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Revista mexicana de biodiversidad

versão On-line ISSN 2007-8706versão impressa ISSN 1870-3453

Rev. Mex. Biodiv. vol.87 no.3 México Set. 2016

http://dx.doi.org/10.1016/j.rmb.2016.06.010 

Ecología

A study on monogenean parasites from the gills of some cichlids (Pisces: Cichlidae) from the Brazilian Amazon

Estudio sobre monogéneos parásitos en branquias de cíclidos (Pisces: Cichlidae) de la Amazonia Brasileña

Aristides Ferreira-Sobrinhoa 

Marcos Tavares-Diasa  b  * 

a Tropical Biodiversity Postgraduate Program (PPGBio), Federal University of Amapá, Rodovia Juscelino Kubitschek, s/n, 69903-419 Macapá, Brazil

b Embrapa Amapa, Rodovia Juscelino Kubitschek, N° 2600, 68903-419 Macapá, Amapá State, Brazil

Abstract:

The aim of this study was to investigate monogenean fauna in gills of Geophagus camopiensis, Pterophyllum scalare, Satanoperca jurupari, and Satanoperca acuticeps in a tributary from the Amazon River system in Brazil. A total of 2,148 monogenean specimens were collected from 140 fish examined from March 2012 to March 2013, and 84.3% of these fish were parasitized by 1 or more species. Such monogeneans were: Sciadicleithrum geophagi, Sciadicleithrum juruparii, Gussevia spiralocirra and Gyrodactylus sp. However, only G. camopiensis was parasitized by more than 1 species of monogenean, while S. jurupari and S. acuticeps were parasitized by the same species. Prevalence, mean intensity and mean abundance varied among host species and the highest levels of infection were by G. spiralocirra followed by S. geophagi, both parasites with aggregated dispersion. Abundance of monogeneans was not influenced by the size of the host. In G. camopiensis, the infection levels by S. geophagi did not vary during the rainy or drainage seasons. This is the first study on monogenean infections for G. camopiensis and S. acuticeps.

Keywords: Amazon; Ectoparasites; Freshwater fish; Helminths; Monogenea

Resumen:

El objetivo de este estudio fue investigar la fauna de monogéneos en las branquias de Geophagus camopiensis, Pterophyllum scalare, Satanoperca jurupari y Satanoperca acuticeps en un afluente del sistema del río Amazonas en Brasil. De marzo de 2012 a marzo del 2013 se examinaron 140 peces, en los cuales se encontraron 2,148 monogéneos, el 84.3% de los peces resultaron parasitados por una o más especies: Sciadicleithrum geophagi, Gyrodactylus sp., Gussevia spiralocirra y Sciadicleithrum juruparii. Sin embargo, solo G. camopiensis albergaba más de una especie de monogéneos, mientras S. jurupari y S. acuticeps resultaron infectadas por la misma especie. La prevalencia, la intensidad media y la abundancia variaron entre especies de hospedero y los niveles más altos de infección fueron causados por G. spiralocirra, seguido por S. geophagi, ambos parásitos con dispersión agregada. La abundancia de monogéneos no resultó influenciada por el tamaño del hospedero. En G. camopiensis, los niveles de infección por S. geophagi no variaron durante la estación seca o la temporada de lluvias. Este es el primer estudio de infecciones de monogéneos en G. camopiensis y S. acuticeps.

Palabras clave: Amazonia; Ectoparásitos; Peces de agua dulce; Helmintos; Monogenea

Introduction

Monogeneans are helminth ectoparasites parasitizing mainly fish. They can fix to body surfaces, fins, swabs or nasal cavities of the hosts. However, a few species are endoparasites, inhabiting the stomach, intestine or urinary bladder of fishes. They have a direct life cycle and consequently a high reproduction rate. Thus, many ectoparasite species are pathogenic to the host, causing serious problems for fish farms (Boeger & Viana, 2006; Cohen, 2013). They are parasites with high host specificity if compared to other helminths (Bellay, Ueda, Takemoto, Lizama, & Pavanelli, 2012; Boeger & Viana, 2006; Braga, Araújo, & Boeger, 2014; Poulin, 1992), and some monogenean species may have a seasonal infection pattern (Boeger & Viana, 2006; Neves, Pereira, Tavares-Dias, & Luque, 2013; Tavares-Dias, Oliveira, Gonçalves, & Silva, 2014).

Neotropical cichlids are often parasitized by species of Gussevia Kohn and Paperna, 1964, SciadicleithrumKritsky, Thatcher, and Boeger, 1989, Trinidactylus Hanek, Molnar and Fernando, 1974, TucunarellaMendoza-Franco, Scholz, and Rozkosna, 2010 (Braga et al., 2014; Melo, Santos, & Santos, 2012; Mendoza-Franco & Vidal-Martínez, 2005; Pariselle et al., 2011; Paschoal, Scholz, Tavares-Dias, & Luque, 2016). However, Brazilian cichlids have been mostly parasitized by Gussevia and Sciadicleithrum species and infection levels are highly variable (Table 1). Therefore, Dactylogyridae species are the most frequent monogeneans in these freshwater cichlids.

