Two new monogenoidean species of Unilatus Mizelle & Kritsky, 1967 found in the gills of loricariids in the Lower Xingu-Iriri rivers are described: Unilatus humboldtii sp. nov. from Baryancistrus niveatus (Castelnau, 1855), Panaque armbrusteri Lujan, Hidalgo & Stewart, 2010, Pseudacanthicus sp. (type-host), and Scobinancistrus aureatus Burgess, 1994; and Unilatus luciarappae sp. nov. from P. armbrusteri. Unilatus humboldtii sp. nov. is distinguished from other congeneric species due to its anterior anchor with well-developed superficial root with depressed or truncated distal portion, and inconspicuous or reduced deep root; anterior bar with posteromedial projection; hooks of pair 1 with dilated shaft comprising 2/3 of the hook length; spiraled male copulatory organ with approximately 16–18 counterclockwise loops. Unilatus luciarappae sp. nov. is characterized by having anterior anchor with well-developed superficial root and reduced deep root, slightly curved shaft, elongated, slightly curved, and tapered point; spiraled MCO with approximately 18–19 counterclockwise loops, with median distal bulbous portion and remaining portion tapered and elongated, comprising 1/4 of the body length; and accessory piece comprising approximately 2/3 of the MCO length. More than fifty years after the description of the type species of Unilatus from an artificial environment (U.S. aquaria), this study represents the first formal record and description of Unilatus species from hosts collected in natural habitats in the Xingu River. Considering the impact of the Belo Monte dam on the formerly pristine conditions of the study region and the importance of loricariids for the ornamental fish trade, we recommend monitoring monogenoidean diversity, parasite-host interaction, as well as the dispersion patterns and pathogenicity of these parasites.

Amazon, Loricariidae, Monogenoidea, parasites, ornamental fish, Unilatus

Brazil is a regional leader in the global exportation of ornamental fish from inland waters, representing 23% of the South American market (Prang 2007). Much of this trade is comprised of fish species from the Amazon basin, which are favorites among Brazilian and foreign aquarists and represent an important source for international trade (Carvalho Júnior et al. 2009). Total revenues in this market are estimated at USD 68,246,689.00 between 2012 and 2019 (Siscomex 2020), with high profitability driving an active global market (Araújo et al. 2017).

The state of Amazonas, especially the Rio Negro region, is the largest source of ornamental fish in Brazil, representing approximately 60% of the country’s total exports, with the state of Pará, accounting for an additional 30% (Lacerda 2005). In Pará, the Xingu region is one of the main centers of ornamental fish extraction, with approximately 422 species with trade interests reported for the region (Carvalho Júnior et al. 2009). Among these species, loricariids (Loricariidae), freshwater rays (Potamotrygonidae), and cichlids (Cichlidae) (Camargo 2011) are noteworthy, in part because several species are endemic to the Xingu region, giving them a high added value (Araújo et al. 2017).

In Brazil, the capture, commercialization, and exportation of fish were regulated by Normative Instruction MPA/MMA 001/2012, which was enforced until 2020. This legislation covered 725 fish species from Brazilian continental waters, of which 125 (~17%) belonged to the Loricariidae. Commercial interest in species of this fish family is considerable in the Xingu River basin since, of the 55 species reported, at least 38 are commercialized as ornamental species (Camargo et al. 2011). Loricariids, widely known as commonly called “plecos” or “L” by aquarists.

Endemic to the Neotropics, the Loricariidae is one of the largest fish families in South America with approximately 916 valid species, encompassing about 1/4 of the diversity of the order Siluriformes (Armbruster 2011, Eschmeyer and Fong 2016, Nelson et al. 2016). Loricariids are highly valued on the international ornamental fish market. For example, species like Scobinancistrus aureatus Burgess, 1994, commonly known as “Goldie Pleco”, can be sold by 1,500% of the Brazilian initial export cost (Araújo et al. 2017). However, loricariid collectors – known as acarizeiros – earn marginal wages. The relatively reduced income of the acarizeiros results in a greater effort of capture. The high individual value of loricariids of commercial interest stimulates intensified selective fishing and may lead to a depletion of natural stocks (Ramos et al. 2015). This is the case of the “Zebra Pleco”, Hypancistrus zebra Isbrücker & Nijssen, 1991, a species endemic to the Xingu River basin, whose capture was prohibited in 2004 (Ibama 2004) due to overfishing.

