Protozoan infections in farmed fish from Brazil: diagnosis and pathogenesis

The Phylum Protozoa brings together several organisms evolutionarily different that may act as ecto or endoparasites of fishes over the world being responsible for diseases, which, in turn, may lead to economical and social impacts in different countries. Apart from the recent advances for the diagnosis of fish diseases in Brazil, little is known on the protozoan parasites and their relationship with environment and host. This revision presents the most important protozoan parasites found in farmed fish from Brazil, not only with emphasis on its diagnosis, biology, transmission and host-parasite relationship, but also on some information that may be useful to researchers in determining the correct diagnosis in fish farms.

Fish parasites; disease; ciliate; dinoflagellate; pathogenicity

Authorship

Mauricio Laterça Martins ^**Corresponding author: Mauricio Laterça Martins, Aquatic Organism Health Laboratory - AQUOS, Aquaculture Department, Federal University of Santa Catarina – UFSC, Rod. Admar Gonzaga, 1346, CEP 88040-900, Florianópolis, SC, Brazil, e-mail: mauricio.martins@ufsc.br

Laboratório de Sanidade de Organismos Aquáticos – AQUOS, Departamento de Aquicultura, Universidade Federal de Santa Catarina – UFSC, Florianópolis, SC, BrasilUniversidade Federal de Santa CatarinaBrasilFlorianópolis, SC, BrasilLaboratório de Sanidade de Organismos Aquáticos – AQUOS, Departamento de Aquicultura, Universidade Federal de Santa Catarina – UFSC, Florianópolis, SC, Brasil

Lucas Cardoso

Natalia Marchiori

Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina – Epagri, Campo Experimental de Piscicultura de Camboriú, Camboriú, SC, BrasilEmpresa de Pesquisa Agropecuária e Extensão Rural de Santa CatarinaBrasilCamboriú, SC, BrasilEmpresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina – Epagri, Campo Experimental de Piscicultura de Camboriú, Camboriú, SC, Brasil

Santiago Benites de Pádua

Aquivet Saúde Aquática, São José do Rio Preto, SP, BrasilAquivet Saúde AquáticaBrasilSão José do Rio Preto, SP, BrasilAquivet Saúde Aquática, São José do Rio Preto, SP, Brasil

*Corresponding author: Mauricio Laterça Martins, Aquatic Organism Health Laboratory - AQUOS, Aquaculture Department, Federal University of Santa Catarina – UFSC, Rod. Admar Gonzaga, 1346, CEP 88040-900, Florianópolis, SC, Brazil, e-mail: mauricio.martins@ufsc.br

SCIMAGO INSTITUTIONS RANKINGS

Aquivet Saúde Aquática, São José do Rio Preto, SP, BrasilAquivet Saúde AquáticaBrasilSão José do Rio Preto, SP, BrasilAquivet Saúde Aquática, São José do Rio Preto, SP, Brasil

Figures

Figures (12)

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Figure 1
Apiosoma attached on the epithelium (a) and scale (b) of Nile tilapia larva Oreochromis niloticus in fresh-mounted slide. Silver nitrate impregnated specimen to observe the ciliary (c) and stained with Giemsa (d) showing the nuclear apparatus.

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Figure 2
Chilodonella hexasticha observed in fresh-mounted slide from the gills of Nile tilapia Oreochromis niloticus (a), with detail of ciliary kineties in silver nitrate impregnation (b), nuclear apparatus and great amount of bacteria when stained by Giemsa (c), transversal fission of the parasite after silver nitrate impregnation (d). Bar: 10 µm (b,d).

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Figure 3
Epistylis sp. (a) in fresh-mounted slide under light microscope. Zooid in binary fission (b) and detail of bacteria (arrow heads) attached on the peduncle of the ciliate. Nile tilapia Oreochromis niloticus (c) with fin erosion and loss of scale (arrowheads) associated with Epistylis colonization, and hybrid surubim Pseudoplatystoma sp. (d) showing total erosion of dorsal fin and colonies of Epistylis sp. on the dorsal fin and head (arrow heads).