Table 1 Monogenean species on native cichlids in Brazil. 

Parasites Host fish p (%) MI Locality References
Gussevia asota Astronotus ocellatus 71.4 17.6 Guandu river (RJ) Abdallah, Azevedo, and Luque (2008)
Gussevia asota Astronotus ocellatus 65.7 11.2 Guandu river (RJ) Azevedo, Abdallah, and Luque (2011)
Gussevia asota Astronotus crassipinnis - - Paraná river (PR) Takemoto et al. (2009)
Gussevia asota Astronotus ocellatus - - Janauacá lake (AM) Kritsky et al. (1989)
Gussevia asota Astronotus ocellatus 100 19.5 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia astronoti Astronotus ocellatus - - Janauacá lake (AM) Kritsky et al. (1989)
Gussevia astronoti Astronotus ocellatus 62.8 17.5 Guandu river (RJ) Abdallah et al. (2008)
Gussevia astronoti Astronotus ocellatus 71.4 7.3 Guandu river (RJ) Azevedo et al. (2011)
Gussevia astronoti Astronotus crassipinnis - - Paraná river (PR) Takemoto et al. (2009)
Gussevia tucunarense Cichla ocellaris 27.0 8.0 Guandu river (RJ) Azevedo et al. (2011)
Gussevia tucunarense Cichla ocellaris - - Negroriver (AM) Kritsky et al. (1986)
Gussevia tucunarense Cichla kelberi 18.4 - Lajes reservoir (RJ) Yamada, Santos, and Takemoto (2011)
Gussevia undulata Cichla ocellaris 60.0 - Guandu river (RJ) Abdallah (2009)
Gussevia undulata Cichla ocellaris 19.0 7.4 Guandu river (RJ) Azevedo et al. (2011)
Gussevia undulata Cichla kelberi - - Paraná river (PR) Takemoto et al. (2009)
Gussevia undulata Cichla ocellaris - - Rio Negro (AM) Kritsky et al. (1986)
Gussevia undulata Cichla piquiti 12.2 - Paraná river (PR) Yamada et al. (2011)
Gussevia undulata Cichla kelberi 23.7 - Lajes reservoir (RJ) Yamada et al. (2011)
Gussevia arilla Cichla kelberi - - Paraná river (PR) Takemoto et al. (2009)
Gussevia arilla Cichlasoma bimaculatum 62.5 2.8 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia longihaptor Cichla kelberi - - Paraná river (PR) Takemoto et al. (2009)
Gussevia longihaptor Cichla ocellaris - - Rio Amazonas (AM) Kritsky et al. (1986)
Gussevia longihaptor Cichla piquiti 19.5 - Paraná river (PR) Yamada et al. (2011)
Gussevia rogersi Astronotus crassipinnis - - Paraná river (PR) Takemoto et al. (2009)
Gussevia rogersi Astronotus ocellatus - - Solimões river (AM) Kritsky et al. (1989)
Gussevia obtusa Uaru amplhiacanthoides - - Negro river (AM) Kritsky et al. (1986)
Gussevia alioides Cichlasoma severum - - Solimões river (AM) Kritsky et al. (1986)
Gussevia alioides Aequides tetramerus - - Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia disparoides Cichlasoma severum - - Rio Solimões (AM) Kritsky et al. (1986)
Gussevia disparoides Aequides tetramerus - - Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia disparoides Cichlassoma amazonarum 16.7 1.8 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia disparoides Chaetobranchus flavescens - - Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia arilla Cichla ocellaris - - Negro river (AM) Kritsky et al. (1986)
Gussevia dispar Cichlasoma severum - - Solimões river (AM) Kritsky et al. (1986)
Gussevia elephus Chaetobranchus flavescens - - Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia spiralocirra Aequidens sp. 100 23.2 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia sp. Astronotus ocellatus 71.4 17.6 Guandu river (RJ) Azevedo, Abdallah, and Luque (2007)
Gussevia sp. Astronotus crassipinnis - - Paraná river (PR) Takemoto et al. (2009)
Sciadicleithrum ergensi Cichla ocellaris 15.0 3.3 Guandu river (RJ) Azevedo et al. (2011)
Sciadicleithrum ergensi Cichla ocellaris - - Negro river (AM) Kritsky et al. (1989)
Sciadicleithrum ergensi Cichla piquiti 29.3 - Paraná river (PR) Yamada et al. (2011)
Sciadicleithrum ergensi Cichla kelberi 76.3 - Lajes reservoir (RJ) Yamada et al. (2011)
Sciadicleithrum guanduensis Geophagus brasiliensis 10.0 11.9 Guandu river (RJ) Carvalho, Tavares, and Luque (2010)
Sciadicleithrum guanduensis Geophagus brasiliensis 36.0 12.1 Guandu river (RJ) Carvalho, Tavares, and Luque (2008)
Sciadicleithrum frequens Geophagus brasiliensis 100 68.5 Paraná river (PR) Bellay et al. (2012)
Sciadicleithrum satanopercae Satanoperca pappaterra 75.0 23 Paraná river (PR) Yamada et al. (2009)
Sciadicleithrum satanoperca Satanoperca jurupari 40.0 5.4 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Sciadicleithrum joanae Crenicichla niederleinii 41.0 11.0 Paraná river (PR) Yamada et al. (2009)
Sciadicleithrum joanae Crenicichla britskii 100 - Paraná river (PR) Yamada et al. (2009)
Sciadicleithrum joanae Mesonauta acora 89.4 8.7 Igarapé Fortaleza (AP) Pantoja, Flores, and Tavares-Dias (2015)
Sciadicleithrum araguariensis Crenicichla labrina 100 - Araguari river (AP) Paschoal et al. (2016)
Sciadicleithrum joanae Mesonauta acora 85.7 25.7 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Sciadicleithrum uncinatum Cichla ocellaris - - Negro river (AM) Kritsky et al. (1989)
Sciadicleithrum uncinatum Cichla piquiti 17.1 - Paraná river (PR) Yamada et al. (2011)
Sciadicleithrum tortrix Uaru amplhiacanthoides - - Negro river (AM) Kritsky et al. (1989)
Sciadicleithrum umbilicum Cichla ocellaris - - Negro river (AM) Kritsky et al. (1989)
Sciadicleithrum iphthimum Pterophyllum scalare - - Solimões river (AM) Kritsky et al. (1989)
Sciadicleithrum iphthimum Pterophyllum scalare 100 13.4 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Gussevia spiralocirra Pterophyllum scalare 92.8 32.8 Igarapé Fortaleza (AP) Pantoja et al. (2015)
Sciadicleithrum geophagi Geophagus surinamensis - - Negro river (AM) Kritsky et al. (1989)
Sciadicleithrum geophagi Chaetobranchopsis orbicularis 58.1 12.8 Igarapé Fortaleza (AP) Bittencourt et al. (2014)
Sciadicleithrum variabillum Symphysodon discus - - Amazon river (AM) Kritsky et al. (1989)
Sciadicleithrum aequidens Aequidens maroni - - Guiana Inglesa Kritsky et al. (1989)
Sciadicleithrum juruparii Satanoperca jurupari - - Guamá river (PA) Melo et al. (2012)
Sciadicleithrum edgari Satanoperca jurupari 50.0 - Araguari river (AP) Paschoal et al. (2016)
Sciadicleithrum cavanaughi Aequidens maroni - - Guiana Inglesa Kritsky et al. (1989)
Sciadicleithrum sp. Crenicichla niederleini 41.5 11.0 Paraná river (PR) Yamada et al. (2008)
Sciadicleithrum sp. Crenicichla niederleini - - Paraná river (PR) Takemoto et al. (2009)
Sciadicleithrum sp. Satanoperca pappaterra - - Paraná river (PR) Takemoto et al. (2009)
Sciadicleithrum sp. Satanoperca pappaterra 64.7 23.0 Paraná river (PR) Yamada et al. (2008)
Sciadicleithrum sp. Crenicichla britskii - - Paraná river (PR) Takemoto et al. (2009)
Sciadicleithrum spp. Geophagus brasiliensis 40.9 20.3 Parque Ingá lake (PR) Graça and Machado (2007)
Sciadicleithrum spp. Geophagus proximus - - Paraná river (PR) Takemoto et al. (2009)
Cleidodiscus sp. Satanoperca pappaterra - - Paraná river (PR) Takemoto et al. (2009)
Cleidodiscus sp. Laetacara sp. - - Paraná river (PR) Takemoto et al. (2009)

