Neotrop. Helminthol., 8(1), 2014

2014 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

ISSN: 2218-6425 impreso / ISSN: 1995-1043 on line

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

PARASITOLOGICAL ASSESSMENT AND HOST-PARASITE RELATIONSHIP IN FARMED

CACHARA CATFISH FINGERLINGS (PSEUDOPLATYSTOMA RETICULATUM EIGENMANN &

EIGENMANN 1889), MATO GROSSO DO SUL, BRAZIL

EVALUACIÓN PARASITOLÓGICA Y RELACIÓN HOSPEDERO-PARÁSITO EN ALEVINES

DEL BAGRE CACHARA (PSEUDOPLATYSTOMA RETICULATUM EIGENMANN &

EIGENMANN 1889), MATO GROSSO DO SUL, BRASIL

1,3 2 4

Santiago Benites de Pádua , Gabriela Tomas Jerônimo , Mácia Mayumi Ishikawa ,

5 2 6

Marco Antonio de Andrade Belo , Maurício Laterça Martins , Thais Pelisari ,

7 8

Rodrigo Yutaka Dichoff Kasai & Juliana Rosa Carrijo-Mauad

Abstract

Farmed fingerlings of South American catfish are frequently exposed to several parasites, but

little information is available for implementing health programs for control and prevention of

parasitic diseases in the hatcheries. This study evaluated the parasitic fauna of cachara catfish

fingerlings (Pseudoplatystoma reticulatum Eingenmann & Eigenmann, 1889) and the host-

parasite relationship during the early stages of rearing. A total of 302 cachara fingerlings were

used for parasitic diagnosis and histopathological analysis. Ichthyophthirius multifiliis and

Trichodina heterodentata were diagnosed as the most prevalent parasites, followed by Cryptobia

sp., Henneguya sp., Monogenea and Nematoda. There was a positive correlation between the size

of the fish and the mean intensity of parasitism by I. multifiliis. Proliferation of mucus cells, club

cells, multifocal area of degeneration, epithelial necrosis on the body surface, skin ulceration,

fusion of secondary gill lamellae and inflammatory infiltration were observed in I. multifiliis-

infected fish. Ciliated protozoans were the main etiological agents diagnosed, and the cachara (P.

reticulatum) is a new host for T. heterodentata. In addition, ichthyophthiriasis induced severe

tissue damage thus making the fingerlings susceptible to opportunistic infections.

Keywords: Fish parasites – histopathology - Ichthyophthirius multifiliis - Pseudoplatystoma reticulatum -

Trichodina heterodentata.

Suggested citation: de Pádua, SB, Jerônimo, GT, Ishikawa, MM, Belo, MAA, Martins, ML, Pelisari, T, Kasai, RYD & Carrijo-

Mauad, JR. 2014. Parasitological assessment and host-parasite relationship in farmed cachara catfish fingerlings

(Pseudoplatystoma reticulatum Eigenmann & Eigenmann 1889), Mato Grosso do Sul, Brazil. Neotropical Helminthology, vol.

8, n°1, jan-jun, pp. 37 - 45.

1AquiVet Saúde Aquática, São José do Rio Preto, SP, Brazil.

2AQUOS - Aquatic Organism Health Laboratory, Aquaculture Department, Federal University of Santa Catarina (UFSC), SC, Brazil.

3 4

Aquaculture Center of São Paulo State University (CAUNESP), Jaboticabal, SP, Brazil. Embrapa Western Agriculture, Dourados, MS, Brazil.

5College of Veterinary Medicine, Laboratory of Pharmacology and Clinical Pathology, Camilo Castelo Branco University (Unicastelo), Descalvado, SP, Brazil.

6 7

Anhanguera Faculty, Dourados, MS, Brazil. Piraí Piscicultura, Terenos, MS, Brazil.

8School of Biological and Environmental Sciences, Federal University of Grande Dourados (UFGD), Dourados, MS, Brazil. S.B. Pádua

Aquaculture Center of São Paulo State University (CAUNESP), Via de Acesso Prof. Paulo Donato Castellane, s/n, CEP: 14884-900, Jaboticabal, SP, Brazil.

PABX: +55 17 3215 3223

E-mail addresses: santiago@aquivet.com.br

Resumen

Palabras clave: Trichodina heterodentata.

