Outbreak of mortality among cage-reared cobia (Rachycentron canadum) associated with parasitism

Surto de mortalidade em bijupirá (Rachycentron canadum) criado em tanque-rede associado ao parasitismo

Cauê Bonucci Moreira Gabriela Sayuri de Oliveira Hashimoto Artur Nishioka Rombenso Fernanda Braz Candiotto Maurício Laterça Martins Mônica Yumi Tsuzuki About the authors

Abstracts

This study reports a disease outbreak among juvenile cobia (Rachycentron canadum) farmed in cages in the state of Rio de Janeiro, Brazil, caused by the dinoflagellate Amyloodinium ocellatum and the monogenean Neobenedenia melleni. Two thousand five hundred fish were stocked at 0.4 kg/m3 in a set of 12 m3 tanks, in autumn (mean weight 15.0 ± 7.3 g) and in winter (mean weight 43.0 ± 5.6 g). Freshwater baths were administered as a routine treatment, as the symptoms were detected followed by two collection samples. Firstly in May 2011 (n = 5) and secondly in September 2011 (n = 10). In the first sample, the prevalence of N. melleni on the body surface was 100% and the mean intensity was 42.0 ± 1.7, while in the second sample the prevalence was 60% with a mean intensity 3.0 ± 0.2 and mean abundance 1.8 ± 0.4. Amyloodinium ocellatum was only found in the second sample, at a prevalence 100% and mean intensity 46.8 ± 3.4. The cause of fish mortality was possibly associated with a decrease in fish resistance after the first contact with monogenean parasites, allied with respiratory difficulty caused by the presence of A. ocellatum in the gills.

Marine fish; parasitology; disease; culture; Brazil


Este estudo relata a mortalidade em massa de juvenis de bijupirá (Rachycentron canadum) criados em tanques-rede no estado do Rio de Janeiro, Brasil, causada pelo dinoflagelado Amyloodinium ocellatum e o monogenea Neobenedenia melleni. Dois mil e quinhentos peixes estavam estocados à densidade de 0,4 kg/m3 em tanques-rede de 12 m3, no período do outono (15,0 ± 7,3 g; peso médio ± DP) e inverno (peso médio de 43,0 ± 5,6 g). Banhos de água doce foram realizados rotineiramente à medida que os sintomas eram detectados, quando então, foram efetuadas duas colheitas, sendo a primeira em maio de 2011 (n = 5) e a segunda em setembro de 2011 (n = 10). Na primeira colheita, a prevalência de N. melleni foi de 100% e a intensidade média de 42,0 ± 1,7, e na segunda, a prevalência foi de 60% e intensidade média de 3,0 ± 0,2 e abundância média de 1,8 + 0,4. Na segunda colheita, observou-se a presença de A. ocellatum (prevalência de 100%, intensidade média de 46,8 ± 3,4). Possivelmente, a causa da mortalidade estava relacionada à redução na resistência dos peixes após o primeiro contato com o parasito monogenea, juntamente com a dificuldade respiratória causada pelo dinoflagelado nas brânquias.

