Aquatic Invasions (2020) Volume 15, Issue 3: 455–472

CORRECTED PROOF

Research Article Non-native freshwater molluscs in the Neotropics: what can be learned from Brazilian reservoirs?

Igor Christo Miyahira*, Larissa Strictar Pereira and Luciano Neves dos Santos Instituto de Biociências, Universidade Federal do Estado do Rio de Janeiro (IBIO/UNIRIO). Avenida Pasteur, 458 – Urca, 22290-250, Rio de Janeiro – RJ, Brazil *Corresponding author E-mail: [email protected]

Citation: Miyahira IC, Pereira LS, dos Santos LN (2020) Non-native freshwater Abstract molluscs in the Neotropics: what can be learned from Brazilian reservoirs? Aquatic Habitat modification and the establishment of non-native species are two major Invasions 15(3): 455–472, https://doi.org/10. causes of biodiversity loss. Reservoirs modify habitat, can restrain the occurrence 3391/ai.2020.15.3.06 of native species, and allow the establishment of non-native undesirable organisms. Received: 16 April 2019 Non-native species are widespread. However, the status and distribution of some Accepted: 20 April 2020 invaders in these man-made systems remains unclear, especially in the Neotropics. Published: 24 June 2020 In this study, we surveyed digital databases to determine the distribution of non- native molluscs in Brazilian reservoirs. Studies on non-native molluscs in Brazilian Handling editor: Demetrio Boltovskoy reservoirs had been increasing steadily until they reached their peak in 2015. Eight Thematic editor: Ian Duggan non-native mollusc species were recorded in reservoirs in all river basins except for Copyright: © Miyahira et al. the Amazonas River. Non-native molluscs were reported in 74 reservoirs, mostly This is an open access article distributed under terms located within the Paraná River basin. The co-occurrence of multiple non-native of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). molluscs was common. Time lapsed since first introduction of species was not correlated with their distribution in Brazilian reservoirs. This study was a first step OPEN ACCESS. toward understanding the distribution of non-native molluscs, and their possible impacts, in Neotropical reservoirs.

Key words: invasive species, dams, reservoir, distribution, Mollusca, Brazil

Introduction Establishment of non-native species is commonly found to impact the environment negatively (Crowl et al. 1992; Simberloff 2005; Vitule et al. 2009; Kovacs et al. 2012); non-native species have been frequently associated with species extinction since at least 1500 AD (Bellard et al. 2016), although a wide range of other effects are possible (Davis and Chew 2017; Boltovskoy et al. 2018). Non-native species can compete with natives for essential resources, alter nutrient cycling, decrease the diversity of native communities, and exert strong predation pressure on native prey species (Salo et al. 2007; Pelicice and Agostinho 2009; Rocha et al. 2011; Cataldo et al. 2012; Paolucci et al. 2013; Fleming and Dibble 2015; Pereira et al. 2015). The gradual replacement of native by non-native species, along with severe habitat modification, has led to the biotic homogenization, which is considered one of the most prominent forms of biotic impoverishment

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worldwide (Olden et al. 2004). The establishment of non-native species and environmental modifications are two leading causes of molluscan biodiversity loss (Lydeard et al. 2004; Lopes-Lima et al. 2014; Vogler et al. 2016; Cowie et al. 2017). These are also the two main sources of molluscan extinctions particularly common in reservoirs, as river damming causes hydrological, limnological, and habitat disturbances, such as the removal of physical barriers, natural competitors, and predators, and as they act as stepping stones for the spread and establishment of non-native species (Havel et al. 2005; Johnson et al. 2008; Oliveira et al. 2015; Thomaz et al. 2015). The Neotropical region is a large area, which can facilitate the spread of non-native aquatic species; as most countries, particularly Brazil, rely widely on hydroelectric power, the construction of several new dams is planned, especially in the Amazonas and Tocantins rivers basins (Ansar et al. 2014; Winemiller et al. 2016; Pereira et al. 2018). Dam construction also favors certain non-native molluscs that, overall, succeed in more lentic and eutrophic systems (Thiengo et al. 2005; Johnson et al. 2008; Fernandez et al. 2014). The few documented records of mollusc extinctions in South America are associated with the construction of dams (Vogler et al. 2015, 2016). As a consequence, freshwater molluscs are among the most threatened taxa in the world (Lydeard et al. 2004; Pereira et al. 2012, 2014; Regnier et al. 2015; Cowie et al. 2017). Non-native molluscs are, overall, opportunistic species that can reach high population sizes. One example is the golden mussel Limnoperna fortunei (Dunker, 1857), which has modified benthic habitat (e.g., Boltovskoy et al. 2006; Darrigran et al. 2007; Mansur et al. 2012). Other non-native mollusc species have different impacts on native species (Mansur et al. 2003, 2012; França et al. 2007; Braga et al. 2014; Thomaz et al. 2015; Ferreira-Rodriguez et al. 2018). Seven freshwater mollusc species were registered in the official Brazilian list of non-native species (Latini et al. 2016). Since this report was published, other non-native species have been registered (Lacerda et al. 2015). Due to the recent introduction of some non-native species in Brazilian reservoirs (Pereira et al. 2018), their status and the temporal evolution of the invasion process are little known. The aim of this study was to evaluate these trends for non-native molluscs recorded in Brazil through an extensive literature survey. The invasion dynamics of freshwater molluscs in the Neotropics was evaluated in Brazil, as this is the country harboring the highest number of reservoirs in the region.

Materials and methods A literature search was conducted using Google Scholar (access: https:// scholar.google.com.br) owing to the broader coverage it offers on the topic non-native molluscs in Brazil in comparison with other similar databases. Other scientific databases, such as Scopus (https://www.scopus.com/), do not include several Brazilian scientific journals, where most studies on

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non-native mollusc species in Brazil have been published. Theses, reports, and other materials were used when well substantiated. The keywords “reservoir” OR “dam” AND “name of non-native mollusc – see below” AND “Brazil” were used to perform the search, with November 30, 2017 set as the deadline of the literature search. The listed species in the official list of Ministry of the Environment of Brazil (Latini et al. 2016) were Corbicula fluminalis (Müller, 1774), Corbicula fluminea (Müller, 1774), Corbicula largillierti (Philippi, 1844), Limnoperna fortunei, Melanoides tuberculata (Müller, 1774), Physa acuta Draparnaud, 1805 and Helisoma duryi (Wetherby, 1879). The authority names were not used to fulfill the searches. Ferrissia fragilis (Tryon, 1863), Helisoma sp., and Corbicula sp. were not nominated in the official list but appeared in our primary search, so new searches, using the same criteria applied previously, were performed for these three non-native species. The SpeciesLink database (http://splink. cria.org.br), a network of scientific collections, was also searched using the names of all non-native species as keywords. In all reports where no clear reference was made to the place of origin, geographical coordinates were used to determine whether the record was obtained from a reservoir. Thus, our keywords were designed to detect mollusc records in reservoirs of all types and sizes. We did not search for specific reservoirs. The records obtained from the literature and SpeciesLink were classified into eight catchments: the Amazonas River, North/Northeast Atlantic coastal rivers (including Parnaíba River), São Francisco River, Tocantins River (including Araguaia River with which it converges), East Atlantic coastal rivers (including the Paraíba do Sul and Doce rivers), Paraná River (including Paraguay River with which it merges), Uruguay River, and South Atlantic coastal rivers (including Guaíba Lake). The searches described above returned positive records; to assess the representativity of these records, an estimate of the overall number of Brazilian reservoirs was required. The exact number of Brazilian reservoirs is unknown, as these come in different sizes and are built for distinct purposes, and information about them, when available, is usually fragmented and inconsistent (Agostinho et al. 2007). According to ANEEL (2019), there are 987 planned, under construction, or operating medium to large hydroelectric power plants (UHEs) and small hydroelectric power plants (PCHs) in Brazil. For the purposes of this study, only active dams were taken into account, i.e., those reservoirs with start of operation data in the ANEEL (2019) database (see also Supplementary material). Some reservoirs that appeared on the literature search, but were not recorded in the ANEEL database were included in the Supplementary Material list of reservoirs, as these were probably constructed for reasons other than energy production. The reservoirs were distributed on the following catchments: 58 in the Amazonas River, 16 in North/Northeast Atlantic coastal rivers, 32 in São Francisco River, 26 in Tocantins River, 103 in East Atlantic coastal rivers, 173 in Paraná River, 50 in Uruguay River, and 50 in South Atlantic coastal rivers.