P, prevalence; MI, mean intensity.

Studies on infections by monogeneans in populations of Amazonian wild cichlids are scarce. For species of economic importance, such as Satanoperca jurupari Heckel, 1840; Satanoperca acuticeps Heckel, 1840 and Geophagus camopiensis Pellegrin, 1903, as well as for fish important for food consumption of riverine populations from Amazon and for ornamental aquaculture information is limited (Soares et al., 2011). In addition, the monogenean fauna is also unknown for Pterophyllum scalare Schultze, 1823, a fish utilized in Amazonian aquaculture and the ornamental industry in Asia, Europe and North America (Tavares-Dias, Lemos, & Martins, 2010). However, some monogenean species have been reported in some cichlids from the Amazon Basin.

In the Amazon region, Gussevia spiralocirra Kritsky, Thatcher and Boeger, 1986 (Kritsky et al., 1986), and Sciadicleithrum iphthimum Kritsky, Thatcher and Boeger, 1989 were described from P. scalare (Kritsky et al., 1989). Recently, Tripathi, Agrawal, and Sriivastana (2010) found S. iphthimum parasitizing the gills of P. scalare in aquariums in India, due to intercontinental translocation of this ornamental fish from the Amazon. Sciadicleithrum juruparii Melo, Santos and Portes-Santos, 2012 (Melo et al., 2012), Sciadicleithrum satanopercae Yamada, Takemoto, Bellay and Pavanelli, 2009 (Mendoza-Franco, Scholz, & Rozkošná, 2010) and Sciadicleithrum edgari Paschoal, Scholz, Tavares-Dias & Luque, 2016 (Paschoal et al., 2016) were described from S. jurupari. Therefore, since there are no other studies on parasites of wild P. scalare, S. jurupari, G. camopiensis and S. acuticeps, this study investigated the fauna of monogeneans of these hosts from a tributary of the Amazon River system, in Northern Brazil.

