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Revista Brasileira de Parasitologia Veterinária

Print version ISSN 0103-846XOn-line version ISSN 1984-2961

Rev. Bras. Parasitol. Vet. vol.23 no.1 Jaboticabal Jan./Mar. 2014

http://dx.doi.org/10.1590/S1984-29612014006 

Original Article

Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil)

Parasitos de populações de Cichlidae nativos e invasora Oreochromis niloticus (Linnaeus, 1758) em tributário do Rio Amazonas (Brasil)

Luana Silva Bittencourt1 

Douglas Anadias Pinheiro2 

Melissa Querido Cárdenas3 

Berenice Maria Fernandes3 

Marcos Tavares-Dias1  2  * 

1Programa de Pós-graduação em Biodiversidade Tropical – PPGBio, Universidade Federal do Amapá – UNIFAP, Macapá, AP Brazil

2Laboratório de Aquicultura e Pesca, Embrapa Amapá, Macapá, AP, Brazil

3Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz –Fiocruz, Rio de Janeiro, RJ, Brasil

ABSTRACT

This study provides the first investigation on acquisition of parasites in invasive O. niloticus by parasite species of native Cichlidae from the Igarapé Fortaleza basin, Northern Brazil. There were examined 576 specimens of 16 species of native cichlids and invasive O. niloticus collected in the main channel and the floodplain area of this tributary of Amazon River. The invasive O. niloticus was poorly parasitized having only Ichthyophthirius multifiliis, Trichodina centrostrigeata, Paratrichodina africana, Trichodina nobilis (Protozoa) and Cichlidogyrus tilapiae (Monogenoidea), and this host has not acquired any parasite species common to the native ichthyofauna region. In contrast, species of native cichlids showed rich fauna of parasites with predominance of Monogenoidea species, larvae and adults of Nematoda, Digenea, Cestoidea and Acanthocephala, besides four species of Protozoa and four Crustacea. However, only T. nobilis was acquired by native fish, the Aequidens tetramerus, which is a new host for this exotic Trichodinidae. In O. niloticus, well established in the region, the small number of helminth species may be associated with its rusticity, good adaptation in the new environment and also the presence of native parasites with relative specificity, but without ability to complete its life cycle in this invasive host of this ecosystem.

Key words: Colonization; biological invasion; fish parasites

RESUMO

Este estudo é a primeira investigação da aquisição de parasitos na invasora O. niloticus por espécies de parasitos Cichlidae nativos da bacia Igarapé Fortaleza, Norte do Brasil. Foram examinados 576 espécimes pertencentes a 16 espécies de ciclídeos nativos e à invasora O. niloticus coletados no canal principal e área da planície de inundação deste tributário do Rio Amazonas. A invasora O. niloticus foi pobremente parasitada, pois teve somente Ichthyophthirius multifiliis, Trichodina centrostrigeata, Paratrichodina africana e Trichodina nobilis (Protozoa) e Cichlidogyrus tilapiae (Monogenoidea) e não adquiriu qualquer espécie comum à ictiofauna nativa da região. Em contraste, as espécies de ciclídeos nativos apresentaram uma rica fauna de parasitos com predominância de espécies de helmintos Monogenoidea, larvas e adultos de Nematoda, Digenea, Cestoidea e Acanthocephala, além de quatro espécies de Protozoa e quatro Crustacea. Porém, somente T. nobilis foi encontrado em peixe nativo, Aequidens tetramerus, que é um novo hospedeiro para esse Trichodinidae exótico. Em O. niloticus, já bem estabelecida na região, o reduzido número de espécies de helmintos pode estar associado à sua rusticidade, boa adaptação ao novo ambiente e também à presença de parasitos nativos com relativa especificidade, mas sem habilidade em completar seu ciclo de vida nesse hospedeiro invasor desse ecossistema.

Palavras-Chave: Colonização; invasão biológica; parasitos de peixes

Introduction

Biological invasions are occurring worldwide at alarming rates being widely recognized as threats to the integrity and functioning of natural ecosystems (GALLI et al., 2007; POULIN et al., 2011). Whenever a species in a given region is moved to another one, there is always the possibility that its parasites can be taken with it (MENDOZA-FRANCO et al., 2006; GALLI et al., 2007) forming a biotic unit called symbiota by Galli et al. (2005).

In Brazil, despite the introduction of Oreochromis niloticus for culture purposes for over 40 years, some studies on this exotic fish fauna in the natural environment were performed (RANZANI-PAIVA et al., 2005), but studies on the transmission of parasites to native ichthyofauna are still scarce (GRAÇA; MACHADO, 2007). However, when a non-native fish is introduced, the exchange of parasites between native and non-native hosts can be expected depending on many factors related to the host-parasite system.

In a new habitat, the establishment success of an exotic parasite species depends on the acceptable abiotic conditions and complexity of the parasites' life cycle (GALLI et al., 2005; RIBEIRO; LEUNDA, 2012). The transmission of exotic parasites depends, primarily, on biological factors, host-parasite interaction, congeniality of host species and parasite specificity (JIMÉNEZ-GARCÍA et al., 2001; GALLI et al., 2005; ROCHE et al., 2010; RIBEIRO; LEUNDA, 2012). Thus, the intensity and type of native parasites (ectoparasites and endoparasites) acquired vary among different invasive exotic hosts (PATERSON et al., 2012).

