis Koellikerioides splenalis llikeria abdominalis Ko llikeria bipartita Ko llikeria globosa Ko llikeria orientalis Ko llikeria pylorica Ko llikeria reniformis Ko llikeria retrorbitalis Ko llikeria submaxillaris Ko Lecithaster gibbosus Lecithocladium excisum Lobatozoum multisacculatum Metanematobothrium guernei Nematobothrium latum Nematobothrium sp. Neonematobothrioides poonui Neophrodidymotrema ahi Oesophagocystis sp. Opisthorchinematobothrium nephrodomus Opisthorchinematobothrium parathunni Orbitonematobothrium perioculare Phyllodistomum thunni Platocystis alalongae Platocystis meridionalis Platocystis sp. Prosorhynchoides sibi Rhipidocotyle pentagonum Rhipidocotyle septpapillata Sterrhurus imocavus Syncoelium liferum Umatrema indica Univietellodidymocystis lingualis Univietellodidymocystis neothunni Uroproctinella attenuata Uroproctinella spinulosa Wedlia bipartita Wedlia lingualis Wedlia musseliusae Wedlia orientalis Yamaguticystis ariellii Cestoda Callitetrarhynchus gracilis Dasyrhynchus talismani Echeneibothrium sp. Grillotia sp. Gymnorhynchus gigas Hepatoxylon trichiuri Lacistorhynchus tenuis Monorygma grimaldi Nybelinia lingualis Nybelinia sp. Pelichnibothrium speciosum Pseudobothrium grimaldi Pterobothrium heteracanthum Species infected Alb, BFT, NBT, SBT, YFT BET BET, YFT BET, YFT BET Alb, NBT, YFT YFT YFT Alb, NBT, YFT NBT, PBT, YFT Alb, LTT, NBT, YFT BET PBT BET, YFT BET, YFT NBT NBT PBT Alb Alb BET, PBT BET YFT PBT Alb BET BET, YFT YFT Alb Alb YFT PBT PBT NBT NBT, PBT Alb, SBT YFT Alb, BET, YFT BET, YFT YFT Alb, YFT Alb, NBT YFT Alb Alb, NBT, YFT YFT YFT, NBT, SBT YFT, BET YFT YFT, PBT YFT Alb, YFT NBT Alb SBT YFT YFT, NBT, PBT Alb SBT Reference Gibson & Bray (1977), Williams & Bunkley-Williams (1996), Rough (2000) Yamaguti (1970) Yamaguti (1970) Yamaguti (1970) Yamaguti (1970) Pozdnyakov (1992) Nikolaeva (1988) Yamaguti (1970) Yamaguti (1971), Williams & Bunkley-Williams (1996) Ishii (1935), Williams & Bunkley-Williams (1996) Yamaguti (1971), Shen (1990) Yamaguti (1970) Ishii (1935) Yamaguti (1970) Yamaguti (1970) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Ishii (1935) Yamaguti (1938) Dollfus (1952) Nikolaeva & Dubina (1985), Williams & Bunkley-Williams (1996) Yamaguti (1970) Yamaguti (1970) Williams & Bunkley-Williams (1996) Nikolaeva & Dubina (1978) Yamaguti (1970) Yamaguti (1970) Baudin-Laurencin & Richard (1973) Yamaguti (1938) Pozdnyakov (1987b) Nikolaeva & Parukhin (1968) Yamaguti (1940) Eckmann (1932) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996), Rough (2000) Srivastava & Sahai (1978) Nikolaeva & Dubina (1985) Yamaguti (1970) Hafeezullah (1971) Nikolaeva & Parukhin (1968), Bussieras & Baudin-Laurencin (1973) Linton (1940), Dollfus (1952) Nikolaeva & Dubina (1985) Nikolaeva & Dubina (1985) Yamaguti (1934), Dollfus (1952) Nikolaeva & Dubina (1985) Dollfus (1942), Bussieras & Baudin-Laurencin (1973), Rough (2000) Bussieras & Aldrin (1965), Baudin-Laurencin (1971) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Bussieras & Baudin-Laurencin (1973), Jones (1991a) Dollfus (1942) Williams & Bunkley-Williams (1996) Rough (2000) Williams & Bunkley-Williams (1996) Schmidt (1986), Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Rough (2000)

2003 Blackwell Publishing Ltd

194

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Table 1 Continued
Parasite Scolex pleuronectis Sphyriocephalus dollfusi Sphyriocephalus tergestinus Sphyriocephalus sp. Tentacularia coryphaenae Tentacularia sp. Tetraphyllidean larvae Nematoda Anisakis simplex Anisakis sp. Capsularia marina Contracaecum sp. Heptachona caudata Hysterothylacium aduncum Hysterothylacium cornutum Metanisakis sp. Monhysterides sp. Oncophora albacarensis Oncophora melanocephala Philometroides sp. Spirurida Terranova sp. Acanthocephala Bolbosoma vasculosum Bolbosoma sp. Gorgorhynchus sp. Neorhadinorhynchus nudus Neorhadinorhynchus sp. Rhadinorhynchus cadenati Rhadinorhynchus pristis Rhadinorhynchus trachuri Rhadinorhynchus sp. Copepoda Brachiella thynni Caligus alalongae Caligus asymmetricus Caligus balistae Caligus bonito Caligus coryphaenae Caligus elongatus Caligus productus Caligus quadratus Caligus sp. Caligus robustus Euryphorus brachypterus Euryphorus nordmanni Pennella losa Pennella sp. Pseudocynus appendiculatus Isopoda Rocinella signata Species infected LTT BET Alb YFT, BET Alb, BFT, NBT, YFT YFT Alb, BFT, NBT, YFT, YFT Alb, YFT, PBT SBT Alb, PBT PBT Alb, NBT Alb, NBT, SBT, YFT YFT YFT YFT Alb, BFT, NBT, YFT BET, YFT SBT LTT Alb, PBT, YFT YFT Alb PBT YFT YFT Alb, SBT, YFT YFT YFT Alb, BET, NBT, SBT, YFT Alb, BET YFT NBT NBT Alb, BET, BFT, NBT, YFT SBT Alb, BET, BFT, NBT, YFT YFT YFT YFT Alb, BET, BFT, NBT, YFT Alb, BET, YFT Alb, NBT, YFT YFT Alb, BET, BFT, LTT, NBT, YFT Alb Reference Murugesh (1995) Bussieras & Aldrin (1965) Williams & Bunkley-Williams Williams & Bunkley-Williams Williams & Bunkley-Williams Williams & Bunkley-Williams Williams & Bunkley-Williams

(1996) (1996) (1996) (1996) (1996)

Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Humphrey (1995) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Humphrey (1995), Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996), Moravec, Kohn & Santos (1999) Williams & Bunkley-Williams (1996) Rough (2000) Cannon (1977) Williams Williams Williams Williams Williams Williams Williams Williams Williams & & & & & & & & & Bunkley-Williams Bunkley-Williams Bunkley-Williams Bunkley-Williams Bunkley-Williams Bunkley-Williams Bunkley-Williams Bunkley-Williams Bunkley-Williams (1996) (1996) (1996) (1996) (1996) (1996) (1996), Rough (2000) (1996) (1996)

Jones (1991b), Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Hogans (1985), Williams & Bunkley-Williams (1996) Rough et al. (1999) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Walters (1980), Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996) Williams & Bunkley-Williams (1996)

Alb, albacore Thunnus alalunga (Bonnaterre); BET, bigeye tuna Thunnus obesus (Lowe); BFT, blackn tuna Thunnus atlanticus (Lesson); LTT, longtail tuna Thunnus tonngol (Bleeker); NBT, northern bluen tuna Thunnus thynnus (L.); PBT, Pacic bluen tuna Thunnus orientalis (Temminck & Schlegel); SBT, southern bluen tuna Thunnus maccoyii (Castelnau); YFT, yellown tuna Thunnus albacares (Bonnaterre).

Clinical signs. The parasite does not cause mortality

Pathology. Rough (2000) described white patches

but Rough (2000) stated that heavy infections lead to respiratory stress.
2003 Blackwell Publishing Ltd

on the gills which appear histologically as areas of focal lamellar fusion.

195

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Figure 2 Kudoa sp. nodule in muscle of southern bluen tuna. Note the small nerve (arrowhead) embedded in/apposed to, the capsule surrounding the mass of spores (H & E, bar 100 lm).

Figure 3 Gill of southern bluen tuna with Cardicola forsteri infection. Note the focal, pale lesions arranged in an arc formation (arrows).

permits a presumptive diagnosis. A denitive diagnosis is currently not possible in the absence of a description of the parasite. Treatment. Therapeutic treatment would not be practicable nor warranted. Prevention. Control would most likely be achieved by reducing stocking densities for both cages and sh in cages, i.e. fewer cages per site and fewer sh per cage. Blood uke infections of tuna
Aetiology. Cardicola ahi has been reported from

Epidemiology. Rough (2000) stated It is more common in farmed sh but its distribution is often conned to only a few cages, and heavy infections to individual sh. Diagnosis. The presence of white patches on the gills together with the presence of monogeneans

yellown and bigeye tunas (Smith 1997). Cardicola forsteri (Cribb, Daintith & Munday 2000) occurs in southern bluen tuna.

Figure 4 Gill of southern bluen tuna with Cardicola forsteri infection. Note the presence of sanguinicolid eggs (arrows) and associated cellular response (H & E, bar 100 lm).
2003 Blackwell Publishing Ltd

196

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Figure 5 Spongiosa of southern bluen tuna heart with Cardicola forsteri infection showing myocardial hypertrophy and presence of granulomas surrounding parasite eggs (arrows) (H & E, bar 250 lm). Illustration from Colquitt et al. (2001).

Clinical signs. Cardicola forsteri infections of cultured

southern bluen tuna lead to increased mucus on the gills and have been associated with signs of respiratory distress, lethargy and slightly increased mortality (Rough 2000; B.L. Munday, unpublished data). Pathology. Colquitt, Munday & Daintith (2001) described multifocal, white to yellow lesions involving the gills of infected southern bluen tuna. The lesions ranged in size from 2 to 12 mm and often extended in an arc across the gills (Fig. 3). Histopathological lesions in the gills of southern bluen tuna have been described in detail by Colquitt et al. (2001). The lesions appeared to be the result of the uke ova impacting in the afferent lamentary arteries where they stimulated a host response (Fig. 4). Bussieras & BaudinLaurencin (1973) also reported similar lesions in yellown tuna infected with a Cardicola sp. (probably C. ahi). Cardiac lesions were also reported by Colquitt et al. (2001) who noted many ova surrounded by granulomas. There was marked hypertrophy of the cardiac spongiosa (Fig. 5), presumably because of increased resistance to blood passing through the partly occluded branchial vasculature. It may not be a coincidence that bigeye tuna, which are known to be infected with Cardicola ahi, have a much more compact ventricular myocardium (74%) compared with northern bluen tuna (3050%) which have not been reported to be to be infected with blood ukes (Santer & Greer-Walker 1980; Smith 1997). Epidemiology. The intermediate hosts of Cardicola ahi and C. forsteri are not known. It is also not known if teleosts, other than Thunnus spp., act as
2003 Blackwell Publishing Ltd

nal hosts. Colquitt et al. (2001) reported that the prevalence and severity of the infection increased with the time that southern bluen tuna were held in captivity suggesting that the life cycle was maintained in the vicinity of the cages. Additionally, tuna farmers have reported that infections tend to be more severe at new cage sites suggesting that the parasite may also have a deleterious effect on the intermediate host (B.L. Munday, unpublished data). Diagnosis. In southern bluen tuna the gross lesions are characteristic enough to enable a presumptive diagnosis. Histopathology is even more diagnostic, but denitive diagnosis depends upon ushing the adults from the heart and identifying them. Treatment. There is no practicable treatment at present. Prevention. Prevention of blood uke infections depends upon an understanding of the parasites life cycle and, therefore, is not possible at present. Larval cestode infection
Aetiology. Larval cestodes (plerocercoids) do not usually cause disease in tunas and, therefore, it is only those which involve the musculature which are of commercial importance. Tentacularia coryphaenae does produce muscle lesions in a range of tuna species and will be considered here. Clinical signs. The infection is covert. Pathology. Plerocercoids up to 9.5 mm in length have been reported in albacore, T. alalunga (Bonnaterre), blackn tuna T. atlanticus (Lesson), northern bluen tuna, bigeye tuna and yellown tuna (Williams & Bunkley-Williams 1996).

197

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Epidemiology. Sharks are denitive hosts for this

cestode which also occurs in a range of pelagic sh apart from tuna. Diagnosis. Presumptive diagnosis can be made on the basis of the plerocercoids having a long scolex with four shallow, elongate bothridia and four short, retractile, hook-bearing tentacles. Treatment and prevention. Not practicable at present. Anisakid nematode infection
Aetiology. These parasites are of importance because they can potentially infect humans. Parasites of interest are Anisakis simplex and Hysterothylacium cornutum (Williams & Bunkley-Williams 1996). Clinical signs. The infections are covert. Pathology. The small third-stage larvae are found encapsulated in the peritoneal mesenteries and, sometimes, the liver. If the sh are not quickly eviscerated it is possible for the larvae to migrate to the abdominal muscles. Epidemiology. The denitive hosts of these parasites are marine mammals. Many other species of sh can act as intermediate hosts. Diagnosis. The presence of tightly coiled, encapsulated larval nematodes in the mesenteries of tunas is suggestive of anisakid nematode infection, but denitive identication of the larvae can be difcult. Treatment. There is no practicable treatment. Prevention. Human infection can be prevented by rapid evisceration of the sh and/or cooking of the esh. In most instances tuna destined for sashimi are eviscerated soon after capture.