Materials and methods

The Matapi River basin, with 2,518 km2, crosses the city of Porto Grande, flowing into the mouth on the Amazon River, in the municipality of Santana, Amapá State (eastern Amazon, Brazil). This watershed spreads over different cities and has several tributaries, including rivers and streams (Fig. 1), all used by various human riverine communities that earn their living from agriculture, livestock and fisheries. It is strongly influenced by a high rainfall in the Amazon region and also by the daily tides of the Amazon River (Takiyama et al., 2007).

Figure 1 Geographic location of the study area and sampling sites along the Matapi River, eastern Amazon, Brazil. 

From March 2012 to March 2013, 75 specimens of G. camopiensis (12.5 ± 3.1 cm and 62.0 ± 43.0 g), 38 specimens of P. scalare (4.5 ± 0.8 cm and 6.0 ± 4.4 g), 15 specimens of S. jurupari (11.8 ± 1.6 cm and 58.5 ± 10.4 g) and 12 specimens of S. acuticeps (11.6 ± 1.1 cm and 50.0 ± 14.5 g) were collected along the Matapi River (Fig. 1). Fish were caught with cast nets, matapi, longlines, handlines and gillnets (20, 30, 40 and 50 mm between nodes) to study monogeneans from gills.

For G. camopiensis, the most captured host species, 39 specimens were collected during the rainy period and 36 during the drought period aiming to study the effects of seasonality in levels of infection. Seasonality was based on rainy and dry seasons, as the region is a tropical forest characterized by a rainy season that runs from December to May (summer and fall) and a dry season that runs from June to November (autumn and winter) (Souza & Cunha, 2010).

For each fish, standard length (cm) and body weight (g) were obtained. The gills were collected and fixed in 5% formalin to collect monogeneans, which were then quantified and preserved in 70% alcohol. To analyze the internal morphology of monogeneans, GAP (picric acid and glycerin) and Hoyer methods were used to study the sclerotized structures. Some parasites were also stained with Masson trichrome (Boeger & Viana, 2006).

The ecological terms used are those recommended by Bush, Lafferty, Lotz, and Shostak (1997). The index of dispersion (ID) and index of discrepancy (D) were calculated using the Quantitative Parasitology 3.0 software to detect the distribution pattern for each infracommunity of parasites (Rózsa, Reiczigel, & Majoros, 2000) in species with a prevalence ≥10%. The significance of ID for each parasite species was tested using the d-statistics (Ludwig & Reynolds, 1988).

To study seasonality, the prevalence of parasites was compared between seasons using the Chi-square (χ 2) test, and the abundance was calculated using the Mann-Whitney (U) test. Spearman correlation coefficient (rs) was used to determine possible correlations between abundance of parasites and length and body weight of hosts (Zar, 2010).

During fish collection, in each sampling site along the Matapi River, the pH, water temperature and dissolved oxygen were measured using the appropriate digital devices for each purpose. The mean rainfall was obtained from the Center for Hydrometeorology and Renewable Energy (NHMET) of the Institute of Scientific and Technological Research of Amapá State (IEPA).

Results

From a total of 140 fish, 84.3% were parasitized by Sciadicleithrum geophagi Kritsky et al., 1989, Gussevia spiralocirra Kohn & Paperna 1964, S. juruparii and/or Gyrodactylus sp., and 2,148 parasites were collected. Satanoperca jurupari was the host with the lowest level of infection, and only G. camopiensis was parasitized by more than 1 parasite species. Gussevia spiralocirra was the monogenean species with the highest level of infection, followed by S. geophagi and S. juruparii, which infected more than 1 host (Table 2).

Table 2 Infection by monogeneans in the gills of cichlid species from eastern Amazon, Brazil. 

Host fish Parasite species EF P (%) MI MA TNP
Geophagus camopiensis Sciadicleithrum geophagi 75 88 6.3 5.5 416
  Gyrodactylussp. - 1 6.0 0.08 6
Pterophyllum scalare Gussevia spiralocirra 38 100 39.3 39.3 1492
Satanoperca acuticeps Sciadicleithrum juruparii 12 67 25.3 16.8 202
Satanoperca jurupari Sciadicleithrum juruparii 15 40 5.3 2.1 32

EF, examined fish; P, prevalence; MI, mean intensity; MA, mean abundance; TNP, total number of parasites.

During the rainy season, the mean water temperature was 28.4 ± 0.9 °C, pH 5.7 ± 0.5, dissolved oxygen 5.4 ± 2.7 mg/L and mean rainfall 357.2 ± 88.5 mm. In the dry season, the mean water temperature was 28.4 ± 1.1 °C, pH 5.5 ± 0.07, dissolved oxygen 3.5 ± 1.6 mg/L and mean rainfall 43.4 ± 47.8 mm.