Studies on the pathogens or parasites that affect ornamental fishes exported from Brazil (Fujimoto et al. 2013, Tavares-Dias et al. 2017, Cardoso et al. 2018, Hoshino et al. 2018) and abroad (Mehdizadeh Mood and Rassouli 2016, Mendoza-Franco et al. 2018) are still in their early stages. Recent data on monogenoidean platyhelminths, for example, suggest that only 8% of ornamental fish species regularly sold in Brazil are examined for these parasites (Cohen et al. 2013). For monogenoidean parasites, it is currently estimated that only approximately 4% of this diversity has been revealed (Cohen et al. 2013, Branches and Domingues 2014, Acosta et al. 2017a, 2017b, Franceschini et al. 2018, Vianna and Boeger 2019, Kritsky et al. 2020). Currently, 40 species of monogenoids are known from species of Loricariidae, of which 27 species were reported to parasitize the gills and 13 the body surface (Table 1). However, there are no records of monogenoidean parasites from species of Loricariidae in the Xingu basin, despite their importance of the Loricariidae in the regional ichthyofauna (Winemiller et al. 2016).

While investigating the monogenoidean parasite diversity from the gills of Baryancistrus niveatus (Castelnau, 1855), Panaque armbrusteri Lujan, Hidalgo & Stewart, 2010, Pseudacanthicus sp., and S. aureatus of Volta Grande, Xingu River, Pará, two new species of Unilatus Mizelle & Kritsky, 1967 were found. These two new species are described here, representing the first species of the genus formally described from loricariids in the Xingu River basin.

The first known monogenoidean species in fish from Brazilian continental waters were initially described and reported from ornamental fishes in aquaria in the U.S. Mizelle and Price (1965) proposed Anacanthorus Mizelle & Price, 1965 and described eight new species from material collected from the gills of Pygocentrus nattereri Kner, 1858 (Characiformes: Serrasalmidae) in the Steinhart Aquarium in San Francisco, California. From this same aquarium, Mizelle and Kritsky (1967) described Unilatus unilatus Mizelle & Kritsky, 1967 from the gills of Hypostomus sp. (Loricariidae); Mizelle et al. (1968) described Jainus jainus Mizelle, Kritsky & Crane, 1968 from the gills of Chalceus macrolepidotus Cuvier, 1818 (Characiformes: Chalceidae), Unilatus brittani from the gills of Hypostomus sp., and Urocleidoides carapus Mizelle, Kritsky & Crane, 1968, and U. gymnotus Mizelle, Kritsky & Crane, 1968 from the gills of Gymnotus carapo Linnaeus, 1758 (Gymnotiformes: Gymnotidae).

Subsequently, several monogenoidean species probably originating from the Neotropical region were described and/or reported in freshwater ornamental fish exported from Brazil to aquariums abroad. Jogunoori et al. (2004) reported three species of monogenoids belonging to the genera Heteropriapulus Jogunoori Kritsky & Venkatanarasaiah, 2004, Diaphorocleidus Jogunoori Kritsky & Venkatanarasaiah, 2004, and Urocleidoides Mizelle & Price, 1964, collected from the gills of Hypostomus sp., Gymnocorymbus ternetzi (Boulenger, 1895) (Characidae), and Xiphophorus helleri Heckel, 1848 (Ciprinodontifomes, Poeciliidae), respectively, sold in Indian ornamental fish trade. Mehdizadeh et al. (2016) investigated the occurrence of monogenoids of exotic fish sold in Iranian ornamental fish markets and found Gonocleithrum cursitans Kritsky & Thatcher, 1983 and U. unilatus parasitizing the gills of the South American fishes Osteoglossum bicirrhosum (Cuvier, 1829) (Osteoglossiformes: Osteoglossidae) and Hypostomus plecostomus (Linnaeus, 1758), respectively. Mendoza-Franco et al. (2018) evaluated the occurrence of monogenoids in exotic freshwater fish from the production units of Mexican aquaria. These authors evaluated 13 fish species and found 29 species of monogenoids, four of which parasitize fish commonly exported from Brazil. Monogenoids were also recorded in freshwater fish imported from South America that became co-invasive species in rivers in Europe and Asia. Boeger et al. (2002) reported Mymarothecium viatorum Boeger, Piasecki & Sobecka, 2002 from the gills of Piaractus brachypomus (Cuvier, 1818) (Serrasalmidae) captured in a channel system of a power plant in Poland. Li et al. (2009) found Trinigyrus hypostomatis Hanek, Molnar & Fernando, 1974 and U. unilatus in the gills of H. plecostomus introduced in the Pearl River, Guangzhou, China. In the same fish species, Li and Huang (2012) found the first record of Heteropriapulus in a fish market, also in Guangzhou. Nitta and Nagasawa (2013, 2016) reported Heteropriapulus heterotylus Jogunoori Kritsky & Venkatanarasaiah, 2004; Trinigyrus peregrinus Nitta & Nagasawa, 2016; Unilatus unilatus, and U. britanni from the gills of Pterygoplichthys disjunctivus (Weber, 1991), which had been introduced into the inland waters of Okinawa Island, Japan.