Histopatología - Ichthyophthirius multifiliis - Parasitos de peces - Pseudoplatystoma reticulatum -

Los alevines de bagres del Sur de América en cautiverio están frecuentemente expuestos a muchos

parásitos, pero poca información es evaluada para implementar programa de salud para control y

prevención de enfermedades en criaderos. Este estudio evaluó la fauna de parásitos de alevines de

cachara (Pseudoplatystoma reticulatum Eingenmann & Eingenmann, 1889) y la relación

huésped-parásito durante las fases iníciales de cultivo. Un total de 302 alevines fueran sometidos a

diagnóstico y análisis histopatológicos. Ichthyophthirius multifiliis y Trichodina heterodentata

fueran diagnosticados como los parásitos mas prevalentes, seguidos de Cryptobia sp., Henneguya

sp., Monogenea y Nematoda. Ha sido observada una correlación positiva entre la longitud de los

peces y la intensidad promedio de I. multifiliis. Proliferación de células de moco, células club,

áreas multifocales de degeneración, necrosis epitelial en la superficie del cuerpo, ulceración de

piel, fusión de laminillas branquiales secundarias e infiltración inflamatoria fueron observados en

peces infectados por I. multifiliis. Los protozoarios ciliados fueran los agentes etiológicos mas

importantes y el cachara (P. reticulatum) es un nuevo huésped para T. heterodentata. En adición, la

ictioftiriasis indujo un daño severo favoreciendo las infecciones oportunistas en los alevines.

In order to minimize these problems and

improve the conservation of pure species the

production of native fish in captivity is a

sustainable alternative. The cachara from the

Pantanal (P. reticulatum Eigenmann &

Eigenmann, 1889) has a great genetic similarity

with the cachara from Amazonia (P. fasciatum

Linnaeus, 1766). However, some doubts exist

regarding the validity of the species (Carvalho-

Costa et al., 2011), but at the present time it is

considered to be a valid species, according to the

Fish Base (Frose & Pauly, 2013). This South

American carnivorous catfish presents a real

potential for exploitation in industrial scale, due

to its easy reproduction (Leonardo et al., 2004;

Batlouni et al., 2006) and the strategies for

feeding training at the early stages are known

(Inoue et al., 2009). No data on the diagnosis of

diseases of these fish in farmed settings have

been reported. Most investigators have focused

the studies on parasite diagnosis on adult fish

from the natural environment (Campos et al.,

2008; Campos et al., 2009; Naldoni et al., 2011;

Adriano et al. 2012).

Information on the physiology and nutritional

requirements of cachara as well as

parasitological assessment are needed to

Production of native catfish is an expanding

agribusiness in Brazil, in which production is

concentrated in the central region. Interbreeding

between species from two major river basins, the

River Plate basin (which includes the Pantanal

region) and the Amazon basin is a common

practice. Among the fish used to perform this

artificial interbreeding, carnivorous species of

the genus Pseudoplatystoma, such as P.

corruscans, P. tigrinum (sensu lato) and P.

fasciatum (sensu lato), are one of the most

appreciated fish (Carvalho-Costa et al., 2011).

The state of Mato Grosso do Sul is responsible

for the hybrid surubim catfish production (P.

corruscans male x P. reticulatum female), while

in the state of Mato Grosso the Amazonian

hybrid pintado (Leiarius marmoratus male x

Pseudoplatystoma spp. female) is the most

important fish produced. However, production

of hybrid fish with reproductive ability, as in the

case of the hybrid surubim catfish, can cause an

irreversible impact on natural stocks when they

escape from fish farms to the natural

environment, as has recently been demonstrated

by Prado et al. (2012).

INTRODUCTION

Páduaet al.

Host-Parasite relationship in Pseudoplatystoma reticulatum

Neotrop. Helminthol., 8(1), 2014

colorimetric kit (Alfakit , Santa Catarina,

Brazil). The mean values ± standard deviation

were as follows: dissolved oxygen 5.9 ± 0.4 mg

-1

L , temperature 25.6 ± 0.4°C, pH 7.3 ± 0.2, total

-1

ammonia 0.3 ± 0.1 mg L .

Biometry and parasitological assessment

The fingerlings were captured with nets,

-1

euthanized using clove oil (50 mg·L ), measured

with caliper and weighed on a semi-analytical

balance (0.001) (Shimadzu , Japan). The

parasitological analysis consisted of

exami na ti on o f the fish u nder a

stereomicroscope to search for ectoparasites.