In G. camopiensis, the prevalence of S. geophagi was 87% in the rainy season and 89% during the dry season, thus indicating no seasonal differences (χ 2 = 0.052, p = 0.820). The mean abundance of S. geophagi in the rainy season was 5.4 and 5.7 in the dry season; therefore, there were no differences (U = 652.0, p = 0.595) between these 2 seasons.

The helminths S. geophagi and G. spiralocirra, showed an aggregated dispersion pattern (Table 3). No significant correlation between the abundance of monogenean species and length and weight of hosts was found (Table 4).

Table 3 Dispersion index (DI), index of discrepancy (D) and d-statistic for infracommunities of monogeneans in cichlid species of the eastern Amazon, Brazil. 

Host fish Parasite species DI d D
Geophagus camopiensis Sciadicleithrum geophagi 2.542 7.3 0.43
Pterophyllum scalare Gussevia spiralocirra 1.577 2.3 0.31

Table 4 Spearman correlation coefficient (rs) between the abundance of monogenean species and the length and weight of cichlid species of the eastern Amazon, Brazil. 

Host fish Parasites Length Weight
rs p rs p
Geophagus camopiensis S. geophagi 0.019 0.870 0.012 0.919
Pterophyllum scalare G. spiralocirra −0.084 0.618 −0.089 0.597
Satanoperca jurupari S. juruparii 0.148 0.598 0.022 0.937
Satanoperca acuticeps S. juruparii 0.115 0.649 0.085 0.736

p, probability.

Discussion

Thirty-one monogenean species for native cichlids from South America are listed, and 80.6% of these parasites are known to infect cichlids from Brazil (Cohen, Just, & Kohn, 2013). In wild populations of G. camopiensis, P. scalare, S. acuticeps and S. jurupari, the monogenean fauna was composed by S. geophagi, S. juruparii, G. spiralocirra, and Gyrodactylus sp., parasite species known to parasitize cichlid species. Only G. camopiensis was parasitized by more than 1 monogenean, S. geophagi and Gyrodactylus sp. Although, S. acuticeps and S. jurupari, are probably phylogenetically close hosts, were parasitized by S. juruparii. The richness of monogeneans may vary among different cichlids, since some ancirocephalid species of South America and Africa have a low host specificity, infecting different hosts (Pariselle et al., 2011), while others infect only a few host species (Boeger & Viana, 2006; Braga et al., 2014; Cohen et al., 2013), as occurred in the present study. Nevertheless, monogeneans seem to infect potentially available hosts when both have experienced a co-evolution (Braga et al., 2014; Poulin, 1992).

The monogenean S. iphthimum, from the gills of P. scalare of central Amazon, was not found in this host in the present study. Anyhow, S. geophagi, described from gills of Geophagus surinamensis Bloch, 1791 from Solimões River (Table 1), was found to parasitize G. camopiensis for the first time. It was also found that only 1 individual of G. camopiensis had 6 specimens of Gyrodactylus von Nordmann, 1932, thereby precluding identification of the species. In South America, few species of Gyrodactylus are known to parasitize cichlid species. Gyrodactylus cichlidarum Paperna, 1968 has been reported in Oreocromis niloticus Linnaeus, 1758 from Colombia and Ecuador (García-Vásquez et al., 2010), and Gyrodactylus geophagensis Boeger & Popazoglo, 1995 in G. brasiliensis from Brazil (Cohen et al., 2013). However, the Gyrodactylus specimens found in G. camopiensis present no resemblance to G. geophagensis. This is the first report of the monogenean S.juruparii in S. acuticeps.

The lentic environment, preferred by G. camopiensis, P. scalare, S. acuticeps and S. jurupari, favors dispersal and reproduction of monogeneans, ectoparasites with free-living stages during some phases of its lifecycle (Bittencourt, Pinheiro, Cárdenas, Fernandes, & Tavares-Dias, 2014; Dogiel, 1961; Neves et al., 2013). Pterophyllum scalare and S. acuticeps were the hosts with the highest level of infection when compared to G. camopiensis and S. jurupari. However, a low number of S. acuticeps and S. jurupari, were examined over an annual cycle, due to low population densities. Nevertheless, the prevalence of S. juruparii in these 2 hosts does not seem to be underestimated. Marques and Cabral (2007) reported that, for helminths with an aggregated dispersion pattern, as in the present study, the mean intensity and mean abundance may be under or overestimated when a small sample of host fish are examined, while prevalence is not affected. In the gills of S. jurupari, the intensity of S. juruparii ranged from 1 to 12 parasites per host, but in S. acuticeps it ranged from 3 to 152, demonstrating a pattern of differentiated infection. However, a lower intensity of S. juruparii in the gills of S. jurupari from Guamá River, Brazil (Table 1) was reported. Sciadicleithrum satanopercae also parasitized the gills of S. jurupari farmed in the Peruvian Amazon (Mendoza-Franco et al., 2010), but infection levels were not studied. Therefore, these results suggest that S. jurupari is host to both species of monogeneans depending on their geographic location.

