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Multiparasitism in gills of Metynnis lippincottianus from the environmental protection area of Curiau river, Eastern Amazon/Multiparasitismo em branquias de Metynnis lippincottianus da area de protecao ambiental do rio Curiau, Amazonia Oriental.


The high ichthyological diversity of Amazon has been a subject of study for researchers (TAVARES et al., 2018; DE ANDRADE et al., 2018; ZATTI et al., 2018; BITTENCOURT et al., 2014), but still many issues are need to be studied and understood. (MOREIRA et al., 2010). This geographic area also encompasses ecosystems that are vital for maintaining the surrounding environment, such as floodplain forests (BATISTA et al., 2015). In the state of Amapa, floodplain forests are the second largest ecosystem in the state, occupy 4.8% of the territory while the rainforest occupies approximately 70% of the state of the Amapa. Since this area is a suitable habitat for many native species (QUEIROZ et al, 2013; PINTO, 2016), 20.83% of these floodplain forest (4,632.71 hectares) are designated as the Environmental Protection Area (APA) of the Curiau River (LIMA et al., 2013).

The APA of the Curiau River is composed of permanent and temporary lakes within the floodplain forests, favoring a rich diversity of fish species, such as Serrasalmus rhombeus (piranha), Hoplosternum littorale (tamoata), Cichla temensis (tucunare), Hoplias malabaricus (traira), and Piaractus mesopotamicus (pacu). Among these, a species of ornamental importance, Metynnis lippincottianus (Serrasalmidae) known popularly as Pratinha is widely distributed in the Brazilian basins and some French Guiana rivers. It has a diet based on vegetables, seeds, phytoplankton, mollusks and some arthropods and detritus (MOREIRA et al., 2009; HOSHINO et al., 2014).

In the Amazon, several factors influence the parasitic load of fish, such as seasonality, abiotic and biotic factors in aquatic environment water, and host ecology (NEVES et al., 2013). The diversity and ecological function of the parasites in an ecosystem can be used as tools for a better understanding of the biosphere, as well as the parasitic indexes that support parasite-host relationship analysis (TAVARES-DIAS et al. 2014 CARDOSO et al., 2018). TAKEMOTO et al. (2004) stated that all fish hosted at least one species of parasite and the location of the parasites may vary, where no organ is free from parasitism, but one organ may have more parasites than another organ.

Multiple studies have reported that gills are one of the most parasitized organs (CARDOSO et al., 2018; JERONIMO et al., 2014, GONCALVES et al., 2014, VENTURA et al., 2013, SANTOS et al. 2013; OLIVEIRA et al., 2016). Gills are easily damaged by parasitic infections, being the first organ in contact with the external environment. Additionally, gills perform several functions, such as respiration, osmoregulation, and excretion. Gills are an indicator of the rate of parasitism, based on histopathological changes, such as respiratory disorders and electrolyte imbalance (FLORESLOPES et al., 2011; NASCIMENTO et al., 2012). Fish parasites may reflect the environmental quality, as well as habits of their host, considering the importance of understanding and contributing to the expansion of studies on fish parasites (FALKENBERG et al., 2019). Therefore, the present study aimed to investigate the gills of Metynnis lippincottianus from the Curiau River basin in Macapa (eastern Amazon).


Study area

The Curiau river basin measures approximately 584.47 [km.sup.2], almost 40% of the Curiau River's Environmental Protection Area (APA) (LIMA et al., 2013). The Curiau River's mouth in the Amazon River presents meandric characteristics, which may be due to the greater turbulence in the river, caused by the speed of the water current and the Amazonian river tidal regime (VASCONCELOS et al., 2011).

Specimens of M. lippincottianus (COPE, 1870), common fish species of the Curiau River (Point 1: 51[degrees]2'57,205" W 0[degrees]8'29" N; Point 2:51[degrees]2'30",743 W 0[degrees]8'43,087" N), were collected during a 12-month period, from August 2017 to August 2018. Collections were carried out twice per month for parasitological analysis, using a 20 mm net between knots measuring five meters long and two meters high, being placed in points with intense activity of fishing by the local population (Figure 1).