The consequences of acquiring new parasites are also difficult to predict, but severe illness may occur in native fish at the beginning, because they do not share a co-evolutionary history with new parasites (ROCHE et al., 2010; GENDRON et al., 2012) and may even suffer a dynamics change of their relationship with their native parasites (PATERSON et al., 2012). Invasive fish may lose parasites from their place of origin during translocation and, then its parasitic fauna may be dominated by native species of parasites common to the local ichthyofauna (ROCHE et al., 2010; PATERSON et al., 2012). In this case, they may represent a very important role in the life cycle of species of endohelminthic parasites (POULIN et al., 2011) depending on lifestyle and diet of invasive fish. The omnivorous feeding habit of O. niloticus favors the occurrence of endohelminthic species and indicates this fish as part of intermediate levels in the food web (GRAÇA; MACHADO, 2007). Regarding fish, one of the factors influencing the composition of parasites fauna is its origin in the area, that is, whether it is a native or exotic host.

The biological invasions can still cause a sudden increase in the incidence or severity diseases in previously existing native host, due to the pressure on these populations (GALLI et al., 2007; POULIN et al., 2011; GENDRON et al., 2012), when they change their behavior or their immunocompetence. However, when these impacts cause the extinction of essential hosts in the life cycle of a native parasite, the population of this area will decline considerably, thus, benefiting other native hosts of this parasite (POULIN et al., 2011). Nonetheless, these negative impacts on native populations are only detected late, due to the difficulty of quick perception of the transition of exotic parasites in the natural aquatic environment. Therefore, since future consequences of invasion of exotic parasites are difficult to estimate (ROCHE et al., 2010), it is necessary to monitor the establishment of exotic parasites in order to identify species translocated from its area of origin and transmitted to local ichthyofauna. By doing this, it will be possible to understand and predict potential impacts caused to native ichthyofauna in invaded natural ecosystem.

In the State of Amapá, Northern Brazil, 18 years after the introduction of O. niloticus in several fish farms there were invasion and establishment of this fish in the Igarapé Fortaleza basin, an important tributary of the Amazon River. This invasion is causing strong pressure on the biomass of Cichlidae species of the local ichthyofauna, due to competition for food and occupation of breeding areas, shelter and feeding (BITTENCOURT person communication). However, it has not been investigated yet the impacts of introducing Nile tilapia on the fauna of parasites in native ichthyofauna of this natural ecosystem with important species of scientific and applied interest. However, the introduction of trichodinids Paratrichodina africana Kazubski & El-Tantawy, 1986 (PANTOJA et al., 2012) was reported recently for O. niloticus farmed in this same region of Brazil.

The aim of this study was to investigate the parasites of O. niloticus and species of native Cichlidae from the Igarapé Fortaleza basin (State of Amapá) and to identify whether there was transfer of parasites between such ecologically similar fish species inhabiting the same environment.

Materials and Methods

Characterization of the studied area

The Igarapé Fortaleza basin, in the State of Amapá, (Eastern Amazon), is composed by a main channel and the floodplain area (Figure 1). This basin is a tributary of the Amazon River, and then the main channel of the basin and Amazon River are both responsible for forming the floodplain area. This floodplain area is a fluvial physical system drained by freshwater and influenced by high rainfall and tides of the Amazon River (TAKYAMA et al., 2004). Several fish, including Cichlidae species are known throughout this basin (main channel and floodplain area), because the floodplain area form a propitious environment to the development of small and medium size fish species being important to subsistence fishing and aquarium. In the rainy season (December to June), waters spread over the plain, when favorable conditions lead to most fish to reproduce earlier in the season. This is the main period for feeding, growth and accumulation of energy reserves used to support the short food supply during the drainage season (GAMA; HALBOTH, 2004) from June to November.

Figure 1. Collection localities of native Cichlidae species and Oreochromis niloticus in the Igarapé Fortaleza basin, eastern Amazon, Brazil. 

Fish and sampling procedures

In the period from December 2009 to June 2011, in the main channel of the Igarapé Fortaleza and area under the floodplain action, specimens of O. niloticus and Cichlidae species were captured by using cast nets of 30 and 40 mm and gill nets of 20, 25 and 30 mm (ICMBio License: 23276-1). The caught fish were then transported on ice to the Laboratory of Aquaculture and Fisheries of Embrapa Amapá, Macapá (AP) for parasitological analysis.

Parasitological analysis

For each caught fish, the mouth and gills were examined for ectoparasites, and gastrointestinal tract for collection of endoparasites. The techniques used for collection, fixation, conservation and staining of parasites were according to previous recommendations (AMATO et al., 1991; EIRAS et al., 2006). For Trichodinidae identification, gills smears were carried out, dried at room temperature and impregnated with silver nitrate using the Klein's method (VAN AS; BASSON, 1989) and other samples were stained with Giemsa (LOM, 1958). The parasitological terminology used throughout follows that described by to Rohde et al. (1995) and Bush et al. (1997).