In G. camopiensis infection levels by S. geophagi are higher than in Chaetobranchopsis orbicularis Steindachner, 1875 (Table 1), and were not influenced by seasonality due to the low environmental variation during the rainy and dry seasons. In contrast, due to seasonal environmental changes that occurred during the Amazon dry season, high levels of infection by Gussevia asota Kritsky et al., 1989, Gussevia astronoti Kritsky et al., 1989 and Gussevia rogersi Kritsky et al., 1989 in Astronotus ocellatus Agassiz in Spix and Agassiz, 1831 (Neves et al., 2013), and Gussevia alioides Kritsky, Thatcher & Boeger, 1986 and Gussevia disparoides Kritsky, Thatcher & Boeger, 1986 in Aequidens tetramerus Heckel, 1840 (Tavares-Dias et al., 2014) were reported. An aggregated dispersion for S. geophagi and G. spiralocirra was observed, a distribution pattern also reported for other species of dactylogirids from the gills of A. ocellatus (Neves et al., 2013) and A. tetramerus (Tavares-Dias et al., 2014), both cichlids from the Amazon. This aggregated pattern is common in fish and it can be related to the reproductive strategy of monogeneans (Scott, 1987), as well as to differences in susceptibility to infection caused by the genetic and immunological heterogeneity of hosts and environmental characteristics.

In the gills of G. camopiensis, P. scalare, S. acuticeps and S. jurupari, the high abundance of monogeneans was not influenced by host size. For S. acuticeps and S. jurupari, this lack of correlation was due to sampling of hosts with a reduced size variation. Furthermore, most specimens of G. camopiensis (5.3-17.5 cm) examined were adults with a low abundance of parasites. However, the abundance of Sciadicleithrum frequens Bellay, Takemoto, Yamada & Pavanelli, 2008 was positively correlated with the length of hosts in Geophagus brasiliensis Quoy & Gaimard, 1824, reflecting an accumulation of these parasites throughout fish growth (Bellay et al., 2012). On the other hand, the abundance of G. alioides and G. disparoides was negatively correlated with the length of A. tetramerus (Tavares-Dias et al., 2014). Therefore, different infracommunities of monogeneans may have different responses to host size, thus determining different levels of infection.

In summary, this is the first report on infection levels by monogeneans in wild populations of S. geophagi. For G. camopiensis and S. juruparii in S. acuticeps we found that parasitism was not influenced by host size. In G. camopiensis, the infection of S. geophagi also had a constant annual pattern, indicating that in these Amazonian hosts, other factors are involved in the parasitism levels of monogenean species. S. juruparii was found in 2 congeneric hosts and most likely may infect other Satanoperca species, but this needs to be further researched.

Acknowledgements

The present work was conducted according to the principles adopted by the Brazilian College of Animal Experiments (COBEA) and under the authorization from ICMBio (# 23276-1). M. Tavares-Dias was supported by a Research fellowship from Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq, Brazil).

References

Abdallah, 2009 Abdallah, V. D. (2009). Biodiversidade dos monogenéticos (Platyhelminthes: Monogenea) parasitos de peixes do Rio Guandu, Estado do Rio de Janeiro, Brasil. Tesis. Rio de Janeiro: Seropédia, Universidade Federal Rural do Rio de Janeiro. [ Links ]

Abdallah et al., 2008 Abdallah V.D, Azevedo R.K, Luque J.L. Notes on the morphology of two species of Gussevia Kohn & Paperna (Monogenea: Dactylogyridae) parasitic on Astronotus ocellatus (Agassiz) (Perciformes: Cichlidae) from Brasil. Pan-American Journal of Aquatic Sciences. 2008; 3:101-4 [ Links ]

Azevedo et al., 2007 Azevedo R.K, Abdallah V.D, Luque J.L. Ecologia da comunidade de metazoários parasitos do apaiarí Astronotus ocellatus (Cope, 1872) (Perciformes: Cichlidae) do Rio Guandu, Estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária. 2007; 16:15-20 [ Links ]

Azevedo et al., 2011 Azevedo R.K, Abdallah V.D, Luque J.L. Biodiversity of fish parasites from Guandu River, Southeastern Brazil: an ecological approach. Neotropical Helminthology. 2011; 5:185-99 [ Links ]

Bellay et al., 2012 Bellay S, Ueda B.H, Takemoto R.M, Lizama M.L.A.P, Pavanelli G.C. Fauna parasitária de Geophagus brasiliensis (Perciformes: Cichlidae) em reservatórios do Estado do Paraná, Brasil. Revista Brasileira de Biociências. 2012; 10:74-8 [ Links ]

Bittencourt et al., 2014 Bittencourt L.S, Pinheiro D.A, Cárdenas M.Q.B, Fernandes M.B.M, Tavares-Dias M. Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Brazilian Journal of Veterinary Parasitology. 2014; 23:44-54 [ Links ]

Boeger and Viana, 2006 Boeger W.A, Viana R.T. Monogenoidea. In V. E. Thatcher (Ed.), Amazon fish parasites. Sofia, Moscow: Pensoft Publishers; 2006. 42-116 [ Links ]