Copepod infections
Aetiology. A number of copepods parasitise Thunnus

spp. (Table 1) but only C. elongatus, Euryphros brachypterus and Penella losa are potentially pathogenic. Clinical signs. Rough et al. (1999) reported that C. elongatus grazes on the integument of southern bluen tuna and may produce grazing trails including over ocular tissues. Damage to the eye results in keratitis, panopthalmitis and cataract formation. Very heavy infections of Euryphorus brachypterus have been reported in northern bluen tuna in which the pseudobranch has been carpeted with the parasite leading to ulceration and bleeding. Similar, but less severe lesions may be present on the gills and skin (Williams & Bunkley-Williams 1996.
2003 Blackwell Publishing Ltd

The very large copepod Penella losa (50 mm long) penetrates into the muscles of a number of tuna species. It has been reported to cause the sh considerable discomfort (Williams & BunkleyWilliams 1996). Pathology. Lesions because of the above copepods are related to their grazing behaviour (C. elongatus) or the damage caused by their attachment to the host (Euryphorus brachypterus and Penella losa). Epidemiology. As C. elongatus and Penella losa have multiple hosts, tuna may become infected from a variety of sources. However, Euryphorus brachypterus is almost genus specic for Thunnus spp. (Williams & Bunkley-Williams 1996). In the case of C. elongatus infecting captive southern bluen tuna, capture trauma and high stocking densities are believed to predispose to heavy infections (Rough et al. 1999). Diagnosis. Experienced diagnosticians can make a presumptive diagnosis of these copepod infections based on the morphology of the parasites and the types of lesions induced by their activities. However, denitive diagnosis is only possible by a scientist skilled in identifying the parasites. Treatment. Although a number of therapeutants are capable of killing copepod parasites (Lester & Roubal 1999) it is impracticable to use these agents under current tuna aquaculture conditions. In addition, at the present level of loss of production, such treatments would be uneconomical. Prevention. As Rough et al. (1999) have suggested that trauma may predispose to Caligus elongatus infections then reduction of damage because of capture, towing and harvesting should simultaneously reduce the level of infestation/damage caused by this copepod. Additionally, as this parasite and Penella losa are carried by other species of sh, it would be appropriate to keep other forms of aquaculture separate from tuna farms.

Non-infectious diseases

Nutritional diseases In the early stage of the Pacic bluen tuna aquaculture in Japan, morbidity and mortality was reported caused by a shortage of thiamin (Yamaguchi 1986). At that stage only Pacic saury, Cololabis saira (Brevoort), and/or Japanese anchovy, Engraulis japonicus Temminck & Schlegel, was fed to the sh resulting in a large reduction of thiamin stores in the cultured sh. These baitsh contain

198

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

thiaminase which is capable of producing an induced thiamin deciency in tuna. At present, several kinds of baitsh are fed to tuna in Japan and this disease no longer occurs. There have been no reports of nutritional diseases in cultured southern bluen tuna. However, relatively low levels of vitamin E have been found in the livers (mean 33 lg g)1) of southern bluen tuna fed on baitsh (B.L. Munday, unpublished data). These are comparable with those (40 lg g)1) reported by McLoughlin, Kennedy & Kennedy (1992) in rainbow trout with vitamin E-responsive myopathy.

Toxicoses Microalgal toxicosis

Aetiology. There are no unequivocal reports of

mortalities in tuna because of toxic microalgae but the evidence for Chattonella marina causing the mass mortality episode in southern bluen tuna at Port Lincoln, South Australia in 1996 is compelling (Munday & Hallegraeff 1998). Clinical signs. Ishimatsu, Sameshima, Tamura & Oda (1996) reported that sh affected by Chattonella toxicosis had excessive production of gill mucus leading to respiratory distress. These signs were reported in southern bluen tuna dying in the 1996 incident. In that incident mortalities varied from 22 to 92%. Pathology. Munday & Hallegraeff (1998) reported histopathological lesions in the gills with epithelial swelling, variable lifting of the epithelium (Fig. 6a,b) and apparent blockage of gill fenestrations by mucus. These lesions are consistent with those produced experimentally in yellowtail exposed to Chattonella marina (Ishimatsu et al. 1996). Epidemiology. The toxicity of Chattonella marina and other toxic algae is governed by a range of variables including the stage of growth, temperature, availability of iron and level of irradiation (Kawano, Oda, Ishimatsu & Muramatsu 1996; Khan, Haruyama, Iwashita, Ono & Onoue 2000; Pickell & Trick 2000). In relation to the latter it is important to note that the Australian Chattonella marina isolates are adapted to much higher irradiances than Japanese isolates (Marshall & Hallegraeff 1999). Diagnosis. Unequivocal diagnosis of microalgal toxicosis can often be problematic unless facilities for microalgal collection, identication and quantication are already in place when an episode occurs.
2003 Blackwell Publishing Ltd

Even when such facilities are available, diagnosis depends upon observing typical clinical signs and pathology in association with appropriate levels of microalgal cells in the water column at the time of the mortality. Okaichi, Ochi, Nishio, Takano, Matsuno, Morimoto, Murakami & Shimada (1989) reported that 500 Chatonella marina cells mL)1 were lethal to yellowtail. Additionally, Hishida, Katoh, Oda & Ishimatsu (1998) found that yellowtail were much more suceptible to this toxicosis than red sea bream or Japanese ounder and the relative susceptibilities were directly related to the ventilation volumes of these sh. As yellowtail have a ventilation volume of 1099.6 mL/kg/min and yellown tuna (no data are available for southern bluen tuna) have a ventilation volume of 3900 mL kg)1 min)1 (Bushnell, Brill & Bourke 1990) then it is to be expected that a much lower concentration of Chattonella marina (170 mL)1) would be toxic for Thunnus spp. Other host-associated factors to be considered are the additive effects of low dissolved oxygen in the water and cardiopathy because of blood uke infection. Treatment. There are no practicable treatments. Prevention. The most efcacious means of prevention is by towing the tuna cages away from the bloom (Rensel 2000). Other strategies are the use of perimeter skirts in association with airlifts and spreading certain types of clays to remove toxic microalgae from net-pens by occulation (Rensel 2000).

