Abstract

This study reports the presence of Enterogyrus cichlidarum Paperna, 1963 (Monogenoidea:

Ancyrocephalidae) in the stomach of Nile tilapia, Oreochromis niloticus Linnaeus, 1758, cultured in the

State of Santa Catarina, Southern Brazil. A total of 98 fish originating from a fish pond culture in Joinville,

South Brazil, were examined. The fish were collected in the winter of 2007, in the summer, autumn, winter

and spring of 2008. After anesthetized and sacrificed in a benzocaine solution, their stomachs were removed,

bathed in 55°C water, fixed in 5% formalin for quantification and attainment of the prevalence rate, mean

intensity, mean abundance and mounted in Hoyer's. Prevalence rate throughout the period was 94%. The

greatest mean intensities occurred in August 2008 and November 2008, followed by July 2007, January and

May 2008. The great majority of Monogenoidea are branchial and cutaneous ectoparasites, however reports

of its invasion in the internal organs are rare. This study is the first report of Enterogyrus in Nile tilapia

cultured in Brazil.

Keywords: Brazil - Enterogyrus cichlidarum - stomach - Nile tilapia.

Resumen

Palabras clave: Brasil - Enterogyrus cichlidarum - estómago - tilapia del Nilo.

El presente estudio reporta la presencia de Enterogyrus cichlidarum Paperna, 1963 (Monogenoidea:

Ancyrocephalidae) en el estomago de tilapia del Nilo, Oreochromis niloticus Linnaeus, 1758, de cautiverio

en el Estado de Santa Catarina, Sur de Brasil. Un total de 98 peces de cautiverio en Joinville, Santa Catarina

fueron examinados. Los peces fueron colectados en invierno del 2007, en primavera, otoño, invierno y

primavera del 2008. Después de la anestesia y muerte en benzocaina, sus estómagos fueron removidos,

bañados en agua caliente a 55 C, fijados en formalina 5% para el conteo y evaluación de las tasas de

prevalencia, intensidad de infección, abundancia media y montaje en Hoyer. La tasa total de prevalencia por

todo el periodo fue 94%. Las más altas intensidades de infección ocurrieron en agosto 2008 y noviembre

2008 seguidas de julio 2007, enero y mayo 2008. La mayor parte de Monogenoidea habitan las branquias y

cuerpo de los peces, pero pocos son los encontrados en otros órganos. Este estudio es el primer caso de

Enterogyrus en tilapia del Nilo en Brasil.

NOTA CIENTÍFICA/ RESEARCH NOTE

FIRST REPORT OF ENTEROGYRUS CICHLIDARUM PAPERNA 1963

(MONOGENOIDEA: ANCYROCEPHALIDAE)

ON NILE TILAPIA OREOCHROMIS NILOTICUS CULTURED IN BRAZIL

PRIMER CASO DE ENTEROGYRUS CICHLIDARUM PAPERNA 1963

(MONOGENOIDEA: ANCYROCEPHALIDAE) EN TILAPIA DEL NILO

OREOCHROMIS NILOTICUS DE CAUTIVERIO EN BRASIL

Gabriela Tomas Jerônimo , Giselle Mari Speck & Mauricio Laterça Martins

1 1,2

Suggested citation: Jeronimo, G,T., Speck, G.M. & Martins, M.L. 2010. First report of Enterogyrus cichlidarum Paperna 1963

(Monogenoidea: Ancyrocephalidae) on Nile Tilapia Oreochromis niloticus cultured in Brazil. Neotropical

Helminthology, vol. 4, nº1, pp.75-80.

Neotrop. Helminthol., 4(1), 2010

2010 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

1AQUOS Laboratory of Aquatic Organisms Health, Aquaculture Department,

Federal University of Santa Catarina (UFSC) - Rod. Admar Gonzaga, 1346, 88040-900 - Florianpóolis, SC, Brazil

2Aquaculture Department, Federal University of Santa Catarina (UFSC),

Rod. Admar Gonzaga, 1346, 88040-900, Florianpóolis, SC, Brazil. E-mail: mlaterca@cca.ufsc.br

INTRODUCTION

Monogenoidea are commonly found on the

surface and gills of freshwater and marine fish

(Thatcher, 2006; Bakke et al., 2002).

Differently, some species can be found in the

stomach and viscera of cichlid fish (Noga &

Flowers, 1995).