Physicochemical parameters

Water physicochemical analyses were performed in main channel of the Igarapé Fortaleza and the floodplain area during the mornings and certain pH (pH: YSI-100), dissolved oxygen levels and temperature (DO: 200-YSI) of water, ammonia and nitrite levels (HI93715-Hanna) by using digital devices for each purpose. In the main channel of the Igarapé Fortaleza, water temperature ranged from 27.8 to 28.5°C; pH 6.4 to 6.9; dissolved oxygen levels 1.5 to 2.4 mg/L; total ammonia levels 0.121 to 0.364 mg/L and nitrite 0.030 to 0.032 mg/L. In floodplain area, the water temperature ranged from 26.0 to 33°C; pH 6.2 to 7.5; dissolved oxygen levels from 0.5 to 4.7 mg/L; total ammonia levels from 0.243 to 0.486 mg/L and nitrite 0.010 to 0.098 mg/L.

Results

A total of 576 fish was collected in Igarapé Fortaleza basin, out of which 218 were O. niloticus and 358 were species of native cichlids occurring in higher number of species in the main channel of this basin compared to floodplain area (Table 1).

Table 1. Mean weight and total length of Cichlidae species captured at two sites of the Igarapé Fortaleza basin, Amapá State, eastern Amazon, Brazil. 

Fish species Main channel Floodplain area
N Weight (g) Length (cm) N Weight (g) Length (cm)
Aequidens sp. 4 71.0 ± 24.4 13.9 ± 1.5 3 37.7 ± 5.7 11.7 ± 0.7
Aequidens tetramerus 33 57.1 ± 18.2 13.5 ± 1.6 59 69.0 ± 27.5 14.5 ± 2.2
Astronotus ocellatus 13 212.0 ± 65.0 20.1 ± 2.6 4 236.3 5± 104.5 21.5 ± 4.8
Chaetobranchus flavescens 14 94.4 ± 62.6 17.0 ± 4.4 - - -
Chaetobranchopsis orbicularis 31 105.2 ± 43.9 16.6±3.0 - - -
Cichlassoma amazonarum 6 34.6 ± 7.0 10.7±1.0 54 49.2 ± 19.6 12.8 ± 2.2
Cichlassoma bimaculatum 8 59.0 ± 21.1 14.1 ± 2.9 - - -
Geophagus brasiliensis 01 76.0 ± 0.0 14.5 ± 0.0 - - -
Heros efasciatus 3 64.6 ± 43.9 12.1 ± 4.1 - - -
Hypselecara temporalis 1 56.0 ± 0.0 13.2 ± 0.0 - - -
Laetacara curviceps 17 55.4 ± 24.3 13.6 ± 2.0 3 18.5 ± 4.0 9.1 ± 1.2
Mesonauta sp. 2 34.0 ± 0.0 12.0 ± 0.5 29 54.6 ± 31.6 12.6 ± 2.2
Mesonauta acora 7 22.0 ± 7.3 10.0 ± 1.4 30 62.1 ± 18.7 13.6 ± 1.5
Mesonauta guyanae 9 19.3 ± 7.7 9.5 ± 2.1 - - -
Oreochromis niloticus 37 275.2 ± 51.5 23.2 ± 1.7 181 115.4 ± 77.5 17.2 ± 4.9
Pterophyllum scalare 7 11.1 ± 3.8 8.5 ± 1.1 - - -
Satanoperca jurupari 20 41.3 ± 32.8 12.0 ± 4.0 - - -

The fauna of parasites of O. niloticus was about seven times lower than of the 16 native cichlids species and it consists of monogenoidean species and protozoan ciliates. However, 79.0% of parasites were helminthes species in native cichlids; 10.5% were protozoans and the other 10.5% were species of ectoparasite crustaceans (Table 2). This reduced parasitic fauna in O. niloticusoccurred exclusively in the gills (ectoparasites). In the native host, there was also high parasitism in the gills, but more than half of helminthes were parasites of the gastrointestinal tract, parasitizing the intestine, pyloric cecum and/or liver of hosts (Figure 2).

Figure 2. Richness of parasite species according to the local of infection and collection sites of Cichlidae species in the Igarapé Fortaleza basin, Amapá State, eastern Amazon, Brazil. 

Table 2. Richness of parasite species by taxonomic groups in native host fish and the exotic host fish in the Igarapé Fortaleza basin, Amapá State, eastern Amazon, Brazil. 

Taxon Native Cichlidae O. niloticus
Protozoa 4 4
Crustacea 4 0
Monogenoidea 11 1
Nematoda 6 0
Digenea 7 0
Acanthocephala 4 0
Cestoidea 2 0
Total number of species 38 5

The richness of parasite species and infection levels have differed comparing fish (native and exotic) examined in the floodplain area and the main channel of Igarapé Fortaleza basin. In floodplain area, the dominance was of protozoan species due to the predominance of O. niloticus in this environment and with infection caused by Ichthyophthirius multifiliis Fouquet, 1876, Paratrichodina africana, Trichodina nobilis Chen, 1963 and Trichodina centrostrigeata Basson, Van As & Paperna, 1983. However, in the main channel, where there is higher prevalence and diversity of native cichlids species, it was higher the level of infection and the richness of helminthes ecto- and endoparasites. These hosts native were parasitized by larval and adult forms of Nematoda, Digenea, Acanthocephala and Cestoidea, while in the hosts of floodplain area only a few Digenea and Nematoda species were found. However, in the gills and intestine of native hosts collected in both environments there were found metacercariae of Digenea in different stages of development. Ectoparasite crustaceans were also found only in native cichlids of the main channel of this Amazonian ecosystem (Table 3, 4).

