Neotrop. Helminthol., 7(1), 2013

2013 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

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

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

MICROHABITAT OF MONOGENEA AND COPEPODIDS OF LERNAEA CYPRINACEA ON THE

GILLS OF FOUR BRAZILIAN FRESHWATER FISH

MICRO HÁBITAT BRANQUIAL DE MONOGENEA Y COPEPODITOS DE LERNAEA

CYPRINACEA EN LAS BRANQUIAS DE CUATRO PECES BRASILEÑOS DE AGUA DULCE

Abstract

This study evaluated the ectoparasite distribution on the gill archs of pond-reared pacu (Piaractus

mesopotamicus Holmberg, 1887), hybrid patinga (P. mesopotamicus female x P. brachypomus (Cuvier,

1817) male), hybrid tambacu (Colossoma macropomum (Cuvier, 1816) female x P. mesopotamicus male)

and hybrid surubim (Pseudoplatystoma reticulatum female x P. corruscans Spix & Agassiz, 1829 male). A

total of 300 fish were examined from fish farms in West-Central Brazil for parasitological assessment of the

gill arches I, II, III and IV, from the outer to inner arch, respectively. Only the monogenean Mymarothecium

boegeri Cohen & Kohn, 2005 and Anacanthorus penilabiatus Boeger, Husak & Martins, 1995 from the

hybrid patinga showed the greatest (p<0.05) mean intensities on the gill arch I when compared to gill arch

IV. Microhabitat preference was not observed in the other fish examined. Copepodids of Lernaea

cyprinacea Linnaeus 1758 showed no microhabitat preference. This study highlighted the fact that under

culture conditions, homogeneous distribution of parasites on the gills may occur.

Keywords: Anacanthorus - Copepoda - Characidae - Mymarothecium - parasitologia - Siluriformes.

Suggested citation: Jerônimo, GT, Gonçalves, ELT, Bampi, D, Paseto, A, Pádua, SB, Ishikawa, MM & Martins, ML. 2013.Gill

microhabitat of monogenea and copepodids of Lernaea cyprinacea on the gills of four Brazilian freshwater fish. Neotropical

Helminthology, vol. 7, N°1, jan-jun, pp. 65 - 74.

1AQUOS – Aquatic Organisms Health Laboratory, Aquaculture Department, Federal University of Santa Catarina (UFSC), Rod. Admar Gonzaga, 1346, 88040-

900, Florianópolis, Santa Catarina, Brazil.

2Aquaculture Center of São Paulo State University, UNESP, Via de Acesso prof. Paulo Donato Castellane, s/n, Bairro Rural, 14884-900, Jaboticabal, São Paulo,

Brazil.

3Embrapa Western Agriculture, EMBRAPA, BR 163, km 253.6, Cx. Postal 661, 79804-970, Dourados, Mato Grasso do Sul, Brazil.

mlaterca@cca.ufsc.br

1 1 1 1

Gabriela Tomas Jerônimo , Eduardo Luiz Tavares Gonçalves , Daniela Bampi , Ágata Paseto , Santiago Benites de

2 3 1

Pádua , Márcia Mayumi Ishikawa & Maurício Laterça Martins

Resumen

Este estudio evaluó la distribución de ectoparásitos en los arcos branquiales de pacu (Piaractus

mesopotamicus), hibrido patinga (P. mesopotamicus hembra x P. brachypomus macho), híbrido tambacu

(Colossoma macropomum hembra x P. mesopotamicus macho) e híbrido surubim (Pseudoplastystoma

reticulatum hembra x P. corruscans macho) cultivados en viveros. Un total de 300 peces fueran

examinados en piscifactorías del Centro Oeste de Brasil para un levantamiento parasitológico en los arcos

branquiales denominados I, II, III y IV, del arco más externo al más interno, respectivamente. Solamente los

monogeneos Mymarothecium viatorum y Anacanthorus penilabiatus, parásitos del híbrido patinga,

presentaran mayores (p<0,05) intensidades promedios en el I arco cuando es comparado con el IV arco

branquial. Aun así, ninguna preferencia por micro-hábitat por los parásitos en los otros peces fuera

observado. Copepoditos de Lernaea cyprinacea no presentan preferencia por micro-hábitat. Este estudio

muestra que en condiciones de cautiverio puede ocurrir una distribución homogénea de los parásitos en las

branquias.