Parasites sampling procedures

All fish were transported alive in vats containing water from the environment and artificial aeration, to the Laboratory of Morphophysiology and Animal Health (LABMORSA) at the State University of Amapa (UEAP). The specimens were desensitized through a medullary incision, using pincers and a scalpel. Then, biometric data such as total length (cm), standard length (cm) and weight (g) were measured.

The entire external surface, mouth, nostrils, fins, and gills were analyzed using stereoscopic binocular microscopes, to verify the existence of parasites, cysts, or lesions. During the necropsy, small gills fragments were separated between slides and coverslips, wherein foci of parasite development were identified via light microscope analysis.

Prevalence was used to analyze the infection level of the parasites following the recommendations of BUSH et al. (1997). A relative condition factor for the host was determined using body weight (g) and total length (cm) data following LECREN (1951) where the expected and observed weight are used to calculate, which has a value equal to one (Kn=1) under normal conditions.

The project was submitted to the Ethics Committee for Animal Use (CEUA), no 012-CEUA/ CPAFAP and to the System of Authorization and Information on Biodiversity (SISBIO) no 50376-1. A license was also obtained from the Secretary of the Environment of the State of Amapa (SEMA-AP) (letter no 1014 / 2016), due to the status of the research site as an Environmental Protection Area.


The 200 specimens of M. lippincottianus examined from the Curiau River, had a mean total length of 7.77 [+ or -] 0.78 cm; standard mean length of 6.21 [+ or -]0.64 cm; and mean weight of 9.17 [+ or -] 2.82 g. Eighty-nine percent were parasitized by one or more species. Three taxa (Ciliophora, Cnidaria and Platyhelminthes) and 6 groups of parasites: Piscinoodinium pillulare, Trichodina sp., Henneguya sp., Myxobolus sp., monogenoids from the family Dactylogyridae, and unidentified digenetics (metacercariae) (Figure 2). Cnidarian Henneguya sp. presented the highest prevalence (89%) among the parasites reported in gills; metacercariae showed the lowest prevalence (15%).

The dinoflagellata Piscinoodinium pillulare was found in the gills of 44% of the analyzed M. lippincottianus specimens, which was lower than the prevalence reported by FLORINDO et al. (2017) in ornamental fish from Santa Catarina, which was 75% in all fish. This same parasite was reported in Cichlasoma amazonarum and in Hemibrycon surinamensis of the Igarape of Fortaleza basin, Macapa, with a prevalence of 49% and 17.2%, respectively (CARVALHO et al., 2017; HOSHINO et al. 2014; HOSHINO et al., 2014). Piscinoodinium pillulare is common in cold season of the year and is responsible for outbreaks in aquaculture, which may cause discomfort and asphyxia in hosts, as described by SANT'ANA et al (2012).

Parasitic infection of the gills in the genus Trichodina is the main cause of mortality among fish farms (MACIEL et al., 2018). In this study, the prevalence of Trichodina sp. in the gills was 19%, which was higher than the prevalence (10.4%) reported by NEVES et al. (2013) in Astronotus ocelatus from Pracuuba Lake, Amapa. Trichodina spp. was found in gills of Carnegiella strigata, Carnegiella martae, and Nannostomus eques, with a prevalence of 14.3%, 7.9%, and 9.7%, respectively; all of these fish were collected from the middle Rio Negro (TAVARES-DIAS et al., 2010). Trichodina nobilis parasitized the gills in 64.3% and 84.2%, respectively, of in Pterophyllum scalare and Mesonauta acora individuals (FARIAS PANTOJA et al., 2015).