Table 3. Parasite species of native and exotic Cichlidae in floodplain area from the Igarapé Fortaleza basin, Amapá State, eastern Amazon, Brazil. 

Parasite species P (%) MI Host fish
Trichodinidae
Paratrichodina africana 29.5 8333.4 Oreochromis niloticus
Paratrichodina africana and Trichodina nobilis 45.9 11358.7 Oreochromis niloticus
Paratrichodina africana and Trichodina centrostrigeata 100 18422.8 Oreochromis niloticus
Tripartiella tetramerii and Trichodina nobilis 10.2 5974.8 Aequidens tetramerus
Dinoflagellida
Piscinoodinium pillulare 14.8 422.2 Cichlassoma amazonarum
10.0 352.6 Mesonauta acora
Ciliophora
Ichthyophthirius multifiliis 70.7 31040.4 Oreochromis niloticus
100 64607.3 Astronotus ocellatus
100 8303.3 Mesonauta acora
100 18619.0 Mesonauta sp.
100 17600.3 Laetacara curviceps
98.1 36453.9 Cichlassoma amazonarum
100 22493.3 Aequidens tetramerus
100 5026.3 Aequidens sp.
Monogenoidea
Cichlidogyrus tilapiae 3.3 0.11 Oreochromis niloticus
Gussevia asota 100 19.5 Astronotus ocellatus
Sciadicleithrum joanae 26.7 6.5 Mesonauta acora
6.9 2.5 Mesonauta sp.
Gussevia disparoides 16.7 1.8 Cichlassoma amazonarum
Nematoda
Procamallanus sp. 3.4 7.0 Mesonauta sp.
1.8 1.0 Cichlassoma amazonarum
Digenea
Posthodiplostomum sp. (metacercariae) 10.3 2.3 Mesonauta sp.
35.2 3.6 Cichlassoma amazonarum
66.7 1.0 Laetacara curviceps
75.0 27.0 Astronotus ocellatus
53.3 6.7 Mesonauta acora

P: Prevalence, MI: Mean intensity.

Table 4. Parasite species of native and exotic Cichlidae in the main channel from the Igarapé Fortaleza basin, Amapá State, eastern Amazon, Brazil. 