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12

10

8

6

4 Number of publications

2

0 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017 Year of publication Figure 1. Papers on the topic of non-native freshwater molluscs in Brazilian reservoirs between 1987 and 2017. Only the results retrieved from Google Scholar were showed.

Maps on the geographic distribution of non-native molluscs (i.e., plots of the records retrieved from the literature search) were built in the software R Programming Environment (R Core Team 2019), using the “maptools” (Bivand and Lewin-Koh 2018) and “ggplot2” (Wickham 2016) packages. The expansion rate of non-native molluscs in dammed environments was estimated using the number of years that passed since the first record of a species in Brazil (i.e., the time that lapsed since its introduction) and the number of reservoirs in which the species was recorded.

Results A total of 75 documents and 85 records on non-native molluscs in Brazilian reservoirs were retrieved from Google Scholar and SpeciesLink searches, respectively (see Supplementary Material for details). Most papers were published after 2005; since this time, the number of studies on this topic has had a clear increasing tendency (Figure 1, Supplementary material). Only one paper was published in the 1980s, two during the 1990s, and four between 2001 and 2002, while all the remaining papers were published after 2005. A total of eight non-native mollusc species were recorded in Brazilian reservoirs: M. tuberculata, P. acuta, F. fragilis, Helisoma sp., C. fluminea, C. largillierti, Corbicula sp., and L. fortunei. The molluscs were distributed in 74 reservoirs in all catchments, except for the Amazonas River basin where no non-native species were recorded in reservoirs (Figure 2). This is equivalent to almost 15% of the total estimated dams (including Amazonas basin). The Paraná River basin harbored the greatest number of reservoirs in which non-native molluscs were recorded (N = 40 which represented 23% of the estimated total number of reservoirs in this basin). Despite the

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 458 Non-native molluscs in Brazilian reservoirs

Figure 2. Overall distribution of non-native freshwater molluscs in Brazilian reservoirs. Intense dark red means higher number of records of non-native molluscs in reservoirs, whereas the lighter colors means the opposite situation, and white absence. Filled circles – reservoir with at least one record of non-native molluscs; open circles – reservoirs without non-native molluscs records. Numbers inside the map mean basin codes: 1 – Amazonas River, 2 – Tocantins River, 3 – North/Northeast Atlantic coastal rivers, 4 – São Francisco River, 5 – East Atlantic coastal river, 6 – Paraná River, 7 – Uruguay River, and 8 – South Atlantic coastal river.

lower absolute number of invaded reservoirs in the North/Northeast coastal rivers (N = 11), this basin included the highest percentage of reservoirs with non-native species (69%). In the East Atlantic coastal rivers and the Uruguay River (N = 2 and 1, respectively, which represented 2% and 2% of the estimated total number of reservoirs for this basin, respectively) lower numbers of non-native molluscs, in terms of absolute numbers and percentages, were obtained. The other basins (São Francisco River, the South Atlantic coastal rivers, and Tocantins River) had intermediate values (N = 11, 5, and 4, respectively, which represented 34%, 10%, and 15% of the estimated total number of reservoirs, respectively). Most molluscs introduced in Brazilian reservoirs were native to Asia, although two species originated from other regions (one from the USA and the other from France) (Table 1). Melanoides tuberculata was the most widespread molluscan species in reservoirs recorded in all Brazilian basins, except for the Amazonas and Uruguay basins. Limnoperna fortunei and C. fluminea were found in half of the basins (Figure 3). Corbicula largillierti and P. acuta were recorded in three basins each. Ferrissia fragilis, Helisoma sp., and Corbicula sp. were rarer in reservoirs; Ferrissia fragilis was found in two basins (the Tocantins

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Table 1. Expansion of non-native molluscs in Brazilian reservoirs. Helisoma sp. and Corbicula sp. were not included. * – Based on original data by Leme (1966), Vaz et al. (1986), Mansur et al. (1999), Callil and Mansur (2002), Mansur et al. (2004, 2012), Lacerda et al. (2015). ** – There is a historic record of Physa sowerbyana recoded by d’Orbigny to Peru, Brazil, Chile, Argentina and Uruguay, that Paraense (1987) considered this as a synonym of Physa cubensis (= P. acuta). Introduction Years in Brazil Colonized Reservoirs Species First record in Brazil* Origin* in Brazil* (as of 2017) reservoirs colonized by year Melanoides East of Africa 1967 Santos (São Paulo) 50 49 0.98 tuberculata and South of Asia artificial lake in Rio de Physa acuta 1966** France 51 9 0.18 Janeiro localities in Rio de Ferissia fragilis 2012 Janeiro and Minas USA 5 2 0.40 Gerais Corbicula Porto Alegre (Rio Asia, Korea and 1979 38 35 0.92 fluminea Grande do Sul) Southeast Russia Itaqui and São Borja at Corbicula China and 1988 the margins of Uruguay 29 6 0.21 largillierti Korean Peninsula River Corumbá (Mato Grosso Limnoperna 1998 do Sul); Lagoa Guaíba Asia 19 32 1.68 fortunei (Rio Grande do Sul)

and São Francisco rivers basins), while Corbicula sp. and Helisoma sp. were observed in a single basin (the Paraná and São Francisco rivers basins). The southernmost basins (those of the Uruguay and the South Atlantic coastal rivers) were characterized by the presence of L. fortunei, the single non-native mollusc species recorded in these basins. The other two coastal basins (East and North/Northeast) were characterized by the presence of M. tuberculata, with some records of C. largillierti, and a single report of P. acuta and C. fluminea in the basins of East Atlantic coastal rivers. Other basins located at the central region of Brazil (Paraná, São Francisco, and Tocantins) presented higher richness of non-native molluscs, as six species were detected in the São Francisco River and five in the Paraná and Tocantins rivers basins. Melanoides tuberculata, C. fluminea, and L. fortunei were the three most widespread invasive molluscs in reservoirs. These same three species were also the fastest in expanding their domains. Limnoperna fortunei was the quickest spreading species in Brazilian reservoirs (1.68 reservoirs per year). Melanoides tuberculata and C. fluminea also had high expansion rates (0.98 and 0.95, respectively). Physa acuta and C. largillierti were the species with the lowest expansion rates (0.18 and 0.21, respectively) (Table 1). Melanoides tuberculata was the species with the broadest distribution along the colonized reservoirs of the North Atlantic coastal rivers (100% of reservoirs had records at this basin, N = 11), the São Francisco River basin (100%, N = 11), the East Atlantic coastal rivers (100%, N = 2), and the Tocantins River basin (75%, N = 3). Limnoperna fortunei occurred in 100% of reservoirs with records of non-native molluscs in the basins of the South Atlantic coastal (N = 5) and the Uruguay rivers (N = 1). Corbicula fluminea predominated in the Paraná River basin (73% of reservoirs, N = 29) followed by L. fortunei (55%, N = 22) and M. tuberculata (51%, N = 21).

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 460 Non-native molluscs in Brazilian reservoirs

Figure 3. Detailed distribution of non-native freshwater molluscs in Brazilian reservoirs. Intense dark red means higher number of records of the considered non-native molluscs in reservoirs, whereas the lighter colors mean the opposite situation. Filled circles – reservoir with at least one record of non-native molluscs; open circles – reservoirs without non-native molluscs. Corbicula spp. refers to: C. fluminea and C. largillieti records. Others refers to those species with the lowest number of occurrences: Ferrisia fragilis, Helisoma sp. and Physa acuta. For basin codes see Figure 2.

Melanoides tuberculata, C. fluminea, and L. fortunei occurred simultaneously in seven reservoirs of the Paraná River basin and in the Sobradinho reservoir (São Francisco River basin). Two of these three species, in different combinations, occurred in 23 more reservoirs; thus, 42% of the reservoirs with reports of non-native species included multiple records of at least two of these three species. The Três Irmãos Resevoir (Paraná River basin) had the highest number of non-native species (N = 5), which were M. tuberculata, Helisoma sp., P. acuta, C. fluminea and L. fortunei. Four non-native species occurred simultaneously in six reservoirs

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(four within the Paraná River basin, and in a single reservoir in each of the São Francisco and the East coastal rivers basins). Most reservoirs had either one (N = 32) or two (N = 29) non-native species records.

