From Africa to Brazil: detection of African Oreochromis niloticus parasites in Brazilian fish farms

Abstract Aim To evaluate the introduction of Oreochromis niloticus gill parasites in the Paranapanema River basin, northern Paraná, southern Brazil, as well as to inventory its occurrences in Brazilian fish farms and discuss the risks of transmission to native fauna. Methods The gills of 632 fish specimens from four fish farms in the Paranapanema Basin were analyzed. The parasites were collected, processed and identified according to specific procedure. Literature review was carried out to compile records of occurrence of gill parasites species in other Brazilian river basins. Results A total of seven (7) species of parasites were recorded, five (5) of the genus Cichlidogyrus, one (1) of Scutogyrus (Ancyrocephalidae, Monogenoidea) and one (1) of Lamproglena, Lamproglena monodi (Copepoda, Lernaeidae). All native from Africa. Some of these species have been reported in fish farms located in five other Brazilian watersheds. However, in this study a greater number of African gill parasite species was recorded in fish farms in northern Paraná (seven species), in the Paranapanema Basin, with Cichlidogyrus rognoni reported only for this basin. Conclusions The results confirm the introduction of these African parasites along with their host, O. niloticus, and the establishment of these species in Brazilian waters, since many specimens belonging to the species identified herein presented breeding activity for at least one period of the year. Although, only L. monodi has been recorded parasitizing Brazilian native species, data reported for other countries demonstrates the imminent risk of transmission of these O. niloticus parasites to native cichlids.

potential (Froese & Pauly, 2017;Cassemiro et al., 2018). The introduction of this species is of concern due to its ability to alter the invaded environment (Cassemiro et al., 2018), threatening native fish fauna by preying on fish in early development stages (i.e., eggs and larvae) and competing for space and food (Martin et al., 2010;Sanches et al., 2012). In the Americas, this species has promoted competitive displacement and alterations of reservoir water quality and phytoplankton communities (Figueredo & Giani, 2005;Martin et al., 2010).
As well as representing a direct biological risk for native fish fauna, O. niloticus invasion may also lead to the presence of other organisms, like parasitic species non-natives (Jiménez-García et al., 2001;Azevedo et al., 2012;Bittencourt et al. 2014a;Zago et al., 2014;Šimková et al., 2019). Co-introductions include parasitic species, and are a rarely documented risk, particularly in Brazil (Azevedo et al., 2012;Bittencourt et al., 2014a;Zago et al., 2014), as, most of the time, parasite introductions by hosts are neglected. Diseases caused by ectoparasites are variable, and may cause destruction of scales, abundant secretion of mucus, hyperplasia and necrosis of cells (Eiras, 1994). In some cases, fungi and bacteria invade the lesions, which can cause more serious consequences than those due to the parasitosis itself, in both farmed and wild fish (Eiras, 1994). Non-native parasite species alter natural parasite-host interactions, which may lead to anemia, low coefficient of condition (Yamamoto et al., 1984), and increase mortality among native host species (Prenter et al., 2004;Goedknegt et al., 2016).
In this context, we aimed to evaluate the introduction of O. niloticus gill parasites in earthen

Introduction
Fish translocation has been carried out by human activities for a long time and for various purposes. Translocation is mainly intentional, with aquaculture, improvement of wild populations (fish stocking), fishing, biological control, and aquarium dumping as the main introduction vectors worldwide (Leprieur et al., 2008;Gozlan et al., 2010). Several negative effects caused by the introduction and subsequent invasion of fish species may occur, such as predation, habitat degradation, increased competition for resources, hybridization and disease transmission (Gozlan et al., 2010;Cucherousset & Olden, 2011). Thus, invasive fish can affect a wide variety of native organisms, both directly and indirectly, at levels ranging from the genome to the ecosystem (Cucherousset & Olden, 2011).
The native distribution of Nile tilapia, Oreochromis niloticus (Linnaeus, 1758) (Cichliformes, Cichlidae), is from North and East Africa, throughout the coastal rivers of Israel, the Nile River basin and several African lakes (Trewavas, 1983). It is widely distributed throughout several tropical and subtropical countries, due to aquaculture introduction (Eschmeyer et al., 2017;Froese & Pauly, 2017).
In Brazil, the introduction of O. niloticus first ensued in the 1970s in the Brazilian Northeast, as the National Department of Drought Works (Departamento Nacional de Obras Contra a Seca -DNOCS) sought to populate dams during programs developed to fight hunger (Castagnolli, 1996). Since this event, the species has become intensely farmed in fish farms and 'fish and pay' establishments in several States and is currently farmed in practically the entire country (Borghetti & Teixeira da Silva, 2008;Boscardin, 2008).
Although the introduction of O. niloticus was initiated with the aim of promoting the creation of developing economies, this species has caused serious environmental problems and threats to the native fish fauna in several countries, including the United States, Mexico, Australia, the Philippines, Madagascar, and Brazil, due to its high invasive Conclusões: Os resultados confirmam a introdução destes parasitos africanos juntamente com o hospedeiro O. niloticus e o estabelecimento dessas espécies em águas brasileiras, uma vez que muitos espécimes pertencentes às espécies aqui identificadas apresentaram atividade reprodutiva por pelo menos um período do ano. Embora apenas L. monodi tenha sido registrada parasitando espécies nativas brasileiras, dados relatados para outros países demonstram o risco iminente de transmissão desses parasitos de O. niloticus para ciclídeos nativos.
ponds and net cages in the Paranapanema River basin, southern Brazil, and compare this event with other Brazilian fish farms. In addition, we discuss the risks of transmission to native fish fauna.
A large literature review was carried out in order to compile records of occurrence of parasitic gill species in other Brazilian river basins, during January to May 2018. Only data published in scientific journals were considered. The research was conducted on the Web of Science, Scopus, Scielo and Google Scholar platforms, using the term 'Brazil' and combinations of the following terms:

Results and Discussion
The literature review resulted in the compilation of nine studies on the occurrence of gill parasites in Brazilian river basins ( Table 1). The following monogenoidean species were identified in fish farms in the Paranapanema River basin: Cichlidogyrus rognoni Pariselle, Bilong Bilong & Euzet, 2003, C. sclerosus Paperna & Thurston, 1969, C. thurstonae Ergens, 1981, C. halli (Price & Kirk, 1967, Table 1. Oreochromis niloticus gill parasites species of African origin detected in different Brazilian river basins. C. tilapiae Paperna, 1960, and Scutogyrus longicornis (Paperna & Thurston, 1969), all originating from Africa (Table 1). These six monogenoidean species recorded herein in O. niloticus gills were found in an earthen pond from another fish farm in northern Paraná (Britto & Silva-Souza, 2017). Five Cichlidogyrus species, comprising C. sclerosus and four unidentified species, were recorded infesting O. niloticus gills in specimens raised in ponds in the state of São Paulo, also in the Paranapanema River basin (Lizama et al., 2007). Four Cichlidogyrus species were recorded in net cages, two of which unidentified, in addition to S. longicornis, in the Água Vermelha Reservoir, Grande River basin, located in the state of São Paulo (Zago et al., 2014). Nile tilapia reared in net cages in the Guarapiranga Reservoir, also in the state of São Paulo, were infested by Cichlidogyrus sp.

Species Geographical distribution in Brazil References
In southern Brazil, five species have also been reported in ponds in different fish farms in the state of Santa Catarina, in the Itajaí River basin (Ghiraldelli et al., 2006a, Jerônimo et al., 2011 and in the Uruguay River basin (Martins et al., 2014). On the other hand, only C. tilapiae was recorded in the state of Amapá, northern Brazil, in four fish farms (Pantoja et al., 2012). Thus, the high number of African parasitic gill species recorded in northern Paraná fish farms, in the Paranapanema Basin, is noteworthy, with C. rognoni being found only in this basin to date.
The six species of Monogenoidea recorded displayed breeding activity for at least one period of the year in fish farming activities also carried out in northern Paraná (Britto & Silva-Souza, 2017). In the present study, although they were not quantified, individuals from the same species of egg-containing gill parasites were found in all evaluated fish farms. These results allow us to consider that these African species are established and adjusted to the environments where their hosts are being reared and, therefore, propagule pressure of the recorded parasites has been potentiated.
The lack of data on fish farmed during the last 15 years does not allow for conclusions regarding L. monodi introduction in Brazil (Martins et al., 2010). However, this crustacean was found as a parasite in Amazonian cichlid populations introduced in the Guandu River, in the state of Rio de Janeiro, namely Astronotus ocellatus (Agassiz, 1831) and Cichla ocellaris Bloch & Schneider, 1801   (Table 1). According to Tavares-Dias et al. (2015), L. monodi is distributed throughout the Paraná, Uruguay and Atlantic Ocean River systems.
A lower number of gill parasites species was recorded infesting O. niloticus in fish farms located in the states of Minas Gerais, Rio de Janeiro, São Paulo, Santa Catarina and Amapá (Table 1). Oreochromis niloticus was introduced in 1994 in some fish farms in the municipality of Macapá, in the state of Amapá, eastern Amazon region, in northern Brazil (Tavares-Dias, 2011 Paperna, 1983, Paratrichodina africana Kazubski & El-Tantawy, 1986, Trichodina nobilis Chen, 1963 (Jiménez-García et al., 2001). This monogenoidean species was detected in four Brazilian watersheds.
In Brazil, O. niloticus is the most farmed species and corresponds to 45.4% of the total fish production in the country, with the state of Paraná (southern region) as the largest producer, totaling 28.8% (Brasil, 2017). The species is farmed both in earthen ponds and in net cages located in reservoirs. Even if the species is only reared in earthen ponds, these constructions are usually built close to riverine areas subject to flooding, and fish escapes may occur during rainy periods (Casimiro et al., 2018).
In the summer of 2015/16, about 1.14 million fish belonging to 21 species and three hybrids escaped from fish farms to the Paranapanema River basin. Of this total, 96% comprised O. niloticus and C. rendalli specimens (Casimiro et al., 2018). It is important to note that O. niloticus specimens had already been recorded in the Capivara Reservoir (Paranapanema River) (Orsi & Britton, 2014). The presence of O. niloticus in the Grande and Uruguay river reservoirs and in the Amazonas River were reported, respectively, by Azevedo-Santos et al. (2011), Schork et al. (2013) and Bittencourt et al. (2014a). On the other hand, no records of O. niloticus in natural Itajaí River basin environments are available.
In this context, and according to the findings for fish farms in northern Paraná, in the Paranapanema River basin, as well as other Brazilian watersheds, an imminent risk of transmission of O. niloticus parasites to cichlids, such as Australoheros Rican & Kullander, 2006, Aequidens Eigenmann & Bray, 1894, Cichlasoma Swainson, 1839, Crenicichla Heckel, 1840, Geophagus Heckel, 1840, and Gymnogeophagus Miranda Ribeiro, 1918, is noted (Langeani et al., 2007). The consequences of the association of these Africa parasites to native fish are still unclear, but there may be a risk of increased mortality as recorded for cichlids in Florida (Noga & Flowers, 1995). Ectoparasites may cause injuries of scales, secretion of mucus and necrosis of cells, which allow the entry of fungi and bacteria (Eiras, 1994). The pathogens caused by these parasites alter parasite-host interactions and reduce the native host population (Prenter et al., 2004;Goedknegt et al., 2016). Therefore, fish translocation by human intervention provides a window of opportunity for new interactions that threaten biodiversity.
It is important to note that the results presented and reported herein may not represent the actual distribution of parasitic species in Brazil, as these findings represent only the places where published studies took place. Due to the large size of the Brazilian territory, we detected the lack of information on the distribution of these parasites in several regions of the country, such as the northeast region where the first case of introduction of O. niloticus occurred. However, such records confirm that O. niloticus has introduced non-native parasites.
Thus, we suggest that, safety ponds should be installed in fish farms, to allow the water treatment prior to release in nearby springs. Fish farm inspection should be increased, and if escape events are proven, the National Environmental Policy that establishes the 'polluter pays' principle should be applied to the fish farmer. Non-native species are considered a form of environmental pollution and may be a serious impact on aquatic ecosystems (França et al., 2017;Casimiro et al., 2018). Therefore, the correct identification and survey of the distribution of non-native parasites are essential to maintain the integrity of Brazilian aquatic ecosystems. In addition, lay people, fish farmers and fishermen should be made aware of how to combat non-native species.