Resumen

Abstract

ORIGINAL ARTICLE / ARTÍCULO ORIGINAL

HELMINTHES PARASITIZING SEMAPROCHILODUS INSIGNIS JARDINE, 1841

(OSTEICHTHYES: PROCHILODONTIDAE) FROM THE CENTRAL AMAZONIA

(BRAZIL), AND THEIR RELATIONSHIP WITH THE HOST

HELMINTOS PARÁSITOS DE SEMAPROCHILODUS INSIGNIS JARDINE, 1841

(OSTEICHTHYES: PROCHILODONTIDAE) DEL CENTRO DE LA AMAZONÍA

(BRASIL), Y SU RELACIÓN CON EL HOSPEDERO

1 2 1

Ana Mara Oliveira da Silva , Marcos Tavares-Dias & Joelma dos Santos Fernandes

1Instituto de Saúde e Biotecnologia, Universidade Federal do Amazonas (UFAM), Coari, Estado do Amazonas, Brasil.

2Laboratório de Aquicultura e Pesca, Embrapa Amapá, Macapá, Estado do Amapá, Brasil.

Suggested citation: Silva, O.A.M., Tavares-Dias, M. & Fernandes, J.S. 2011. Helminthes parasitizing Semaprochilodus insignis Jardine, 1841

(Osteichthyes: Prochilodontidae) from the central Amazonia (Brazil), and their relationship with the host. Neotropical Helminthology, vol 5,

nº 2, pp. 225-233.

Key words: Amazonia - Condition factor - Freshwater fish - Helminthes - Parasites.

Este estudio describe la fauna de parásitos y la relación hospedero-parásito en Semaprochilodus

insignis Jardine, 1841, encontrados en el Lago Coari, tributario en el centro del Rio Solimões (estado

del Amazonas, Brasil) en la Amazonia central. De 56 peces examinados, el 23,2% tenía las branquias

parasitadas por Gyrodactylus gemini Ferraz, Shinn y Sommerville 1994 (Monogenoidea:

Gyrodactylidae) y el intestino por Procamallanus inopinatus Travassos, Artigas y Pereira, 1928

(Nematoda: Camallanidae). La tasa más alta de infección fue causada por G. gemini. El factor de

condición relativa (Kn) no se vio afectado por el parasitismo, pero había una correlación positiva entre

la intensidad de los helmintos y Kn, y la longitud total de los hospederos. Este es el primer registro de la

fauna de parásitos de S. insignis con la ocurrencia de G. gemini y P. inopinatus para este hospedero

Neotropical de la Amazonía.

Palabras clave: Amazonía - Factor de condición – Helmintos – Parásitos - Peces de agua dulce.

INTRODUCTION

In South America, there are six known species of

Prochilodontidae of the genus Semaprochilodus. In

the Amazon and Orinoco basins and in some rivers

in Guyana, three species of this genus can be found:

Semaprochilodus insignis Jardine, 1841;

Semaprochilodus taeniurus Valenciannes, 1821

Neotrop. Helminthol., 5(2), 2011

2011 Asociación Peruana de Helmintología e Invertebrados Afines (APHIA)

Versión Impresa: ISSN 2218-6425 / Versión Electrónica: ISSN 1995-1043

This study describes the parasitic fauna and the host-parasite relationship of Semaprochilodus insignis

Jardine, 1841 from Coari Lake, a tributary of the middle Solimões River (state of Amazonas, Brazil) in

Central Amazonia. Of 56 fish examined, 23.2% had gills parasitized by Gyrodactylus Gemini Ferraz,

Shinn & Sommerville 1994 (Monogenoidea: Gyrodactylidae), and the intestine by Procamallanus

inopinatus Travassos, Artigas & Pereira, 1928 (Nematoda: Camallanidae). The highest rates of

infection were caused by G. gemini. Even though the relative condition factor (Kn) was not affected by

parasitism, there was a positive correlation between the intensity of both helminthes, the Kn and the total

length of the hosts. This is the first report on the parasitic fauna of S. insignis with occurrences of G.

gemini and P. inopinatus for this Neotropical host fromthe Amazonia.