Parasite species P (%) MI Host fish
Trichodinidae
Paratrichodina africana 100 2019.4 Oreochromis niloticus
Dinoflagellida
Piscinoodinium pillulare 57.1 324.5 Pterophyllum scalare
14.3 758.0 Chaetobranchus flavescens
14.3 160.0 Mesonauta acora
64.5 5254.0 Chaetobranchopsis orbicularis
55.0 1347.7 Satanoperca jurupari
12.5 320.0 Cichlassoma bimaculatum
Ciliophora
Ichthyophthirius multifiliis 100 16142.2 Oreochromis niloticus
100 7105.0 Geophagus brasiliensis
100 3330.1 Pterophyllum scalare
76.9 8554.2 Astronotus ocellatus
100 40866.7 Heros efasciatus
100 45562.2 Chaetobranchus flavescens
100 13458.4 Mesonauta acora
100 10875.0 Mesonauta sp.
55.5 2034.0 Mesonauta guyanae
100 20541.3 Chaetobranchopsis orbicularis
100 8229.7 Cichlassoma amazonarum
100 51512.1 Cichlassoma bimaculatum
100 22614.6 Aequidens tetramerus
100 1568.0 Aequidens sp.
100 5935.4 Laetacara curviceps
80.0 10508.6 Satanoperca jurupari
100 1305.0 Hypselecara temporalis
Branchiura
Dolops longicauda 6.4 1.0 Chaetobranchopsis orbicularis
6.0 2.0 Aequidens tetramerus
Argulus multicolor 7.7 1.0 Astronotus ocellatus
Copepoda
Ergasilus sp. 28.6 3.5 Aequidens sp.
Isopoda
Braga patagonica 7.1 1.0 Chaetobranchus flavescens
Monogenoidea
Gussevia asota 92.3 63.1 Astronotus ocellatus
Gussevia disparoides 100 37.3 Heros efasciatus
66.7 4.0 Cichlassoma amazonarum
82.3 14.1 Laetacara curviceps
Sciadicleithrum joanae 85.7 25.7 Mesonauta acora
Sciadicleithrum geophagi 58.1 12.8 Chaetobranchopsis orbicularis
Gussevia disparoides and Gussevia alioides 78.8 19.4 Aequidens tetramerus
Gussevia elephus and Gussevia spiralocirra 78.6 5.2 Chaetobranchus flavescens
Gussevia arilla 62.5 2.8 Cichlassoma bimaculatum
Gussevia spiralocirra 100 23.2 Aequidens sp.
Sciadicleithrum satanoperca 40.0 5.4 Satanoperca jurupari
Sciadicleithrum iphthimum 100 13.4 Pterophyllum scalare
Urocleidoides sp. 33.3 1.3 Mesonauta guyanae
Nematoda
Icthyouris sp. 85.7 6.7 Pterophyllum scalare
33.3 4.0 Heros efasciatus
15.0 10.3 Satanoperca jurupari
44.4 35.3 Mesonauta guyanae
Icthyouris sp.1, Icthyouris sp.2, Procamallanus sp. and Pseudoproleptus sp. 71.4 16.2 Mesonauta acora
Procamallanus sp. 50.0 2.7 Cichlassoma amazonarum
Pseudoproleptus sp. 51.5 8.7 Aequidens tetramerus
76.5 25.8 Laetacara curviceps
Anisakidae gen. sp. (larvae) 9.1 13.0 Aequidens tetramerus
10.0 5.0 Laetacara curviceps
Contracaecum sp. 38.5 2.4 Astronotus ocellatus
Cestoidea
Proteocephalidea gen. sp. (plerocercoid) 12.1 1.0 Aequidens tetramerus
5.0 1.0 Laetacara curviceps
Proteocephalus gibsoni 23.1 7.0 Astronotus ocellatus
Digenea
Digenea gen. sp. 14.3 4.0 Pterophyllum scalare
93.9 53.2 Aequidens tetramerus
Cladorchiidae gen. sp. (metacercariae) 100 5.0 Heros efasciatus
Acanthostomidae gen. sp. and Posthodiplostomum sp. (metacercariae) 92.3 38.8 Astronotus ocellatus
Acanthostomidae gen. sp. and Thometrema sp. (metacercariae) 57.1 42.0 Aequidens sp.
Cladorchiidae gen. sp. and Posthodiplostomum sp. (metacercariae) 100 26.0 Mesonauta acora
57.1 23.8 Mesonauta acora
83.3 8.6 Cichlassoma amazonarum
Clinostomum marginatum 9.6 8.7 Chaetobranchopsis orbicularis
7.7 2.0 Astronotus ocellatus
Thometrema sp. 30.7 6.2 Astronotus ocellatus
Derogenidae gen. sp. (metacercariae) 20.0 3.3 Satanoperca jurupari
Posthodiplostomum sp. (metacercariae) 100 11.0 Mesonauta sp.
41.9 70.3 Chaetobranchopsis orbicularis
Acanthocephala
Gorytocephalus spectabilis 33.3 5.0 Heros efasciatus
28.6 7.0 Mesonauta acora
12.1 2.5 Aequidens tetramerus
10.0 44.0 Satanoperca jurupari
Echinorhynchus paranensis and Gorytocephalus spectabilis 50.0 31.1 Chaetobranchus flavescens
Echinorhynchus paranensis and Neoechinorhynchus pterodoridis 77.4 22.8 Chaetobranchopsis orbicularis

P: Prevalence, MI: Mean intensity.

Most of the parasites were native species and only four parasites were exotic species (Cichlidogyrus tilapiae Paperna, 1960, P. africana, T. nobilis and T. centrostrigeata) occurred in fish of this natural environment after 9-10 years of the invasion of O. niloticus. These exotic parasites were found only in invasive O. niloticus, except T. nobilis that was also transferred to Aequidens tetramerus Heckel, 1840, a native cichlid species. Protozoans Piscinoodinium pillulare Schäperclaus, 1954 and I. multifiliis were also found mainly in natives fish, but both are ectoparasites of unknown origin in Brazil. However, only one native ciliated was found, Tripartiella tetramerii, a trichodinid of A. tetramerus (Tables 3, 4).

Discussion

In Brazil, more than 40 years after introducing O. niloticus, the parasitic fauna of this fish in fish farms consists primarily of species from its place of origin such as P. africana(Trichodinidae), C. tilapiae, Cichlidogyrus aegypticus Ergens, 1981, Cichlidogyrus cirratusPaperna, 1964, Cichlidogyrus halli Price & Kirk, 1967, Cichlidogyrus thurstonae Ergens, 1981, Cichlidogyrus arthracanthus Paperna, 1960, Scutogyrus longicornisPaperna & Thurston, 1969, Gyrodactylus cichlidarum Paperna, 1968 and Enterogyrus cichlidarum Paperna, 1963 (Monogenoidea); besides Trichodina compacta Van As & Basson, 1989, Trichodina magna Van As & Basson, 1989 (Trichodinidae) and Lamproglena monodi Capart, 1944 (Copepoda), parasites originally described as species of cichlids from Africa, Taiwan and the Philippines, as wells as Clinostomum complanatum Rudolphi, 1814, Diplostomum sp. (Digenea), Argulus spinulosus Silva, 1980 (Branchiura), Dolops carvalhoi Lemos de Castro, 1949 (Branchiura) and Ergasilus sp. (Copepoda) acquired from species of Brazilian ichthyofauna (PANTOJA et al., 2012).