Peixe marinho; parasitologia; doença; cultivo; Brasil


Cobia (Rachycentron canadum Linnaeus, 1766; known as bijupirá in Brazil) have aroused great interest in the aquaculture sector and scientific community, and are an emerging species for marine aquaculture (CAVALLI; HAMILTON, 2007Cavalli RO, Hamilton S. A piscicultura marinha no Brasil: afinal, quais as espécies boas para cultivar? Panorama da Aqüicultura 2007; 17(104): 50-55.). Cobia production started in Asia and has spread rapidly to other continents because of their positive characteristics such as rapid weight gain (around 4.5 kg per year), easy spawning in captivity (ARNOLD et al., 2002Arnold CR, Kaiser JB, Holt GJ. Spawning of cobia Rachycentron canadum in captivity. J World Aquacult Soc 2002; 33(2): 205-208. http://dx.doi.org/10.1111/j.1749-7345.2002.tb00496.x
http://dx.doi.org/10.1111/j.1749-7345.20...
; SOUZA-FILHO; TOSTA, 2008Souza-Filho JJ, Tosta GAM. Bijupirá: as primeiras desovas da geração F1. Panorama da Aqüicultura 2008; 18 (110): 50-53.) and availability of technology for fingerling production (HOLT et al., 2007Holt GJ, Faulk CK, Schwarz MH. A review of the larviculture of cobia Rachycentron canadum, a warm water marine fish. Aquaculture 2007; 268(1-4): 181-187. http://dx.doi.org/10.1016/j.aquaculture.2007.04.039
http://dx.doi.org/10.1016/j.aquaculture....
). On the other hand, it presents some problems relating to diseases caused by the monogenean helminth Neobenedenia melleni MacCallum, 1927 (Monogenea: Capsalidae), which is one of the main constraining factors on cobia aquaculture development (LIAO et al., 2004Liao IC, Huang TS, Tsai WS, Hsueh CM, Chang SL, Leaño EM. Cobia culture in Taiwan: current status and problems. Aquaculture 2004; 237(1-4): 155-165. http://dx.doi.org/10.1016/j.aquaculture.2004.03.007
http://dx.doi.org/10.1016/j.aquaculture....
; OGAWA et al., 2006Ogawa K, Miyamoto J, Wang HC, Lo CF, Kou GH. Neobenedenia girellae (Monogenea) infection of cultured cobia Rachycentron canadum in Taiwan. Fish Pathol 2006; 41(2): 51-56. http://dx.doi.org/10.3147/jsfp.41.51
http://dx.doi.org/10.3147/jsfp.41.51...
; CAVALLI et al., 2011Cavalli RO, Domingues EC, Hamilton S. Desenvolvimento da produção de peixes em mar aberto no Brasil: possibilidades e desafios. Rev Bras Zootec 2011; 40: 155-164.). The dinoflagellate protozoan Amyloodinium ocellatum Brown, 1931, has been reported in larval stages of these fish (LIAO et al., 2004Liao IC, Huang TS, Tsai WS, Hsueh CM, Chang SL, Leaño EM. Cobia culture in Taiwan: current status and problems. Aquaculture 2004; 237(1-4): 155-165. http://dx.doi.org/10.1016/j.aquaculture.2004.03.007
http://dx.doi.org/10.1016/j.aquaculture....
; BENETTI et al., 2008Benetti DD, Orhun MR, Sardenberg B, O'Hanlon B, Welch A, Hoenig R, et al. Advances in hatchery and grow-out technology of cobia Rachycentron canadum (Linnaeus). Aquacult Res 2008; 39(7): 701-711. http://dx.doi.org/10.1111/j.1365-2109.2008.01922.x
http://dx.doi.org/10.1111/j.1365-2109.20...
). Nevertheless, no information on dinoflagellate infestation in juvenile cobia in Brazil has been registered. This study reports an outbreak of mortality among juvenile cobia caused by the monogenean N. melleni and the dinoflagellate A. ocellatum.

In order to ascertain the cause of symptoms, two collections were made. In the first, in May 2011 (autumn), the fish (n = 5) weighed 15.0 ± 7.3 g and had a total length of 16.0 ± 2.3 cm. The second sample was taken soon after the first observations of mortality, in September 2011 (winter), when the fish (n = 10) presented weight and total length of 43.0 ± 5.6 g and 22.0 ± 2.5 cm, respectively. The water temperature, dissolved oxygen and pH were measured using a Hanna HI 9828 multiparameter meter and the salinity using an Atago HHR-2N refractometer.