There are eleven species of Enterogyrus:

Enterogyrus cichlidarum Paperna, 1963 was

first identified in “redbelley tilapia” Tilapia zilli

Gervais, 1848, and “Nile tilapia” Oreochromis

niloticus Linnaeus, 1758 by Paperna (1963); E.

globodiscus and E. papernai in “banded

etropuls” Etroplus suratensis Bloch, 1790

(Gussev & Fernando, 1973); E. melensis in

“banded jewelfish” Hemichromis fasciatus

Peters, 1857 (Bilong Bilong et al., 1989); E.

malmbergi in Nile tilapia; E. barombiensis in

“pungu” Pungu maclareni Trewavas, 1962,

“pindu” Stomatepia pindu Trewavas, 1972 and

“konye” Konia eisentrauti Trewavas, 1962

(Bilong-Bilong et al., 1991); E. foratus and E.

coronatus in “guinean tilapia” Tilapia

guineensis Gunther, 1862 (Parisele et al., 1991);

E. crassus in Tilapia nyongana Thys van den

Audenaerde, 1971; E. amieti in “chinese

tilapia” Sarotherodon galilaeus sanagaensis

Thys van den Audenaerde, 1966 (Bilong-

Bilong et al., 1996), E. hemihaplochromi in

“egyptian mouthbrooder” Hemihaplochromis

multicolor Schlöler, 1903 (Cone et al., 1987).

This genus is well adapted to live in the stomach

and to withstand the digestive enzymes (Cone et

al., 1987). These authors argued that the body

thickness of the parasites might be responsible

for their survival in the stomach. Occasionally,

the worms may cause chronic mortality in

Tilapia mossambica Peters, 1852 fry as

observed by Noga & Flowers (1995). In this

case, the fish showed skin darkness, loss of

appetite, muscular softening, invasion of the

submucosa of the intestinal tract and

inflammatory reaction in the visceral cavity

(Noga & Flowers, 1995). This study describes

the presence of E. cichlidarum in the stomach of

Nile tilapia cultured in Brazil for the first time.

Ninety eight fish from two ponds and two

different brood stocks in a fish farm located in

the City of Joinville, Santa Catarina, South

o o

Brazil (26 18'16''S, 48 50'44''W) were

examined, in winter 2007 (n=20), summer 2008

(n=20), fall 2008 (n=20), winter 2008 (n=20)

and spring 2008 (n=18). The water quality was

measured on the sample days. Dissolved

-1

oxygen varied from 5.9 to 8.9 mg·L ,

transparency from 38 to 77 cm, pH from 6.0 to

-1

7.7, ammonia from 0.1 to 0.5 mg L and water

temperature from 18.0 to 25.1 °C.

After anesthetized and sacrificed and

-1

maintained in a benzocaine solution (50 mg·L )

( a p p r o v e d b y E t h i c C o m i t t e e n °

23080055748/2006-04/UFSC/CEUA), their

stomachs were removed, bathed in warm water

at 55°C, fixed in a 5% formalin solution for

parasite counting. Prevalence rate, mean

intensity and mean abundance were calculated

(Bush et al., 1997) and the specimens mounted

using the Hoyer's method for identification

through the esclerotised parts of the parasites

(Fig. 1) (Kritsky et al., 1995).

The data were submitted to variance analysis

and when significant they were submitted for

Tukey test to mean comparison at a significant

level of 5% (Zar, 1999).

The water quality was maintained at the normal

values for freshwater fish culture (Boyd &

Tucker, 1992) during samples. As shown in

Table 1, the highest dissolved oxygen level

observed in 2008 was possibly related to the low

water temperature. In summer of 2008 the

smallest fish (P<0.05) in relation to the other

months.

The worms were identified as E. cichlidarum

based on the descriptions of Paperna (1963) and

Gussev & Fernando (1973) and Bilong-Bilong

Enterogyrus on nile tilapia Jeronimo et al.

RESULTS

MATERIAL AND METHODS

et al. (1989). The total prevalence rate was 94%

during the whole period. The highest mean

intensity was observed in winter of 2008 (17.4

Figure 1. Sclerotized structures of Enterogyrus cichlidarum from Nile tilapia reared in Brazil. A-

copulatory organ, b-ventral hamuli, c-ventral hooklet, d-dorsal hamuli. Bar = 10 µm

parasites) and spring of 2008 (17.3) with mean

abundance 16.5 and 17.3, respectively (Table

1).

Table 1. Mean values and standard deviation of fish weight and length, and parasitological data of

Nile tilapia cultured in South Brazil. Different letters indicate significant difference amongst

seasons (P<0.05).