225

and Semaprochilodus brama Valenciannes, 1850.

The jaraqui S. brama occurs only in the Tocantins-

Araguaia and Xingu River. The jaraqui S. insignis

and S. taeniurus are widely distributed in the

Amazon River basin and in its tributaries (Castro &

Vari, 2003; Oliveira et al., 2003). Both species

migrate twice a year towards nutrient-rich rivers

and return to the same tributary with nutrient-poor

waters, where they feed for 3 to 4 months. Adults of

both species are found in flooded areas, in the main

channel of rivers, in floodplain and in streams

(Ruffino, 2005; Batista & Lima, 2010). In the

Brazilian Amazonia, these fish are an important

source of protein for the riverine populations

(Soares et al., 2007; Batista & Lima, 2010) and are

popularly known as jaraqui.

The continental extractive fishery of jaraqui S.

insignis and S. taeniurus occurs in every state in

northern Brazil and also in the state of Maranhão.

In 2007, the production of these fish was 17,474.0

tons in which the contribution of the state of

Amazonas was 16,086.0 tons (Ibama, 2007). These

two species of jaraqui are the second most-caught

fish in the State of Amazonas (Ruffino, 2005), with

a 30.7% share of the total fishery production

(Ruffino et al., 2006). However, overfishing

threatens the natural stocks of these two species

(Ruffino, 2005), since they are not yet farmed for

lack of fingerling production and knowledge about

their biology.

The jaraqui S. Insignis is larger than the jaraqui S.

taeniurus and it reaches its first sexual maturation

with 22.0-23.5 cm when it is around two years old

(Ruffino, 2005; Batista & Lima, 2010). It is diurnal

and feeds on detritus, rotifers, microscopic and

filamentous algae, but detritus and inorganic

particles are predominant in its diet (Castelo, 1992;

Soares et al., 2007; Batista & Lima, 2010). It forms

schools and conducts spawning migration at the

beginning of the rivers flooding season, from

December through March (Ruffino, 2005; Soares

et al., 2007).

Among all vertebrate, fish are the ones with the

highest rates of parasitic infection because the

characteristics of the aquatic environment are

conducive to the development and lifecycle of

different groups of parasites (Guidelli et al., 2006;

Takemoto et al., 2009; Silva et al., 2011),

especially those of direct transmission. Therefore,

studies on the impact of parasites on natural

populations of fish are intended to increase

knowledge about the host-parasite-environment

relationships and the different strategies used by

different parasites, as well as their ecological

aspects (Feltran et al., 2004; Eiras et al., 2006;

Guidelli et al., 2006; Silva et al., 2011).

Condition factor is an important tool for the study

of fish welfare reflecting directly on its health.

Analysis of variations in this indicator has been

used to evaluate the effects of different parasites on

hosts populations or individuals (Guidelli et al.,

2006; Silva et al., 2011; Guidelli et al., 2011). Some

parasites seem not to exert negatives effects on

their hosts, while others can have deleterious

effects in the health of the hosts.

Even though the jaraqui S. insignis is a species of

the ichthyofauna that has great social and economic

importance for the Amazonia, little is known about

its parasitic fauna. The copepod Ergasilus

jaraquensis Thatcher & Robertson, 1982 (Thatcher

& Robertson, 1982) was described in gill filaments

of jaraqui S. insignis collected in Manaus, in the

state of Amazonas. The copepod Gamidactylus

jaraquensis Thatcher & Boeger, 1984 (Thatcher &

Boeger, 1984) was described in the nasal fossae of

this same host from the Amazonas River. Eiras et

al. (2005) described Myxobolus insignis Eiras,

Malta, Varella and Pavanelli, 2005 parasitizing the

gills of jaraqui S. insignis from the Amazonas

River. The monogenoidea Gyrodactylus gemini

Ferraz, Shinn & Sommerville 1994 was described

parasitizing the body surface and fins of jaraqui S.

taeniurus (Ferraz et al., 1994). However, all these

studies aforementioned are taxonomic reports and

none of them refers to the infection levels in S.

insignis. Thus, the present study aimed to describe

the parasitic fauna of S. insignis from Coari Lake, a

tributary of the Middle Solimões River, in the state

of Amazonas, Brazil, and also to study the host-

parasite relationship.

