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Distribution of invasive bivalves in Paraguay: filling the gaps in the heart of South America

Distribuição de bivalves invasores no Paraguai: preenchendo as lacunas no coração da América do Sul

Abstracts

Abstract

La Plata Basin is the second largest hydrographic system in South America but the most impacted by invasive species of molluscs in the continent. Paraguay is a land-surrounded South American country with scarce information about malacological fauna. To fill some of these gaps, a large field expedition was conducted to analyze the distribution of invasive freshwater bivalves in Paraguay. The field survey encompassed 41 sampling stations in seven Departments of Paraguay. The mussels were searched using bare hands and feet. All stations were georeferenced and some environmental parameters were measured. Results indicated the presence of three invasive species of freshwater bivalves in Paraguay: Corbicula fluminea, C. largillierti, and Limnoperna fortunei. The Asiatic clam Corbicula fluminea was the most widespread invasive species, covering main rivers and small tributaries in the four freshwater ecoregions of Paraguay. The two remaining invasive species were more restricted. Corbicula largillierti were found at the lower section of the Paraná River, and Limnoperna fortunei inhabits the main river canals of the Paraguay River and the lower section of the Paraná River. The invasive species were found in three protected areas of Paraguay and can represent a threat to the mostly unknown fauna of native mussels. The invasive bivalves are widespread in Paraguay. Mitigation measurements must be taken to avoid the spread of these species and more drawbacks over native fauna.

Keywords:
South America; La Plata Basin; Paraguay; Limnoperna; Corbicula


Resumo

A bacia do Plata é a segunda maior da América do Sul, mas a mais impactada pelas espécies invasoras de moluscos nesse continente. O Paraguai é uma país cercado por terra com pouca informação sobre a sua malacofauna. Com o objetivo de preencher algumas destas lacunas, uma expedição de campo foi organizada a fim de analisar a distribuição dos bivalves invasores no Paraguai. Foram realizadas 41 estações de coleta em sete departamentos do Paraguai. A busca pelos bivalves foi feita utilizando pés e mãos. Todos os pontos foram georreferenciados e algumas variáveis ambientais foram medidas. Os resultados indicam a presença de três espécies de bivalves invasores no Paraguai: Corbicula fluminea, C. largillierti e Limnoperna fortunei. O berbigão asiático Corbicula fluminea foi a espécie com a distribuição mais ampla, cobrindo os principais rios e tributários, em quatro ecoregiões de água doce do Paraguai. As outras duas espécies apresentaram uma distribuição mais restrita. Corbicula largillierti foi encontrado no Baixo rio Paraná, enquanto Limnoperna fortunei foi encontrado na calha principal do rio Paraguai e no Baixo rio Paraná. As espécies invasoras foram encontradas em três unidades de conservação e pode representar a ameaça para a pouco conhecida fauna de bivalves nativos do Paraguai. As espécies de bivalves invasores estão amplamente distribuídas no Paraguai. Medidas de mitigação são necessárias para evitar que estas espécies se dispersem ainda mais, provocando mais efeitos negativos sobre as espécies nativas.

Palavras-chave:
América do Sul; Bacia do Río de La Plata; Paraguai; Limnoperna; Corbicula