Parameters Winter

2007

Summer

2008

Fall

2008

Winter

2008

Spring

2008

Weight (g)

230.7+46.2 b

118.0+50.4 c

30.3 b

239.9+86.7 b

302.7±34.54 a

Length (cm)

20.8+1.5 b

17.5+2.2 c 20.1+1.4 b

21.9+2.3 b

25.8±0.9 a

Parasitized fish/

Examined fish

19/20

17/20

19/20

18/18

Prevalence (%)

100

Mean intensity 4.1+1.8 b

2.3+1.4 b

1.5+0.8 b

17.4+9.4 a

17.3±14.0 a

Range 1 a 7 1 a 5 1 a 3

5 a 44

3 a 61

Mean abundance 3.9+2.0 b

2.1+1.4 b

1.2+0.8 b

16.5+10.0 a

17.3+14.0 a

Neotrop. Helminthol., 4(1), 2010

showed that the dorsal hamulus of E.

cichlidarum remained firmly attached into host

tissue. In heavy infection the attachment of

enterogyrids can cause an inflammatory

reaction and loss of intestinal epithelium (Noga

& Flowers, 1995).

It must be emphasized that the presence of

enterogyrids in the Brazilian cultured tilapia

might be common. The fish farmers must be

encouraged to utilize fish health diagnostics and

to follow an adequate sanitary plan.

Consequently, the fish farmers must to know

what parasite level their fish present. Moreover,

the parasitological exam of fry is important to

avoid mortalities caused by a heavy fish

infection. However, studies on histopathology

are also necessary to verify eventual changes

and the degree of injury of enterogyrids on the

stomach epithelium.

The authors thank CAPES and CNPq for MS

grants to Gabriela T. Jerônimo and Giselle M.

Speck, financial support (CNPq 301072/2007-

8) to Mauricio L. Martins and technical support,

(CNPq 501176/2005-5), to MPA (Ministério da

Pesca e Aquicultura) and EMBRAPA (Empresa

Brasileira e Pesquisa Agropecuaria) for

financial support. The authors are indebted to

Walter A. Boeger (Zoology Departament of

Federal University of Paraná, PR, Brazil) who

kindly identified Monogenoidea; Juan R.

Esquivel (Fish farm Panamá, Paulo Lopes, SC,

Brazil) and Ricardo M. Takemoto (NUPELIA,

State University of Maringá, PR, Brazil) for

critical review of the manuscript; and to

Roberto Hoppe (Fish farm Fundação 25 de

Julho, Joinville, SC, Brazil) for fish donation.

Bakke, TA, Harris, PD & Cable, J. 2002. Host

specificity dynamics: observations on

gyrodactylid monogeneans. International

These results are in agreement with Khidr

(1990) wich studying the populational dynamic

of E. cichlidarum in, O. niloticus and T. zilli

from Nile River, Egypt, observed the highest

prevalence and mean intensity of parasites in

the winter.

The mean intensity of infection observed in this

research was similar to that of Noga & Flowers

(1995) in severe infection by the same parasite.

An important consideration is that fish

examined by those authors were smaller than

that were utilized in this work. They argued that

the infection was age dependent, in which

younger fish were more affected. With this point

of view, the smallest fish examined in summer

2008 possibly showed neither clinical signs

ofarasitosis nor mortality due to low number of

parasites that corroborate the observations of

Noga & Flowers (1995).

The mean abundance observed in this work was

higher than that related by Jiménez-Garcia et al.

(2001) which described new species of

Monogenoidea in native cichlid fish from

México. In this case, the authors observed the

presence of E. malmbergi Bilong-Bilong, 1988

in O. niloticus and Cichlasoma callolepis

Regan, 1904, with an abundance of 0.15 and 1,

respectively. Jiménez-Garcia et al. (2001) have

also argued that the parasite may have been

introduced with tilapia from the African

continent. As a result of the lack of studies on

parasitological analysis in the stomachs of

tilapia, the parasite had not yet been detected in

Brazil until this moment.

The relation among host/parasite/environment

is easily broken into conditions of poor water

quality, inadequate feeding, high stocking

density and stress of handling, as supported by

Moraes & Martins (2004) and Martins et al.

(2004). Contrary to that observed by Noga &

Flowers (1995), in this study, no clinical signs

were noticed, especially on fish collected in

winter 2008 that had the highest number of

parasites. The studies of Cone et al. (1987)

DISCUSSION

ACKNOWLEDGEMENTS

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Neotrop. Helminthol., 4(1), 2010

Recibido el 22 de marzo del 2010.

Aceptado el 18 de junio del 2010.

*Correspondence to author/Autor para correspondencia:

E-mail/correo electrónico:

Maurício L. Martins.

Aquaculture Department, Federal University of

Santa Catarina (UFSC),

Rod. Admar Gonzaga, 1346, 88040-900,

Florianpóolis, SC, Brazil.

mlaterca@cca.ufsc.br

Enterogyrus on nile tilapia Jeronimo et al.