Trauma Trauma to wild-caught sh

Aetiology. Seedlings (2040 cm total length) for Pacic bluen tuna aquaculture in Japan are caught by trolling and these sh are sometimes injured in their jaws or other parts of the body. In the case of southern bluen tuna caught by seine net when about 3 years of age, trauma can occur during capture, towing, transfer and eventual harvest. Often this is exacerbated by unfavourable weather conditions. Attempts by predators to attack sh in cages can lead to substantial trauma. Clinical signs. Affected sh have skin wounds of variable size and commonly there is damage to the eyes which may lead to blindness. Severely damaged sh usually die.

199

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Figure 6 Comparison of normal and abnormal southern bluen tuna gills. (a) Normal southern bluen tuna gill secondary lamellae (H & E, bar 50 lm). (b) Abnormal southern bluen tuna gill secondary lamellae in a sh exposed to Chattonella marina. Note subepithelial oedema (o) (H & E, bar 50 lm).

Pathology. As would be expected damaged sh

frequently have local and systemic infections with opportunistic bacteria such as Aeromonas and Vibrio spp. Epidemiology. Although most tuna harvesters and/or farmers use basically the same techniques there are differences based on the species and age of the tuna and the distance between the capture site and the farms. Pacic bluen tuna caught by Japanese operators are usually between 0.2 and 1 kg and are rarely more than 48 h in transit (Miyashita, Sawada, Hattori, Nakatsukasa, Okada, Murata & Kumai 2000). In contrast, southern bluen tuna sourced by Australian operators are usually 1220 kg and may be towed for up to 2 weeks before reaching the farming sites. However, it is suggested by operators that southern bluen tuna are more robust and, therefore, do not suffer as much injury, especially once in farm cages, as might be expected. The mesh size of nets is important otherwise sh may become gilled and die or are damaged. In addition, operators suggest that a degree of net 2003 Blackwell Publishing Ltd

fouling makes the net more visible and, therefore, less likely to be impacted by the sh. Siting net cages near seal colonies can lead to increased attacks and discharge of blood during harvesting can attract sharks. Diagnosis. The injuries are usually self-evident but determining the cause(s) can be problematic. Treatment. Treatment is usually not practicable. Prevention. Prevention is mainly by applying good husbandry principles such as not towing cages at an excessive speed. Areas which require special attention are selection of mesh sizes for net pens and methods of harvesting (hook and line rather than gafng). Predators should be excluded by use of predator nets or tightly tensioned, heavy nets. Morbidity and mortality of Pacic bluen tuna during hatchery and early growout culture
Aetiology. The end cause of the syndrome is collision of juvenile tuna with the walls of tanks or mesh of nets (Miyashita et al. 2000).

200

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Figure 7 Juvenile Pacic bluen tuna embedded in PVC sheeting used to prevent the sh impacting directly on the walls of the tank. Illustration from Miyashita et al. (2000).

Clinical signs. The sh have been observed to

Management problems Cannibalism in Pacic bluen larvae

Aetiology. Cannibalism is related to the predatory nature of tuna and becomes a problem when there are variable sizes in a cohort of these sh. Clinical signs. There is a continual reduction in numbers of larvae from 14 to 20 days post-hatch (Sawada, Kato, Okada, Kurata, Mukai, Miyashita, Murata & Kumai 1999). Also, some sh may be observed swallowing smaller sh. Pathology. Cannibalism is often accompanied by n and eye nipping with resultant damage to these areas. Epidemiology. As indicated above, the predatory nature of tuna is a major factor. Also, stocking densities, feed availability and other managerial factors may be involved. Treatment. Treatment is not possible. Prevention. Stocking densities may be reduced and care taken that sh do not become excessively hungry.

respond to external stimuli by panicking and colliding with the sides of tanks or net pens (Fig. 7). Miyashita, Sawada, Hattori, Nakatsukasa, Okada, Murata & Kumai (2000) reported that mortality increased from 4.9% on day 33 after hatch to 8.9% on day 52 and then stabilized at about 4% day)1 leading to very few survivors at day 60 after hatch. Pathology. Affected sh have had considerable damage to the vertebral column and the parasphenoid bones. Epidemiology. The syndrome is apparently the result of conning free-ranging young sh in a restricted area. Such sh usually escape danger by rapid ight, but this is not possible within the connes of tanks or cages. In addition, Miyashita et al. (2000) make the point that in Pacic tuna juveniles development of muscle and caudal n shape occurs earlier than development of pectoral ns and caudal keels, i.e. swimming ability develops in advance of steering ability. Even weak stimuli such as ashes of light or vibrations were reported to lead to panic responses in the juvenile tuna resulting in collisions with the sides of the culture vessels/nets. Diagnosis. Diagnosis can be made by observing the sh and/or by nding the typical skeletal lesions. Treatment. Treatment is impracticable. Prevention. Miyashita et al. (2000) reported that apart from minimizing stimuli, the most useful preventive measure was to institute a 24-h light regime so that the sides of the tanks/nets were visible to the sh at all times.
2003 Blackwell Publishing Ltd

Adhesion of Pacic bluen larvae to the water surface

Aetiology. The thick skin mucus layer which is present from hatching and develops with age causes the larvae to adhere to the surface of the water when carried there by aeration currents. As the sh become older and more competent swimmers they are able to extricate themselves (Sawada 1999). Clinical signs. The condition is quite characteristic with the larvae being trapped at the surface of the water and suffering from desiccation.

201

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Pathology. The pathology has not been described. Epidemiology. As larval Pacic bluen tuna have a

very high oxygen requirement (Miyashita, Hattori, Sawada, Ishibashi, Nakatsukasa, Okada, Murata & Kumai 1999) aeration must be vigorous, thus inducing the condition. Diagnosis. The presence of larvae trapped at the surface of the water is quite obvious. Treatment. Affected larvae can be removed to static containers but are not likely to survive. Prevention. Use of oxygen rather than air as a source of water oxygenation over the rst 7 days after hatch may allow less vigorous aeration and thus reduce losses. Additionally, providing an oil lm on the water surface is very effective. The oil lm prevents the larvae being exposed to the air when they are transported to the water surface. This preventive measure is used for other sh larvae, such as grouper larvae, in which the same problem occurs during seedling production (Sawada et al. 1999). Neoplasia
Clinical signs. Supercial lipomas constitute the majority of reported tumours in Thunnus spp. (Easa, Harshbarger & Hetrick 1989; Harshbarger, personal communication; Lester & Kelly 1983) and may constitute up to 10% of body mass. Pathology. Of eight reported tumours, three were lipomas (op.cit.), two were osteomas (J.C. Harshbarger, personal communication) and one each a broma, an invasive schwannoma (J.C. Harshbarger, personal communication) and a melanoma (Anders 1988). Diagnosis. Diagnosis relies upon histological examination of the tumours.