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Figure 4
Hybrid surubim Pseudoplatystoma sp. presenting white spots on the skin and fins (a). Ichthyophthirius multifiliis observed in fresh-mounted slide from the skin: mature trophont and its horse-shoe shaped macronucleus (b - arrowhead) and several imature trophonts in developmental stages (b - continued arrow). Histological section of the gill lamellae (c), with inflammatory infiltrate (c - asterisk), and the parasite inserted in the skin of infected fish (d - arrow head). Proliferation of mucous cells next to the parasite attachment (d - dotted arrows). Bar: 150 µm (c) and 100 µm (d). Figure 4 a was obtained from Pádua et al. (2012b)Pádua SD, Ishikawa MM, Kasai RYD, Jerônimo GT, Carrijo-Mauad JR. Parasitic infestations in hybrid surubim catfish fry ( x . Pseudoplatystoma reticulatumP. corruscans)Rev Bras Med Vet 2012b; 34(3): 235-240. and Figure 4 d from Pádua et al. (2014)Pádua SB, Jerônimo GT, Ishikawa MM, Belo MAA, Martins ML, Pelisari T, et al. Parasitological assessment and host-parasite relationship in farmed cachara catfish fingerlings Pseudoplatystoma reticulatum (Eigenmann & Eigenmann 1889). Neotrop Helminthol 2014; 8(1): 37-45..

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Figure 5
Trichodinids in fresh-mounted smear from the skin (a), Trichodina centrostrigeata in differential interference contrast microscope (b), adhesive disc of Trichodina magna in silver nitrate impregnation (c) and an adhesive disc of a trichodinid during binary fission in silver nitrate impregnation (d). Bar: 50 µm (b) and 10 µm (c,d).

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Figure 6
Life-cycle of Amyloodinium ocellatum. Modified from Pereira et al. (2011)Pereira JC, Abrantes I, Martins I, Barata J, Frias P, Pereira I. Ecological and morphological features of occurrences in cultivated gilthead seabream L.: a case study. Amyloodinium ocellatumSparus aurataAquaculture 2011; 310(3): 289-297. http://dx.doi.org/10.1016/j.aquaculture.2010.11.011.
http://dx.doi.org/10.1016/j.aquaculture.... .

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Figure 7
Piscinoodinium pillulare from gill scraps of tambaqui Colossoma macropomum. Pear-shaped trophonts, rounded (arrowheads) and one dinospore (arrow). In detail, two parasites stained in Giemsa exhibiting oval to rounded nucleus with the absence of micronucleus.

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Figure 8
Pathological changes in fish with piscinoodiniasis. Brownish gill of tambaqui Colossoma macropomum (a), hundreds of parasites adhered in gill filaments observed in stereomicroscope (b), as well as from histological section (c), rhizocysts penetrating host's skin (d - arrow). Bar: 100 µm (c) and 25 µm (d).

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Figure 9
Trypanosoma sp. (a) observed from blood extension of tuvira Gymnotus aff. inaequilabiatus; Cryptobia sp. (b) from gill scraps of hybrid tambacu (C. macropomum x P. mesopotamicus) observed in a phase-contrast microscope and Ichthyobodo sp. (c) from skin of Nile tilapia Oreochromis niloticus previously stained with Giemsa. Figure 9 a was obtained from Pádua et al. (2011b)Pádua SB, Ishikawa MM, Satake F, Jerônimo GT, Pilarski F. First record of Trypanosoma sp. (Protozoa: Kinetoplastida) in tuvira (Gymnotus aff. inaequilabiatus) in the Pantanal wetland, Mato Grosso do Sul State, Brazil. Rev Bras Parasitol Vet 2011b; 20(1): 85-87. http://dx.doi.org/10.1590/S1984-29612011000100019. PMid:21439241
http://dx.doi.org/10.1590/S1984-29612011... .

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Figure 10
Tetrahymena sp. from the skin of guppy (Poecilia sp.) observed in light microscope at 40 x magnification.

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Figure 11
Geographical distribution of (a) ciliated protozoan and (b) other protozoan parasite groups of fishes from Brazil. Symbols indicate the register of the below-mentioned species: ☉ Entamoeba pimelodi; ※ Amyloodinium;  Cryptobia; ☽ Hexamita; ✕ Ichthyobodo; ⓿ Piscinoodinium;  Trypanosoma; ▣ Calyptospora; ⊗ Cyrilia lignieresi;  Eimeria lepidosirensis; ◊ Haemogregarina; ◗ Apiosoma; ⁂ Balantidium;  Chilodonella; ★ Epistylis; ⬤ Ichthyophthirius multifiliis;  Nyctotherus piscicola;  Rynchodinium paradoxum;  Tetrahymena and Trichodinidae. Colour black indicates previous reports; colour red indicates unpublished data from the present authors.

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Figure 12
Constructed wetland in freshwater fish farm for use as a sanitary barrier and water cleaning.

Figure 1 Apiosoma attached on the epithelium (a) and scale (b) of Nile tilapia larva Oreochromis niloticus in fresh-mounted slide. Silver nitrate impregnated specimen to observe the ciliary (c) and stained with Giemsa (d) showing the nuclear apparatus.

Figure 2 Chilodonella hexasticha observed in fresh-mounted slide from the gills of Nile tilapia Oreochromis niloticus (a), with detail of ciliary kineties in silver nitrate impregnation (b), nuclear apparatus and great amount of bacteria when stained by Giemsa (c), transversal fission of the parasite after silver nitrate impregnation (d). Bar: 10 µm (b,d).

Figure 3 Epistylis sp. (a) in fresh-mounted slide under light microscope. Zooid in binary fission (b) and detail of bacteria (arrow heads) attached on the peduncle of the ciliate. Nile tilapia Oreochromis niloticus (c) with fin erosion and loss of scale (arrowheads) associated with Epistylis colonization, and hybrid surubim Pseudoplatystoma sp. (d) showing total erosion of dorsal fin and colonies of Epistylis sp. on the dorsal fin and head (arrow heads).

Figure 4 Hybrid surubim Pseudoplatystoma sp. presenting white spots on the skin and fins (a). Ichthyophthirius multifiliis observed in fresh-mounted slide from the skin: mature trophont and its horse-shoe shaped macronucleus (b - arrowhead) and several imature trophonts in developmental stages (b - continued arrow). Histological section of the gill lamellae (c), with inflammatory infiltrate (c - asterisk), and the parasite inserted in the skin of infected fish (d - arrow head). Proliferation of mucous cells next to the parasite attachment (d - dotted arrows). Bar: 150 µm (c) and 100 µm (d). Figure 4 a was obtained from Pádua et al. (2012b)Pádua SD, Ishikawa MM, Kasai RYD, Jerônimo GT, Carrijo-Mauad JR. Parasitic infestations in hybrid surubim catfish fry ( x . Pseudoplatystoma reticulatumP. corruscans)Rev Bras Med Vet 2012b; 34(3): 235-240. and Figure 4 d from Pádua et al. (2014)Pádua SB, Jerônimo GT, Ishikawa MM, Belo MAA, Martins ML, Pelisari T, et al. Parasitological assessment and host-parasite relationship in farmed cachara catfish fingerlings Pseudoplatystoma reticulatum (Eigenmann & Eigenmann 1889). Neotrop Helminthol 2014; 8(1): 37-45..

Figure 5 Trichodinids in fresh-mounted smear from the skin (a), Trichodina centrostrigeata in differential interference contrast microscope (b), adhesive disc of Trichodina magna in silver nitrate impregnation (c) and an adhesive disc of a trichodinid during binary fission in silver nitrate impregnation (d). Bar: 50 µm (b) and 10 µm (c,d).

Figure 6 Life-cycle of Amyloodinium ocellatum. Modified from Pereira et al. (2011)Pereira JC, Abrantes I, Martins I, Barata J, Frias P, Pereira I. Ecological and morphological features of occurrences in cultivated gilthead seabream L.: a case study. Amyloodinium ocellatumSparus aurataAquaculture 2011; 310(3): 289-297. http://dx.doi.org/10.1016/j.aquaculture.2010.11.011.
http://dx.doi.org/10.1016/j.aquaculture.... .

Figure 7 Piscinoodinium pillulare from gill scraps of tambaqui Colossoma macropomum. Pear-shaped trophonts, rounded (arrowheads) and one dinospore (arrow). In detail, two parasites stained in Giemsa exhibiting oval to rounded nucleus with the absence of micronucleus.

Figure 8 Pathological changes in fish with piscinoodiniasis. Brownish gill of tambaqui Colossoma macropomum (a), hundreds of parasites adhered in gill filaments observed in stereomicroscope (b), as well as from histological section (c), rhizocysts penetrating host's skin (d - arrow). Bar: 100 µm (c) and 25 µm (d).

Figure 9 Trypanosoma sp. (a) observed from blood extension of tuvira Gymnotus aff. inaequilabiatus; Cryptobia sp. (b) from gill scraps of hybrid tambacu (C. macropomum x P. mesopotamicus) observed in a phase-contrast microscope and Ichthyobodo sp. (c) from skin of Nile tilapia Oreochromis niloticus previously stained with Giemsa. Figure 9 a was obtained from Pádua et al. (2011b)Pádua SB, Ishikawa MM, Satake F, Jerônimo GT, Pilarski F. First record of Trypanosoma sp. (Protozoa: Kinetoplastida) in tuvira (Gymnotus aff. inaequilabiatus) in the Pantanal wetland, Mato Grosso do Sul State, Brazil. Rev Bras Parasitol Vet 2011b; 20(1): 85-87. http://dx.doi.org/10.1590/S1984-29612011000100019. PMid:21439241
http://dx.doi.org/10.1590/S1984-29612011... .

Figure 10 Tetrahymena sp. from the skin of guppy (Poecilia sp.) observed in light microscope at 40 x magnification.

Figure 11 Geographical distribution of (a) ciliated protozoan and (b) other protozoan parasite groups of fishes from Brazil. Symbols indicate the register of the below-mentioned species: ☉ Entamoeba pimelodi; ※ Amyloodinium;  Cryptobia; ☽ Hexamita; ✕ Ichthyobodo; ⓿ Piscinoodinium;  Trypanosoma; ▣ Calyptospora; ⊗ Cyrilia lignieresi;  Eimeria lepidosirensis; ◊ Haemogregarina; ◗ Apiosoma; ⁂ Balantidium;  Chilodonella; ★ Epistylis; ⬤ Ichthyophthirius multifiliis;  Nyctotherus piscicola;  Rynchodinium paradoxum;  Tetrahymena and Trichodinidae. Colour black indicates previous reports; colour red indicates unpublished data from the present authors.

Figure 12 Constructed wetland in freshwater fish farm for use as a sanitary barrier and water cleaning.

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Colégio Brasileiro de Parasitologia Veterinária FCAV/UNESP - Departamento de Patologia Veterinária, Via de acesso Prof. Paulo Donato Castellane s/n, Zona Rural, , 14884-900 Jaboticabal - SP, Brasil, Fone: (16) 3209-7100 RAMAL 7934 - Jaboticabal - SP - Brazil
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Protozoan infections in farmed fish from Brazil: diagnosis and pathogenesis

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[1] *Corresponding author: Mauricio Laterça Martins, Aquatic Organism Health Laboratory - AQUOS, Aquaculture Department, Federal University of Santa Catarina – UFSC, Rod. Admar Gonzaga, 1346, CEP 88040-900, Florianópolis, SC, Brazil, e-mail: mauricio.martins@ufsc.br