In the present study, the parasite that presented the highest prevalence of infection was Henneguya sp., which infected 89% of the specimens analyzed. This prevalence was greater than thatported re in Hypophthalmus marginatus of the municipality of Cameta, in the state of Para, in which 80% of the individuals were parasitized by Henneguya sp. (VELASCO et al., 2015), this higher prevalence can be related directly as the feeding habit of the fish species, as well as the behavioral, biological and physiological differences of these fish (ISAAC et al., 2004) because these factors can affect the structure of the parasite community (CARVALHO et al., 2017). Henneguya sp. was also described in Pimelodus maculatus, infecting 13.4% of the gills (MARTINS et al., 2018). Henneguya paraensis was reported in 60% of the gills of Cichla temensis specimens studied (VELASCO et al., 2016). Henneguya aequidens occurred in 33.3% of the gills of Aequidens plagiozonatus individuals (VIDEIRA et al., 2015); whereas in Arapaima gigas, Henneguya arapaima parasitized the gill arches and gall bladder with a prevalence of 11.7% and 82.3%, respectively (FEIJO et al., 2008). This parasite has high specificity for its host fish, and its parasitic action brings not only ultrastructural damages that can result in death, but also cause sterility of the host when housed in the gonads and testicles (MATOS et al., 2001).

Myxobolus spp. parasitized 65% of gills of the fish examined, a value higher than that reported in the heart of Pimelodus ornatus, from the Arari Waterfall, which had a prevalence of 13.9% in the 43 specimens analyzed (MATOS et al., 2014). LACERDA et al (2013) explained that the discrimination of the fish parasitic fauna can be based on premise that the different biogeographic regions showed a range of possibilities for the parasitic fauna structure in the host, thus explaining the differences in parasites prevalence in their hosts. A species of Myxobolus, Myxobolus maculatus, was found to parasitize 40% of the kidneys of Metynnis maculatus, a fish of the same genus as those researched in this study, collected in the Amazon River estuary (CASAL et al., 2002). Myxobolus insignis infected the gills of 66.6% of Semaprochilodus insignis (EIRAS et al., 2005) and Myxobolus sp. of 5.5% of Colossoma macropomum (MACIEL et al., 2011), both fish species being from the Amazon basin. Myxobolus marajoensis, was found to parasitize the intestinal musculature of 20% of fish from Paracauri River, in the Island of Marajo-PA, Rhamdia quelen (ABRUNHOSA et al., 2017).

Monogenoids of the family Dactylogyridae presented the second highest prevalence, at 81.5% of the specimens examined. HOSHINO & TAVARESDIAS (2014) described the presence of a species of the family Dactylogyridae in M. lippincottianus of the Igarape Fortaleza basin / AP. The species reported was Anacanthorus jegui, with a prevalence of 95% in the 80 specimens analyzed. In another study, conducted by REVERTER et al. (2016) in gills of butterflies fishes of the Tropical Islands of the Western Pacific, parasitism by monogenea communities of the Dactylogyridae family to occurred with prevalences between 40% and 100% in the analyzed species; members of the family Dactylogyridae are thus present in both freshwater and marine environments. According to MENDOZA-FRANCO et al. (2018), the occurrence of monogenea in ornamental freshwater fish is due to the introduction of exotic fish that harbor these parasites and the pollution of the natural environment.

The presence of digenetic metacercariae larvae in the gills of M. lippincottianus was observed with the lowest prevalence among the parasites reported--only 15% of the individuals examined were infected. It was not possible to identify the individual species of metacercariae. In studies conducted in Lago Guaiba / RS, 13 species belonging to the phylum Platyhelminthes were parasitizing the intestines, gills, and stomach of Megaleporinus obtusidens, with prevalence between 1.66% and 86.66% in the 60 specimens analyzed (WENDT et al., 2018). There were metacercariae of Posthodiplostomum sp. parasitizing the gills of Auchenipterus nuchalis (TAVARES-DIAS, 2017) and metacercariae in the gills of 77.5% of M. lippincottianus (HOSHINO et al., 2014); both fish species distributed the Igarape of Fortaleza basin. MORAIS et al., (2011) reported metacercariae of Clinostomun marginatum and Austrodiplostomum compactum, parasitizing 100% and 15%, respectively, present in Pygocentrus nattereri of central Amazon.