Discussion Recent interest in non-native species is reflected in studies on Brazilian reservoirs. However, this concern has been addressed belatedly in Brazil compared with the rest of the world (Quiroz et al. 2009; Lowry et al. 2013; Frehse et al. 2016). Thus, the body of knowledge concerning non-native freshwater molluscs in Brazilian reservoirs is more recent. Almost all non-native species found in Brazil have also been observed in Brazilian reservoirs. Corbicula fluminalis, an introduced clam registered in Brazil (Mansur et al. 2004, 2012; Latini et al. 2016; Martins et al. 2006), was not recorded in reservoirs. Additionally, an unidentified Corbicula species found in Brazilian waters, is restricted to Rio Grande do Sul state (not listed in Latini et al. 2016, see Santos et al. 2012) and, apparently, it is not related to the Northeast Brazil Corbicula sp. records, probably owing to taxonomical limitations. If this relationship was confirmed, the number of introduced molluscs in reservoirs would drop to seven. Indeed, the taxonomy of Corbicula spp. is still confusing and requires more research (e.g., Pigneur et al. 2011; Komaru et al. 2013). It is quite probable that H. duryi accounted for most of the Helisoma sp. records in reservoirs, despite the occurrence of another congener in Brazil, Helisoma trivolvis (Say, 1817), which is restricted to the Rio de Janeiro state (Fernandez et al. 2010; Santos et al. 2012). In Brazil, most reservoirs had few introduced species (one or two), rarely attaining a maximum of five species, a number that is quite similar to those of other reservoirs. In some Russian reservoirs, the number of non-native mollusc species (Bivalvia and Gastropoda) ranged from two to six (Yakovleva and Yakovlev 2010; Zinchenko and Kurina 2011). Most of the impacts related to non-native freshwater molluscs in Brazilian reservoirs could be attributed to M. tuberculata, C. fluminea and L. fortunei (e.g., Freitas et al. 1987; Fernandez et al. 2003; Mansur et al. 2003, 2004; Giovaneli et al. 2005; Suriani et al. 2007; Santos et al. 2012; Braga et al. 2014; Pereira et al. 2014). Limnoperna fortunei can cause a decrease in the particulate nitrogen and phosphorus levels and a simultaneous increase in the ammonium, nitrate, and phosphate concentrations, and water transparency (Cataldo et al. 2011, 2012; Mariñelarena et al. 2014). All of these modifications can contribute to toxic cyanobacterial blooms, as has been observed in Salto Grande reservoir (Cataldo et al. 2011), which can also affect the feeding and survival of fish larvae in the same reservoir (Paolucci et al. 2017) or even the reproduction of L. fortunei (Boltovskoy et al. 2013). Melanoides tuberculata has been used widely as a potential biological control agent of Biomphalaria spp., the major vectors of schistosomiasis; despite controversial results regarding the effectiveness of this species, non-native M. tuberculata

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populations always flourish (Pointier et al. 1989; Cowie 2001; Santos et al. 2012; Braga et al. 2014). Freitas et al. (1987) observed the overgrowth of M. tuberculata over native molluscs in Pampulha reservoir; additionally, high densities of this invasive snail altered the substrate composition of an Asiatic reservoir (Dudgeon 1982). Limnoperna fortunei, C. fluminea, and M. tuberculata can reach high population levels as invasive species. In extreme cases, these high populations can cause die-offs that lead to hypoxia and increased concentrations of toxic ammonia owing to the decomposition of dead animals, although these events can benefit adjacent terrestrial environments (Bódis et al. 2014). These die-offs can also result from low water levels, a common feature of dammed systems (Darrigran et al. 2004; Cherry et al. 2005; Cooper et al. 2005; Oliveira et al. 2006; Ilarri et al. 2011; Paschoal et al. 2015). The ecological impact of the three most widespread non-native species found in Brazilian reservoirs (M. tuberculata, L. fortunei, and C. fluminea) is possibly synergistic (Johnson et al. 2009; Linares et al. 2017). One possible hypothesis is that L. fortunei and Corbicula spp. filter large volumes of water, increasing water transparency and favoring biofilm growth (Way et al. 1990; Pigneur et al. 2014; Cataldo et al. 2012; Boltovskoy and Correa 2015); these biofilms can be used as a food source by M. tuberculata (Benthem- Jutting 1956; Beeston and Morgan 1979) and other snails, including Helisoma spp. and P. acuta. The predictability of this scenario is even higher for dammed environments, where low flows and lentic zones prevail. On the other hand, L. fortunei grows over any available hard substratum, such as C. fluminea shells (Mansur et al. 2003, 2008; Boltovskoy and Correa 2015). However, C. fluminea is smaller and buried deeper than most large native mussels (Unionida), which makes individuals of these latter species easier targets for golden mussel larvae. Moreover, M. tuberculata can use the clusters of golden mussels as a refuge, as has been observed in other native and non-native snails (Mansur et al. 2008; Spaccesi and Capítulo 2012). Finally, it has been suggested that the establishment of M. tuberculata is facilitated by the introduction of non-native bivalves in some reservoirs of Southeast Brazil (Linares et al. 2017), while non-native macrophytes could facilitate the establishment of golden mussels in reservoirs of the upper Paraná River (Michelan et al. 2014). The prevalence of records of non-native molluscs on the Paraná River basin matched the distribution pattern found for non-native freshwater species in Brazil (Pereira et al. 2018). Since impoundments usually favor non-native species, Paraná River is the most prone to invasions, owing to having the highest number of impoundments in Brazil (Agostinho et al. 2007; Thomaz et al. 2015; Linares et al. 2017; Pereira et al. 2018). Our records of non-native mollusc species were concentrated in the Paraná River mainstem, in contrast to the few records concerning Paraguay River (i.e., the second largest contributor to this basin), which also held a lower

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number of reservoirs (Agostinho et al. 2007). The least-altered conditions in the upper Paraguay River (e.g., the Pantanal wetlands), with prolonged wet and dry periods, may be a limiting factor for the establishment of non- native species, including molluscs (Oliveira et al. 2006). An increase in the number of reservoirs in this river could modify the flood pulse regime (Junk and Cunha 2005), thus increasing the invasibility of such an ecosystem. On the other hand, the shortest flood pulse on less modified areas of the Paraná River can indeed facilitate golden mussel larvae dispersal (Ernandes-Silva et al. 2016). Although the highest number of records concerned the Paraná Basin, the highest percentage of invaded dams was observed on the North/Northeast Atlantic coastal river basin. The basin is dominated by small-sized catchments and reservoirs that are naturally poor in freshwater molluscs. This lack of native competitors can represent a “vacant niche” to be filled by invasive molluscs. Nevertheless, there are fewer research centers in the North/Northeast Atlantic coastal river basins compared to South/Southeast Brazil. These findings may thus suggest that the occurrence of non-native molluscs in reservoirs of the East/South Atlantic, Uruguay and, possibly, Tocantins rivers basins are underestimated. The lack of records for a widely distributed species, such as C. fluminea, in reservoirs of the Uruguay and South Atlantic coastal rivers basins appears to be related more to low sampling efforts than to the absence of these invaders per se. A recent survey on Guandu reservoir (East Atlantic coastal rivers basin) revealed a large number of non-native molluscan species (Miyahira et al. 2017); a similar trend is expected for other nearby reservoirs. To our knowledge, there is only a single study that has reported the absence of a non-native mollusc in Brazilian waters. The absence of golden mussels in the Piraquara I reservoir, located in the Paraná basin, was attributed to the low propagule pressure in the region, as this reservoir is closed to recreational activities (e.g., sport fishing, sailing, and boats are not allowed; Frehse et al. 2018). Molluscs are generally introduced by chance (unwanted introductions); thus, higher movement of people and boats (increased propagule pressure) raises the chances of finding introduced molluscs. Moreover, some reservoirs are unexplored from a malacological point of view and may represent false negatives. Additional studies in other reservoirs for which there are no records of non-native molluscs would thus be of importance in determining whether the absence of records can be attributed to a lack of studies or, as in the case of the Piraquara I reservoir, if there is a singular condition that increases the reservoir’s resistance against invasions. The reservoirs of the Amazonas River basin are apparently free of non- native molluscs. However, it should be highlighted that several dams are planned or under construction in this basin (Ansar et al. 2014; Winemiller et al. 2016), which increases the chances of the introduction and establishment

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of these species in the near future. Nevertheless, in a limiting factor to the establishment of non-native molluscs in this region is the naturally or human-induced acidic waters of the Amazon (Pimpão and Martins 2008). In the Curuá-Una reservoir, for example, the pH ranges from 4.6 to 5.7 (Fearnside 1989; Vieira and Darwich 1999). Until 2015, L. fortunei was limited to southern Brazilian basins (i.e., the Paraná, Uruguay, and South Atlantic coastal rivers basins). However, this species was recently recorded at Sobradinho reservoir in São Francisco River (Barbosa et al. 2016). The recent transposition of São Francisco River waters to the Northeast coastal rivers basin can facilitate the dispersal of this and other non-native mollusc species. Some L. fortunei individuals were found near the channels that carry water to the inner semi-arid regions (Barbosa et al. 2016) in the North/Northeast coastal rivers basin. Melanoides tuberculata, C. fluminea, and C. largillierti were also found in the water channels and reservoirs near cities supplied with water from São Francisco River (Azevêdo et al. 2014, 2015; Thiengo et al. 2017). There are small reservoirs used for water storage along the water channels that can yield golden mussel populations. Thus, these are clear cases of reservoirs acting as stepping stones for non-native species; golden mussel can reproduce and grow at Sobradinho reservoir, a large and more stable water body, which could provide larvae for sink populations into small reservoirs. Knowledge of the origin of non-native molluscs introduced in reservoirs can facilitate the development of protocols to prevent and avoid future introductions. It is possible that P. acuta, originally described as indigenous to France, is actually native to the USA, being thus described during its early invasion stages throughout Europe (Taylor 2003). Considering this alternative hypothesis, all non-native mollusc species in Brazil may have originated primarily from Asia and secondarily from the USA. In a financial limitation scenario, the vessels arriving from freshwater piers of areas that have already donated molluscan species, may deserve special attention with respect to ballast water management, for example. This is not a solution to the problem but could help decrease propagule pressure, thus preventing new introductions. Regulation measures on the aquarium industry should also be enforced, as this is also a usual manner of mollusc introductions. This trade is generally unregulated and favors the spread of non-native species (Padilla and Williams 2004; Duggan 2010; Duggan et al. 2018). On the other hand, ballast water can only be used to explain the initial arrival of these bivalves in Brazil, but not their expansion (except for a few cases in large rivers) throughout the country. Their regional spread was probably facilitated by the careless transport of vessels, boats, fish cages, fishing devices, and water transfer facilities (of larvae and juveniles) among reservoirs and basins (Johnson et al. 2001; Santos et al. 2012; Barbosa et al. 2016; Boltovskoy 2015, 2017; Costa et al. 2017; Godoy et al. 2018).

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 465 Non-native molluscs in Brazilian reservoirs

The lapse of a long time since the introduction of a species does not necessarily equate its wide distribution in reservoirs. Physa acuta, the first freshwater mollusc thought to be introduced in Brazil, did not expand its distribution greatly in reservoirs (0.18 reservoirs colonized per year), showing the lowest expansion rate among other introduced species. On the other hand, M. tuberculata, which was introduced a few years later, has one of the highest expansion rates (0.98 reservoirs per year). Melanoides tuberculata is a parthenogenetic species, with high reproduction rates, and tolerance against desiccation (Berry and Kadri 1974; Facon et al. 2004). Physa acuta is more vulnerable to desiccation (Collas et al. 2014) and probably does not reproduce as fast. It is estimated that P. acuta produces approximately 20 eggs in 40 days in optimal environmental conditions (183 per year; Cope and Winterbourn 2004), while M. tuberculata is capable of producing 365 juveniles per year (Keller et al. 2007). Tolerance to desiccation and higher reproduction rates can be important characteristics for the colonization of dammed environments, which are commonly subjected to continuous water level fluctuations. Dudgeon (1982) observed that M. tuberculata was the first macroinvertebrate to colonize new flooded areas in Plover Cove reservoir (Hong Kong). These features allow this snail a rapid and efficient colonization of the new available habitat. As observed in Brazilian reservoirs, Keller et al. (2007) also noted a similar pattern for P. acuta introduced in the Great Lakes (USA), in which the lapse of a long time since introduction did not necessarily result in increased environmental harm. However, the potential of this species to outcompete native species cannot be neglected (Zukowski and Walker 2009). Currently, the golden mussel has the highest rate of reservoir colonization (1.68 reservoirs per year), agreeing with the overall dispersion rate calculated for Paraná River, which is approximately 250 km/year. However, these rates probably depend on specific characteristics of the invaded system, as the dispersion of golden mussels on Uruguay River is 10 times slower than that observed in Paraná River (Boltovskoy et al. 2006; Boltovskoy and Correa 2015). Limnoperna fortunei also has high reproduction rates and its free-swimming larvae can also be favored by passive dispersion downstream. Moreover, the attachment of golden mussels to ship and boat hulls can lead to their dispersion upstream or among interconnected catchments or reservoirs (Boltovskoy et al. 2006; Boltovskoy 2015). The other species that colonized several reservoirs, C. fluminea, also has an efficient method of dispersal; Corbicula spp. juveniles are capable of floating a mucous thread (Prezant and Chalernwat 1984). It is possible that this mucous thread attaches to some structures. Additionally, some of these invaders may have been registered soon after their introduction, which may interfere with the calculation of expansion rates. However, it is improbable that species that attain high population numbers, such as L. fortunei and C. fluminea, remained unnoticed for long time periods.

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 466 Non-native molluscs in Brazilian reservoirs

Despite the low sampling efforts in some areas, it is clear that non-native molluscs were already widespread in Brazilian reservoirs. These man-made systems seem to favor the introduction, establishment, and spread of non- native molluscs. Nowadays, the high interconnectedness of countries owing to globalization promotes the exchange of more goods, but also of unwanted non-native molluscs. Non-native molluscs are expanding in lentic environments of the Neotropics, and Brazil is an accurate illustration of this situation. Although our study is the first to attempt to depict the distribution and invasion status of the non-native freshwater mollusc species in Neotropical reservoirs, similar studies should be conducted in other countries to better comprehend the overall situation in this species-rich region.

Acknowledgements

We thank the two anonymous reviewers, and the editor Demetrio Boltovskoy, who helped to improve the manuscript with comments and suggestions.

Funding declaration

This work was funded by Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro, (FAPERJ) Brazil (research grant to LNS, E-26/202.840/2015; E-26/202.755/2018), National Council for Scientific and Technological Development (CNPq), Brazil (research grant to LNS, ref. 312194/2015-3; E-26/202.755/2018), and Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES), Brazil.

References

Agostinho AA, Gomes LC, Pelicice FM (2007) Ecologia e manejo de recursos pesqueiros em reservatórios do Brasil. EDUEM, Maringá, Brazil, 501 pp ANEEL (2019) Agência Nacional de Energia Elétrica. Banco de Informações de Geração - Matriz de Energia Elétrica, http://www2.aneel.gov.br/aplicacoes/capacidadebrasil/OperacaoCapaci dadeBrasil.cfm (accessed 13 December 2019) Ansar AB, Flyvbjerg A, Budzier, Lunn D (2014) Should we build more large dams? The actual costs of hydropower megaproject development. Energy Policy 69: 43–56, https://doi.org/ 10.1016/j.enpol.2013.10.069 Azevêdo EL, Barbosa JEL, Vidigal THDA, Callisto M, Molozzi J (2014) First record of Corbicula largillierti (Philippi, 1844) in the Paraíba River Basin and potential implications from water diversion of the São Francisco River. Biota Neotropica 14: e20140036, https://doi.org/10.1590/1676-0603003614 Azevêdo DJS, Barbosa JEL, Gomes WIA, Porto DE, Marques JC, Molozzi J (2015) Diversity measures in macroinvertebrates and zooplankton communities related to the trophic status of subtropical reservoirs: Contradictory or complementary responses? Ecological Indicators 50: 135–149, https://doi.org/10.1016/j.ecolind.2014.10.010 Barbosa NPU, Silva FA, Oliveira MD, Santos Neto MA, Carvalho MD, Cardoso AV (2016) Limnoperna fortunei (Dunker, 1857) (Mollusca, Bivalvia, Mytilidae): first record in the São Francisco River basin, Brazil. Checklist 12: 1–6, https://doi.org/10.15560/12.1.1846 Beeston DC, Morgan E (1979) A crepuscular rhythm of locomotor activity in the freshwater prosobranch, Melanoides tuberculata (Müller). Animal Behaviour 27: 284–291, https://doi.org/ 10.1016/0003-3472(79)90148-9 Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biology Letters 12: 20150623, https://doi.org/10.1098/rsbl.2015.0623 Benthem-Jutting WSS (1956) Systematic studies on the non-marine Mollusca of the Indo- Australian archipelago. V - Critical revision of the Javanese freshwater gastropods. Treubia 23: 259–477 Berry AJ, Kadri ABH (1974) Reproduction in the Malayan freshwater cerithiacean gastropod Melanoides tuberculata. Journal of Zoology 172: 369–381, https://doi.org/10.1111/j.1469-7998. 1974.tb04113.x Bivand R, Lewin-Koh N (2018) maptools: Tools for Reading and Handling Spatial Objects. R package version 0.8-10, http://CRAN.R-project.org/package=maptools Bódis E, Tóth B, Sousa R (2014) Massive mortality of invasive bivalves as a potential resource subsidy for the adjacent terrestrial food web. Hydrobiologia 735: 253–262, https://doi.org/10. 1007/s10750-013-1445-5

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 467 Non-native molluscs in Brazilian reservoirs

Boltovskoy D (2015) Distribution and Colonization of Limnoperna fortunei: Special Traits of an Odd Mussel. In: Boltoskoy D (ed), Limnoperna fortunei - The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling Mussel. Springer International, Switzerland, pp 301–311, https://doi.org/10.1007/978-3-319-13494-9_16 Boltovskoy D (2017) Traits and impacts of invasive species: myths and evidences from the perspective of introduced freshwater mussels. Aquatic Ecosystem Health & Management 20: 334–343, https://doi.org/10.1080/14634988.2017.1397483 Boltovskoy D, Correa N (2015) Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiologia 746: 81–95, https://doi.org/10.1007/s10750- 014-1882-9 Boltovskoy D, Correa N, Cataldo D, Sylvester F (2006) Dispersion and ecological impact of the invasive freshwater bivalve Limnoperna fortunei in the Río de la Plata watershed and beyond. Biological Invasions 8: 947–963, https://doi.org/10.1007/s10530-005-5107-z Boltovskoy D, Correa N, Bordet F, Leites V, Cataldo D (2013) Toxic Microcystis (cyanobacteria) inhibit recruitment of the bloom-enhancing invasive bivalve Limnoperna fortunei. Freshwater Biology 58: 1968–1981, https://doi.org/10.1111/fwb.12184 Boltovskoy D, Sylvester F, Paolucci EM (2018) Invasive species denialism: Sorting out facts, beliefs, and definitions. Ecology and Evolution 8: 11190–11198, https://doi.org/10.1002/ ece3.4588 Braga RMR, Miyahira IC, Lacerda LEM, Gonçalves ICB, Santos SB (2014) The influence of an invasive gastropod on the population dynamics of Pisidium punctiferum (Sphaeriidae) in an insular impacted stream in Rio de Janeiro, Brazil. In: Piza ART, Tallarico LF, Introíni GO, Santos SB (eds), Medical and Applied Malacology Crossing Boundaries: Integrative Approaches to Malacology. Cambridge Scholars Publishing, Newcastle, England, pp 97–114 Callil CT, Mansur MCD (2002) Corbiculidae in the Pantanal: history of invasion in southeast and central South America and biometrical data. Amazoniana 17: 153–167 Cataldo D, Vincour A, O’Farrell I, Paolucci E, Leites V, Boltovskoy D (2011) The introduced bivalve Limnoperna fortunei boosts Microcystis growth in Salto Grande reservoir (Argentina): evidence from mesocosm experiments. Hydrobiologia 680: 25–38, https://doi.org/10.1007/s10750-011-0897-8 Cataldo D, O’Farrell I, Paolucci E, Sylvester F, Boltovskoy D (2012) Impact of the invasive golden mussel (Limnoperna fortunei) on phytoplankton and nutrient cycling. Aquatic Invasions 7: 91–100, https://doi.org/10.3391/ai.2012.7.1.010 Cherry DS, Scheller JL, Cooper NL, Bidwell JR (2005) Potential effects of Asian clam (Corbicula fluminea) die-offs on native freshwater mussels (Unionidae) I: water-column ammonia levels and ammonia toxicity. Journal of North American Benthological Society 24: 369–380, https://doi.org/10.1899/04-073.1 Collas FPL, Koopman KR, Hendriks AJ, van der Velde G, Verbrugge LNH, Leuven RSEW (2014) Effects of desiccation on native and nonnative molluscs in rivers. Freshwater Biology 59: 41–55, https://doi.org/10.1111/fwb.12244 Cooper NL, Bidwell JR, Cherry DS (2005) Potential effects of Asian clam (Corbicula fluminea) die-offs on native freshwater mussels (Unionidae) II: porewater ammonia. Journal of North American Benthological Society 24: 381–394, https://doi.org/10.1899/04-074.1 Cope NJ, Winterbourn MJ (2004) Competitive interactions between two successful molluscan invaders of freshwaters: an experimental study. Aquatic Ecology 38: 83–91, https://doi.org/ 10.1023/B:AECO.0000021018.20945.9d Costa JI, Martins MIE, Ayroza DMMR (2017) Impact of control of the golden mussel on the production costs of tilapia bred in net cages. Boletim do Instituto de Pesca 44: 110–115, https://doi.org/10.20950/1678-2305.2018.284 Cowie RH (2001) Can snails ever be effective and safe biocontrol agents? International Journal of Pest Management 47: 23–40, https://doi.org/10.1080/09670870150215577 Cowie RH, Régnier C, Fontaine B, Bouchet P (2017) Measuring the Sixth Extinction: what do mollusks tell us? The Nautillus 131: 3–41 Crowl TA, Townsend CR, Mcintosh AR (1992) The impact of introduced brown and rainbow trout on native fish: the case of Australasia. Reviews in Fish Biology and Fisheries 2: 217–241, https://doi.org/10.1007/BF00045038 Darrigran GA, Maroñas ME, Colautti DC (2004) Air Exposure as a control mechanism for the golden mussel, Limnoperna fortunei, (Bivalvia: Mytilidae). Journal of Freshwater Ecology 19: 461–464, https://doi.org/10.1080/02705060.2004.9664920 Darrigran G, Damborenea C, Greco N (2007) An evaluation pattern for antimacrofouling procedures: Limnoperna fortunei Larvae study in a hydroelectric power plant in South America. Ambio 36: 575–579, https://doi.org/10.1579/0044-7447(2007)36[575:AEPFAP]2.0.CO;2 Davis MA, Chew MK (2017) ‘The denialists are coming!’ Well, not exactly: A response to Russell and Blackburn. Trends in Ecology & Evolution 32: 229–230, https://doi.org/10. 1016/j.tree.2017.02.008 Dudgeon D (1982) An investigation into some physical and biotic effects of flooding on reservoir mud previously subjected to a period of aerial exposure. Hydrobiologia 97: 27–35, https://doi.org/10.1007/BF00014957

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 468 Non-native molluscs in Brazilian reservoirs