Unilatus presently comprises eight species, including the two described in this study. Of these, seven have been reported in loricariids sold on the Brazilian ornamental fish market. Species of the genus have only been recorded in fish exported from Brazil in the cases of U. unilatus and U. britanni. There are no records of these parasites being transferred to other hosts after their introduction, and their pathogenicity is unknown in native and alien environments.

Jogunoori et al. (2004) suggest that possible economic losses and environmental impacts may occur due to the introduction of monogenoidean species into new environments and hosts. However, they note a low potential for monogenoids to transfer between alien and native host species. Jiménez-Garcia et al. (2001) found that monogenoidean species typically found in African cichlids used worldwide in aquaculture systems had parasitized freshwater cichlid species native to Mexico. Also, García-Vásquez et al. (2017) recorded Gyrodactylus cichlidarum Paperna, 1968, a monogenoidean parasite typically reported from the African “tilapia”, on poeciliids (Cyprinodontiformes) in Mexico. However, even if there is no evidence of problems these parasites can provoke after becoming established, care should be taken to prevent their establishment in new ecosystems. Adopting prophylactic measures and quarantine procedures to mitigate the transfer of parasites among fish sold on the Brazilian ornamental fish market is important. However, studies on the diversity of parasites that occur in these fish are also needed, as they shed light on the potential of dispersion of these parasites as well as their pathogenicity.

More than 50 years after the description of the type species of Unilatus from an artificial environment (U.S. aquariums), this study is the first formal record and description of Unilatus species from hosts collected in natural habitats in the Xingu River basin. Considering the loss of pristine conditions in the studied region as a result of the construction of the Belo Monte Dam, we recommend monitoring monogenoidean diversity, parasite-host interactions, parasite indices, and parasite dispersion patterns and pathogenicity. Such studies may provide important insights into the impacts of changes to the hydrological regime in the Xingu River caused by the Belo Monte Dam.

Studies of the Belo Monte Dam’s impacts on the persistence of the diversity of the loricariid hosts and the associated helminth fauna recently described for the Xingu basin are urgently and continuously required. The changes in ecological dynamics are characterized by the ‘lentification’ of the aquatic environment once formed by rapids in the region upstream of the dam and by the reduced flow stretch for the 100-km stretch of the ‘Big Bend’. These changes have caused high mortality of ichthyofauna in the region while decreasing oxygenation and increasing water temperature due to the Xingu River’s rocky bed. Thus, the risks for the conservation of the diversity of the recently described helminth fauna and the parasite-host ecological dynamics are increased. Furthermore, all aquatic biota and the livelihood of human populations in the region have been negatively impacted.

We would like to Geusivam Barbosa Soares for assistance during the collecting trips. This work was partially supported by Research grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, PROTAX 001/2015-440526/2015-9), and Fundação Amazônia de Amparo a Estudos e Pesquisas do Pará (FAPESPA) (ICAAF 017-2018) to M.V.D. Specimens were collected under the license for collection of biological material (43381) granted by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio).