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

Da África para o Brasil: detecção de parasitos africanos de Oreochromis niloticus em pisciculturas brasileiras

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.

Keywords:
freshwater; non-native species; invasion; Neotropical; Nile tilapia

Resumo

Objetivo

Avaliar a introdução de parasitos branquiais de Oreochromis niloticus na bacia do rio Paranapanema, norte do Paraná, sul do Brasil, assim como inventariar suas ocorrências em pisciculturas brasileiras e discutir os riscos de transmissão para a fauna nativa.

Métodos

As brânquias de 632 espécimes de peixes de quatro estações de piscicultura na bacia do rio Paranapanema foram analisadas. Os parasitos foram coletados, processados e identificados de acordo com procedimento específico. A revisão da literatura foi realizada para compilar registros de ocorrência de espécies parasitas branquiais em outras bacias hidrográficas brasileiras.

Resultados

Um total de sete (7) espécies de parasitos foi registrado, sendo cinco (5) do gênero Cichlidogyrus, uma (1) de Scutogyrus (Ancyrocephalidae, Monogenoidea) e uma (1) de Lamproglena, Lamproglena monodi (Copepoda, Lernaeidae), todas nativas da África. Algumas dessas espécies foram registradas em pisciculturas localizadas em outras cinco bacias hidrográficas brasileiras. No entanto, neste estudo, um número maior de espécies parasitas africanas foi registrado em pisciculturas no norte do Paraná (sete espécies), na bacia do rio Paranapanema, sendo Cichlidogyrus rognoni relatada apenas para essa bacia.

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.

Palavras-chave:
água doce; espécies não nativas; invasão; Neotropical; tilápia do Nilo

1. 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., 2008LEPRIEUR, F., BEAUCHARD, O., BLANCHET, S., OBERDORFF, T. and BROSSE, S. Fish invasions in the world’s river systems: when natural processes are blurred by human activities. PLoS Biology, 2008, 6(2), e28. http://dx.doi.org/10.1371/journal.pbio.0060322. PMid:18254661.
http://dx.doi.org/10.1371/journal.pbio.0...
; Gozlan et al., 2010GOZLAN, R.E., BRITTON, J.R., COWX, I. and COPP, G.J. Current knowledge on non-native freshwater fish introductions. Journal of Fish Biology, 2010, 76(4), 751-786. http://dx.doi.org/10.1111/j.1095-8649.2010.02566.x.
http://dx.doi.org/10.1111/j.1095-8649.20...
). 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., 2010GOZLAN, R.E., BRITTON, J.R., COWX, I. and COPP, G.J. Current knowledge on non-native freshwater fish introductions. Journal of Fish Biology, 2010, 76(4), 751-786. http://dx.doi.org/10.1111/j.1095-8649.2010.02566.x.
http://dx.doi.org/10.1111/j.1095-8649.20...
; Cucherousset & Olden, 2011CUCHEROUSSET, J. and OLDEN, J.D. Ecological impacts of nonnative freshwater fishes. Fisheries (Bethesda, Md.), 2011, 36(5), 215-230. http://dx.doi.org/10.1080/03632415.2011.574578.
http://dx.doi.org/10.1080/03632415.2011....
). 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, 2011CUCHEROUSSET, J. and OLDEN, J.D. Ecological impacts of nonnative freshwater fishes. Fisheries (Bethesda, Md.), 2011, 36(5), 215-230. http://dx.doi.org/10.1080/03632415.2011.574578.
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).

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, 1983TREWAVAS, E. Tilapiine fishes of the genera Sarotherodon, Oreochromis and Danakilia. London: British Museum, 1983. Natural History, no. 878. https://doi.org/10.5962/bhl.title.123198.
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). It is widely distributed throughout several tropical and subtropical countries, due to aquaculture introduction (Eschmeyer et al., 2017ESCHMEYER, W.N., FRICKE, R. and VAN DER LAAN, R. Catalog of fishes: genera, species, references. 2017 [viewed 30 November 2017]. Available from: http://www.calacademy.org/scientists/projects/catalog-of-fishes/
http://www.calacademy.org/scientists/pro...
; Froese & Pauly, 2017FROESE, R. and PAULY, D. FishBase. 2017 [viewed 30 November 2017]. Available from: http://www.fishbase.org
http://www.fishbase.org...
).

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, 1996CASTAGNOLLI, N. Aquicultura para o ano 2000. Brasília: CNPq, 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, 2008BORGHETTI, J.R. and TEIXEIRA DA SILVA, U.A. Principais sistemas produtivos empregados comercialmente. In: OSTRENSKY, A., BORGHETTI, J.R. and SOTO, D., eds. Aquicultura no Brasil: o desafio é crescer. Brasília: FAO, 2008, pp. 73-94.; Boscardin, 2008BOSCARDIN, N.D. A produção aquícola brasileira. In: OSTRENSKY, A., BORGHETTI, J.R. and SOTO, D., eds. Aquicultura no Brasil: o desafio é crescer. Brasília: FAO, 2008, pp. 27-72.).

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 potential (Froese & Pauly, 2017FROESE, R. and PAULY, D. FishBase. 2017 [viewed 30 November 2017]. Available from: http://www.fishbase.org
http://www.fishbase.org...
; Cassemiro et al., 2018CASSEMIRO, F.A.S., BAILLY, D., DA GRAÇA, W.J. and AGOSTINHO, A.A. The invasive potential of tilapias (Osteichthyes, Cichlidae) in the Americas. Hydrobiologia, 2018, 817(1), 133-154. http://dx.doi.org/10.1007/s10750-017-3471-1.
http://dx.doi.org/10.1007/s10750-017-347...
). The introduction of this species is of concern due to its ability to alter the invaded environment (Cassemiro et al., 2018CASSEMIRO, F.A.S., BAILLY, D., DA GRAÇA, W.J. and AGOSTINHO, A.A. The invasive potential of tilapias (Osteichthyes, Cichlidae) in the Americas. Hydrobiologia, 2018, 817(1), 133-154. http://dx.doi.org/10.1007/s10750-017-3471-1.
http://dx.doi.org/10.1007/s10750-017-347...
), 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., 2010MARTIN, C.W., VALENTINE, M.M. and VALENTINE, J.F. Competitive interactions between invasive Nile tilapia and native fish: the potential for altered trophic exchange and modification of food webs. PLoS One, 2010, 5(12), e14395. http://dx.doi.org/10.1371/journal.pone.0014395. PMid:21200433.
http://dx.doi.org/10.1371/journal.pone.0...
; Sanches et al., 2012SANCHES, F.H.C., MIYAI, C.A., COSTA, T.M., CHRISTOFOLETTI, R.A., VOLPATO, G.L. and BARRETO, R.E. Aggressiveness overcomes body-size effects in fights staged between invasive and native fish species with overlapping niches. PLoS One, 2012, 7(1), e29746. http://dx.doi.org/10.1371/journal.pone.0029746. PMid:22272244.
http://dx.doi.org/10.1371/journal.pone.0...
). In the Americas, this species has promoted competitive displacement and alterations of reservoir water quality and phytoplankton communities (Figueredo & Giani, 2005FIGUEREDO, C.C. and GIANI, A. Ecological interactions between Nile tilapia (Oreochromis niloticus, L.) and the phytoplanktonic community of the Furnas Reservoir (Brazil). Freshwater Biology, 2005, 50(8), 1391-1403. http://dx.doi.org/10.1111/j.1365-2427.2005.01407.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
; Martin et al., 2010MARTIN, C.W., VALENTINE, M.M. and VALENTINE, J.F. Competitive interactions between invasive Nile tilapia and native fish: the potential for altered trophic exchange and modification of food webs. PLoS One, 2010, 5(12), e14395. http://dx.doi.org/10.1371/journal.pone.0014395. PMid:21200433.
http://dx.doi.org/10.1371/journal.pone.0...
).

In Lakes Victoria and Kyoga, after its invasion, O. niloticus has predominated and drastically reduced the native Oreochromis esculentus (Graham, 1928) and Oreochromis variabilis (Boulenger, 1906) populations (Ogutu-Ohwayo, 1990OGUTU-OHWAYO, R. The decline of the native fishes of lakes Victoria and Kyoga (East Africa) and the impact of introduced species, especially the Nile perch, Lates niloticus, and Nile tilapia, Oreochromis niloticus. Environmental Biology of Fishes, 1990, 27(2), 81-96. http://dx.doi.org/10.1007/BF00001938.
http://dx.doi.org/10.1007/BF00001938...
; Maithya et al., 2012MAITHYA, J., NJIRU, M., OKEYO-OWUOR, J.B. and GICHUKI, J. Some aspects of the biology and life-history strategies of Oreochromis variabilis (Boulenger 1906) in the Lake Victoria Basin. Lakes & Reservoirs, 2012, 17(1), 65-72. http://dx.doi.org/10.1111/j.1440-1770.2012.00496.x.
http://dx.doi.org/10.1111/j.1440-1770.20...
). The invasion of African tilapia (Oreochromis spp.) in Nicaragua lakes has also led to decreased native cichlid biomass and richness (McCrary et al., 2007MCCRARY, J.K., MURPHY, B.R., STAUFFER JUNIOR, J.R. and HENDRIX, S.S. Tilapia (Teleostei: Cichlidae) status in Nicaraguan natural waters. Environmental Biology of Fishes, 2007, 78(2), 107-114. http://dx.doi.org/10.1007/s10641-006-9080-x.
http://dx.doi.org/10.1007/s10641-006-908...
).

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., 2001JIMÉNEZ-GARCÍA, M.I., VIDAL-MARTÍNEZ, V.M. and LÓPEZ-JIMÉNEZ, S. Monogeneans in introduced and native cichlids in México: evidence for transfer. The Journal of Parasitology, 2001, 87(4), 907-909. http://dx.doi.org/10.2307/3285151. PMid:11534657.
http://dx.doi.org/10.2307/3285151...
; Azevedo et al., 2012AZEVEDO, R.K., ABDALLAH, V.D., SILVA, R.J., AZEVEDO, T.M., MARTINS, M.L. and LUQUE, J.L. Expanded description of Lamproglena monodi (Copepoda: Lernaeidae), parasitizing native and introduced fishes in Brazil. Revista Brasileira de Parasitologia Veterinária, 2012, 21(3), 263-269. http://dx.doi.org/10.1590/S1984-29612012000300015. PMid:23070437.
http://dx.doi.org/10.1590/S1984-29612012...
; Bittencourt et al. 2014aBITTENCOURT, L.S., PINHEIRO, D.A., CÁRDENAS, M.Q., FERNANDES, B.M. and TAVARES-DIAS, M. Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Revista Brasileira de Parasitologia Veterinária, 2014a, 23(1), 44-54. http://dx.doi.org/10.1590/S1984-29612014006. PMid:24728360.
http://dx.doi.org/10.1590/S1984-29612014...
; Zago et al., 2014ZAGO, A.C., FRANCESCHINI, L., GARCIA, F., SCHALCH, S.H.C., GOZI, K.S. and SILVA, R.J. Ectoparasites of Nile tilapia (Oreochromis niloticus) in cage farming in a hydroelectric reservoir in Brazil. Revista Brasileira de Parasitologia Veterinária, 2014, 23(2), 171-178. http://dx.doi.org/10.1590/S1984-29612014041. PMid:25054495.
http://dx.doi.org/10.1590/S1984-29612014...
; Šimková et al., 2019ŠIMKOVÁ, A., ŘEHULKOVÁ, E., RASOLOARINIAINA, J.R., JORISSEN, M.W.P., SCHOLZ, T., FALTÝNKOVÁ, A., MAŠOVÁ, Š. and VANHOVE, M.P.M. Transmission of parasites from introduced tilapias: a new threat to endemic Malagasy ichthyofaunal. Biological Invasions, 2019, 21(3), 803-819. http://dx.doi.org/10.1007/s10530-018-1859-0.
http://dx.doi.org/10.1007/s10530-018-185...
). Co-introductions include parasitic species, and are a rarely documented risk, particularly in Brazil (Azevedo et al., 2012AZEVEDO, R.K., ABDALLAH, V.D., SILVA, R.J., AZEVEDO, T.M., MARTINS, M.L. and LUQUE, J.L. Expanded description of Lamproglena monodi (Copepoda: Lernaeidae), parasitizing native and introduced fishes in Brazil. Revista Brasileira de Parasitologia Veterinária, 2012, 21(3), 263-269. http://dx.doi.org/10.1590/S1984-29612012000300015. PMid:23070437.
http://dx.doi.org/10.1590/S1984-29612012...
; Bittencourt et al., 2014aBITTENCOURT, L.S., PINHEIRO, D.A., CÁRDENAS, M.Q., FERNANDES, B.M. and TAVARES-DIAS, M. Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Revista Brasileira de Parasitologia Veterinária, 2014a, 23(1), 44-54. http://dx.doi.org/10.1590/S1984-29612014006. PMid:24728360.
http://dx.doi.org/10.1590/S1984-29612014...
; Zago et al., 2014ZAGO, A.C., FRANCESCHINI, L., GARCIA, F., SCHALCH, S.H.C., GOZI, K.S. and SILVA, R.J. Ectoparasites of Nile tilapia (Oreochromis niloticus) in cage farming in a hydroelectric reservoir in Brazil. Revista Brasileira de Parasitologia Veterinária, 2014, 23(2), 171-178. http://dx.doi.org/10.1590/S1984-29612014041. PMid:25054495.
http://dx.doi.org/10.1590/S1984-29612014...
), 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, 1994EIRAS, J.C. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida, 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, 1994EIRAS, J.C. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida, 1994.). Non-native parasite species alter natural parasite-host interactions, which may lead to anemia, low coefficient of condition (Yamamoto et al., 1984YAMAMOTO, K., TAKAGI, S. and MATSUOKA, S. Mass mortality of the Japanese anchovy (Engraulis japonica) caused by a gill monogenean Pseudanthocotyloides sp. (Mazocraeidae) in the Sea of Iyo (“Iyo-nada”), Ehime Prefecture. Fish Pathology, 1984, 19(2), 119-123. http://dx.doi.org/10.3147/jsfp.19.119.
http://dx.doi.org/10.3147/jsfp.19.119...
), and increase mortality among native host species (Prenter et al., 2004PRENTER, J., MACNEIL, C., DICK, J.T.A. and DUNN, A.M. Roles of parasites in animal invasions. Trends in Ecology & Evolution, 2004, 19(7), 385-390. http://dx.doi.org/10.1016/j.tree.2004.05.002. PMid:16701290.
http://dx.doi.org/10.1016/j.tree.2004.05...
; Goedknegt et al., 2016GOEDKNEGT, M.A., FEIS, M.E., WEGNER, K.M., LUTTIKHUIZEN, P.C., BUSCHBAUM, C., CAMPHUYSEN, K.C., VAN DER MEER, J. and THIELTGES, D.W. Parasites and marine invasions: ecological and evolutionary perspectives. Journal of Sea Research, 2016, 113(1), 11-27. http://dx.doi.org/10.1016/j.seares.2015.12.003.
http://dx.doi.org/10.1016/j.seares.2015....
).

In this context, we aimed to evaluate the introduction of O. niloticus gill parasites in earthen 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.