Fish presenting erratic swimming and gasping at the water surface were randomly caught with a net, anesthetized in eugenol solution (75 mg.L-1), weighed and measured. After that, gills and mucus from the body surface were collected and fixed in a 5% formalin solution for parasitological analysis. The dinoflagellates were quantified using a Sedgewick Rafter chamber, following the methodology developed by Jerônimo et al. (2011)Jerônimo GT, Speck GM, Cechinel MM, Gonçalves ELT, Martins ML. Seasonal variation on the ectoparasitic communities of Nile tilapia cultured in three regions in southern Brazil. Braz J Biol 2011; 71(2): 365-373. PMid:21755153. http://dx.doi.org/10.1590/S1519-69842011000300005
http://dx.doi.org/10.1590/S1519-69842011...
, and were identified in accordance with Eiras et al. (2006)Eiras M, Daròs JA, Flores R, Kitajima EW. Viróides e virusóides: relíquias do mundo de RNA. Fitopatol Bras 2006; 31(3): 229-246. http://dx.doi.org/10.1590/S0100-41582006000300001
http://dx.doi.org/10.1590/S0100-41582006...
and Martins et al. (2001)Martins ML, Moraes JRE, Andrade PM, Schalch SHC, Moraes FR. Piscinoodinium pillulare (SchÄperclaus 1954) Lom, 1981 (Dinoflagellida) infection in cultivated freshwater fish from Northeast region of São Paulo State, Brazil. Parasitological and pathological aspects. Braz J Biol 2001; 61(4): 639-644. PMid:12071320. http://dx.doi.org/10.1590/S1519-69842001000400013
http://dx.doi.org/10.1590/S1519-69842001...
. The monogeneans were counted under a stereomicroscope, mounted in Hoyer's medium and identified in accordance with Whittington and Horton (1996)Whittington ID, Horton MA. A revision of Neobenedenia Yamaguti, 1963 (Monogenea: Capsalidae) including a redescription of N. melleni (MacCallum, 1927) Yamaguti, 1963. J Nat Hist 1996; 30(8): 1113-1156. http://dx.doi.org/10.1080/00222939600770611
http://dx.doi.org/10.1080/00222939600770...
.

Fifteen days after the second collection, a total of 2,500 juvenile cobia died. In May 2011, the water temperature was 24.0 ± 0.8 °C, pH 7.9 ± 0.3, dissolved oxygen 6.0 ± 0.7 mg.L-1 and salinity 30.0 ± 1.2 g.L-1. At the first sampling, the prevalence of N. melleni was 100%, with mean intensity of 42.0 ± 8.7 and abundance of 42.0 ± 8.7 was found in the body surface mucus. In September 2011, the water temperature was 20.8 ± 1.1 °C, pH 7.9 ± 0.4, dissolved oxygen 6.8 ± 0.7 mg.L-1 and salinity 30.0 ± 0.9 g.L-1. At the second sampling, the prevalence of N. melleni was 60%, with mean intensity of 3.0 ± 0.2 and abundance of 1.8 ± 0.4. In the gills, the observed prevalence of A. ocellatum was 100%, with mean intensity of 46.8 ± 3.4 and abundance of 46.8 ± 3.4.