Braga et al., 2014 Braga M.P, Araújo S.B.L, Boeger W.A. Patterns of interaction between Neotropical freshwater fishes and their gill Monogenoidea (Platyhelminthes). Parasitology Research. 2014; 113:481-90 [ Links ]

Bush et al., 1997 Bush A.O, Lafferty K.D, Lotz J.M, Shostak W. Parasitology meets ecology on its own terms: Margolis et al., revisited. Journal of Parasitology. 1997; 83:575-83 [ Links ]

Carvalho et al., 2008 Carvalho A.R, Tavares L.E.R, Luque J.L. A new species of Sciadicleithrum (Monogenea, Dactylogyridae) parasitic on Geophagus brasiliensis (Perciformes, Cichlidae) from Guandu River, Southeastern Brazil. Acta Parasitologica. 2008; 53:237-9 [ Links ]

Carvalho et al., 2010 Carvalho A.R, Tavares L.E.R, Luque J.L. Variação sazonal dos metazoários parasitos de Geophagus brasiliensis (Perciformes: Cichlidae) no Rio Guandu, Estado do Rio de Janeiro, Brasil. Acta Scientiarum Biological Sciences. 2010; 32:159-67 [ Links ]

Cohen, 2013 Cohen S.C. On diversity of the monogenoidean fauna in a megadiverse country, Brazil. Neotropical Helminthology. 2013; 7:1-6 [ Links ]

Cohen et al., 2013 Cohen S.C, Just M.C.N, Kohn A. South American Monogenoidea parasites of fishes, amphibians and reptiles. Rio de Janeiro: Oficina de Livros; 2013. [ Links ]

Dogiel, 1961 Dogiel V.A. Ecology of the parasites of freshwater fishes. In V. A. Dogiel, G. K. Petrushevsky, & Y. I. Polyanski (Eds.), Parasitology of fishes. Leningrad: University Press; 1961. 1-47 [ Links ]

García-Vásquez et al., 2010 García-Vásquez A, Hansen H, Christison K.W, Rubio-Godoy M, Bron J.E, Shinn A.P. Gyrodactylids (Gyrodactylidae, Monogenea) infecting Oreochromis niloticus niloticus (L.) and O. mossambicus (Peters) (Cichlidae): a pan-global survey. Acta Parasitologica. 2010; 55:215-29 [ Links ]

Graça and Machado, 2007 Graça R.J, Machado M.H. Ocorrência e aspectos ecológicos de metazoários parasitos de peixes do Lago do Parque do Ingá, Maringá, Estado do Paraná. Acta Scientiarum Biological Sciences. 2007; 29:321-6 [ Links ]

Kritsky et al., 1986 Kritsky D.C, Thatcher V.E, Boeger W.A. Revision of Urocleidoides (Dactylogyridae, Ancyrocephalinae). Proceedings of the Helminthological Society of Washington. 1986; 53:1-37 [ Links ]

Kritsky et al., 1989 Kritsky D.C, Thatcher V.E, Boeger W.A. Neotropical Monogenea. 15. Dactylogyrids from the gills of Brazilian Cichlidae with proposal of Sciadicleithrum gen. n. (Dactylogyridae). Proceedings of the Helminthological Society of Washington. 1989; 56:128-40 [ Links ]

Ludwig and Reynolds, 1988 Ludwig J.A, Reynolds J.F. Statistical ecology: a primer on methods and computing. New York: Wiley-Interscience Publications; 1988. [ Links ]

Marques and Cabral, 2007 Marques S.J.F, Cabral H.N. Effects of sample size on fish parasite prevalence, mean abundance and mean intensity estimates. Journal of Applied Ichthyology. 2007; 23:158-62 [ Links ]

Melo et al., 2012 Melo M.F.C, Santos J.N, Santos C.P. Sciadicleithrum juruparii n. sp. (Monogenea: Ancyrocephalidae) from the gills of Satanoperca jurupari (Heckel) (Osteichthyes: Cichlidae) in the Guamá River, Amazon Delta, Brazil. Systematic Parasitology. 2012; 82:125-9 [ Links ]

Mendoza-Franco et al., 2010 Mendoza-Franco E.F, Scholz T, Rozkošná P. Tucunarella n. gen. and other dactylogyrids (Monogenoidea) from cichlid fish (Perciformes) from Peruvian Amazonia. Journal of Parasitology. 2010; 96:491-8 [ Links ]

Mendoza-Franco and Vidal-Martínez, 2005 Mendoza-Franco E.F, Vidal-Martínez V.M. Phylogeny of species of Sciadicleithrum (Monogenoidea: Ancyrocephalinae), and their historical biogeography in the Neotropics. Journal of Parasitology. 2005; 91:253-9 [ Links ]

Neves et al., 2013 Neves L.R, Pereira F.B, Tavares-Dias M, Luque J.L. Seasonal influence on the parasite fauna of a wild population of Astronotus ocellatus (Perciformes: Cichlidae) from the Brazilian Amazon. Journal of Parasitology. 2013; 99:718-21 [ Links ]

Pantoja et al., 2015 Pantoja W.M.F, Flores L.V, Tavares-Dias M. Parasites component community in wild population of Pterophyllum scalare Schultze, 1823 and Mesonauta acora Castelnau, 1855, cichlids from the Brazilian Amazon. Journal of Applied Ichthyology. 2015; 31:1043-8 [ Links ]