2. Material and Methods

A total of 632 of juveniles and adults of O. niloticus specimens sexually reverted (males) donated by four fish farms in the northern Paraná State, Paranapanema Basin, were examined, from two net cages (22°47’22.36”S, 51°17’46.53”W and 22°41’09.10”S, 51°17’49.88”W) and two earthen ponds (23°16’25.82”S, 51°26’23.70”W and 23°16’57.59”S, 51°25’30.81”W). Of the 632 individuals, 156 specimens were obtained from earthen ponds and 476 from net cages. Samplings were carried out seasonally, from April 2010 to February 2011. Each specimen collected were dead and cooled. The gills of each specimen were removed and examined closely under stereomicroscope magnification. The parasites were collected and processed adequately according to Eiras et al. (2000)EIRAS, J.C., TAKEMOTO, R.M. and PAVANELLI, G.C. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá: EDUEM, 2000.. Each monogenoidean was identified according to the descriptions reported by Paperna (1964)PAPERNA, I. Parasitic helminths of inland-water fishes in Israel. Israel Journal of Zoology, 1964, 13(1), 1-26., Paperna & Thurston (1969)PAPERNA, I. and THURSTON, J.P. Monogenetic Trematodes collected from cichlid fish in Uganda; including the description of five new species of Cichlidogyrus. Revue de Zoologie et de Botanique Africaines, 1969, 79(1-2), 15-33., Ergens & Yukhimenko (1987)ERGENS, R. and YUKHIMENKO, S.S. Contribution to the knowledge of Gyrodactylus gurleyi Price, 1937 (Monogenea: Gyrodactylidae). Folia parasitologica, 1987, 34(3), 205-209. PMid:3666611., Douëllou (1993)DOUËLLOU, L. Monogeneans of the genus Cichlidogyrus Paperna, 1960 (Dactylogyridae: Ancyrocephalinae) from cichlid fishes of Lake Kariba (Zimbabwe) with descriptions of five new species. Systematic Parasitology, 1993, 25(3), 159-186. http://dx.doi.org/10.1007/BF00007007.
http://dx.doi.org/10.1007/BF00007007...
, Pariselle & Euzet (1995)PARISELLE, A. and EUZET, L. Scutogyrus gen. n. (Monogenea: Ancyrocephalidae) for Cichlidogyrus longicornis minus Dossou, 1982, C. l. longicornis, and C. l. gravivaginus Paperna and Thurston, 1969, with description of three new species parasitic on african cichlids. Journal of the Helminthological Society of Washington, 1995, 62(2), 157-173., Pariselle et al. (2003)PARISELLE, A., BILONG, C.F.B. and EUZET, L. Four new species of Cichlidogyrus Paperna, 1960 (Monogenea, Ancyrocephalidae) all gill parasites from African mouthbreeder tilapias of the genera Sarotherodon and Oreochromis (Pisces, Cichlidae), with a re-description of C. thurstonae Ergens, 1981. Systematic Parasitology, 2003, 56(3), 201-210. http://dx.doi.org/10.1023/B:SYPA.0000003807.27452.bd. PMid:14707506.
http://dx.doi.org/10.1023/B:SYPA.0000003...
and the determination key proposed by Pariselle & Euzet (2009)PARISELLE, A. and EUZET, L. Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema, 2009, 31(4), 849-898. http://dx.doi.org/10.5252/z2009n4a6.
http://dx.doi.org/10.5252/z2009n4a6...
. Copepods were identified based on the redescriptions of Ibraheem & Izawa (2000)IBRAHEEM, M.H. and IZAWA, K. On the morphology of Lamproglena monodi Capart, a parasitic copepod on the gills of Tilapia in Egypt. Zoology in the Middle East, 2000, 21(1), 103-108. http://dx.doi.org/10.1080/09397140.2000.10637837.
http://dx.doi.org/10.1080/09397140.2000....
and Azevedo et al. (2012)AZEVEDO, R.K., ABDALLAH, V.D., SILVA, R.J., AZEVEDO, T.M., MARTINS, M.L. and LUQUE, J.L. Expanded description of Lamproglena monodi (Copepoda: Lernaeidae), parasitizing native and introduced fishes in Brazil. Revista Brasileira de Parasitologia Veterinária, 2012, 21(3), 263-269. http://dx.doi.org/10.1590/S1984-29612012000300015. PMid:23070437.
http://dx.doi.org/10.1590/S1984-29612012...
.

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: ‘Monogenea’, ‘Monogenoidea’, ‘Ancyrocephalidae’, ‘Dactylogyridae’, ‘Cichlidogyrus’, ‘Scutogyrus’, ‘Lamproglena’, ‘Oreochromis’, ‘Nile tilapia’.

3. 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), C. tilapiae Paperna, 1960, and Scutogyrus longicornis (Paperna & Thurston, 1969PAPERNA, I. and THURSTON, J.P. Monogenetic Trematodes collected from cichlid fish in Uganda; including the description of five new species of Cichlidogyrus. Revue de Zoologie et de Botanique Africaines, 1969, 79(1-2), 15-33.), 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, 2017BRITTO, Y.C.T. and SILVA-SOUZA, Â.T. Temporal variation of monogenoideans component community in the gills of Oreochromis niloticus (Cichlidae) in fish farming in northern Parana state, Brazil. Pan-American Journal of Aquatic Sciences, 2017, 12(4), 333-342.). 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., 2007LIZAMA, M.A.P., TAKEMOTO, R.M., RANZANI-PAIVA, M.J.T., AYROZA, L.M.S. and PAVANELLI, G.C. Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. 1. Oreochromis niloticus (Linnaeus, 1758). Acta Scientiarum. Biological Sciences, 2007, 29(2), 223-231. http://dx.doi.org/10.4025/actascibiolsci.v29i2.594.
http://dx.doi.org/10.4025/actascibiolsci...
). 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., 2014ZAGO, A.C., FRANCESCHINI, L., GARCIA, F., SCHALCH, S.H.C., GOZI, K.S. and SILVA, R.J. Ectoparasites of Nile tilapia (Oreochromis niloticus) in cage farming in a hydroelectric reservoir in Brazil. Revista Brasileira de Parasitologia Veterinária, 2014, 23(2), 171-178. http://dx.doi.org/10.1590/S1984-29612014041. PMid:25054495.
http://dx.doi.org/10.1590/S1984-29612014...
). Nile tilapia reared in net cages in the Guarapiranga Reservoir, also in the state of São Paulo, were infested by Cichlidogyrus sp.

Table 1
Oreochromis niloticus gill parasites species of African origin detected in different Brazilian river basins.

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., 2006aGHIRALDELLI, L., MARTINS, M.L., JERÔNIMO, G.T., YAMASHITA, M.M. and ADAMANTE, W.B. Ectoparasites communities from Oreochromis niloticus cultivated in the state of Santa Catrina, Brazil. Su Ürünleri Dergisi, 2006a, 1(2), 181-190., Jerônimo et al., 2011JERÔNIMO, G.T., SPECK, G.M., CECHINEL, M.M., GONÇALVES, E.L.T. and MARTINS, M.L. Seasonal variation on the ectoparasitic communities of Nile tilapia cultured in three regions in southern Brazil. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2011, 71(2), 365-373. http://dx.doi.org/10.1590/S1519-69842011000300005. PMid:21755153.
http://dx.doi.org/10.1590/S1519-69842011...
) and in the Uruguay River basin (Martins et al., 2014MARTINS, M.L., SÁ, A.R.S., JERÔNIMO, G.T., TANCREDO, K.R., GONÇALVES, E.L.T., BAMPI, D., SPECK, G.M. and SANDIN, A.M. Microhabitat preference and seasonality of gill monogeneans in Nile Tilapia reared in Southern Brazil. Neotropical Helminthology, 2014, 8(1), 47-58.). On the other hand, only C. tilapiae was recorded in the state of Amapá, northern Brazil, in four fish farms (Pantoja et al., 2012PANTOJA, W.M.F., NEVES, L.R., DIAS, M.K.R., MARINHO, R.G.B., MONTAGNER, D. and TAVARES-DIAS, M. Protozoan and metazoan parasites of Nile tilapia Oreochromis niloticus cultured in Brazil. Revista Mvz Cordoba, 2012, 17(1), 2812-2819. http://dx.doi.org/10.21897/rmvz.248.
http://dx.doi.org/10.21897/rmvz.248...
). 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.