MATERIAL AND METHODS

Fish and collection site

From April to June 2008, specimens of jaraqui

Semaprochilodus insignis were collected from

flooded areas (Fig. 1) of Coari Lake (04º00'582”S,

063º19'225'W), a tributary of the Middle Solimões

River, in the municipality of Coari ( state of

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Helminthes parasitizing Semaprochilodus insignis from Brazil Silva et al.

Amazonas, Brazil, in central Amazonia) for

parasitological studies. All fish were collected with

appropriate gillnets (ICMBio license: 11884-1)

and transported to the laboratory of Universidade

Federal do Amazonas (UFAM), Coari (AM).

Parasitological Examination

All fish were weighed (g) and measured in length

(cm) and necropsy was performed for the analysis

of parasites.

The gills and the gastrointestinal tract of each

specimen were examined. These organs were

removed and analyzed using a common light

microscope and a stereo microscope. The

methodology used for collecting, fixating (Eiras et

al., 2006; Thatcher, 2006) and quantifying the

parasites (Tavares-Dias et al., 2001) followed

previous recommendations. The identification of

the collected parasites was done according to

Moravec (1998), Ferraz et al. (1994) and Thatcher

(2006). Ecological terms followed Bush et al.

(1997) and Rohde et al. (1995).

Relative condition factor (Kn) and host - parasite

relationship

The length and weight of the hosts were used to

calculate the relative condition factor (Kn) of

parasitized and non-parasitized fish according to

Le-Cren (1951), and the differences were

evaluated by t-test. Spearman's rank correlation

coefficient (rs) was used to determine the possible

correlations between the total length of the host and

the number of parasites and to verify correlations

between the number of monogenoideans and the

relative condition factor (Zar, 1999).

RESULTS

Of the 56 jaraqui S. insignis examined, 23.2% were

parasitized by Gyrodactylus gemini Ferraz, Shinn

& Sommerville 1994 (Monogenoidea:

Gyrodactylidae) and by Procamallanus inopinatus

Travassos, Artigas & Pereira, 1928 (Nematoda:

Camallanidae). However, the highest rates of

infection were those by G. gemini in the gills

(Table 1).

There was no significant difference (p>0.05) in the

relative condition factor (Kn) of parasitized and

non-parasitized fish (Table 2 and Fig. 2). However,

a positive correlation was observed between the

intensity of helminthes G. gemini and P. inopinatus

and the total length of hosts (r= 0.442, p = 0.021),

but not with the weight (r= 0.156, p =0.137).

Nevertheless, the Kn showed a highly positive

correlation with the intensity of helminthes (G.

gemini and P. inopinatus) in the hosts (Fig. 3).

Physicochemical parameters of the water

-1

Levels of dissolved oxygen (mg.L ), water

temperature ( C) and pH were measured at the time

of fish collection. The water temperature ranged

from 27.7 to 28.8 ºC; dissolved oxygen levels

ranged from 4.2 to 5.3 mg/L and the pH ranged

from 5.1 to 5.6.

Table 1. Parasitological indexes in jaraqui Semaprochilodus insignis from the Coari Lake, middle Solimões River,

State of Amazonas, Brazil.

227

Neotrop. Helminthol., 5(2), 2011

Table 2. Mean values ± standard deviation of body weight, total length and relative condition factor (Kn) in jaraqui

Semaprochilodus insignis from the Coari Lake, middle Solimões River, State of Amazonas, Brazil. ns: Indicates that

there was not significant difference (p>0.05) between groups by t-test.

Figure 1. Collection of tick-scaled jaraqui Semaprochilodus insignis to flooded area from the Coari Lake, middle

Solimões River, State of Amazonas, Brazil.

228

Helminthes parasitizing Semaprochilodus insignis from Brazil Silva et al.

Figure 2. Length-weight relationship of parasitized ( ) and non-parasitized ( ) jaraqui Semaprochilodus insignis

(n=56) from the Coari Lake, middle Solimões River, State of Amazonas, Brazil.

Figure 3. Correlation between Kn and intensity of helminthes parasites in jaraqui Semaprochilodus insignis from the

middle Solimões River, State of Amazonas, Brazil.

229

Neotrop. Helminthol., 5(2), 2011

DISCUSSION

Most species of Monogenoidea have a high degree

of parasite host specificity, selecting only one host

species or groups of hosts that are phylogenetically

close (Cribb et al., 2002; & Buchmann & Brescani,

2006; Silva et al., 2011). Species of the genus

Gyrodactylus are viviparous and the embryo

develops inside the mother's womb and sexual and

asexual reproduction alternate (Huyse et al., 2003;

Tinsley, 2006). Almost all gyrodactylids are

transferred directly from host to host, but others

monogenoideans taxa, usually have a free-

swimming oncomiracidium that finds and attaches

to the host (Cribb et al., 2002; Tinsley, 2006).

Gyrodactylus gemini, a monogenoidea of jaraqui S.

taeniurus (Ferraz et al., 1994; Thatcher, 2006) was

found in the gills of thick-scaled jaraqui S. insignis

from the Middle Solimões River. However, in

some periods of the year, both the jaraqui S.

insignis and the S. taeniurus, wich are species with

ecologically similar habits, form schools that

migrate together (Ruffino, 2005; Soares et al.,

2007). These factors explain the infection by this

same species of monogenoidean on gills of thick-

scaled S. insignis, too.

In jaraqui S. insignis from the Coari Lake, a

tributary of the Middle Solimões River, the

infection rates by G. gemini were higher than those

reported for Prochilodus lineatus Valenciennes,

1837 from the floodplain of the Paraná River that

were infected by Gyrodactylus sp. (Lizama et al.,

2006). In contrast, they were lower than the

infection rates by Gyrodactylus sp. in Carnegiella

martae Myers, 1927 from the middle Rio Negro

( Ta v a re s - D i a s e t a l . , 2 0 1 0 ) a nd b y

Cosmetocleithrum spp. in Oxydoras niger

Valenciennes, 1821 from Lago Coari (Silva et al.,

2011). On the other hand, they were higher than

the infection rates by Gyrodactylus sp. in the gills

of Paracheirodon axelrodi Schultz, 1956 and

Carnegiella strigata Günther, 1864, both

ornamental fish from the middle Rio Negro, state

of Amazonas (Tavares-Dias et al., 2010).

Nevertheless, Gyrodactylus infrapopulation

growth is highly influenced by environmental

factors such as temperature, water chemistry and

pollution, and also by biotic and host genetic

factors (Tinsley, 2006).

In fish, the diversity of endohelminthes can vary

according to the environment or the species of host,

and it can be related to size, longevity and specially

the diet of the host. The intermediate host is

necessarily part of the diet of the definitive host. In

addition, fish with a longer lifespan present more

time of exposure to parasites, favoring cumulative

processes in the host (Feltran et al., 2004; Guidelli

et al., 2006; Takemoto et al., 2009).

Detritivorous fish such as the jaraqui S. insignis

(Castelo, 1992; Soares et al., 2007; Batista & Lima,

2010) have showed low rates of parasitism by P.

inopinatus, since they are primary consumers and

occupy lower trophic levels in the food chain. They

can act as paratenic, intermediate or final hosts for

this endohelminth (Thatcher, 2006; Takemoto et

al., 2009; Silva et al., 2011). Procamallanus

inopinatus is the most common and abundant

species of Nematoda in Brazilian fish (Feltran et

al., 2004; Takemoto et al., 2009) because it has no

host specificity. Recently, Eiras et al. (2010) have

listed this nematode as a parasite of 51 species of

freshwater fish in Brazil. However, the number of

hosts is greater, since the present study extends its

occurrence to one more host in Brazil, in the central

Amazonia.

In jaraqui S. insignis from the Coari Lake, in the

Middle Solimões River, the rates of infection by P.

inopinatus were lower than those reported for

Leporinus friderici Bloch, 1794 and Leporinus

obtusidens Valenciennes, 1836 from the dam of

Nova Ponte, in Perdizes, state of Minas Gerais

(Feltran et al., 2004) and for Leporinus lacustris

Amaral-Campos, 1945 and L. friderici from the

floodplain of the Paraná River (Guidelli et al.,

2006). Moreover, the prevalence was lower than in

Astyanax altiparanae Garutti & Britski, 2000

(Azevedo et al., 2007) from lakes of Campinas, in

the state of São Paulo, while the intensity and

abundance were higher. Even though nematodes

rarely lead to mortality, these endohelminthes can

cause damages to the physiology and behavior of

fish and delays in their growth and sexual

maturation, depending on the species, parasitized

organ and intensity of infection (Feltran et al.,

2004; Eiras et al., 2010). However, in Leporinus

macrocephalus Garavello and Britski, 1988,

infection by nematodes Goezia leporini Martins &

Yoshitoshi, 2003 caused severe microcytic-

hypochromic anemia (Martins et al., 2004), due to

pathogenicity of parasite.

230

Helminthes parasitizing Semaprochilodus insignis from Brazil Silva et al.

The relative condition factor is an indicator of the

welfane of fish (Le-Cren, 1951; Lizama et al.,

2006; Guidelli et al., 2011; Silva et al., 2011) and

therefore may be useful to detect the species of

parasite that affects the health of the host fish

(Santos & Brasil-Sato, 2006; Guidelli et al., 2011).

However, in jaraqui S. insignis parasitized by

helminthes G. gemini and P. inopinatus, the

average Kn was equal to the standard (Kn=1.00),

but the Kn and the length of the hosts increased

with the intensity of these helminthes. In

Franciscodoras marmoratus Reinhardat, 1874

from São Francisco River (Santos & Brasil-Sato,

2006) and O. niger from the Coari Lake (Silva et

al., 2011), Kn was not influenced by parasitism

either. Similarly, a positive correlation was

described between the Kn of O. niger and the

intensity of Monogenoidea Cosmetrocleitrum spp.

(Silva et al., 2011), as well as between the Kn of P.

lineatus and the abundance of monogenoidean R.

pseudocapsaloideum, copepod Gamispatulus sp.

and digenean Saccocoelioides magnorchis

Thatcher, 1978 because larger fish with a higher Kn

can endure relatively higher levels of parasitism

(Lizama et al., 2006).

In conclusion, the results indicate the presence of

few infectious forms in the flooded areas of collect

of S. insignis. Thus, the health of host was not

affected by the low parasitism. This was the first

report on the rates of parasitic infection in S.

insignis and also on the occurrence of G. gemini for

this host examined in the central Amazonia.

ACKNOWLEDGEMENTS

The authors would like to thank Conselho Nacional

de Pesquisa e Desenvolvimento Tecnológico

(CNPq) by scholarship to the first author and for

Grant to Tavares-Dias, M. (300472/2008-0).

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Correspondence to author /Autor para correspondência:

Marcos Tavares-Dias.

Embrapa Amapá, Rodovia Juscelino Kubitschek, km

5, N° 2600, 68903-419, Macapá, AP, Brasil.

E-mail/ correo electrónico:

marcostavares@cpafap.embrapa.br

Received July 31, 2011.

Accepted October 31, 2011.

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