Fish larvae were evaluated on the whole on

slides under a coverslip with saline solution

(0.65%) during the first two weeks, because of

the small size of the larvae. In the remaining

days gills, body, liver and gastrointestinal tract

of fingerlings were separated and mounted

individually on slides under a coverslip with

saline solution (0.65%), examined and parasite

enumerated under a light microscope (Nikon

E100, Japan). The parasites were processed and

identified in accordance with Lom & Dyková

(1992) and Thatcher (2006). For the trichodinid

identification, the material was dried out under

dim light, and some smears were impregnated

with silver nitrate using Klein's method (Klein,

1958) for the posterior examination of adhesive

disc structures and denticles under a light

microscope as suggested by Lom (1958), Arthur

& Lom (1984) and Van As & Basson (1989). The

parasitological indexes were calculated as

proposed by Bush et al. (1997).

Histopathological analysis

With occurrence of some deaths, ten fish with

white spots on the skin were fixed in 10%

buffered formalin solution for histopathological

analysis. The skin and gills were embedded in

paraffin and sliced into 5 µm thick sections for

staining with hematoxylin and eosin (HE) and

Periodic acid-Schiff stain (PAS). The

histological sections were photographed using a

photomicroscope (Nikon E200, Japan)

equipped with an image capture system (Motic

Moticam 2.300, Canada).

optimize the fish production. According to the

topic, the nutritional and operational

management could be established for better

development and preventive measures against

diseases. This study presents new information

on parasitological assessment in cachara

fingerlings and the host-parasite relationship

during the early stages of rearing.

Study area and fish

This study was developed in a commercial

hatchery located in the municipality of Terenos

(20º25'57.7” S; 55º17'08.9” W), Mato Grosso do

Sul, Brazil. In February 2010, artificial

reproduction of cachara (P. reticulatum) was

performed and the offspring were examined for

30 days. The larvae hatched approximately 16 h

after fertilization, at a water temperature 26°C.

The exogenous food was offered 48 h post-

hatching, after the time required opening the

mouth of the larvae. The food consisted

primarily of nauplii of Artemia salina until the

tenth day of rearing. Concurrent provision of

wild zooplankton was then started, after prior

fertilization of the earth ponds with poultry litter.

After this period, the larvae were transferred to

glass fiber tanks 1000 L of capacity and water

renewal rate 14 L min-1, in which the fish were

submitted to feed training (Inoue et al., 2009).

This process must be gradual starting from

natural feeding to commercial extruded diet with

45% crude protein. Fish tanks were cleaned

every day to reduce the levels of organic

residues, especially coming from leftover feed.

During the study, a total of 302 fingerlings of

mean weight 0.2 ± 0.3 g and length 2.4 ± 1.1 cm

were analyzed (Ethics Committee Approval

756/CEUA/UFSC).

Water quality

The water supply was from natural source, the

dissolved oxygen and temperature were

measured daily using an oxygen meter (YSI

550 , YSI Inc., Yellow Springs, USA) and pH

using a pHmeter (PH10 , YSI Inc., Yellow

Springs, USA). Ammonia, nitrite and nitrate

concentrations were measured using a

MATERIAL AND METHODS

Parasites

SI EF/PF P (%) MI

Protozoa

Ichthyophthirius multifiliis Skin, fins and gills 302/89 29.5 32.4 (1 – 154)

I. multifiliis

Skin and fins 302/86 28.5 23.7 (1 – 110)

I. multifiliis

Gills 302/64 21.2 13.2 (1 – 44)

Trichodina heterodentata Skin, fins and gills 302/48 15.9 4.9 (1 – 52)

Cryptobia sp.

Gills 302/5 1.7 20.6 (4 – 50)

Myxozoa

Henneguya sp.

Gills 302/1 0.3 –

Platyhelminthes

Ancyrocephalinae gen. sp. Gills 302/5 1.7 1 (1 – 1)

Nemathelminthes

Nematoda larvae gen. sp.