The relative factor of the host (Kn=1.000 [+ or -] 0.08) was not affected by the parasitism, since it remained very close to the standard value, that is Kn=1.0, according LECREN (1951), thus indicating that the specimens' condition was not impacted, despite the high parasitic load. This relative condition factor indicated the well-being of the fish, thus measuring the state of animal health (VAZZOLER, 1996, LIZAMA et al., 2006). FALKENBERG et al. (2019) said that under natural conditions, fish can be infected by many species, which coexist and show interrelations, demonstrating that each host has its own community of parasites and that hosts acquire resistance, as well as adapt with the presence of parasites and thus not have a negative influence on the condition factor.


The parasitic fauna of the gills of M. lippincottianus comprised micro and macroparasites, was diverse in its composition, and was dominated by the phylum Cnidaria: Myxozoa. Henneguya sp. was the most prevalent parasite, while metacercariae were the least prevalent. The presence of protozoa, Trichodina sp. and Piscinoodinium pillulare, occurred in almost 50% of the specimens, and these are primarily responsible for production losses in aquaculture. The presence of two species of the genus Myxobolus was observed, which were differentiated based on spores of different shapes, since species identification for myxozoa requires molecular and ultrastructural analysis. This is first observed occurrence of species belonging to the phylum Cnidaria: Myxozoa in M. lippincottianus.


The authors declare no conflict of interest. The founding sponsors had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.


This research was approved by the Animal Use Ethics Committee (CEUA) of EMBRAPA-AP, number 012CEUA/CPAFAP and registered in the System of Authorization and Information of Biodiversity (SISBIO), no 50376-1, as well as authorized by the Secretary of Environment of the State of Amapa (SEMA), for the reason of the study being conducted in Environmental Protection Area, under the official number 1014/2016.


All authors contributed equally for the conception and writing of the manuscript. All authors critically revised the manuscript and approved of the final version.


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Abthyllane Amaral de Carvalho (1) Roger Leomar da Silva Ferreira (1) Priscila Gomes de Araujo (1) Marcio Charles da Silva Negrao (2) Marcela Nunes Videira (3) * (iD)

(1) Laboratorio de Morfofisiologia e Sanidade Animal, Programa de Pos-graduacao em Ciencias Ambientais, Universidade Federal do Amapa (UNIFAP), Macapa, AP, Brasil.

(2) Laboratorio de Morfofisiologia de Sanidade Animal, Programa de Pos-graduacao em Biodiversidade Tropical, Universidade Federal do Amapa (UNIFAP), Macapa, AP, Brasil.

(3) Laboratorio de Morfofisiologia de Sanidade Animal, Programa de Pos-graduacao em Ciencias Ambientais, Universidade do Estado do Amapa (UEAP), Campus I, 68900-070, Macapa, AP, Brasil. E-mail: Corresponding author.

Received 01.13.18 Approved 04.09.19 Returned by the author 05.07.19 CR-2019-0028.R2

Caption: Figure 1--Collection sites of Metynnis lippincottianus in the Curiau River, eastern Amazonia (Brazil). Author: Cardoso-Junior, F. S.

Caption: Figure 2--Prevalence of the parasites present in the gills of Metynnis lippincottianus from Curiau River, Eastern Amazon.
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Title Annotation:PARASITOLOGY
Author:de Carvalho, Abthyllane Amaral; Ferreira, Roger Leomar da Silva; de Araujo, Priscila Gomes; Negrao,
Publication:Ciencia Rural
Date:Jun 1, 2019
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