Duggan IC (2010) The freshwater aquarium trade as a vector for incidental invertebrate fauna. Biological Invasions 12: 3757–3770, https://doi.org/10.1007/s10530-010-9768-x Duggan IC, Champion PD, MacIsaac HJ (2018) Invertebrates associated with aquatic plants bought from aquarium stores in Canada and New Zealand. Biological Invasions 20: 3167–3178, https://doi.org/10.1007/s10530-018-1766-4 Ernandes-Silva J, Ragonha FH, Rodrigues LC, Mormul RP (2016) Freshwater invasibility level depends on the population age structure of the invading mussel species. Biological Invasions 18: 1421–1430, https://doi.org/10.1007/s10530-016-1091-8 Facon B, Machline E, Pointier JP, David P (2004) Variation in desiccation tolerance in freshwater snails and its consequences for invasion ability. Biological Invasions 6: 283–293, https://doi.org/10.1023/B:BINV.0000034588.63264.4e Fearnside PM (1989) Brazil’s Balbina Dam: environment versus the legacy of the Pharaohs in Amazonia. Enviromental Management 13: 401–423, https://doi.org/10.1007/BF01867675 Fernandez MA, Thiengo SC, Simone LRL (2003) Distribution of the introduced freshwater snail Melanoides tuberculatus (Gastropoda: Thiaridae) in Brazil. The Nautilus 117: 78–82 Fernandez MA, Thiengo SC, Bezerra FSM, Alencar LMS (2010) Current distribution of the exotic freshwater snail Helisoma duryi (Gastropoda: Planorbidae) in Brazil. The Nautilus 124: 44–50 Fernandez MA, Mattos AC, Silva EF, Santos SB, Thiengo SC (2014) A malacological survey in the Manso Power Plant, State of Mato Grosso, Brazil: new records of freshwater snails, including transmitters of schistosomiasis and exotic species. Revista da Sociedade Brasileira de Medicina Tropical de São Paulo 47: 498–50, https://doi.org/10.1590/0037-8682- 0138-2014 Ferreira-Rodriguez N, Sousa R, Pardo I (2018) Negative effects of Corbicula fluminea over native freshwater mussels. Hydrobiologia 810: 85–95, https://doi.org/10.1007/s10750-016-3059-1 Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiologia 746: 23–37, https://doi.org/10.1007/s10750-014-2026-y França RS, Suriani AL, Rocha O (2007) Composição das espécies de moluscos bentônicos nos reservatórios do baixo rio Tietê (São Paulo, Brasil) com uma avaliação do impacto causado pelas espécies exóticas invasoras. Revista Brasileira de Zoologia 24: 41–51, https://doi.org/ 10.1590/S0101-81752007000100005 Frehse FA, Braga RR, Nocera GA, Vitule JRS (2016) Nonnative species and invasion biology in a megadiverse country: scientiometric analysis and ecological interactions in Brazil. Biological Invasions 18: 3713–3725, https://doi.org/10.1007/s10530-016-1260-9 Frehse F de A, De Andrade PDB, Vitule JRS (2018) Absence of the invasive golden mussel in a reservoir near Curitiba, Brazil: A possible case of invasion failure. Neotropical Biology and Conservation 13: 86–89, https://doi.org/10.4013/nbc.2018.131.10 Freitas JR, Bedê LC, Marco Jr. P, Rocha LA, Santos MBL (1987) Population dynamics of aquatic snails in Pampulha reservoir. Memórias do Instituto Oswaldo Cruz 82: 299–305, https://doi.org/10.1590/S0074-02761987000800057 Giovaneli A, Silva CLPAC, Leal GBE, Baptista DF (2005) Habitat preference of freshwater snails in relation to environmental factors and the presence of the competitor snail Melanoides tuberculatus (Müller, 1774). Memórias do Instituto Oswaldo Cruz 100: 169–176, https://doi.org/10.1590/S0074-02762005000200010 Godoy AC, Corrêia AF, Rodrigues RB, Boscolo WR, Bittencourt F, Nervis JAL, Feiden A (2018) Three native species as possible control for Limnoperna fortunei in net cage farming in the Itaipu Reservoir. Water Air Soil Pollution 229: 241, https://doi.org/10.1007/s11270-018- 3892-0 Havel JE, Lee CE, Zanden JV (2005) Do reservoirs facilitate invasions into landscapes? Bioscience 55: 518–525, https://doi.org/10.1641/0006-3568(2005)055[0518:DRFIIL]2.0.CO;2 Ilarri MI, Antunes C, Guilhermino L, Sousa R (2011) Massive mortality of the Asian clam Corbicula flumínea in a highly invaded area. Biological Invasions 13: 277–280, https://doi.org/10.1007/s10530-010-9833-5 Johnson LE, Ricciardi A, Carlton JT (2001) Overland dispersal of aquatic invasive species: a risk assessment of transient recreational boating. Ecological Applications 11: 1789–1799, https://doi.org/10.1890/1051-0761(2001)011[1789:ODOAIS]2.0.CO;2 Johnson PTJ, Olden JD, Zanden MJV (2008) Dam invaders: impoundments facilitate biological invasions into freshwaters. Frontiers in Ecology and the Environment 6: 357–363, https://doi.org/10.1890/070156 Johnson PTJ, Olden JD, Solomon CT, Zanden MJV (2009) Interactions among invaders: community and ecosystem effects of multiple invasive species in an experimental aquatic system. Oecologia 159: 161–170, https://doi.org/10.1007/s00442-008-1176-x Junk WJ, Cunha CN (2005) Pantanal: a large South American wetland at a crossroads. Ecological Engineering 24: 391–401, https://doi.org/10.1016/j.ecoleng.2004.11.012 Keller RP, Drake JM, Lodge DM (2007) Slow, but steady: dispersal of freshwater molluscs. Conservation Biology 21: 191–200, https://doi.org/10.1111/j.1523-1739.2006.00563.x Komaru A, Yamada M, Houki S (2013) Relationship Between Two Androgenetic Clam Species, Corbicula leana and Corbicula fluminea, Inferred from Mitochondrial cytochrome

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 469 Non-native molluscs in Brazilian reservoirs