Palabras clave: Anacanthorus - Copepoda - Characidae - Mymarothecium - parasitologia - Siluriformes.

Gill microhabitat of monogenea and Lernaea Jerônimo et al.

The Central-Western region of Brazil presents

propitiated characteristics for freshwater fish

culture development. Nowadays, it has been

observed significant increase in the production

of characid and silurid fish and also their

hybrids. According to MPA (2012), in 2010, the

production of those fishes in the region was

responsible for about 70 tons, in which we could

notice the improvement of 35% in relation to

2008.

Besides the intensification and aquaculture

development, fish farms are predisposed to

epizootics being the ectoparasites the most

important agents responsible for economic

losses (Shoemaker et al., 2012). Contrarily to

endoparasites, ectoparasites can be directly

affected by the water quality favoring or not their

reproduction which can culminate to fish

mortality (Moraes & Martins, 2004). According

to Jerônimo et al. (2011a) the relationship

host/parasite consists in an important biotic

factor in fish, both intra and interspecific being

directly related to water temperature, light

intensity, photoperiod, chemical water

composition and stocking density. Moreover,

parasitic fauna of fish depends on the

geographical location of the ecosystem and

seasonality (Jerônimo et al., 2011a), on the

water characteristics and the environmental

fauna (Dogiel, 1970).

The study of parasitic communities is important

for understanding the ecological relationship

between the hosts and parasites once it depends

mostly of populational dynamics, which allow

observing the relation among the different

parasite taxa competing or not by specific sites

of attachment (Luque & Cezar, 2004). The fish

gills represent one of the most exploited

microhabitat by the ectoparasites (Fernando &

Hanek, 1976) revealing the specific site of

preference in the hosts (Jeannette et al., 2010).

There may be different outcomes to explain the

microhabitat selection of ectoparasites on fish

gills. Geets et al. (1997) suggested that the

parasite attachment to different sites in the gills

INTRODUCTION is a result of food availability. Another

hypothesis is that the distribution on the gill

arches may be a result of variation in the water

flow and such mechanism would restrict the

adaptation of parasites to the attachment sites

(Arme & Halton, 1972; Davey, 1980; Etchegoin

& Sardella, 1990; Poulin et al., 1991). The third

hypothesis was due to parasite reproduction in

different sites and that the preference for

microhabitat could be related to the age of

parasite (Rohde, 1994). On this view, Timi

(2003) suggested that parasite selection for

specific site might occur in order to enhance the

parasite reproduction chances or by interspecific

competition.

Some investigators have focused the

microhabitat studies in fish from natural (Geets

et al., 1997; Oliva & Luque, 1998; Lo &

Morand, 2001; Baker et al., 2005; Raymond et

al., 2006; Jeannette et al., 2010; Hermida et al.

2012, Iannacone & Alvariño, 2012) and culture

environment (Buchmann, 1989; Heinecke et al.,

2007; Rubio-Godoy, 2008), but no studies were

performed in Brazilian cultured fish until this

moment.

By supporting the above statements, the

hypothesis of this study was that ectoparasites

may present microhabitat preference depending

on the host and/or parasite taxon in culture

conditions. This study aimed to evaluate the

microhabitat distribution of ectoparasites on the

gills of four fishes of economic importance in

Brazil.

In the period of July 2009 through July 2011, a

total of 300 fishes were captured from ponds

located at Grande Dourados, Mato Grosso do

Sul (2212'54.45''S 5448'26.35''W), Central-

Western region of Brazil. From these, 60 pacu

(Piaractus mesopotamicus Holmberg, 1887), 60

hibrids patinga (P. mesopotamicus fêmea x P.

brachypomus Cuvier 1818 macho), 60 hibrids

tambacu (Colossoma macropomum Cuvier 1818

female x P. mesopotamicus male) and 120

MATERIAL AND METHODS

Neotrop. Helminthol., 7(1), 2013

hibrids surubim (Pseudoplatystoma reticulatum

(Eigenmann & Eigenmnn, 1889) female x P.

corruscans (Spix and Agassiz, 1829) male) were

examined.

The fishes were measured and weighed and the

water quality monitored during the culture of

each fish. Water temperature, dissolved oxygen,

electrical conductivity and pH were measured

with a HANNA multiparameter. The alkalinity

was measured by titulation method,

transparency was measured with a Secchi disc

and total ammonia, nitrate, nitrite, iron and

orthophosphate was measured with a

colorimetric method ALFAKIT.

The fishes were captured with net and

transported to the fish farm Laboratory of

Embrapa Western Agriculture and deeply

-1

anesthetized in clove oil (75 mg.L ) (Ethic

C o m i t t e e 2 3 0 8 0 . 0 2 9 9 7 9 / 2 0 0 9 -

05/CEUA/UFSC) for parasitological analysis.

The gills arches were carefully separated from

the outer to the inner arch and named as I, II, III

and IV, respectively. After that, the gills were

bathed in hot water 60 C, for parasite relax and

fixed in 5% formalin solution for posterior

quantification according to Jerônimo et al.

(2011b). The parasites were identified by the

method of Hoyer's to observe the sclerotic

structures (Kritsky et al., 1995) and identified

according to Boeger et al. (1995, 2002), Cohen

& Kohn (2005) and Thacther (2006). The

prevalence, mean intensity and mean abundance

were calculated as suggested by Bush et al.

(1997), wich for monogeneans were not

separated by species. The monogeneans are

deposited in the Laboratory AQUOS, Santa

Catarina, Brazil collection under the numbers

GTJ 1-20.

For statistical analysis, the hypothesis tests were

used to compare the values parasitic values

among the arches (I, II, III and IV), being the null

hypothesis the absence of microhabitat

preference. The behavior of the data was verified

by analyzing the residual and predictions. The

homocedasticity was analyzed by the Bartlett

test with transformations. The data were

submitted to a one way or factorial ANOVA, and

the averages compared by the Tukey test.

Monogenean values from pacu was transformed

in root (y), once these values presented

proportional variation to the means and

posteriorly submitted to variance analysis. To

other hosts the monogenean values were

transformed to root (y) and the Lernaea

cyprinacea copepodids values were transformed

in root (y+0.5), once these data presented

elevated numbers below 10 and mostly equal

zero.

The means and standard deviation of weight and

total length were as follows, respectively: pacu

689.2 ± 288.7 g and 28.8 ± 3.7 cm, hybrid

patinga 724.3 ± 173.0 g and 32.5 ± 2.3 cm,

hybrid tambacu 1,141.0 ± 295.6 g and 37.6 3.4

cm, and hybrid surubim 784.2 ± 371.3 g and 44.9

± 6.2 cm.

The ectoparasites of the Monogenea class were

identified as Anacanthorus penilabiatus Boeger,

Husak & Martins, 1995 in pacu, hybrid patinga

and hybrid tambacu; Mymarothecium boegeri

Cohen & Kohn 2005 and M. viatorum Boeger,

Piasecki & Sobecka, 2002 in the hybrids

tambacu a nd p atinga, respectively;

Amphocleithrium paraguayensis Price &

Romero 1969, Vancleaveus fungulus Kritsky,

Thatcher & Boeger, 1986, V. ciccinus Kritsky,

Thatcher & Boeger, 1986, V. janacauensis

Kritsky, Thatcher & Boeger, 1986 and

Ameloblastella sp. Kritsky, Mendonza-Franco

& Scholz, 2000 in the hybrid surubim. Crustacea

was identified as Lernaea cyprinacea Linnaeus,

1758 copepodids in the hybrids patinga,

tambacu and surubim.

The water quality was kept within the

recommended levels for freshwater fish (Table

1), except for ammonia concentration that was

slightly higher in pacu culture.

More than 95% prevalence was found in all

monogenean-parasitized fishes (Table 2). The

highest mean intensity of monogenean in the

RESULTS

Gill microhabitat of monogenea and Lernaea Jerônimo et al.

gills was observed in pacu followed by the

hybrids surubim, patinga and tambacu. On the

other hand, the hybrids patinga and tambacu

showed 40% and 36% prevalence of

copepodids, respectively, contrarily to that

found in the hybrid surubim that presented low

prevalence (16%) and pacu that was not found to

be parasitized by copepodids (Table 3).

For monogeneans from pacu neither the

variance analysis nor the Tukey test means

comparison showed significant difference (Fig.

1).

The Fig. 2 presents the parasitic values of

monogeneans transformed in log (y+1) in order

to reduce the intervals between the highest and

the lowest values of the data. Only the hybrid

patinga showed higher mean intensity and mean

abundance of infection in the gill arch I that that

observed in the arch IV (Table 2).

According to the variance analysis and Tukey

test means comparison no significant difference

(p>0.05) was found in the parasitism by

copepodids among the gills arches and fishes

examined.

Figure 1. Variance analysis comparing transformed data of monogeneans among the gill arches of pacu, Piaractus

mesopotamicus. Different letters indicate significant difference among the arches in confidence intervals of 95%.

Monogenean root (y)

Arch:

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

Monogenea

Copepodids

Figure 2. Variance analysis comparing transformed data of monogeneans and copepodids of Lernaea cyprinacea among the gill

arches of the hybrids surubim, patinga e tambacu. Different letters indicate significant difference among the arches in confidence

intervals of 95%.

Neotrop. Helminthol., 7(1), 2013

Table 1. Mean values of water quality during the culture of Brazilian freshwater fishes.

Parameter

Fish Recommended

values by

Pacu

Hybrid

patinga

Hybrid

tambacu

Hybrid

surubim

Boyd & Tucker

(1998)

Alkalinity (mg.L-1)

57.98  8.01

40.72  5.83 49.82 

9.35 39.03  6.43 20 a 300

7.02  0.36

7.41 0.98 7.19  0.45 7.14 

0.49 6 a 8

Conductivity (S.cm-1)

55.11  7.34

34.04  8.11 62.99  9.94 26.00  4.93 < 1.000

Dissolved oxygen (mg.L-1)

4.21  1.99

7.38  2.23 6.61  1.29 6.30  1.47 5 a 15

Temperature (oC)

22.8  2.23

22.17  3.90 21.99  4.09 23.53  4.18 20 a 30

Transparency (cm)

24.55  7.89 17.62  4.68 23.78  8.36 20 a 50

Ammonia (mg.L-1)

0.45  0.21

0.18  0.17 0.15  0.09 0.25  0.15 < 0,3

Iron (mg.L-1 Fe)

0.46  028

0.26  0.37 0.33  0.53 0.12  0.19 0.05 a 0.5

Nitrate (mg.L-1 NO3)

0.00  0.00 0.00  0.00 0.00  0.00 0.2 a 10

Nitrite (mg.L-1 NO2)

0.10  0.32 0.03  0.06 0.02  0.07 < 0.03

Ortophosphate (mg.L-1 PO4) - 0.08  0.24 0.45  0.39 0.17  0.32 0.005 a 2

Table 2. Prevalence (P), mean intensity (MI), mean abundance (MA) and minimum and maximum values (Min –

Max) of monogeneans on the gill arches of the examined hybrids. Different letters indicate significant difference

among the arches (p<0.05).