In its place of origin, the Nile River delta (Egypt), O. niloticus has been parasitized by the following species of helminthes: C. tilapiae, C. aegypticus, C. cirratus, C. halli, C. thurstonae, C. arthracanthus, S. longicornis, G. cichlidarum and E. cichlidarum, Paracamallanus cyathopharynx Baylis, 1923 (Nematoda), Orientocreadium batrochoides Tubangul, 1931 (Digenea), Polyonchobotriun sp. (Cestoidea), Acanthosentis tilapiae Baylis, 1948 (Acanthocephala), I. multifiliis, T. centrostrigeata, T. rectinucinata and Chilodonella hexastica Kiernik, 1909 (Ciliophora), L. monodi, Ergasilus sarsiCapart, 1944 (Copepoda) and Lernaea cyprinacea Linnaeus, 1758 (Copepoda) (EL-SEIFY et al., 2011; EISSA et al., 2011; SOLIMAN; IBRAHIM, 2012). Therefore, with the introduction of O. niloticus in Brazilian fish farms, there was a loss of its species of endohelminthes and crustaceans, which were then replaced by the common species of native ichthyofauna. However, such results in fish farms may not be representative of conditions in natural Brazilian ecosystems that may be invaded by O. niloticus.

In the Igarapé Fortaleza basin, the parasites of O. niloticus were C. tilapiae, T. centrostrigeata, P. africana, T. centrostrigeata and T. nobilis, which are then the species from biotic unit of this host fish (Galli's symbiota concept), besides I. multifiliis, a ciliated with worldwide distribution. However, such exotic parasites have shown little immediate consequence for the native cichlids, since only once A. tetramerus acquired T. nobilis. The low acquisition of exotic parasites by the rich ichthyofauna of native cichlids is due to the introduction of these parasites in a community of hosts with great diversity of native ectoparasites, especially species of monogenoideans, metacercariae of digeneans in different stages, protozoans I. multifiliis, P. pillulare and T. tetramerii, thus resulting in shortage of available niche for newcomer ectoparasites. Furthermore, P. africana, the most frequent trichodinids in O. niloticus, has parasite specificity. For native parasites, it was also difficult to colonize O. niloticus, because none of these parasites infected this invasive host so far. Thus, while the parasitic fauna of this invasive was formed exclusively by ectoparasites, in native host the infections were caused by ectoparasites and endoparasites, but with higher richness of endohelminthic species, mainly in the main channel where the highest diversity of native fish species occurred.

The parasite species with rich fauna generally occur in a few species of hosts fish, since they are experts, while the parasites in poor fauna are mostly general species (KENNEDY; POJMANSKA, 1996; POULIN, 1997), but this relation does not occur in fish that have suffered frequent translocations to the same environment (POULIN, 1997). In the Igarapé Fortaleza basin, the community of parasites in O. niloticus was dominated by species of gills opportunistic ciliates.

Species of native cichlids were also parasitized by protozoa (I. multifiliis, P. pillulare and T. tetramerii) but its parasitic fauna was dominated mainly by a rich diversity of Monogenoidea, adults and larvae of Nematoda, Digenea, Cestoidea and Acanthocephala, indicating that they are intermediate or paratenic hosts of endohelminthic species in the area of this study. On the other hand, O. niloticus, in its original site this host accumulates in the gills eight species of monogenoideans and four species of helminthic endoparasites. In an artificial lake in Maringá, Southern Brazil, O. niloticus was parasitized by C. sclerosus, C. longicornis, Cichlidogyrus sp.; besides larvae of Contracaecum sp. and Cestoidea, endohelminth that also parasitized Geophagus brasiliensis Quoy & Gaimard, 1824 and Crenicichla britskii Kullander, 1982, species of cichlids of ichthyofauna of Brazil (GRAÇA; MACHADO, 2007). For this tilapia introduced into the Guarapiranga Reservoir, southeastern Brazil, the parasitic fauna is constituted only by Cichlidogyrus sp., Trichodina sp., I. multifiliis, Cryptobia sp. and Henneguya sp. (RANZANI-PAIVA et al., 2005). The parasite fauna of native cichlid Vieja maculicauda Regan, 1905 in the Panama Canal is rich in species of Monogenoidea, Trematoda, Nematoda and Acanthocephala. However, the helminth fauna of the invasive O. niloticus consisted of Trematoda and native Nematoda and three Monogenoidea species of its place of origin, out of which only Cichlidogyrus dossoui Douellou, 1993 was acquired by V. maculicauda (ROCHE et al., 2010). Therefore, this parasite fauna in O. niloticus was higher than that in the present study, which shows that during the early establishment of O. niloticus in the Igarapé Fortaleza basin the small number of parasite species is one of the factors favoring their rapid demographic growth and population explosion in this new environment.

Monogenoideans are parasites with direct life cycle and resistant to elimination when translocated (PÉREZ-PONCE DE LEÓN et al., 2000). Thus, species of the genus Cichlidogyrus translocated with O. niloticus colonized species of endemic cichlids of Mexico (JIMÉNEZ-GARCÍA et al., 2001) and Panama (ROCHE et al., 2010), due to its relative parasite specificity. In contrast, C. tilapiae, the only species of helminth parasitizing this invasive fish in the region of this study, was not competent to invade any of the 16 species of native cichlids, fish ecologically similar. However, in Brazilian fish farms, O. niloticus has been parasitized by C. tilapiae and by C. sclerosus, besides other species still unidentified (PANTOJA et al., 2012), possibly the C. longicornis. Thus, the results of this fish introduction in Brazilian fish farms do not reflect what occurs in the natural environment; it indicates loss of monogenoideans species with the translocation of this tilapia from other regions of Brazil to the studied area. Therefore, the acquisition and transmission of exotic parasites depend on a complex set of factors, including biological aspects of host and parasite, host-parasite interaction and scale-space (JIMÉNEZ-GARCÍA et al., 2001; ROCHE et al., 2010; GENDRON et al., 2012; PATERSON et al., 2012).