The mean intensity of N. melleni observed in this study is considered to be high and harmful for farmed fish (JITHENDRAN et al., 2005). Monogenean infestations are common in cultivated marine fish and almost always are responsible for high mortality rates (DEVENEY et al, 2001Deveney MR, Chisholm LA, Whittington ID. First published record of the pathogenic monogenean parasite Neobenedenia melleni (Capsalidae) from Australia. Dis Aquat Org 2001; 46(1): 79-82. PMid:11592706. http://dx.doi.org/10.3354/dao046079
http://dx.doi.org/10.3354/dao046079...
; CRUZ-LACIERDA et al., 2004Cruz-Lacierda ER, Maeno Y, Pineda AJT, Matey VE. Mass mortality of hatchery-reared milkfish (Chanos chanos) and mangrove red snapper (Lutjanus argentimaculatus) caused by Amyloodinium ocellatum (Dinoflagellida). Aquaculture 2004; 236(1-4): 85-94. http://dx.doi.org/10.1016/j.aquaculture.2004.02.012
http://dx.doi.org/10.1016/j.aquaculture....
). The main factors responsible for parasite dissemination are directly associated with water quality and temperature (MORAES; MARTINS, 2004Moraes FR, Martins ML. Condições predisponentes e principais enfermidades de teleósteos cultivados. In: Cyrino JEP, Urbinati EC, Fracalossi DM, Castagnolli N. Tópicos especiais em piscicultura de água doce tropical intensiva. São Paulo: TecArt; 2004. p. 343-383.). Increased water temperature and high organic matter content in floating cages can favor monogenean reproduction (PAN, 2005Pan J. Um jeito taiwanês de criar bijupirá. Panorama da Aqüicultura 2005; 15(90): 36-39.). Water temperature may influence occurrences of fish parasites such as dinoflagellates (MARTINS et al., 2001Martins ML, Moraes JRE, Andrade PM, Schalch SHC, Moraes FR. Piscinoodinium pillulare (SchÄperclaus 1954) Lom, 1981 (Dinoflagellida) infection in cultivated freshwater fish from Northeast region of São Paulo State, Brazil. Parasitological and pathological aspects. Braz J Biol 2001; 61(4): 639-644. PMid:12071320. http://dx.doi.org/10.1590/S1519-69842001000400013
http://dx.doi.org/10.1590/S1519-69842001...
; PEREIRA et al., 2011Pereira JC, Abrantes I, Martins I, Barata J, Frias P, Pereira I. Ecological and morphological features of Amyloodinium ocellatum occurrences in cultivated gilthead seabream Sparus aurata L.; A case study. Aquaculture 2011; 310(3-4): 289-297. http://dx.doi.org/10.1016/j.aquaculture.2010.11.011
http://dx.doi.org/10.1016/j.aquaculture....
) and Neobenedenia sp. (OGAWA et al., 2006Ogawa K, Miyamoto J, Wang HC, Lo CF, Kou GH. Neobenedenia girellae (Monogenea) infection of cultured cobia Rachycentron canadum in Taiwan. Fish Pathol 2006; 41(2): 51-56. http://dx.doi.org/10.3147/jsfp.41.51
http://dx.doi.org/10.3147/jsfp.41.51...
). Monitoring water quality and fish health is important as a prophylactic measure in order to avoid parasite reproduction (JERÔNIMO et al., 2011Jerônimo GT, Speck GM, Cechinel MM, Gonçalves ELT, Martins ML. Seasonal variation on the ectoparasitic communities of Nile tilapia cultured in three regions in southern Brazil. Braz J Biol 2011; 71(2): 365-373. PMid:21755153. http://dx.doi.org/10.1590/S1519-69842011000300005
http://dx.doi.org/10.1590/S1519-69842011...
). In the present study, from the first to the second sampling, the reduction in the water temperature of 3.5 °C may have been responsible for decreased fish resistance and greater parasite occurrence. These data are in agreement with the hypothesis proposed by Pereira et al. (2011)Pereira JC, Abrantes I, Martins I, Barata J, Frias P, Pereira I. Ecological and morphological features of Amyloodinium ocellatum occurrences in cultivated gilthead seabream Sparus aurata L.; A case study. Aquaculture 2011; 310(3-4): 289-297. http://dx.doi.org/10.1016/j.aquaculture.2010.11.011
http://dx.doi.org/10.1016/j.aquaculture....
, which highlights the importance of sanitary surveillance in the summer season in order to avoid fish mortality caused by parasite reproduction.