physical exertion, e.g. yellown tuna caught by handline. Clinical signs. There are no clinical signs as this is a post-mortem condition. Pathology. Instead of being red, translucent and rm affected muscles are pale, watery and soft. Epidemiology. Burnt tuna are mainly associated with the yellown tuna handline shery (Watson 1995) and the condition has been reported occasionally in southern bluen tuna (Williams 1986). As indicated above, Watson (1995) suggested that the stress involved in handline shing leads to catecholamine release which promotes glycogenolysis. If the sh have limited glycogen reserves, ATP is reduced and muscle pH elevated leading to calpain proteolysis of the Z-discs of the musculature. Diagnosis. The condition can be diagnosed by observing the typical muscle lesions. Prevention. Cultured tuna are unlikely to be affected by this condition because they usually have adequate stores of muscle glycogen (B.L. Munday, unpublished data). More efcient catching methods such as polling for wild sh should obviate the problem. Eye lesions
Aetiology. Some are traumatic but the aetiologies of others are unknown. Clinical signs. Abnormalities vary from cataracts, to corneal ulcers, to complete loss of the orbit. Pathology. The pathology has not been described in tunas. Epidemiology. Most of the corneal lesions are probably caused by contact with nets. The aetiology of cataracts is not known, although UV irradiation has been suggested as one possible cause. Diagnosis. The lesions are self-evident although small cataracts can be difcult to detect. Treatment. There are no practicable means of treating captive southern bluen tuna for these conditions. Prevention. Improved management should reduce the prevalence of corneal lesions. Until the cause of cataracts is established it is not possible to suggest means of preventing them.
General discussion including future directions

Other conditions Burnt tuna

Aetiology. The most plausible explanation for this condition is that it is a form of calpain proteolosis (Watson 1995). The suggestion is that low intracellular ATP concentrations lead to the breakdown of calcium homeostasis with an increase in cytosolic calcium, which activates calpain. Calpain is an enzyme which attacks non-contractile proteins, such as the Z-discs of muscle. Low intracellular ATP concentrations are likely to occur in sh which have low glycogen reserves and are subjected to intense
2003 Blackwell Publishing Ltd

The present system of using wild-caught seedstock for aquaculture purposes has been characterized by

202

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

the occurrence of relatively few bacterial diseases. The reasons for this situation are probably manifold but the observation that tunas immune responses may be independent of ambient temperatures would seem to be a key factor when tuna are held at relatively low temperatures (Watts, Munday & Burke 2002). It is paradoxical that a great number of rst class physiological studies have been undertaken on skipjack, Katsuwonas pelamis (L.), and yellown tuna, whereas most tunas used for aquaculture are southern, northern or Pacic bluen tuna. While it is possible to extrapolate from one species to another, there is ample evidence that signicant differences in physiology do occur (Bushnell, Brill & Bourke 1990) and such extrapolation could lead to erroneous decisions being made. Obviously, this is an area requiring urgent attention. The use of oily baitsh as a source of food for captive tuna poses a number of problems. First, the presence of thiaminases and oxidized lipids in these sh has been, or is likely to be, responsible for nutritional problems in the tuna (B.L. Munday, unpublished data; Yamaguchi 1986). Also, baitsh are known to carry important viral diseases such as viral haemorrhagic septicaemia (Kocan, Hershberger, Elder & Winton 2001) and pilchard herpesvirus (Hyatt, Hine, Jones, Whittington, Kearns, Wise, Crane & Williams 1997). Consequently, the development of a palatable articial feed which produces desirable carcass composition is an urgent need. Experiences of Japanese workers with preliminary attempts to hatch and raise tuna have indicated that hatchery propagation is fraught with many problems and it may be some years before such sh will replace seedstock caught from the wild. However, it is important that this research continues because, as in the case of the threatened southern bluen tuna, completing the life cycle has conservation in addition to commercial implications.
Acknowledgements

References
AQIS (1999) Import Risk Analysis on Non-viable Salmonids and Non-salmonid Marine Finsh. Ausinfo, Canberra. Ahmad J. (1983) Studies on digenetic trematodes of the family Opecoelidae Ozaki, 1925 from marine shes of India. Rivista di Parassitologia 44, 233246. Anders K. (1988) Biologie von tumor- und tumorahnlichen Kranheiten der Elbsche. Verlag Heino Moller, Kiel. Arai Y. & Matsumoto K. (1953) On a new sporozoa, Hexacapsula neothunni g. and sp. n. from the muscle of yellown tuna, Neothunnus macropterus. Bulletin of the Japanese Society of Scientic Fisheries 18, 293298. Ariola V. (1902) Contributo per una monograa dei Didymozoon. I. Didymozoon parassiti del tonno. Archives de Parasitologie 6, 99108. Austin B. & Austin D.A. (1987) Bacterial Fish Pathogens: Disease in Farmed and Wild Fish. Ellis Horwood, Chichester. Baudin-Laurencin F. & Richard J. (1973) Phyllodistomum thunni n. sp. (Trematoda, Gorgoderidae). Trematode parasite du um Thon albacore Thunnus albacares. Bulletin du Muse National dHistoire Naturelle 166, 10411043. Baudin-Laurencin F. (1971) Crustaces et helminthes parasites de lalbacore (Thunnus albacares) du Golfe de Guinee note preliminaire. Documents scientiques. Centre de Rechercher anographiques Abidjan 2, 1130. Oce Biavati S. & Manera M. (1991) Acid-fast bacterial granulomatous peritonitis in a tuna sh (Thunnus thynnus). Bollettino, Societa Italiana di Patologie 7, 710 [in Italian]. Brill R.W. (1996) Selective advantage conferred by the high performance physiology of tunas, billshes and dolphin sh. Comparative Biochemistry and Physiology 113A, 315. Buchanan J. (2002) Tuna research farm progress. In: Tuna-Brief. Southern Bluen Tuna Aquaculture Subprogram Newsletter. 2002/03 Experimental Program Edition Number 1. South Australian Research and Development Institute, Adelaide, South Australia. Bushnell P.G., Brill R.W. & Bourke R.E. (1990) Cardiorespiratory responses of skipjack tuna Katsuwonus pelamis, yellown tuna Thunnus albacares and bigeye tuna T.obesus to acute reductions in ambient oxygen. Canadian Journal of Zoology 68, 18571865. Bussieras J. & Aldrin J.F. (1965) Une tetrarhynchose vasculaire des thons du Golfe de Guinee due aux larves plerocercus de Dasyrhynchus talismani R. Ph. Dollfus 1935. Revue dElevage et decine Ve terinaire des Pays Tropicaux 18, 137143. de Me Bussieras J. & Baudin-Laurencin F. (1973) Les helminthes decine parasites des thons tropicaux. Revue dElevage et de Me terinaire des Pays Tropicaux 26, 1319. Ve Cannon L.R.G. (1977) Some ecological relationships of larval ascaridoids from south eastern Queensland marine shes. International Journal for Parasitology 7, 227232. Colquitt S.E., Munday B.L. & Daintith M. (2001) Pathological ndings in southern bluen tuna, Thunnus maccoyii (Castelnau), infected with Cardicola forsteri (Cribb, Daintith & Munday, 2000) (Digenea: Sanguinicolidae), a blood uke. Journal of Fish Diseases 24, 225229.