b and Nuclear 28S rRNA Markers. Zoological Science 30: 360–365, https://doi.org/10.2108/ zsj.30.360 Kovacs EK, Crowther MS, Webb JK, Dickman CR (2012) Population and behavioural responses of native prey to alien predation. Oecologia 168: 947–957, https://doi.org/10.1007/ s00442-011-2168-9 Lacerda LEM, Richau CS, Amaral CRL, Silva DA, Carvalho EF, Barbosa SB (2015) Ferrissia fragilis (Tryon, 1863): a freshwater snail cryptic invader in Brazil revealed by morphological and molecular data. Aquatic Invasions 10: 157–168, https://doi.org/10.3391/ai.2015.10.2.04 Latini AO, Resende DC, Pombo VB, Coradin L (2016) Espécies exóticas invasoras de águas continentais no Brasil. Ministério do Meio Ambiente (MMA), Brasilia, Brazil, 791 pp Leme JLM (1966) Sobre a ocorrência do subgênero Physella no Brasil, e a descrição de uma nova espécie (Mollusca, Gastropoda). Papéis Avulsos de Zoologia 19: 269–278 Linares MS, Callisto M, Marques JC (2017) Invasive bivalves increase benthic communities complexity in neotropical reservoirs. Ecological Indicators 75: 279–285, https://doi.org/10. 1016/j.ecolind.2016.12.046 Lopes-Lima M, Teixeira A, Froufe E, Lopes A, Varandas S, Sousa R (2014) Biology and conservation of freshwater bivalves: past, present and future perspectives. Hydrobiologia 735: 1–13, https://doi.org/10.1007/s10750-014-1902-9 Lowry E, Rollinson EJ, Laybourn AJ, Scott TE, Aiello-Lammens ME, Gray SM, Mickley J, Gurevitch J (2013) Biological invasions: a field synopsis, systematic review, and database of the literature. Ecology and Evolution 3: 182–196, https://doi.org/10.1002/ece3.431 Lydeard C, Cowie RH, Ponder WF, Bogan AE, Bouchet P, Clarck SA, Cummings KS, Frest TJ, Gargominy O, Herbert DG, Hershler R, Perez KE, Roth B, Seddon M, Strong EE, Thompson FG (2004) The global decline of nonmarine mollusks. BioScience 54: 321–330, https://doi.org/10.1641/0006-3568(2004)054[0321:TGDONM]2.0.CO;2 Mansur MCD, Richinitti LMZ, Santos CP (1999) Limnoperna fortunei (Dunker, 1857), molusco bivalve invasor, na bacia do Guaíba, Rio Grande do Sul, Brasil. Biociências 7(2): 147–149 Mansur MCD, Santos CP, Darrigran G, Heydrich I, Callil CT, Cardoso FR (2003) Primeiros dados quali-quantitativos do mexilhão-dourado, Limnoperna fortunei (Dunker, 1857), no Delta do Jacuí, no Lago Guaíba e na Laguna dos Patos, Rio Grande do Sul, Brasil e alguns aspectos da invasão no novo ambiente. Revista Brasileira de Zoologia 20: 75–84, https://doi.org/10.1590/S0101-81752003000100009 Mansur MCD, Callil CT, Carodoso FR, Ibarra JAA (2004) Uma retrospectiva e mapeamento da invasão de espécies de Corbicula (Mollusca, Bivalvia, Veneroida, Corbiculidae) oriundas do sudeste Asiático, na América do Sul. In: Silva JSV, Souza RCCL (eds), Água de lastro e bioinvasão. Editora Interciência, Rio de Janeiro, pp 39–58 Mansur MCD, Santos CP, Richinitti LMZ, Pereira D, Batista CB, Silveira MB, Alberto RMF, Silva MCP (2008) Ocorrência de moluscos límnicos e crustáceo em macroaglomerados do mexilhão dourado, Limnoperna fortunei (Dunker, 1857) sobre sarandi no lago Guaíba (RS, Brasil). Biotemas 21: 179–182, https://doi.org/10.5007/2175-7925.2008v21n4p179 Mansur MCD, Pimpão DM, Bergonci PEA, Santos CP, Figueiredo GCS (2012) Morfologia e ciclo larval comparados de bivalves límnicos invasores e nativos. In: Mansur MCD, Santos CP, Pereira D, Paz ICP, Zurita MLL, Rodriguez MTR, Nehrke MV, Bergonci PEA (eds), Moluscos límnicos invasores no Brasil: biologia, prevenção e controle. Redes Editora, Porto Alegre, pp 95–110 Mariñelarena A, Donadelli J, Hechem M (2014) Cambios en las características limnológicas del embalse del Río Tercero por efecto de la invasión de Limnoperna fortunei (Bivalvia: Mytilidae). Biologia Acuática 30: 151–158 Martins DS, Veitenheimer-Mendes IL, Faccioni-Heuser MC (2006) Aspectos morfológicos e de incubação em três espécies de Corbicula Mühlfeld, no lago Guaíba, Rio Grande do Sul, Brasil (Bivalvia, Corbiculidae). Biota Neotropica 6: 1–11, https://doi.org/10.1590/S1676-06032 006000200016 Michelan TS, Silveira MJ, Petsch DK, Pinha GD, Thomaz SM (2014) The invasive aquatic macrophyte Hydrilla verticillata facilitates the establishment of the invasive mussel Limnoperna fortunei in Neotropical reservoirs. Journal of Limnology 73: 598–602, https://doi.org/10.4081/jlimnol.2014.909 Miyahira IC, Carneiro JB, Gonçalves ICB, Lacerda LEM, Oliveira JL, Vasconcelos MC, Santos SB (2017) Freshwater mollusks and environmental assessment of Guandu River, Rio de Janeiro, Brazil. Biota Neotropica 17: e20170342, https://doi.org/10.1590/1676-0611-bn-2017-0342 Olden JD, LeRoy Poff N, Douglas MR, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends in Ecology & Evolution 19: 18–24, https://doi.org/10.1016/j.tree.2003.09.010 Oliveira MD, Takeda AM, Barros LF, Barbosa DS, Resende EK (2006) Invasion by Limnoperna fortunei (Dunker, 1857) (Bivalvia, Mytilidae) of the Pantanal wetland, Brazil. Biological Invasions 8: 97–104, https://doi.org/10.1007/s10530-005-0331-0 Oliveira MD, Campos MCS, Paolucci EM, Mansur MCD, Hamilton SK (2015) Colonization and spread of Limnoperna fortunei in South America. In: Boltoskoy D (ed), Limnoperna fortunei - The Ecology, Distribution and Control of a Swiftly Spreading Invasive Fouling

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 470 Non-native molluscs in Brazilian reservoirs

Mussel. Springer International, Switzerland, pp 333–355, https://doi.org/10.1007/978-3-319- 13494-9_19 Padilla DK, Williams SL (2004) Beyond the ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and Environment 2: 131–138, https://doi.org/10.1890/1540-9295(2004)002[0131:BBWAAO]2.0.CO;2 Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Diversity and Distribution 19: 988– 995, https://doi.org/10.1111/ddi.12073 Paolucci EM, Leites V, Cataldo DH, Boltovskoy D (2017) Veligers of the invasive bivalve Limnoperna fortunei in the diet of indigenous fish larvae in a eutrophic subtropical reservoir. Austral Ecology 42: 759–771, https://doi.org/10.1111/aec.12493 Paraense WL (1987) Physa cubensis Pfeiffer, 1839 (Pulmonata: Physidae). Memórias do Instituto Oswaldo Cruz 82: 15–20, https://doi.org/10.1590/S0074-02761987000100003 Paschoal LRP, Andrade DP, Darrigran G (2015) How the fluctuations of water levels affect populations of invasive bivalve Corbicula fluminea (Müller, 1774) in a Neotropical reservoir? Brazilian Journal of Biology 75: 135–143, https://doi.org/10.1590/1519-6984.09113 Pelicice FM, Agostinho AA (2009) Fish fauna destruction after the introduction of a nonnative predator (Cichla kelberi) in a Neotropical reservoir. Biological Invasions 11: 1789–1801, https://doi.org/10.1007/s10530-008-9358-3 Pereira D, Mansur MCD, Pimpão DM (2012) Identificação e diferenciação dos bivalves límnicos invasores dos demais bivalves nativos do Brasil. In: Mansur MCD, Santos CP, Pereira D, Paz ICP, Zurita MLL, Rodriguez MTR, Nehrke MV, Bergonci PEA (eds), Moluscos límnicos invasores no Brasil: biologia, prevenção e controle. Redes Editora, Porto Alegre, Brazil, pp 75–94 Pereira D, Mansur MCD, Duarte LDS, Oliveira AS, Pimpão DM, Callil CT, Ituarte C, Parada E, Peredo S, Darrigran G, Scarabino F, Clavijo C, Lara G, Miyahira IC, Rodriguez MTR, Lasso C (2014) Bivalve distribution in hydrographic regions in South America: historical overview e conservation. Hydrobiologia 735: 15–44, https://doi.org/10.1007/s10750-013-1639-x Pereira LS, Agostinho AA, Gomes LC (2015) Eating the competitor: a mechanism of invasion. Hydrobiologia 746: 223–231, https://doi.org/10.1007/s10750-014-2031-1 Pereira LS, Neves RAF, Miyahira IC, Kozlowsky-Suzuki B, Castelo Branco CW, Paula JC, Santos LN (2018) Non-native species in reservoirs: how are we doing in Brazil? Hydrobiologia 817: 71–84, https://doi.org/10.1007/s10750-017-3446-2 Pigneur LM, Marescaux J, Roland K, Etoundi E, Descy JP, van Donick K (2011) Phylogeny and androgenesis in the invasive Corbicula clams (Bivalvia, Corbiculidae) in Western Europe. BMC Evolutionary 11: 147, https://doi.org/10.1186/1471-2148-11-147 Pigneur LM, Falisse E, Roland K, Everbecq E, Deliège J, Smitz JS, Doninck K, Descy J (2014) Impact of invasive Asian clams, Corbicula spp., on a large river ecosystem. Freshwater Biology 59: 573–583, https://doi.org/10.1111/fwb.12286 Pimpão DM, Martins DS (2008) Ocorrência do molusco asiático Corbicula fluminea (Müller, 1774) (Bivalvia, Corbiculidae) no baixo rio Negro, Amazônia central. Acta Amazonica 38: 589–592, https://doi.org/10.1590/S0044-59672008000300026 Pointier JP, Guyard A, Mosser A (1989) Biological control of Biomphalaria glabrata and B. straminea by the competitor Thiara tuberculata in a transmission site of schistomiasis in Martinique, French West Indies. Annals of Tropical Medicine and Parasitology 83: 263–269, https://doi.org/10.1080/00034983.1989.11812342 Prezant RS, Chalermwat K (1984) Floating of the bivalve Corbicula fluminea as a means of dispersal. Science 225: 1491–1493, https://doi.org/10.1126/science.225.4669.1491 Quiroz CL, Pauchard A, Cavieres LA, Anderson C (2009) Análisis cuantitativo de la investigación em invasiones biológicas en Chile: tendências y desafíos. Revista Chilena de Historia Natural 82: 497–505, https://doi.org/10.4067/S0716-078X2009000400005 R Core Team (2019) R: A Language and Environment for Statistical Computing. https://www.R- project.org/ Régnier C, Achaz G, Lambert A, Cowie RH, Bouchet P, Fontaine B (2015) Mass extinction in poorly known taxa. PNAS 112: 7761–7766, https://doi.org/10.1073/pnas.1502350112 Rocha O, Espíndola ELG, Rietzler AC, Fenerich-Verani N, Verani JR (2011) Animal invaders in São Paulo state reservoirs. Oecologia Australis 15: 631–642, https://doi.org/10.4257/oeco. 2011.1503.14 Salo P, Korpimaki E, Banks PB, Nordstrom M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proceedings of the Royal Society B 274: 1237–1243, https://doi.org/10.1098/rspb.2006.0444 Santos SB, Thiengo SC, Fernandez MA, Miyahira IC, Gonçalves IC, Ximenes RF, Mansur MCD, Pereira D (2012) Espécies de moluscos límnicos invasores no Brasil. In: Mansur MCD, Santos CP, Pereira D, Paz ICP, Zurita MLL, Rodriguez MTR, Nehrke MV, Bergonci PEA (eds), Moluscos límnicos invasores no Brasil: biologia, prevenção e controle. Redes Editora, Porto Alegre, Brazil, pp 25–49 Simberloff D (2005) Non-native species DO threaten the natural environment! Journal of Agricultural and Environmental Ethics 18: 595–607, https://doi.org/10.1007/s10806-005-2851-0

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 471 Non-native molluscs in Brazilian reservoirs

Spaccesi FG, Capítulo R (2012) Benthic communities on hard substrates covered by Limnoperna fortunei Dunker (Bivalvia, Mytilidae) at an estuarine beach (Río de la Plata, Argentina). Journal of Limnology 71: 144–153, https://doi.org/10.4081/jlimnol.2012.e15 Suriani AL, França RS, Rocha O (2007) A malacofauna bentónica das represas do médio rio Tietê (São Paulo, Brasil) e uma avaliação ecológica das espécies exóticas invasoras, Melanoides tuberculata (Müller, 1774) e Corbicula fluminea (Müller, 1774). Revista Brasileira de Zoologia 24: 21–32, https://doi.org/10.1590/S0101-81752007000100003 Taylor DW (2003) Introduction to Physidae (Gastropoda: Hygrophila); biogeography, classification, morphology. Revista de Biologia Tropical 51: 1–263 Thiengo SC, Santos SB, Fernandez MA (2005) Malacofauna límnica da área de influência do lago da usina hidrelétrica de Serra da Mesa, Goiás, Brasil. I. Estudo qualitativo. Revista Brasileira de Zoologia 22: 867–874, https://doi.org/10.1590/S0101-81752005000400010 Thiengo SC, Silva EF, Leal RSL, Esteves RA, Fernadez MA (2017) Major water projects and the dispersal of alien molluscs: the São Francisco River large-scale water transposition project in the semi-arid Northeast region of Brasil. Tentacle 25: 11–14 Thomaz SM, Mormul RP, Michelan TS (2015) Propagule pressure, invasibility of freshwater ecosystems by macrophytes and their ecological impacts: a review of tropical freshwater ecosystems. Hydrobiologia 746: 39–59, https://doi.org/10.1007/s10750-014-2044-9 Vaz JF, Teles HMS, Correa MA, Leite SPS (1986) Ocorrência no Brasil de Thiara (Melanoides) tuberculata (O.F. Müller, 1774) (Gastropoda, Prosobranchia), primeiro hospedeiro intermediário de Clonorchis sinensis (Cobbold, 1875) (Trematoda, Plathyhelmintes). Revista de Saúde Pública 20: 318–322, https://doi.org/10.1590/S0034-89101986000400008 Vieira I, Darwich AJ (1999) Sinecologia da ictiofauna de Curuá-Uma, Amazônia: características hidroquímicas, climáticas, vegetação e peixes. Acta Limnologica Brasiliensia 11: 41–64 Vitule JRS, Freire CA, Simberloff D (2009) Introduction of non-native freshwater fish can certainly be bad. Fish and Fisheries 10: 98–108, https://doi.org/10.1111/j.1467-2979.2008.00312.x Vogler RE, Beltramino AA, Strong EE, Peso JG, Rumi A (2015) A phylogeopgraphical perspective on the ex situ conservation of Aylacostoma (Thiaridae, Gastropoda) from High Paraná River (Argentina-Paraguay). Zoological Journal of the Linnean Society 174: 487–499, https://doi.org/10.1111/zoj.12250 Vogler RE, Beltramino AA, Strong EE, Rumi A, Peso JG (2016) Insights into the evolutionary history of an extinct South American freshwater snail based on historical DNA. PLoS ONE 11: e0169191, https://doi.org/10.1371/journal.pone.0169191 Way CM, Hombach DJ, Miller-Way CA, Payne BS, Miller AC (1990) Dynamics of filter feeding in Corbicula fluminea (Bivalvia: Corbiculidae). Canadian Journal of Zoology 68: 115–120, https://doi.org/10.1139/z90-016 Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York, USA, https://doi.org/10.1007/978-3-319-24277-4_9 Winemiller KO, McIntyre PB, Castello L, Fluet-Chouinard E, Giarrizzo T, Nam S, Baird IG, Darwall W, Lujan NK, Harrison I, Stiassny MLJ, Silvano RAM, Fitzgerald DB, Pelicice FM, Agostinho AA, Gomes LC, Albert JS, Baran E, Petrere Jr. M, Zarfl C, Mulligan M, Sullivan JP, Arantes CC, Sousa LM, Koning AA, Hoeinghaus DJ, Sabaj M, Lundberg JG, Armbruster J, Thieme ML, Petry P, Zuanon J, Torrente Vilara G, Snoeks J, Ou C, Rainboth W, Pavanelli CS, Akama A, van Soesbergen A, Sáenz L (2016) Balancing hydropower and biodiversity in the Amazon, Congo, and Mekong. Science 351: 128–129, https://doi.org/10. 1126/science.aac7082 Yakovleva AV, Yakovlev (2010) Modern fauna and quantitative parameters of invasive invertebrates in zoobenthos of upper reaches of the Kuybyshev Reservoir, Russia. Russian Journal of Biological Invasions 1: 232–241, https://doi.org/10.1134/S2075111710030161 Zinchenko TD, Kurina EM (2011) Distributional patterns of alien species in the open shallow areas of the Saratov Reservoir. Russian Journal of Biological Invasions 2: 183–190, https://doi.org/10.1134/S2075111711030209 Zukowski S, Walker KF (2009) Freshwater snails in competition: alien Physa acuta (Physidae) and native Glyptophysa gibbosa (Planorbidae) in the River Murray, South Australia. Marine and Freshwater Research 60: 999–1005, https://doi.org/10.1071/MF08183

Supplementary material The following supplementary material is available for this article: Table S1. Occurrences of non-native molluscs in reservoirs of Brazil. Appendix 1. General information on the Supplementary material. Appendix 2. References for Table S1. This material is available as part of online article from: http://www.reabic.net/aquaticinvasions/2020/Supplements/AI_2020_Miyahira_etal_SupplementaryMaterial.xlsx

Miyahira et al. (2020), Aquatic Invasions 15(3): 455–472, https://doi.org/10.3391/ai.2020.15.3.06 472