Although cobia are considered to be disease-resistant fish, they can harbor a great variety of pathogenic agents over their life cycle, including viral diseases (e.g. lymphocystis), bacterial diseases (vibriosis) and the parasites Neobenedenia sp. and A. ocellatum (LIAO et al., 2004Liao IC, Huang TS, Tsai WS, Hsueh CM, Chang SL, Leaño EM. Cobia culture in Taiwan: current status and problems. Aquaculture 2004; 237(1-4): 155-165. http://dx.doi.org/10.1016/j.aquaculture.2004.03.007
http://dx.doi.org/10.1016/j.aquaculture....
). Infestations by Amyloodinium sp. and Neobenedenia sp. have been reported in other fish species (NOWAK, 2007Nowak BF. Parasitic diseases in marine cage culture - An example of experimental evolution of parasites? Int J Parasitol 2007; 37(6): 581-588. PMid:17316650. http://dx.doi.org/10.1016/j.ijpara.2007.01.003
http://dx.doi.org/10.1016/j.ijpara.2007....
; SANCHES, 2008Sanches EG. Controle de Neobenedenia melleni (MacCallum, 1927) (Monogenea: Capsalidae) em garoupa-verdadeira, Epinephelus marginatus (Lowe, 1834), cultivada em tanques-rede. Rev Bras Parasitol Vet 2008; 17(3): 145-149. PMid:19245760.; KERBER et al., 2011Kerber CE, Sanches EG, Santiago M, Luque JL. First record of Neobenedenia melleni (Monogenea: Capsalidae) in sea-farmed cobia (Rachycentron canadum) in Brazil. Rev Bras Parasitol Vet 2011; 20(4): 331-333. PMid:22166389. http://dx.doi.org/10.1590/S1984-29612011000400013
http://dx.doi.org/10.1590/S1984-29612011...
; HIRAYAMA et al., 2009Hirayama T, Kawano F, Hirazawa N. Effect of Neobenedenia girellae (Monogenea) infection on host amberjack Seriola dumerili (Carangidae). Aquaculture 2009; 288(3-4): 159-165. http://dx.doi.org/10.1016/j.aquaculture.2008.11.038
http://dx.doi.org/10.1016/j.aquaculture....
), and monogeneans are one of the most important parasites affecting cobia cultivation (KERBER et al., 2011Kerber CE, Sanches EG, Santiago M, Luque JL. First record of Neobenedenia melleni (Monogenea: Capsalidae) in sea-farmed cobia (Rachycentron canadum) in Brazil. Rev Bras Parasitol Vet 2011; 20(4): 331-333. PMid:22166389. http://dx.doi.org/10.1590/S1984-29612011000400013
http://dx.doi.org/10.1590/S1984-29612011...
). During the growth phase of Lates calcarifer, this ectoparasite was responsible for the mortality of 200,000 fish in Australia (DEVENEY et al., 2001Deveney MR, Chisholm LA, Whittington ID. First published record of the pathogenic monogenean parasite Neobenedenia melleni (Capsalidae) from Australia. Dis Aquat Org 2001; 46(1): 79-82. PMid:11592706. http://dx.doi.org/10.3354/dao046079
http://dx.doi.org/10.3354/dao046079...
). Recently, the first occurrence of N. melleni among cagereared cobia in southeastern Brazil was registered (KERBER et al., 2011Kerber CE, Sanches EG, Santiago M, Luque JL. First record of Neobenedenia melleni (Monogenea: Capsalidae) in sea-farmed cobia (Rachycentron canadum) in Brazil. Rev Bras Parasitol Vet 2011; 20(4): 331-333. PMid:22166389. http://dx.doi.org/10.1590/S1984-29612011000400013
http://dx.doi.org/10.1590/S1984-29612011...
). Parasite proliferation is associated with a monoxenic life cycle and high stocking densities (THONEY; HARGIS JUNIOR, 1991; TAKEMOTO et al., 2004Takemoto RM, Lizama MAP, Guidelli GM, Pavanelli GC. Parasitos de Peixes de águas continentais. In: Ranzani-Paiva MJT, Takemoto R, Lizama MA. Sanidade de Organismos Aquáticos. São Paulo: Varela; 2004. p. 179-197.).

Fish parasitized by N. melleni showed skin lesions, apathy, anorexia, pale eyes, increased mucus production and hemorrhages, with death due to secondary infections (OGAWA et al., 1995Ogawa K, Bondad-Reantaso MG, Fukudome M, Wakabayashi H. Neobenedenia girellae (Hargis 1955), Yamaguti, 1963 (Monogenea: Capsalidae) from Cultured Marine Fishes of Japan. J Parasitol 1995; 81(2): 223-227. PMid:7707197. http://dx.doi.org/10.2307/3283923
http://dx.doi.org/10.2307/3283923...
; HIRAYAMA et al., 2009Hirayama T, Kawano F, Hirazawa N. Effect of Neobenedenia girellae (Monogenea) infection on host amberjack Seriola dumerili (Carangidae). Aquaculture 2009; 288(3-4): 159-165. http://dx.doi.org/10.1016/j.aquaculture.2008.11.038
http://dx.doi.org/10.1016/j.aquaculture....
). Like in the sample of the present report, Kerber et al. (2011)Kerber CE, Sanches EG, Santiago M, Luque JL. First record of Neobenedenia melleni (Monogenea: Capsalidae) in sea-farmed cobia (Rachycentron canadum) in Brazil. Rev Bras Parasitol Vet 2011; 20(4): 331-333. PMid:22166389. http://dx.doi.org/10.1590/S1984-29612011000400013
http://dx.doi.org/10.1590/S1984-29612011...
also observed lesions on the skin, head and fins, as well as respiratory difficulty and corneal opacity.