The authors wish to acknowledge the valuable assistance provided by Drs I. Beveridge of the University of Melbourne, J. B. Jones of the Western Australian Department of Fisheries and J. Harshbarger of the George Washington University. The authors also thank Dr Miyashiata of Kinki University and three anonymous reviewers for their helpful comments.
2003 Blackwell Publishing Ltd

203

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Cribb T.H., Daintith M. & Munday B. (2000) A new blood uke, Cardicola forsteri (Digenea: Sanguinicolidae) of southern bluen tuna (Thunnus maccoyii) in aquaculture. Records of the South Australian Museum 124, 117120. Crosbie P.B.B. (1996) Environmental Factors and Chemical Agents Affecting the Growth of Uronema nigricans. Honours thesis, University of Tasmania, Tasmania. Dollfus R.-P. (1942) Etudes critiques sur les tetrarhynques du um National dHistoire Museum de Paris. Archives du Muse Naturelle, Paris 19, 1466. Dollfus R. (1952) Parasites du Germo alalunga (J.F. Gmelin 1788). Journal du Conseil International Pour lExploration de la Mer 43, 4244. Easa M.E.-S., Harshbarger J.C. & Hetrick F.M. (1989) Hypodermal lipoma in a striped (grey) mullet Mugil cephalus. Diseases of Aquatic Organisms 6, 157160. Eckmann F. (1932) Beitrage zur Kenntnis der Trematodenr familie Bucephalidae. Zeitschrift fu Parasitenkunde 5, 92 111. Farrell A.P. (1996) Features heightening cardiovascular performance in shes, with special reference to tunas. Comparative Biochemistry and Physiology 113A, 6167. Gibson D.I. & Bray R.A. (1977) The Azygiidae, Hirudinellidae, Ptychogonimidae, Sclerodistomidae and Syncoeliidae of shes from the north-east Atlantic. Bulletin of the British Museum (Natural History) Zoology 32, 167245. Hafeezullah M. (1971) On some new and known digenetic trematodes from marine shes of India. Journal of Helminthology 45, 7388. Hamaguchi M. & Kusuda R. (1992) Studies on virulence of Photobacterium phosphoreum against bluen tuna, Thunnus thynnus. Bulletin of the Nansei National Fish Research Institute 25, 5992 [in Japanese]. Hishida Y., Katoh H., Oda T. & Ishimatsu A. (1998) Comparison of physiological responses to exposure to Chattonella marina in yellowtail, red sea bream and Japanese ounder. Fisheries Science 64, 875881. Hogans W.E. (1985) Occurrence of Caligus coryphaenae (Copepoda, Caligidae) on the Atlantic bluen tuna (Thunnus thynnus L) from Prince Edward Island, Canada. Crustaceana 49, 313314. Humphrey J.D. (1995) Australian Quarantine Policies and Practices for Aquatic Animals and Their Products. A Review for the Scientic Working Party on Aquatic Animal Quarantine. Bureau Of Resource Sciences, Canberra. Hyatt A.D., Hine P.M., Jones J.B., Whittington R.J., Kearns C., Wise R., Crane M.S. & Williams L.M. (1997) Epizootic mortality in the pilchard Sardinops sagax neopilchardus in Australia and New Zealand in 1995. II Identication of a herpes virus within the gill epithelium. Diseases of Aquatic Organisms 28, 1729. Hyatt A.D., Gould A.R., Zupanovic Z., Cunningham A.A., Hengstberger S., Whittington R.J., Kattenbelt J. & Coupar B.E.H. (2000) Comparative studies of piscine and amphibian iridoviruses. Archives of Virology 145, 301331. Inouye K., Yamano K., Maeno Y., Nakajima K., Matsuoka M., Wada Y. & Sorimachi M. (1992) Iridovirus infection of

cultured red seabream, Pagrus major. Fish Pathology 27, 1927 [in Japanese]. Ishii N. (1935) Studies on the family Didymozoidae (Monticelli, 1888). Japanese Journal of Zoology 6, 279335. Ishimatsu A., Sameshima M., Tamura A. & Oda T. (1996) Histological analysis of the mechanisms of Chattonellainduced hypoxemia in yellowtail. Fisheries Science 62, 5058. Jones J.B. (1990) Goussia auxidis (Dogiel, 1984) (Apicomplexa: Calyptosporidae) from tuna (Pisces: Scombridae) in the South Pacic. Journal of Fish Diseases 13, 215223. Jones J.B. (1991a) Movements of albacore tuna (Thunnus alalunga) in the South Pacic: evidence from parasites. Marine Biology 111, 19. Jones J.B. (1991b) Parasitic copepods of albacore tuna (Thunnus alalunga) in the South Pacic. Bulletin of the Plankton Society of Japan Special Volume, 419428. Kailola P.J., Williams M.J., Stewart P.C., Reichelt R.E., McNee A. & Grieve C. (1993) Australian Fisheries Resources. Commonwealth of Australia, Brisbane. Kawakami H. & Nakajima K. (2002) Cultured sh species affected by red sea bream iridoviral disease. Fish Pathology 37, 4547. Kawano I., Oda T., Ishimatsu A. & Muramatsu T. (1996) Inhibitory effect of iron chelator desferrioxamine (Desferal) on the generation of activated oxygen species by Chattonella marina. Marine Biology 126, 765771. Kent M.L., Andree K.B., Bartholomew J.L., El-Matbouli M., Desser S.S., Devlin R.H., Feist S.W., Hedrick R.P., Hoffman R.W., Khattra J., Hallett S.L., Lester R.J.G., Longshaw M., Palenzeula O., Siddall M.E. & Xiao C. (2001) Recent advances in our knowledge of Myxozoa. The Journal of Eukaryotic Microbiology 48, 395413. Khan S., Haruyama M., Iwashita S., Ono K. & Onoue Y. (2000) Environmental factors affecting the neurotoxin production of Chattonella antiqua (Raphidophyceae). Conference abstracts: 9th International Conference on Harmful Algal Blooms, Hobart, 711 February 2000, p. 27. UNESCO, Paris Kocan R.M., Hershberger P.K., Elder N.E. & Winton J.R. (2001) Epidemiology of viral hemorrhagic septicaemia among juvenile Pacic herring and Pacic sand lances in Puget Sound, Washington. Journal of Aquatic Animal Health 13, 7785. Kohn A. & Cohen S.C. (1998) South American Monogenea list of species, hosts and geographical distribution. International Journal for Parasitology 28, 15171554. Korotaeva V.D. & Korjakovtzeva L.P. (1983) On the systematic position and distribution of some trematodes of the genera Dinurus and Ectenurus. Parazitologiya 17, 6465 [in Russian]. Korsmeyer K.E., Dewar H., Lai N.C. & Graham J.B. (1996) The aerobic capacity of tunas: adaption for multiple metabolic demands. Comparative Biochemistry and Physiology 113A, 1724. Ku C.-T. & Shen J.W. (1965) Taxonomic study on the family Didymozidae Poche, 1907. (Trematodes) from some marine shes in China. Acta Scientiarum Naturalium Universitatis Nan Kaiensis 6, 2148. Langdon J.S. (1990) Observations on new Myxobolus species and Kudoa species infecting the nervous system of Australian shes. Journal of Applied Ichthyology 6, 107116.