Arch I Arch II Arch III Arch IV Total

Pacu (n=60)

P (%) 100 100 100 100 100

MI 416.5  353.2a 395.1  348.9a 373.0  328.1a 344.7  327.8a 1529  1312

MA 416.5  353.2a 395.1  348.9a 373.0  328.1a 344.7  327.8a 1529  1312

Min – Max 3 – 1245 2 – 1315 8 – 970 2 – 1008 24 - 4269

Hybrid patinga (n=58)

P (%) 100 98 97 93 100

MI 25.7  22.9a 21.9  17.9ab 20.1  23.7ab 15.7  13.4b 81  58

MA 25.7  22.9a 21.6  18.0ab 19.5  23.6ab 14.6   13.5b 81  58

Min – Max 1 – 87 1 – 81 1 – 171 1 – 71 3 - 314

Hybrid tambacu (n=60)

P (%) 86 78 76 78 97

MI 18  24.8a 18.6  21.4a 16.6  18.4a 12.8  16.6a 60.9  81

MA 15.5  23.9a 14.4  20.3a 12.6  17.5a 9.9  15.5a 52.5  77

Min – Max 1 – 105 1 – 83 1 – 75 1 – 88 1 - 285

Hybrid surubim (n=120)

P (%) 91 92 94 92 95

MI 28.0  27.8a 35.0  39.8a 36.9  38.7a 33.9  43.5a 130  138

MA 25.4  27.7a 32.1  39.2a 34.8  38.2a 31.0  42.5a 123  158

Min – Max 1 – 170 1 – 311 1 – 179 1 – 274 2 - 934

Gill microhabitat of monogenea and Lernaea Jerônimo et al.

Table 3. Prevalence (P), mean intensity (MI), mean abundance (MA) and minimum and maximum values (Min –

Max) of copepodids of Lernaeacyprinaceaon the gill arches of the examined hybrids. Different letters indicate

significant difference among the fishes (p<0.05).

Arch I Arch II Arch III Arch IV Total

Hybrid patinga (n=60)

P (%) 28.3a 18.3a 16.7a 23.3a 40a

MI 3.0  2.9a 3.5  3.1a 2.6  1.7a 1.8  1.3a 6  7

MA 0.9  2.0a 0.6  1.9a 0.4  1.2a 0.4  1.0a 2  5

Min – Max 1 – 10 1 – 12 1 – 6 1 – 6 1 - 30

Hybrid tambacu (n=58)

P (%) 28.3a 26.7a 25a 30a 36a

MI 12.6  12.5a 9.6  7.8a 14.1  15.1a 12.1  11.7a 38  41

MA 3.6  8.8a 2.6  5.9a 3.5  9.8a 3.6  8.5a 14  30

Min – Max 1 – 51 1 – 34 1 – 64 1 – 42 1 - 180

Hybrid surubim (n=120)

P (%) 5.8b 10b 5b 10.8b 16b

MI 2.0  0.6a 1.8  0.6a 2.7  0.7a 3.0  1.2a 5  4

MA 0.1  0.5a 0.2  0.6a 0.1  0.6a 0.3  1.2a 1  3

Min – Max 1 – 4 1 – 4 1 – 5 1 – 7 1 - 11

Neotrop. Helminthol., 7(1), 2013

This study evaluated whether ectoparasites in

Brazilian cultured fishes present microhabitat

preference on the gills under culture conditions.

The greatest monogenean values (p<0.05) in the

arch I of the hybrid patinga were similar to that

found by Rohde & Watson (1985), who reported

high mean intensity of Kuhnia scombri Kuhn,

1829 e K. sprostonae Price, 1961 (Monogenea:

Polyopisthocotylea) in the arches I and II. In

fact, these authors suggested microhabitat

difference on the gills of Scomber australasicus

Cuvier, 1832, S. scombrus Linnaeus, 1758 and S.

japonicas Houttuyn, 1782 captured in Pacific

and Atlantic Ocean. Similarly to the present

results, Ramasamy et al. (1985) also observed

high mean intensity of infection by Vallisia

indica Unnithan, 1962 and Allodiscocotyla

chorinemi Yamaguti, 1953 (Monogenea:

Polyopisthocotylea) in the arch I of

Scomberoides commersonnianus Lacepède,

1801. In European eel, Anguilla Anguilla

Linnaeus, 1758, Buchmann (1989) also stated

high mean intensity of Pseudodactylogyrus bini

Kiknuchi, 1929 in the arches I and II. On the

other hand, Raymond et al. (2006) evaluated the

distribution of Afrodiplozoon polycotyleus

Paperna, 1973 on the gills of Barbus neumayeri

Fischer, 1884 from the river Mpanga, Uganda

and concluded that the parasites have been

concentrated on the gill arches II and IV,

differently of our results. The other fish

examined in this study no difference was found

among the gill arches corroborating the results

of Soylu et al. (2010) on the spatial distribution

of Dactylogyrus crucifer Wagener, 1857 on the

gills of Rutilus rutilus Linnaeus, 1758 in Lake

Spanca, Turkey.

Similarly to that observed by Ramasamy et al.

(1985) in S. commersonnianus Lacepède, 1801

parasitized by copepod Caligus sp., our results

did not show significant difference neither

among the gill arches nor among the fishes

parasitized by the copepodids of L. cyprinacea.

This could be explained by the larval stage of

parasite. According to Timi (2003) adult

parasites of Lernanthropus cynoscicola Timi

and Etchegoin, 1996 in Cynoscion guatucupa

Cuvier, 1830 occupied different sites of

attachment and greater prevalence in the gill

arch IV followed by the arches III, II and I. On

the other hand, females showed high prevalence

and mean abundance in the arch II (Timi, 2003).

Ho & Do (1985) studying the specific niche of

Lernanthropus concluded that the body shape of

these copepods has been developed to minimize

the resistance against the income water stream in

the respiratory process. On this view, copepods

of this genus could be used as model to study the

microhabitat. It can be inferred that the body

shape of Lernaea copepodids also present

resistance to water flow on the gills being

unneeded the specific microhabitat on this stage

in the life cycle.

The analyses found in this study corroborate the

null hypothesis of the non-existence of

microhabitat preference on the gills at least on

these fishes examined.

Unpublished data (Martins et al.) also showed

no preference by gill microhabitat in Nile tilapia

parasitized by the monogeneans Scutogyrus

longicornis Paperna & Thurston, 1969,

Cychlidogyrus sclerosus Paperna & Thurston,

1969, Cychlidogyrus thurstonae Ergens, 1981

and Cychlidogyrus tilapiae Paperna, 1960 in

fish farm in Southern Brazil.

We consider that the differences found between

arch I and arch IV in the hybrid patinga were not

enough to justify our hypothesis once they can

also be related to difference in size between the

arches. Another reason to this support could be

related to culture conditions. Differently from

fish examined in natural environment, high

stocking density in culture conditions could

provoke the homogeneous distribution on the

gills. Further studies must be carried out on other

cultured fish considering the competition of

parasites and specific surface gill tissue.

The authors thank National Council for

Scientific and Technological Development

(CNPq) for financial support (CNPq

DISCUSSION

ACKNOWLEDGEMENTS

Gill microhabitat of monogenea and Lernaea Jerônimo et al.

577657/2008-9) and grant to M.L. Martins

(CNPq 302493/2012-7); Ministry of Fisheries

and Aquaculture; Embrapa Western Agriculture,

Dourados, MS, Brazil; Macroprogama 1 “Bases

Tecnológicas para o Densenvolvimento

Sustentável da Aquicultura - AQUABRASIL”

and Coordination for the Improvement of

Higher Education Personnel (CAPES) for

doctoral schollarship to G.T. Jerônimo

(CAPES/BEX 9655-11-5).

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Received January 8, 2013.

Accepted March 11, 2013.

Correspondence to author/ Autor para

correspondencia:

Maurício Laterça Martins

AQUOS – Aquatic Organisms Health Laboratory,

Aquaculture Department, Federal University of

Santa Catarina (UFSC), Rod. Admar Gonzaga,

1346, 88040-900, Florianópolis, Santa Catarina,

Brazil.

E-mail / Correo electrónico:

mlaterca@cca.ufsc.br