The infestation by N. melleni may have been reduced from the first to the second sampling through treatment for minimizing fish mortality, which consisted of immersion baths in freshwater for 5 min, at 96-hour intervals.

This, along with the gasping behavior of the fish in order to increase gill ventilation, suggests that gas exchange had become impaired, as a consequence of high infection by A. ocellatum in the gills, since no monogenean was found in this organ.

In cobia, occurrences of Amyloodinium sp. have generally been reported in larval stages (LIAO et al., 2004Liao IC, Huang TS, Tsai WS, Hsueh CM, Chang SL, Leaño EM. Cobia culture in Taiwan: current status and problems. Aquaculture 2004; 237(1-4): 155-165. http://dx.doi.org/10.1016/j.aquaculture.2004.03.007
http://dx.doi.org/10.1016/j.aquaculture....
; BENETTI et al., 2008Benetti DD, Orhun MR, Sardenberg B, O'Hanlon B, Welch A, Hoenig R, et al. Advances in hatchery and grow-out technology of cobia Rachycentron canadum (Linnaeus). Aquacult Res 2008; 39(7): 701-711. http://dx.doi.org/10.1111/j.1365-2109.2008.01922.x
http://dx.doi.org/10.1111/j.1365-2109.20...
). Although low numbers of N. melleni were found in the second sampling, it can be inferred that monogeneans may have caused a decrease in fish resistance, thus leading to dinoflagellate attachment. This may be explained by a reduction in fish resistance after the first contact with monogeneans.

According to Noga and Levy (2006)Noga EJ, Levy MG. Phyllum Dinoflagellata. In: Woo PTK. Fish Diseases and Disorders, Volume I: Protozoan and Metazoan Infections ed. Oxford: CAB International; 2006. p. 16-45., A. ocellatum is one of the most important parasites in marine fish cultivation. The fish tend to search for better oxygenated sites in tanks (REED; FRANCIS-FLOYD, 1994). This ectoparasite has been reported in both estuarine and marine fish, especially when reared at high stocking densities (REED; FRANCIS-FLOYD, 1994). However, in the present study, the cobia were stocked at low density (0.4 kg/m3), throughout the observation period.

The pathogenicity of dinoflagellates is associated with attachment of rhizocysts to host cells, performed by trophonts, thereby causing necrosis (PAPERNA, 1980Paperna I. Amyloodinium ocellatum (Brown, 1931) (Dinoflagellida) infestations in cultured marine fish at Eilat, Red Sea: epizootiology and pathology. J Fish Dis 1980; 3(5): 363-372. http://dx.doi.org/10.1111/j.1365-2761.1980.tb00421.x
http://dx.doi.org/10.1111/j.1365-2761.19...
; MARTINS et al., 2001Martins ML, Moraes JRE, Andrade PM, Schalch SHC, Moraes FR. Piscinoodinium pillulare (SchÄperclaus 1954) Lom, 1981 (Dinoflagellida) infection in cultivated freshwater fish from Northeast region of São Paulo State, Brazil. Parasitological and pathological aspects. Braz J Biol 2001; 61(4): 639-644. PMid:12071320. http://dx.doi.org/10.1590/S1519-69842001000400013
http://dx.doi.org/10.1590/S1519-69842001...
). More than 200 trophonts per gill filament can cause hyperplasia, inflammation, hemorrhage and necrosis (PAVANELLI et al., 2008Pavanelli GC, Eiras CJ, Takemoto RM. Doenças de peixes: Profilaxia, diagnóstico e tratamento. 3. Ed. Maringá: EDUEM; 2008. p. 311.).