The colonization of exotic hosts by native parasites is a process that can take a long time (KENNEDY; POJMANSKA 1996) or be slow (GENDRON et al., 2012), caused by variations in the host-parasite system to species of investigated fish. Invasive fish need some time to acquire generalist helminthic parasites of native ichthyofauna (KENNEDY; POJMANSKA, 1996; PATERSON et al., 2012), especially endohelminthes. Thus, in the Igarapé Fortaleza basin, due to the recent history of invasion of O. niloticus (less than a decade), there was not enough time to acquire common helminth species to their native competitors, which had a rich fauna species of endohelminthes, parasites of complex life cycle involving fish communities and also invertebrates (PÉREZ-PONCE DE LEÓN et al., 2000; PATERSON et al., 2012).

Invasive fish are poor in species of helminthes (GUÉGAN; KENNEDY, 1993; KENNEDY; POJMANSKA 1996; GENDRON et al., 2012; PATERSON et al., 2012), mainly fish that have in their fauna specialist endohelminthes, because these fish are not susceptible to invasion by species of specialist parasites of native fish. Pérez-Ponce de León et al. (2000) found only a single species of endohelminth (Nematoda) parasitizing O. niloticus introduced on the Lake Pátzcuaro (Mexico), while for the same host of lakes of the Panama Canal, Roche et al. (2010) reported four species of Digenea and four species of Nematoda. Therefore, more time is necessary for this invasive tilapia being colonized by species of endohelminthes common to the local ichthyofauna of this study; however, the period is difficult to estimate.

Trichodinidae are predominantly opportunistic protozoans that have broad geographic distribution and generally parasitize the skin of their native and exotic hosts. Overall, the most specialized species parasitize gills of certain groups of hosts, and when they are translocated, remain with their hosts of origin (VAN AS; BASSON, 1987). Paratrichodina africana is a parasite of gills of O. niloticus, but rarely of skin (KAZUBSKI; EL-TANTAWY, 1986), is it strongly associated with Oreochromis hosts. Trichodina centrostrigeata from gills, skin and fins of species of Oreochromis mossambicus Peters, 1852, Pseudocrenilabrus philander Weber, 1897, Tilapia rendalli Boulenger, 1897, Tilapia sparrmanii Smith, 1840 (Cichlidae) and Cyprinus carpio Linnaeus, 1758 from Africa (BASSON et al., 1983); subsequently, it has been found parasitizing O. niloticus in Africa (EL-TANTAWY; KAZUBSKI, 1986), Philippines (BONDAD-REANTASO; ARTHUR, 1989) and now in Brazil, due to its translocation. Thus, this species seems to be more specific to the Cichlidae species (BONDAD-REANTASO; ARTHUR, 1989).

Trichodina nobilis originally described to Cyprinidae is associated with skin and gills of fish species of this family, but it has the skin as a preferential habitat (BASSON; VAN AS, 1994; MARTINS et al., 2012). Thus, it has been reported that this trichodinid parasites the skin, gills and fins of different Cichlidae species (BASSON; VAN AS, 1994), skin of Poecilidae (MARTINS et al., 2012), as well as gills of O. niloticus of Nile River (EL-SEIFY et al., 2011) and also the Amazon estuary in Northern Brazil. Van As and Basson (1987) reported that the species of Tripartiella can vary the degree of specificity, because some species are restricted to the gills of particular genus or even to a single host. In fact, it is observed in the studies of Vulpe (2002), Mohilal and Hemananda (2012), and Mitra et al. (2012) that Tripartiella obtusa Ergens & Lom, 1970, Tripartiella copiosa Lom, 1959 and Tripartiella bulbosa Lom, 1959 are often associated with species of Cyprinidae of genera Cirrhinus, Labeo, Catlaand Cyprinus. Furthermore, T. tetramerii was parasite only of A. tetramerus, a native cichlid in region of this study.

Trichodinidae ciliates can be considered the most common parasites in fish of different environments. In gills of O. niloticus of the Igarapé Fortaleza basin, it was found higher levels of infections caused by P. africana when associated with T. centrostrigeata or T. nobilis. Similarly, in the gills of A. tetramerus the parasitism by T. tetramerii(native) was associated to infection by T. nobilis, but levels of infection were lower compared to exotic tricodinids in gills of O. niloticus. However, for the same tilapia species from the Brazilian reservoir, the levels of infection by Trichodina sp. caused by low temperature of the region (RANZANI-PAIVA et al., 2005) were lower than that in this study. In poor environmental conditions of intensive culture and high stocking density (VAN AS; BASSON, 1987; TAVARES-DIAS et al., 2001; JERÔNIMO et al., 2012) or even in a natural environment (RANZANI-PAIVA et al., 2005), the intensity of these ciliates can increase rapidly. Because its reproduction is favored by excess organic matter (TAVARES-DIAS et al., 2001; JERÔNIMO et al., 2012; MARTINS et al., 2012), especially at high temperatures, as it was the case of this study.