Pariselle et al., 2011 Pariselle A, Boeger W.A, Snoeks J, Billon Bilong C.F, Morand S, Vanhove M.P.M. The monogenean parasite fauna of cichlids: a potential tool for host biogeography. International Journal of Evolutionary Biology. 2011; 1-15, http://dx.doi.org/10.4061/2011/471480. [ Links ]

Paschoal et al., 2016 Paschoal F, Scholz T, Tavares-Dias M, Luque J.L. Dactylogyrids (Monogenea) parasitic on cichlids from northern Brazil, with description of two new species of Sciadicleithrum and new host and geographical records. Acta Parasitologica. 2016; 61:158-64 [ Links ]

Poulin, 1992 Poulin R. Determinants of host-specificity in parasites of freshwater fishes. International Journal for Parasitology. 1992; 22:53-758 [ Links ]

Rózsa et al., 2000 Rózsa L.J, Reiczigel J, Majoros G. Quantifying parasites in samples of hosts. Journal of Parasitology. 2000; 86:228-32 [ Links ]

Scott, 1987 Scott M.E. Temporal changes in aggregation: a laboratory study. Parasitology. 1987; 94:583-95 [ Links ]

Soares et al., 2011 Soares M.G.M, Costa E.L, Siqueira-Souza F.K, Anjos H.D.B, Yamamoto K.C, Freitas C.E.C. Peixes de lagos do médio Rio Solimões. 2nd ed.. Revisada, Manaus: Instituto Piatam; 2011. [ Links ]

Souza and Cunha, 2010 Souza E.B, Cunha A.C. Climatologia de precipitação no estado do Amapá e mecanismos climáticos de grande escala. In A. C. Cunha, A. E. B. Souza, & H. F. A. Cunha (Eds.), Tempo, clima e recursos hídricos: resultados do projeto REMETAP no Estado do Amapá. Macapá: IEPA; 2010. 177-95 [ Links ]

Takiyama et al., 2007 Takiyama L.R, Cunha A.C, Silva M.S, Martins M.H.A, Rodrigues L.J.C, Avelar S.B, et al. Subsídios à gestão de recursos hídricos na bacia hidrográfica do Rio Matapi. Relatório técnico final CNPq. Macapá: IEPA/GERCO; 2007. [ Links ]

Takemoto et al., 2009 Takemoto R.M, Pavanelli G.C, Lizama M.A.P, Lacerda A.C.F, Yamada F.H, Moreira L.H.A. Diversity of parasites of fish from the upper Paraná River floodplain, Brazil. Brazilian Journal of Biology. 2009; 69:691-705 [ Links ]

Tavares-Dias et al., 2010 Tavares-Dias M, Lemos J.R.G, Martins M.L. Parasitic fauna of eight species of ornamental freshwater fish species from the middle Negro River in the Brazilian Amazon Region. Revista Brasileira de Parasitologia Veterinária. 2010; 19:103-7 [ Links ]

Tavares-Dias et al., 2014 Tavares-Dias M, Oliveira M.S.B, Gonçalves R.A, Silva L.M.A. Ecology and seasonal variation of parasites in wild Aequidens tetramerus, a Cichlidae from the Amazon. Acta Parasitologica. 2014; 59:158-64 [ Links ]

Tripathi et al., 2010 Tripathi A, Agrawal N, Sriivastana N. Monogenoidea on exotic Indian freshwater fishes. 1. A new geographical record of Sciadicleithrum iphthimum Kritsky, Tatcher, and Boeger, 1989 (Dactylogyridae) with the first description of its egg. Comparative Parasitology. 2010; 77:83-6 [ Links ]

Yamada et al., 2008 Yamada F.H, Takemoto R.M, Pavanelli G.C. Relação entre fator de condição relativo (Kn) e abundância de ectoparasitos de brânquias, em duas espécies de ciclídeos da bacia do Rio Paraná, Brasil. Acta Scientiarum Biological Sciences. 2008; 30:213-7 [ Links ]

Yamada et al., 2009 Yamada F.H, Takemoto R.M, Bellay S, Pavanelli G.C. Two new species of Sciadicleithrum (Monogenea, Dactylogyridae) parasites of Neotropical cichlid fishes from the Paraná River, Brazil. Acta Parasitologica. 2009; 54:6-11 [ Links ]

Yamada et al., 2011 Yamada F.H, Santos L.N, Takemoto R.M. Gill ectoparasite assemblages of two non-native Cichla populations (Perciformes, Cichlidae) in Brazilian reservoirs. Journal of Helminthology. 2011; 85:185-91 [ Links ]

Zar, 2010 Zar J.H. Biostatistical analysis. New Jersey: Prentice Hall; 2010. [ Links ]

** Peer Review under the responsibility of Universidad Nacional Autónoma de México.

Received: June 12, 2015; Accepted: March 03, 2016

* Corresponding author. E-mail address: marcos.tavares@embrapa.br (M. Tavares-Dias).

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