In this study, the events that caused deleterious actions on the organism and the presence of N. melleni may have enhanced the possibility of secondary infections. Control over fish parasites among marine cage-reared fish is the most important challenge for marine aquaculture.

Our report suggests that fish mortality was caused by the first infestation by the monogeneans followed by the dinoflagellates. Prophylactic measures need to be adopted in fish cultivation, so as to avoid parasite reproduction (REED; FRANCIS-FLOYD, 1994).

The authors thank CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for financial support and grants to M.L. Martins and M.Y.Tsuzuki and schoolarship to G.S.O. Hashimoto (ITI schoolarship CNPq 559759/2009-6); and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for Doctoral schoolarship to C.B. Moreira.

References

  • Arnold CR, Kaiser JB, Holt GJ. Spawning of cobia Rachycentron canadum in captivity. J World Aquacult Soc 2002; 33(2): 205-208. http://dx.doi.org/10.1111/j.1749-7345.2002.tb00496.x
    » http://dx.doi.org/10.1111/j.1749-7345.2002.tb00496.x
  • Benetti DD, Orhun MR, Sardenberg B, O'Hanlon B, Welch A, Hoenig R, et al. Advances in hatchery and grow-out technology of cobia Rachycentron canadum (Linnaeus). Aquacult Res 2008; 39(7): 701-711. http://dx.doi.org/10.1111/j.1365-2109.2008.01922.x
    » http://dx.doi.org/10.1111/j.1365-2109.2008.01922.x
  • Cavalli RO, Hamilton S. A piscicultura marinha no Brasil: afinal, quais as espécies boas para cultivar? Panorama da Aqüicultura 2007; 17(104): 50-55.
  • Cavalli RO, Domingues EC, Hamilton S. Desenvolvimento da produção de peixes em mar aberto no Brasil: possibilidades e desafios. Rev Bras Zootec 2011; 40: 155-164.
  • Cruz-Lacierda ER, Maeno Y, Pineda AJT, Matey VE. Mass mortality of hatchery-reared milkfish (Chanos chanos) and mangrove red snapper (Lutjanus argentimaculatus) caused by Amyloodinium ocellatum (Dinoflagellida). Aquaculture 2004; 236(1-4): 85-94. http://dx.doi.org/10.1016/j.aquaculture.2004.02.012
    » http://dx.doi.org/10.1016/j.aquaculture.2004.02.012
  • Deveney MR, Chisholm LA, Whittington ID. First published record of the pathogenic monogenean parasite Neobenedenia melleni (Capsalidae) from Australia. Dis Aquat Org 2001; 46(1): 79-82. PMid:11592706. http://dx.doi.org/10.3354/dao046079
    » http://dx.doi.org/10.3354/dao046079
  • Eiras M, Daròs JA, Flores R, Kitajima EW. Viróides e virusóides: relíquias do mundo de RNA. Fitopatol Bras 2006; 31(3): 229-246. http://dx.doi.org/10.1590/S0100-41582006000300001
    » http://dx.doi.org/10.1590/S0100-41582006000300001
  • Hirayama T, Kawano F, Hirazawa N. Effect of Neobenedenia girellae (Monogenea) infection on host amberjack Seriola dumerili (Carangidae). Aquaculture 2009; 288(3-4): 159-165. http://dx.doi.org/10.1016/j.aquaculture.2008.11.038
    » http://dx.doi.org/10.1016/j.aquaculture.2008.11.038
  • Holt GJ, Faulk CK, Schwarz MH. A review of the larviculture of cobia Rachycentron canadum, a warm water marine fish. Aquaculture 2007; 268(1-4): 181-187. http://dx.doi.org/10.1016/j.aquaculture.2007.04.039
    » http://dx.doi.org/10.1016/j.aquaculture.2007.04.039
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Publication Dates

  • Publication in this collection
    Oct-Dec 2013

History

  • Received
    17 Jan 2013
  • Accepted
    2 Apr 2013
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