Monogenoidea species were not found in O. niloticus of the main channel of the Igarapé Fortaleza. On the other hand, in this invasive fish of floodplain area, the low levels of gill infection by C. tilapiae were associated with high parasitism by opportunistic protozoa (I. multifiliis, P. africana, T. centrostrigeata and T. nobilis), parasites known for their strong influence on low environmental quality (TAVARES-DIAS et al., 2001; JERÔNIMO et al., 2012). Possibly, C. tilapiae has suffered pressure in this new environment and also by habitat competition (in gills) with the ciliates species. In this same region, for this tilapia from fish farms, it was reported high levels of infection caused by C. tilapiae associated with low parasitism by Trichodina sp. (probably T. centrostrigeata), P. africana and I. multifiliis (PANTOJA et al., 2012), indicating that infections caused by ciliates were secondary. Fish with acute and subacute infection become more susceptible (TAVARES-DIAS et al., 2001) to infections by opportunistic species of protozoa showed in this study. In gills of O. niloticus from reservoir, the levels of infections by Cichlidogyrus sp. were also low due to the occurrence in some months of the year (RANZANI-PAIVA et al., 2005). Sanchez-Ramirez et al. (2004) reported that in O. niloticus kept experimentally in polluted environment, the abundance of C. sclerosus decreased, but the infection was chronic. Therefore, C. tilapiae may be sensitive to environmental eutrophication and may have seasonal infection pattern, this is why it was not found parasitizing this invasive fish in the main channel of the natural investigated ecosystem.

The differences in parasitism between fish of the main channel and floodplain area should be due to the highest diversity of native hosts in the main channel, location with low occupancy by invasive O. niloticus. The low acquisition of exotic parasites by the rich fauna of native cichlids species was expected, since our recent studies (PANTOJA et al., 2012) indicated a reduced fauna of exotic parasites in farmed O. niloticus in Brazil. However, it was unexpected non colonization in O. niloticus by parasite species common to native ichthyofauna, since this exotic fish is in this region for almost a decade. Further studies are needed on the factors that have limited the richness of the community of parasites in O. niloticus and influenced the colonization period in this host to understand the mechanisms of recruitment controlling parasites in introduced fish and the influence on the parasitic fauna of other species of native ichthyofauna.

This was the first report on T. nobilis(Trichodinidae) for A. tetramerus and O. niloticus; T. centrostrigeata(Trichodinidae) for O. niloticus; P. pillulare (Dinoflagellida) for Cichlassoma amazonarum, Mesonauta acora, Pterophyllum scalare, Chaetobranchopsis orbicularis, Satanoperca jurupari, Cichlassoma bimaculatumand Chaetobranchus flavescens; I. multifiliis(Ciliophora) for M. acora, Laetacara curviceps, C. amazonarum, A. tetramerus, G. brasiliensis, P. scalare, Heros efasciatus, C. flavescens, Mesonauta guyanae, C. orbicularis, C. bimaculatum, S. jurupari and Hypselecara temporalis; Sciadicleithrum joanae (Monogenoidea) for M. acora; Gussevia disparoides (Monogenoidea) for C. amazonarum, A. tetramerus, L. curviceps and H. efasciatus; G. alioides (Monogenoidea) for A. tetramerus; Gussevia elephus (Monogenoidea) for C. flavescens; Gussevia spiralocirra(Monogenoidea) for C. flavescens; Gussevia arilla(Monogenoidea) for C. bimaculatum; Sciadicleithrum satanoperca (Monogenoidea) for S. jurupari; Urocleidoides sp. (Monogenoidea) for M. guyanae; Posthodiplostomum sp. (Diplostomidae) for C. amazonarum, M. acora and C. orbicularis; Dolops longicauda (Branchiura) for A. tetramerus and C. orbicularis; Braga patagonica (Isopoda) for C. flavescens; Proteocephalus gibsoni(Proteocephalidea) for Astronotus ocellatus; Clinostomum marginatum (Clinostomidae) for C. flavescens and A. ocellatus; Gorytocephalus spectabilis (Neoechinorhynchidae) for H. efasciatus, M. acora, A. tetramerus, S. jurupari and C. flavescens, and Echinorhynchus paranensis (Echinorhynchinae) for C. flavescens and C. orbicularis.

Acknowledgements

This study was developed in accordance with the principles recommended by the Brazilian College of Animal Experimentation (COBEA). The authors thank the National Council for Scientific and Technological Development (CNPq, Brazil) for supporting this project (# 556827/2009-0). Marcos Tavares-Dias was supported by a Research fellowship from CNPq.

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Received: August 21, 2013; Accepted: December 16, 2013

*Corresponding author: Marcos Tavares Dias, Embrapa Amapá, Rod. Juscelino Kubitschek, Km 5, 2600, CEP 68903-419, Macapá, AP, Brasil, e-mail: marcos.tavares@embrapa.br; mtavaresdias@pq.cnpq.br

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