Stomach 302/2 0.7 1 (1 – 1)

the weight and the mean intensity of infection by

Trichodina heterodentata (rs = -0.09) and I.

multifiliis (rs = 0.31). On the other hand, there

was a positive correlation (p < 0.0001) between

the size of the fish and the mean intensity of

infection by I. multifiliis (rs = 0.78). This was not

observed on T. heterodentata (rs = -0.07) and the

other parasites.

Histopathological analysis

On the histological sections, the presence of I.

multifiliis in the epithelium of the host, both in

the skin (Figure 2a) and in the gill tissue, was

responsible for epithelial proliferation (Fig. 2b),

as well as proliferation of the club and mucous

cells (Fig. 2a, 2a). Multifocal to coalescing areas

of degeneration (Fig. 2b,c) and epithelial

necrosis were also observed, with multifocal

areas of ulceration (Fig. 2d) and inflammatory

infiltration composed of PAS-positive

granulocytes located in the epithelium (Fig. 3c-

d) and around and within the parasite (Figure 3b,

d). In the gill tissue, epithelial proliferation with

fusion of the secondary lamellae, areas of

necrosis, presence of mononuclear

inflammatory infiltrate and mild congestion

were found.

Statistical analysis

Spearman's rank correlation was used between

the parasite intensity and the weight and size of

the fish.

Identification of parasites and parasitological

index

From a total of 302 cachara fingerlings, 140

(46.4%) were parasitized by at least one parasite

taxon. Ecto and endoparasites were diagnosed in

cachara fingerlings (Table 1). However, in the

skin, fins and gill, the most frequent parasites

were the ciliated protozoan's Ichthyophthirius

multifiliis Fouquet, 1876 and Trichodina

heterodentata Duncan, 1977 (Figure 1a, b). In

addition, the main infection sites by I. multifiliis

in cachara fingerlings were the skin and fins,

which showed greater infection than the gill

tissue. It was not possible to identify the species

of Monogenea and Nematoda because the

numbers of parasites were too low for secure

identification.

Host-parasite relationship

No correlation was observed (p > 0.05) between

Páduaet al.

Host-Parasite relationship in Pseudoplatystoma reticulatum

RESULTS

Table 1. Parasitological analysis in cachara catfish fingerlings (Pseudoplatystoma reticulatum). SI: Site of

infection; EF: Examined fish; PF: Parasitized fish, P: Prevalence; MI: Mean intensity (minimum - maximum

values).

Neotrop. Helminthol., 8(1), 2014

Figure 1. Ichthyophthirius multifiliis Fouquet, 1876 observed in gill fresh mount (a) and Klein's silver-impregnated Trichodina

heterodentata Duncan, 1977, that show adhesive discs (b). Magnification 100 x (a) and bar scale 10 µm (b).

Figure 2. Histological alterations caused by Ichthyophthirius multifiliis in cachara fingerlings. Parasite in the epithelium

showing the horseshoe-shaped nucleus (a – arrow) and in the adjacent tissue, mucous cell proliferation (a – dotted arrow).

Hyperplasia and a multifocal to coalescing area with hydropic degeneration and necrosis can be seen (2b,c). Ulceration at the

parasite site of attachment is shown in 2d. Hematoxylin-eosin staining. Bar = 100 µm (a,d), 150 µm (b) and 30 µm (d).

Figure 3. Histological alterations caused by Ichthyophthirius multifiliis in cachara fingerlings. Mucous cells marked with PAS

(a), and parasite under the epithelium (b – asterisk), with several engulfed host cells and inflammatory cells adhering to the

parasite surface (b - arrow). Inflammatory infiltrate composed of PAS-positive granular leukocyte (c and d – arrows); parasite

inserted in the tissue (d – asterisk); and inflammatory cells engulfed and adhering to the surface (d – arrows). PAS staining. Bar =

10 µm (a) and 30 µm (b – d).

cosmopolitan parasite. It causes inflammatory

and structural disturbance in the gills of the hosts

with desquamated epithelial cells (Tang & Zhao,

2007), that can culminate to asphyxia and

mortality.

Ichthyophthirius multifiliis was the main

parasite found in this study, thereby confirming

the findings of Pádua et al. (2012b) from the

hybrid surubim catfish (P. reticulatum x P.

corruscans) and Carneiro et al. (2005) from

silver catfish [Rhamdia quelen (Quoy &

Gaimard, 1824)] in central-western and

southern Brazil, respectively. Pantoja et al.

(2012) observed a positive correlation between

the mean intensity of infection by I. multifiliis

and the size and weight of juvenile tilapias. In

the present study, it was observed only a positive

correlation between the size of the fingerlings

In this study, the protozoan ciliates were the

most prevalent parasites both I. multifiliis and T.

heterodentata. In Brazil, T. heterodentata was

first recorded in tadpoles of Rhinella pombali

Baldissera, Caramaschi & Haddad, 2004 (Dias

et al. 2009), and were subsequently diagnosed in

channel catfish [Ictalurus punctatus

(Rafinesque, 1818)] reared in southern Brazil

(Martins et al. 2010a) and pacu fingerlings

(Piaractus mesopotamicus Holmberg, 1887)

farmed in the southeastern region (Pádua et al.

2012a). This study describes cachara (P.

reticulatum) as a new host for T. heterodentata,

in which more than 40 species of fish have

already been described worldwide as hosts

(Martins et al. 2010a), thus making this a

DISCUSSION

Páduaet al.

Host-Parasite relationship in Pseudoplatystoma reticulatum

Neotrop. Helminthol., 8(1), 2014

Important pathogenic parasites such as I.

multifiliis, T. heterodentata, followed by

C r y p y o b i a s p . , H e n n e g u y a s p . ,

Ancyrocephalinae monogenean and Nematoda

larvae were diagnosed in cachara fingerlings.

Besides the ciliated protozoans I. multifiliis and

T. heterodentata were the main etiological

agents diagnosed, T. heterodentata was firstly

reported on cachara. Ichtyophthyrius multifiliis

infection induced severe tissue damage in

cachara fingerlings, mostly damaging the skin

and fins which can cause a portal of entry to

secondary infections.

The authors thank Pedro Henrique de Oliveira

Viadanna (Caunesp) for histopathological

a n a l y s i s , A Q U A B R A S I L p r o j e c t

(Technological Basis for Sustainable

Development of Aquaculture), EMBRAPA, the

Ministry of Fisheries and Aquaculture and

National Council for Scientific and

Technological Development (CNPq

577657/2008-9) for financial support and grant

to M.L. Martins (CNPq 302493/2010-7), and

Coordination for the Improvement of Higher

Education Personnel (CAPES) for doctoral

schollarship to G.T. Jerônimo (CAPES/BEX

9655-11-5).

and the mean intensity of infection by I.

multifiliis. These differences might be related to

different development stages of the fish, since

fingerlings were used in our study, while Pantoja

et al. (2012) used juveniles. Parasitism by I.

multifiliis in cachara fingerlings was higher in

the skin and fins than that observed in the gill

tissue. We admit that greater intensity of

infection in the skin and fins could be strongly

associated to greater surface area for theront

attachment.

The histopathological analysis showed severe

tissue alterations due to I. multifiliis infection,

that coincides with the findings of other

investigators (Ventura & Paperna, 1985;

Dickerson, 2006; Päkk et al. 2011). Moreover,

the ulcers formation on the skin after theront

entrance might cause a portal of entry to

secondary infections as demonstrated by Xu et

al. (2012). In addition, the epithelial

hyperplasia, mucous cell proliferation and

necrosis in the gill tissue limit the

osmoregulatory gas and ion exchanges in fish

(Hines & Spira, 1974), leading to metabolic

misregulation, being lethal to the host, mostly

damaging the skin and fins represent a portal of

entry to secondary infections.

The other parasites Cryptobia, myxosporeans,

monogeneans and nematode larvae were found

in prevalences less than 2%. In addition, the

presence of Myxozoa, Monogenea and

Nematoda in cachara fingerlings was lower than

the studies on adult cachara from the natural

environment (Campos et al. 2009; Naldoni et al.

2011; Adriano et al. 2012). As a result of rapid

proliferation of parasites with monoxenic life-

cycle in culture conditions an increase in the

prevalence of I. multifiliis and T. heterodentata

was found. However, adequate water quality

conditions present a strong influence on the

reproduction and maintenance of infection

(Martins et al. 2010b; Jerônimo et al. 2011). In

order to avoid the use of chemotherapics and

consequently outbreaks the regular monitoring

of fingerlings in nursery farms must be

encouraged.

ACKNOWLEDGEMENTS

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Received September 9, 2013.

Accepted December 18, 2013.