In Africa, Ancyrocephalidae (Monogenoidea) is the family with most representatives of gill parasites infesting Oreochromis Günther, 1889, Coptodon Gervais, 1853 (=Tilapia Smith, 1840), and Sarotherodon Rüppell, 1852. Oreochromis niloticus gill parasites are distributed in two genera: Cichlidogyrus Paperna, 1960 and Scutogyrus Pariselle & Euzet, 1995 (Pariselle, 1995; Pariselle & Euzet, 2009PARISELLE, A. and EUZET, L. Systematic revision of dactylogyridean parasites (Monogenea) from cichlid fishes in Africa, the Levant and Madagascar. Zoosystema, 2009, 31(4), 849-898. http://dx.doi.org/10.5252/z2009n4a6.
http://dx.doi.org/10.5252/z2009n4a6...
). Cichlidogyrus sclerosus, present in three Brazilian hydrographic basins (Table 1), was introduced in Colombia (Kritsky & Thatcher, 1974KRITSKY, D.C. and THATCHER, V.E. Monogenetic trematodes (Monopisthocotylea: Dactylogyridae) from freshwater fishes of Colombia, South America. Journal of Helminthology, 1974, 48(1), 59-66. http://dx.doi.org/10.1017/S0022149X00022604. PMid:4825435.
http://dx.doi.org/10.1017/S0022149X00022...
) and in Mexico (Kritsky et al., 1994KRITSKY, D.C., VIDAL-MARTINEZ, V.M. and RODRIGUEZ-CANUL, R. Neotropical Monogenoidea. 19. Dactylogyridae of Cichlids (Perciformes) from the Yucatan Peninsula, with Descriptions of Three New Species of Sciadicleithrum Kritsky, Thatcher, and Boeger, 1989. Journal of the Helminthological Society of Washington, 1994, 61(1), 26-33.). On the other hand, C. tilapiae, also reported in three Brazilian basins, including the Amazon Basin, was registered in Cuba by Prieto et al. (1985)PRIETO, A., FAJER, E. and VINJOY, M. Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinidae) in Tilapia hornorum x Tilapia mossambica (perca dorada) en cultivo intensivo. Revista de Salud Animal, 1985, 7, 291-295.. These records demonstrate that this group of African parasites presents a wide distribution in the Neotropical region, where they presented tolerance and adjustment to the new environment.

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, 2017BRITTO, Y.C.T. and SILVA-SOUZA, Â.T. Temporal variation of monogenoideans component community in the gills of Oreochromis niloticus (Cichlidae) in fish farming in northern Parana state, Brazil. Pan-American Journal of Aquatic Sciences, 2017, 12(4), 333-342.). 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.

Lamproglena monodi Capart, 1944 (Copepoda Lernaeidae), also from Africa, was registered in one of the fish farms containing earthen ponds (Table 1). Lamproglena von Nordmann, 1832 comprises 41 freshwater fish parasite species (Piasecki, 2008PIASECKI, W. Comparative morphology of the three species of Lamproglena (Copepoda, Cyclopoida, Lernaeidae) described by von Nordmann, based on re-examination of the types. Zoosystematics and Evolution, 2008, 69(2), 307-315.) distributed throughout Africa (Douëllou & Erlwanger, 1994DOUËLLOU, L. and ERLWANGER, K.H. Crustacean parasites of fishes in Lake Kariba, Zimbabwe, preliminary results. Hydrobiologia, 1994, 287(3), 233-242. http://dx.doi.org/10.1007/BF00006372.
http://dx.doi.org/10.1007/BF00006372...
; Ibraheem & Izawa, 2000IBRAHEEM, M.H. and IZAWA, K. On the morphology of Lamproglena monodi Capart, a parasitic copepod on the gills of Tilapia in Egypt. Zoology in the Middle East, 2000, 21(1), 103-108. http://dx.doi.org/10.1080/09397140.2000.10637837.
http://dx.doi.org/10.1080/09397140.2000....
; Hassan et al., 2013HASSAN, E.S., MAHMOUD, M.M., METWALLY, A.M. and MOKHTAR, D.M. Lamproglena monodi (Copepoda: lernaeidae), infesting gills of Oreochromis niloticus and Tilapia zillii. Global Journal of Fisheries and Aquaculture Researches, 2013, 6(6), 1-16.; Marzouk et al., 2013MARZOUK, M.S.M., MAHDY, O.A., EL-KHATIB, N.R. and YOUSEF, N.S.I. A contribution in ectoparasitic infection and its control in cultured Oreochromis niloticus in Egypt. American Journal of Research Communication, 2013, 1(12), 326-338.; Sinaré et al., 2016SINARÉ, Y., BOUNGOU, M., OUÉDA, A., GNÉMÉ, A. and KABRÉ, G.B. Diversity and seasonal distribution of parasites of Oreochromis niloticus in semi-arid reservoirs (West Africa, Burkina Faso). African Journal of Agricultural Research, 2016, 11(13), 1164-1170. http://dx.doi.org/10.5897/AJAR2015.10408.
http://dx.doi.org/10.5897/AJAR2015.10408...
), Asia (Kumari et al., 1989KUMARI, P., KHERA, S. and GUPTA, N.K. On six new species of the genus Lamproglena Nordmann (Copepoda: Eudactylinidae), ectoparasitic on freshwater fishes of India. Research Bulletin of the Panjab University Science, 1989, 40(1), 9-23.; Yambot & Lopez, 1997YAMBOT, A.V. and LOPEZ, E.A. Gill parasite, Lamproglena monodi Capart, infecting the Nile tilapia, Oreochromis niloticus L., cultured in the Phillipines. In: Proceedings of the 3rd Symposium on Diseases in Asian Aquaculture. Manila: Asian Fisheries Society, 1997. pp. 175-177.) and Europe (Galli et al., 2001GALLI, P., CROSA, G., BERTOGLIO, S., MARINIELLO, L., ORTIS, M. and AMELIO, S.D. Populations of Lamproglena pulchella von Nordmann, 1832 (Copepoda: Eudactylinidae) in cyprinid fish in rivers with different pollution levels. Journal of Applied Ichthyology, 2001, 17(2), 93-96. http://dx.doi.org/10.1046/j.1439-0426.2001.00282.x.
http://dx.doi.org/10.1046/j.1439-0426.20...
). In Brazil, Lamproglena sp. has been reported since the year 2000 in the states of São Paulo, Rio de Janeiro and Santa Catarina (Alves et al., 2000ALVES, D.R., LUQUE, J.L. and PARAGUASSÚ, A.R. Ectoparasitos de tilápia nilótica Oreochromis niloticus (Osteichthyes: Cichlidae) da Estação de Piscicultura da UFRRJ. Revista de Ciências da Vida, 2000, 22(1), 81-85.; Azevedo et al., 2006AZEVEDO, T.M.P., MARTINS, M.L., BOZZO, F.R. and MORAES, F.R. Haematological and gill responses in parasitized tilapia from valley of Tijucas River, SC, Brazil. Scientia Agrícola, 2006, 63(2), 115-120. http://dx.doi.org/10.1590/S0103-90162006000200002.
http://dx.doi.org/10.1590/S0103-90162006...
; Ghiraldelli et al., 2006aGHIRALDELLI, L., MARTINS, M.L., JERÔNIMO, G.T., YAMASHITA, M.M. and ADAMANTE, W.B. Ectoparasites communities from Oreochromis niloticus cultivated in the state of Santa Catrina, Brazil. Su Ürünleri Dergisi, 2006a, 1(2), 181-190.; Ghiraldelli et al., 2006bGHIRALDELLI, L., MARTINS, M.L., YAMASHITA, M.M. and JERÔNIMO, G.T. Ectoparasites influence on the hematological parameters of Nile tilapia and carp cultured in the State of Santa Catarina, Brazil. Su Ürünleri Dergisi, 2006b, 1(3), 270-276.; Lizama et al., 2007LIZAMA, M.A.P., TAKEMOTO, R.M., RANZANI-PAIVA, M.J.T., AYROZA, L.M.S. and PAVANELLI, G.C. Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. 1. Oreochromis niloticus (Linnaeus, 1758). Acta Scientiarum. Biological Sciences, 2007, 29(2), 223-231. http://dx.doi.org/10.4025/actascibiolsci.v29i2.594.
http://dx.doi.org/10.4025/actascibiolsci...
; Martins et al., 2010MARTINS, M.L., AZEVEDO, T.M., GHIRALDELLI, L. and BERNARDI, N. Can the parasitic fauna on Nile tilapias be affected by different production systems? Anais da Academia Brasileira de Ciências, 2010, 82(2), 493-500. http://dx.doi.org/10.1590/S0001-37652010000200024. PMid:20563429.
http://dx.doi.org/10.1590/S0001-37652010...
). According to Douëllou & Erlwanger (1994)DOUËLLOU, L. and ERLWANGER, K.H. Crustacean parasites of fishes in Lake Kariba, Zimbabwe, preliminary results. Hydrobiologia, 1994, 287(3), 233-242. http://dx.doi.org/10.1007/BF00006372.
http://dx.doi.org/10.1007/BF00006372...
, Lamproglena monodi, a gill parasite of several species of cichlids, has Coptodon rendalli (Boulenger, 1897) as one of its preferred hosts. However, in Brazil, L. monodi has been recorded in freshwater environments as both a parasite of O. niloticus and C. rendalli (Azevedo et al., 2010AZEVEDO, R.K., ABDALLAH, V.D. and LUQUE, J.L. Acanthocephala, Annelida, Arthropoda, Myxozoa, Nematoda and Platyhelminthes parasites of fishes from the Guandu river, Rio de Janeiro, Brazil. Check List, 2010, 6(4), 659-667. http://dx.doi.org/10.15560/6.4.659.
http://dx.doi.org/10.15560/6.4.659...
; Azevedo et al., 2012AZEVEDO, R.K., ABDALLAH, V.D., SILVA, R.J., AZEVEDO, T.M., MARTINS, M.L. and LUQUE, J.L. Expanded description of Lamproglena monodi (Copepoda: Lernaeidae), parasitizing native and introduced fishes in Brazil. Revista Brasileira de Parasitologia Veterinária, 2012, 21(3), 263-269. http://dx.doi.org/10.1590/S1984-29612012000300015. PMid:23070437.
http://dx.doi.org/10.1590/S1984-29612012...
; Tavares-Dias et al., 2015TAVARES-DIAS, M., DIAS-JÚNIOR, M.B., FLORENTINO, A.C., SILVA, L.M. and CUNHA, A.C. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Revista Brasileira de Parasitologia Veterinária, 2015, 24(2), 136-147. http://dx.doi.org/10.1590/S1984-29612015036. PMid:26154954.
http://dx.doi.org/10.1590/S1984-29612015...
). Such records confirm that O. niloticus has brought along partly or all of its native parasites when introduced in Brazil (Britto & Silva-Souza, 2017BRITTO, Y.C.T. and SILVA-SOUZA, Â.T. Temporal variation of monogenoideans component community in the gills of Oreochromis niloticus (Cichlidae) in fish farming in northern Parana state, Brazil. Pan-American Journal of Aquatic Sciences, 2017, 12(4), 333-342.).

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., 2010MARTINS, M.L., AZEVEDO, T.M., GHIRALDELLI, L. and BERNARDI, N. Can the parasitic fauna on Nile tilapias be affected by different production systems? Anais da Academia Brasileira de Ciências, 2010, 82(2), 493-500. http://dx.doi.org/10.1590/S0001-37652010000200024. PMid:20563429.
http://dx.doi.org/10.1590/S0001-37652010...
). 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 (Azevedo et al., 2010AZEVEDO, R.K., ABDALLAH, V.D. and LUQUE, J.L. Acanthocephala, Annelida, Arthropoda, Myxozoa, Nematoda and Platyhelminthes parasites of fishes from the Guandu river, Rio de Janeiro, Brazil. Check List, 2010, 6(4), 659-667. http://dx.doi.org/10.15560/6.4.659.
http://dx.doi.org/10.15560/6.4.659...
) (Table 1). According to Tavares-Dias et al. (2015)TAVARES-DIAS, M., DIAS-JÚNIOR, M.B., FLORENTINO, A.C., SILVA, L.M. and CUNHA, A.C. Distribution pattern of crustacean ectoparasites of freshwater fish from Brazil. Revista Brasileira de Parasitologia Veterinária, 2015, 24(2), 136-147. http://dx.doi.org/10.1590/S1984-29612015036. PMid:26154954.
http://dx.doi.org/10.1590/S1984-29612015...
, 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, 2011TAVARES-DIAS, M. Piscicultura continental no estado do Amapá: diagnóstico e perspectivas. Amapá: Embrapa, 2011. Boletim de Pesquisa e Desenvolvimento.). Between 2000 and 2001, several reports were made of O. niloticus escapes due to pond overflowing by heavy rains (Tavares-Dias, 2011TAVARES-DIAS, M. Piscicultura continental no estado do Amapá: diagnóstico e perspectivas. Amapá: Embrapa, 2011. Boletim de Pesquisa e Desenvolvimento.). Oreochromis niloticus, an invasive species in the Igarapé Fortaleza basin, was infested with Ichthyophthirius multifiliis Fouquet, 1876, Trichodina centrostrigeata Basson, Van As & Paperna, 1983, Paratrichodina africana Kazubski & El-Tantawy, 1986, Trichodina nobilis Chen, 1963, and Cichlidogyrus tilapiae, with no common parasite species to the native Amazonian ecosystem fish fauna. On the other hand, T. nobilis, a trichodinid parasite of O. niloticus, was transmitted to the native basin cichlid, Aequidens tetramerus (Heckel, 1840) (Bittencourt et al., 2014aBITTENCOURT, L.S., PINHEIRO, D.A., CÁRDENAS, M.Q., FERNANDES, B.M. and TAVARES-DIAS, M. Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Revista Brasileira de Parasitologia Veterinária, 2014a, 23(1), 44-54. http://dx.doi.org/10.1590/S1984-29612014006. PMid:24728360.
http://dx.doi.org/10.1590/S1984-29612014...
, bBITTENCOURT, L.S., SILVA, U.R.L., SILVA, L.M.A. and DIAS, M.T. Impact of the invasion from Nile tilapia on natives Cichlidae species in tributary of Amazonas River, Brazil. Biota Amazônia, 2014b, 4(3), 88-94. http://dx.doi.org/10.18561/2179-5746/biotaamazonia.v4n3p88-94.
http://dx.doi.org/10.18561/2179-5746/bio...
). However, nothing is known about Brazilian watershed native fish infestations by African monogenoidean parasites of O. niloticus gill. Nevertheless, in Mexico, after the introduction of O. niloticus, infestation of the native species Vieja fenestrata (Günther, 1860) (= Cichlasoma fenestratum) (Cichlidae) by Scutogyrus longicornis (= Cichlidogyrus longicornis) was observed (Jiménez-García et al., 2001JIMÉNEZ-GARCÍA, M.I., VIDAL-MARTÍNEZ, V.M. and LÓPEZ-JIMÉNEZ, S. Monogeneans in introduced and native cichlids in México: evidence for transfer. The Journal of Parasitology, 2001, 87(4), 907-909. http://dx.doi.org/10.2307/3285151. PMid:11534657.
http://dx.doi.org/10.2307/3285151...
). 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, 2017BRASIL. Produção de tilápia cresce mais de 200% em dez anos no Brasil. Ministério da Agricultura, 2017 [viewed 04 Dec. 2017]. Available from: http://www.brasil.gov.br/economia-e-emprego/2017/04/producao-de-tilapia-cresce-200-em-dez-anos-no-brasil/
http://www.brasil.gov.br/economia-e-empr...
). 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., 2018CASIMIRO, A.C.R., GARCIA, D.A.Z., VIDOTTO-MAGNONI, A.P., BRITTON, J.R., AGOSTINHO, A.A., DE ALMEIDA, F.S. and ORSI, M.L. Escapes of non-native fish from flooded aquaculture facilities: the case of Paranapanema River, southern Brazil. Zoologia, 2018, 35, e14638. http://dx.doi.org/10.3897/zoologia.35.e14638.
http://dx.doi.org/10.3897/zoologia.35.e1...
).

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., 2018CASIMIRO, A.C.R., GARCIA, D.A.Z., VIDOTTO-MAGNONI, A.P., BRITTON, J.R., AGOSTINHO, A.A., DE ALMEIDA, F.S. and ORSI, M.L. Escapes of non-native fish from flooded aquaculture facilities: the case of Paranapanema River, southern Brazil. Zoologia, 2018, 35, e14638. http://dx.doi.org/10.3897/zoologia.35.e14638.
http://dx.doi.org/10.3897/zoologia.35.e1...
). It is important to note that O. niloticus specimens had already been recorded in the Capivara Reservoir (Paranapanema River) (Orsi & Britton, 2014ORSI, M.L. and BRITTON, J.R. Long-term changes in the fish assemblage of a neotropical hydroelectric reservoir. Journal of Fish Biology, 2014, 84(6), 1964-1970. http://dx.doi.org/10.1111/jfb.12392. PMid:24787281.
http://dx.doi.org/10.1111/jfb.12392...
). 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)AZEVEDO-SANTOS, V.M., RIGOLIN-SÁ, O. and PELICICE, F.M. Growing, losing or introducing? Cage aquaculture as a vector for the introduction of nonnative fish in Furnas Reservoir, Minas Gerais, Brazil. Neotropical Ichthyology, 2011, 9(4), 915-919. http://dx.doi.org/10.1590/S1679-62252011000400024.
http://dx.doi.org/10.1590/S1679-62252011...
, Schork et al. (2013)SCHORK, G., HERMES-SILVA, S. and ZANIBONI-FILHO, E. Analysis of fishing activity in the Itá reservoir, Upper Uruguay River, in the period 2004-2009. Brazilian Journal of Biology = Revista Brasileira de Biologia, 2013, 73(3), 559-571. http://dx.doi.org/10.1590/S1519-69842013000300014. PMid:24212697.
http://dx.doi.org/10.1590/S1519-69842013...
and Bittencourt et al. (2014a)BITTENCOURT, L.S., PINHEIRO, D.A., CÁRDENAS, M.Q., FERNANDES, B.M. and TAVARES-DIAS, M. Parasites of native Cichlidae populations and invasive Oreochromis niloticus (Linnaeus, 1758) in tributary of Amazonas River (Brazil). Revista Brasileira de Parasitologia Veterinária, 2014a, 23(1), 44-54. http://dx.doi.org/10.1590/S1984-29612014006. PMid:24728360.
http://dx.doi.org/10.1590/S1984-29612014...
. 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., 2007LANGEANI, F., CASTRO, R.M.C., OYAKAWA, O.T., SHIBATTA, O.A., PAVANELLI, C.S. and CASATTI, L. Diversidade da ictiofauna do Alto Rio Paraná: composição atual e perspectivas futuras. Biota Neotropica, 2007, 7(3), 181-197. http://dx.doi.org/10.1590/S1676-06032007000300020.
http://dx.doi.org/10.1590/S1676-06032007...
). 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, 1995NOGA, E.J. and FLOWERS, J.R. Invasion of Tilapia mossambica (Cichlidae) viscera by the monogenean Enterogyrus cichlidarum. The Journal of Parasitology, 1995, 81(5), 815-817. http://dx.doi.org/10.2307/3283988. PMid:7472888.
http://dx.doi.org/10.2307/3283988...
). Ectoparasites may cause injuries of scales, secretion of mucus and necrosis of cells, which allow the entry of fungi and bacteria (Eiras, 1994EIRAS, J.C. Elementos de Ictioparasitologia. Porto: Fundação Eng. António de Almeida, 1994.). The pathogens caused by these parasites alter parasite-host interactions and reduce the native host population (Prenter et al., 2004PRENTER, J., MACNEIL, C., DICK, J.T.A. and DUNN, A.M. Roles of parasites in animal invasions. Trends in Ecology & Evolution, 2004, 19(7), 385-390. http://dx.doi.org/10.1016/j.tree.2004.05.002. PMid:16701290.
http://dx.doi.org/10.1016/j.tree.2004.05...
; Goedknegt et al., 2016GOEDKNEGT, M.A., FEIS, M.E., WEGNER, K.M., LUTTIKHUIZEN, P.C., BUSCHBAUM, C., CAMPHUYSEN, K.C., VAN DER MEER, J. and THIELTGES, D.W. Parasites and marine invasions: ecological and evolutionary perspectives. Journal of Sea Research, 2016, 113(1), 11-27. http://dx.doi.org/10.1016/j.seares.2015.12.003.
http://dx.doi.org/10.1016/j.seares.2015....
). 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., 2017FRANÇA, E.J., ALMEIDA, C.A.C., ALMEIDA-NETO, M.S., SANTOS, R.E., MAGALHÃES, A.L.B., EL-DEIR, A.C.A. and SEVERI, W. Novelty on the market, novelty in the environment: The invasion of non-native fish jaguar guapote (Perciformes) in northeastern Brazil. Neotropical Biology and Conservation, 2017, 12(1), 12-18. http://dx.doi.org/10.4013/nbc.2017.121.02.
http://dx.doi.org/10.4013/nbc.2017.121.0...
; Casimiro et al., 2018CASIMIRO, A.C.R., GARCIA, D.A.Z., VIDOTTO-MAGNONI, A.P., BRITTON, J.R., AGOSTINHO, A.A., DE ALMEIDA, F.S. and ORSI, M.L. Escapes of non-native fish from flooded aquaculture facilities: the case of Paranapanema River, southern Brazil. Zoologia, 2018, 35, e14638. http://dx.doi.org/10.3897/zoologia.35.e14638.
http://dx.doi.org/10.3897/zoologia.35.e1...
). 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.

Acknowledgements

The authors are grateful to students and volunteers who participated in data collection and to the fish farm that donated the fish specimens; and editor and anonymous reviewers for suggesting manuscript improvements. This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (grant number 472648/2009-8).

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Publication Dates

  • Publication in this collection
    14 Nov 2019
  • Date of issue
    2019

History

  • Received
    09 Sept 2018
  • Accepted
    18 Oct 2019
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