2003 Blackwell Publishing Ltd

204

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Lee C.L. (1998) A Study on the Feasibility of the Aquaculture of the Southern Bluen Tuna in Australia. Agriculture, Fisheries and Forestry-Australia, Canberra. Lester R.J.G. & Kelly W.R. (1983) Tumor like growths from southern Australian marine sh. Tasmanian Fisheries Research 25, 2732. Lester R.J.G. & Roubal F.R. (1999) Phylum Arthropoda. In: Fish Diseases and Disorders, Vol. 1, Protozoan and Metazoan Infections (ed. by P.T.K. Woo), pp. 475598. CABI Publishing, Wallingford. Linton E. (1901) Parasites of shes of the Woods Hole Region. Bulletin of the United States Fish Commission 19, 405492. Linton E. (1940) Trematodes from shes mainly from the Woods Hole region, Massachusetts. Proceedings of the United States National Museum 88, 1172. Lom J. & Dykova I. (1992) Protozoan Parasites of Fish. Elsevier, Amsterdam. McLoughlin M.F., Kennedy S. & Kennedy D.G. (1992) Vitamin E-responsive myopathy in rainbow trout fry (Oncorhynchus mykiss). Veterinary Record 130, 224226. Manter H.W. (1970) A new genus of trematode (Digenea: Gorgoderidae) from the ureter of tuna sh (Thunnus maccoyii) in Australia. Transactions of the Royal Society of South Australia 94, 147150. Marshall J.A. & Hallegraeff G.M. (1999) Comparative ecophysiology of the harmful alga Chattonella marina (Raphidophyceae) from South Australian and Japanese waters. Journal of Plankton Research 21, 18091822. Miyashita S., Hattori N., Sawada Y., Ishibashi Y., Nakatsukasa H., Okada T., Murata O. & Kumai H. (1999) Ontogenetic change in oxygen consumption of bluen tuna, Thunnus thynnus. Suisanzoshoku 47, 269275. Miyashita S. & Kumai H. (2002) Present status of Pacic bluen tuna seedling production. Aquaculture Magazine 39, 6871. Miyashita S., Sawada Y., Hattori N., Nakatsukasa H., Okada T., Murata O. & Kumai H. (2000) Mortality of northern bluen tuna Thunnus thynnus due to trauma caused by collision during growout culture. Journal of the World Aquaculture Society 31, 632639. Miyata M., Matsuno K., Jung S.J., Danayadol Y. & Miyazaki T. (1997) Genetic similarity of iridoviruses from Japan and Thailand. Journal of Fish Diseases 20, 127134. Moravec F., Kohn A. & Santos L.A. (1999) New data on Oncophera melanocephala (Nematoda: Camallanidae), a littleknown parasite of scombrid shes. Parasite 6, 7984. Munday B.L. & Hallegraeff G.M. (1998) Mass mortality of captive southern bluen tuna (Thunnus maccoyii) in Boston Bay, South Australia: a complex diagnostic problem. Fish Pathology 33, 343350. Munday B.L., ODonoghue P.J., Watts M., Rough K. & Hawkesford T. (1997) Fatal encephalitis due to the scuticociliate Uronema nigricans (Mueller) in sea-caged, southern bluen tuna, Thunnus maccoyii (Castelnau). Diseases of Aquatic Organisms 30, 1725. Murugesh M. & Madhavi R. (1995) Some new and known species of the genus Didymocystis Ariola, 1902 (Trematoda:
2003 Blackwell Publishing Ltd

Didymozoidae) from scombrid shes of the Visakhapatnam coast, Bay of Bengal. Systematic Parasitology 31, 1124. Murugesh M. (1995) Larval cestode parasites from scombrid sh of the Visakhapatnam coast, Bay of Bengal. Rivista di Parasitologia 56, 371380. Nakai T. & Nakajima K. (2002) Recent advances of nodaviruses and iridoviruses in Asian aquaculture. Conference abstracts: 5th Symposium on Diseases in Asian Aquaculture, Surfers Paradise, 2428 November 2002, p. 44. Asian Fisheries Society, Manila. Nakajima K., Maeno Y., Yokoyama K., Kaji C. & Manabe S. (1998) Antigenic analysis of red sea bream iridovirus and comparison with other sh iridoviruses. Fish Pathology 33, 73 78 [in Japanese]. Nakajima K., Maeno Y., Honda A., Yokoyama K., Tooriyama T. & Manabe S. (1999) Effectiveness of a vaccine against red sea bream iridoviral disease in a eld trial test. Diseases of Aquatic Organisms 36, 7375. Nikolaeva V.M. (1988) New and poorly studied species of Koellikeriinae (Trematoda, Didymoxoidae). Ekologiya Morya 30, 6470 [in Russian]. Nikolaeva V.M. & Dubina V.R. (1978) New species of didymozoids from Indian Ocean sh. Biologiya Morya, Kiev 45, 7190 [in Russian]. Nikolaeva V.M. & Dubina V.R. (1985) On the Didymozoidae of sh in the western Indian Ocean. Ekologia Morya, Kiev 20, 1326 [in Russian]. Nikolaeva V.M. & Parukhin A.M. (1968) To the study of sh helminths in the Gulf of Mexico. In: Explorations of Central American Seas (ed. by E.B. Jankovskaya), pp. 126149. Naukova Dumka, Kiev. Ogawa K. (1996) Marine parasitology with special reference to Japanese sheries and mariculture. Veterinary Parasitology 64, 95105. Okaichi T., Ochi T., Nishio S., Takano H., Matsuno K., Morimoto T., Murakami T. & Shimada S. (1989) The cause of sh kills associated with red tides of Chattonella antiqua (Hada). In: Current Topics in Marine Biotechnology (ed. by S. Miyachi, I. Karube & Y. Ishida), pp. 185188. Japanese Society of Marine Biotechnology, Tokyo. Oshima S., Hata J., Hirasawa N., Ohtaka T., Hirono I., Aoki T. & Yamashita S. (1998) Rapid diagnosis of red sea bream iridovirus infection using the polymerase chain reaction. Diseases of Aquatic Organisms 32, 8790. Payne R.R. (1990) Four new Monogenea (Axinidae and Heteraxinidae) from eastern Pacic Ocean shes. Journal of the Helminthological Society of Washington 57, 93103. Peric Z. (2002) Morphological and histological changes of the parenchymatous organs of blue n tuna, Thunnus thynnus (Linnaeus, 1758). Abstract: First International Conference on the Domestication of Tuna, Thunnus thynnus, Cartegena, Spain, 38 February 2002. DOTT Organizing Committee of the EC, The Spanish Institute of Oceanography and the Politechnical University of Cartegena. Pickell L.D. & Trick C.G. (2000) The effects of iron limitation on growth and physiology of the coastal marine raphidophyte, Heterosigma. Conference abstracts: 9th International

205

Journal of Fish Diseases 2003, 26, 187206

B L Munday et al. Diseases of tunas

Conference on Harmful Algal Blooms, Hobart, 711 February 2000, p. 200. UNESCO, Paris. Pozdnyakov S.E. (1987a) Didymonaja branchialis n.g., n.sp. (Trematoda, Didymozoidae), a parasite of Thunnus alalunga in the north-eastern Pacic Ocean. Parazitologiya 21, 755757 [in Russian]. Pozdnyakov S.E. (1987b) Systematic position of some representatives of the subfamily Didymozoinae (Trematoda; Didymozoidae). Gelminty i vyzyvaemye imi zabolevaniya, 5259 [in Russian]. Pozdnyakov S.E. (1990) Helminths of Scombrid-like Fishes of the Worlds Oceans. DVO AN SSSR, Vladivostok [in Russian]. Rensel J. (2000) Mitigation of harmful algal blooms in sh mariculture. Conference abstracts: 9th International Conference on Harmful Algal Blooms, Hobart, 711 February 2000, p. 49. Rough K.M. (2000) An Illustrated Guide to the Parasites of Southern Bluen Tuna, Thunnus maccoyii. Tuna Boat Owners Association of South Australia, Eastwood. Rough K.M., Lester R.J.G. & Reuter R.E. (1999) Caligus elongatus a signicant parasite of cultured southern bluen tuna Thunnus maccoyii. Book of Abstracts, World Aquaculture 99, 26 April2 May 1999, Sydney, p. 655. World Aquaculture Society. Santer R.M. & Greer-Walker M. (1980) Morphological studies on the ventricle of teleost and elasmobranch hearts. Journal of Zoology (London) 190, 259272. Sawada Y., Kato K., Okada T., Kurata M., Mukai Y., Miyashita S., Murata O. & Kumai H. (1999) Growth and morphological development of larval and juvenile Epinephelus bruneus (Perciformes:Serranidae). Ichthyological Research 46, 254257. Sawada Y. (1999) Larval culture of bluen tuna. Book of Abstracts, World Aquaculture 99, 26 April2 May 1999, Sydney, p. 679. World Aquaculture Society. Schmidt G.D. (1986) CRC Handbook of Tapeworm Identication. CRC Press, Boca Raton. Shen J. (1990) Digenetic Trematodes of Marine Fishes from Hainan Island. Science Publications, Beijing. Smith J.W. (1997) The blood ukes (Digenea: Sanguinicolidae and Spirorchidae) of cold-blooded vertebrates: Part 2. Helminthological Abstracts 66, 329344. Srivastava H.D. & Sahai D. (1978) Trematodes of Indian shes. Part 4. Four new genera, one new subfamily and one new species with a review of the species of Ophiocorchis Srivastava, 1933 (family Hemiuridae Luhe, 1901). Proceedings of the National Academy of Sciences, India, Section B 48, 3952. Taschenberg E.O. (1879) Didymozoon, eine neue Gattung in r Cysten lebender Trematoden. Zeitschrift fu die Gesamte Naturwschrift 52, 605617.

Walters V. (1980) Ectoparasites of eastern and western Atlantic bluen tunas. International Commission for the Conservation of Atlantic Tunas, Collective Volume of Scientic Papers 9, 491498. Watson C. (1995) Burnt tuna: a problem of heat inside and out? In: Biochemistry and Molecular Biology of Fishes, Vol. 5 (ed. by P.W. Hochachk & T.P. Mommsen), pp. 127145. Elsevier, Amsterdam. Watts M., Burke C.M. & Munday B.L. (1996) The development of a uorescent antibody stain to identify a Uronema sp. (Ciliophora: Scuticociliatida) implicated in fatal encephalitis in southern bluen tuna (Thunnus maccoyii). Bulletin of the European Association of Fish Pathologists 16, 104108. Watts M., Munday B.L. & Burke C.M. (2002) Investigation of humoral immune factors from selected groups of southern bluen tuna, Thunnus maccoyii (Castelnau): implications for aquaculture. Journal of Fish Diseases 25, 191200. Wheeler T.A. & Beverley-Burton M. (1987) Nasicola hogansi n.sp. (Monogenea: Capsalidae) from bluen tuna, Thunnus thynnus (Osteichthyes; Scombridae), in the northwest Atlantic.Canadian Journal of Zoology 65, 19471980. Williams E.H. & Bunkley-Williams L. (1996) Parasites of Offshore Big Game Fishes of Puerto Rico and the Western Atlantic. Puerto Rico Department of Natural Environmental Resources and the University of Puerto Rico, Mayaguez. Williams S.C. (1986) Marketing Tuna in Japan. Queensland Fisheries Industry Training Commission, Brisbane. Yamaguchi M. (1986) Pacic bluen tuna. In: Shallow Sea Aquaculture (ed. by Shigenkyokai Corporation), pp. 335355. Taiseishuppansya, Tokyo. Yamaguti S. (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of shes. I. Japanese Journal of Zoology 5, 249 541. Yamaguti S. (1938) Studies on the helminth fauna of Japan. Part 24. Trematodes of shes. V. Japanese Journal of Zoology 8, 15 74. Yamaguti S. (1940) Studies on the helminth fauna of Japan. Part 31. Trematodes of shes, VII. Japanese Journal of Zoology 9, 35 108. Yamaguti S. (1970) Digenetic Trematodes of Hawaiian Fishes. Interscience, New York. Yamaguti S. (1971) Synopsis of Digenetic Trematodes of Vertebrates, I + II. Keigaku Publ. Co., Tokyo. Young P.C. (1970) The species of Monogenoidea recorded from Australian shes and notes on their zoogeography. Annals of the Institute of Biology, University of Mexico 41, 163176. Received: 2 September 2002 Accepted: 29 January 2003

2003 Blackwell Publishing Ltd

206