Paraguay is a landlocked country with a central position in South America, and two main rivers of the La Plata Basin run through the country: Paraná and Paraguay rivers. This is the second-largest basin in South America and harbors an important molluscan fauna (Strong et al., 2008Strong, E.E., Gargominy, O., Ponder, W.F., & Bouchet, P., 2008. Global diversity of gastropods (Gastropoda; Mollusca) in freshwater. Hydrobiologia 595(1), 149-166. http://dx.doi.org/10.1007/s10750-007-9012-6.
http://dx.doi.org/10.1007/s10750-007-901...
; Pereira et al., 2014Pereira, D., Mansur, M.C.D., Duarte, L.D.S., Oliveira, A.S., Pimpão, D.M., Callil, C.T., Ituarte, C., Parada, E., Peredo, S., Darrigran, G., Scarabino, F., Clavijo, C., Lara, G., Miyahira, I.C., & Lasso, C., 2014. Bivalve distribution in hydrographic regions in South America: historical overview and conservation. Hydrobiologia 735(1), 15-44. http://dx.doi.org/10.1007/s10750-013-1639-x.
http://dx.doi.org/10.1007/s10750-013-163...
; Cuezzo et al., 2020Cuezzo, M.G., Gregoric, D.E.G., Pointier, J.P., Vázquez, A.A., Ituarte, C., Mansur, M.C.D., Arruda, J.O., Baker, G., Santos, S.B., Ovando, X.M., Fernandez, M.A., Thiengo, S.C., Mattos, A.C., Silva, E.F., Berning, M.I., Collado, G.A., Miyahira, I.C., Antoniazzi, T.N., Pimpão, D.M., & Damborenea, C., 2020. Phylum Mollusca. In: Damborenea, C., Rogers, D.C. & Thorp, J.H., eds. Thorp and Covich’s Freshwater Invertebrates. London: Academic Press, 261-430, 4 ed., vol. 5: Keys to Neotropical and Antartic Fauna. http://dx.doi.org/10.1016/B978-0-12-804225-0.00011-3.
http://dx.doi.org/10.1016/B978-0-12-8042...
). A total of 16 freshwater species of molluscs were reported as non-native from South America by Darrigran et al. (2020)Darrigran, G., Agudo-Padrón, I., Baez, P., Belz, C., Cardoso, F., Carranza, A., Collado, G., Correoso, M., Cuezzo, M.G., Fabres, A., Gregoric, D.E., Letelier, S., Ludwig, S., Mansur, M.C.D., Pastorino, G., Penchaszadeh, P., Peralta, C., Rebolledo, A., Rumi, A., Santos, S., Thiengo, S., Vigidal, T., & Damborenea, C., 2020. Non-native mollusks throughout South America: emergent patterns in an understudied continent. Biol. Invasions 22(3), 853-871. http://dx.doi.org/10.1007/s10530-019-02178-4.
http://dx.doi.org/10.1007/s10530-019-021...
. These authors reported the presence of seven non-native species in the La Plata Basin, from which were highlighted Corbicula fluminea (Müller, 1774), the Asiatic clam; and Limnoperna fortunei (Dunker, 1857), the golden mussel. Corbicula species arrived in South America in the 1970s and Limnoperna fortunei some years later (around the 1990s), both are widespread now (Darrigran et al., 2020Darrigran, G., Agudo-Padrón, I., Baez, P., Belz, C., Cardoso, F., Carranza, A., Collado, G., Correoso, M., Cuezzo, M.G., Fabres, A., Gregoric, D.E., Letelier, S., Ludwig, S., Mansur, M.C.D., Pastorino, G., Penchaszadeh, P., Peralta, C., Rebolledo, A., Rumi, A., Santos, S., Thiengo, S., Vigidal, T., & Damborenea, C., 2020. Non-native mollusks throughout South America: emergent patterns in an understudied continent. Biol. Invasions 22(3), 853-871. http://dx.doi.org/10.1007/s10530-019-02178-4.
http://dx.doi.org/10.1007/s10530-019-021...
; Miyahira et al., 2020Miyahira, I.C., Pereira, L.S., & dos Santos, L.N., 2020. Non-native freshwater molluscs in the Neotropics: what can be learned from Brazilian reservoirs? Aquat. Invasions 15(3), 455-472. http://dx.doi.org/10.3391/ai.2020.15.3.06.
http://dx.doi.org/10.3391/ai.2020.15.3.0...
; Hermes-Silva et al., 2021Hermes-Silva, S., Ribolli, J., Ávila-Simas, S.D., Zaniboni-Filho, E., Cardoso, G.F.M., & Nuñer, A.P.D.O., 2021. Limnoperna fortunei-Updating the geographic distribution in the Brazilian watersheds and mapping the regional occurrence in the Upper Uruguay River basin. Biota Neotrop. 21(3), e20201175. http://dx.doi.org/10.1590/1676-0611-bn-2020-1175.
http://dx.doi.org/10.1590/1676-0611-bn-2...
). Invasive species can promote modification of environmental and biological aspects of the invaded habitat (e.g., Darrigran & Damborenea, 2011Darrigran, G., & Damborenea, C., 2011. Ecosystem engineering impacts of Limnoperna fortunei in South America. Zool. Sci. 28(1), 1-7. PMid:21186940. http://dx.doi.org/10.2108/zsj.28.1.
http://dx.doi.org/10.2108/zsj.28.1...
; Sousa et al., 2014Sousa, R., Novais, A., Costa, R., & Strayer, D.L., 2014. Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735(1), 233-251. http://dx.doi.org/10.1007/s10750-012-1409-1.
http://dx.doi.org/10.1007/s10750-012-140...
; Boltovskoy & Correa, 2015Boltovskoy, D., & Correa, N., 2015. Ecosystem impacts of the invasive bivalve Limnoperna fortunei (golden mussel) in South America. Hydrobiologia 746(1), 81-95. http://dx.doi.org/10.1007/s10750-014-1882-9.
http://dx.doi.org/10.1007/s10750-014-188...
), affecting not only native molluscs, but also other taxonomic groups. Understanding the distribution of invasive species is the first step to proposing strategies to mitigate the negative impacts.

Main reports of molluscs from Paraguay were done several years ago by Schade (1965)Schade, F.H., 1965. Lista de los moluscos del Guaíra (Villarica - Paraguay) conocidos hasta la presente. Comun Soc. Malacol. Urug. 7(62-63), 209-221. and Quintana (1982)Quintana, M.G., 1982. Catálogo preliminar de la malacofauna del Paraguay. Rev. Mus. Argent. Cienc. Nat. Zoologia 11(3), 61-158. and were before the arrival of invasive species in the country. The Paraguayan territory is a gap in the malacological information of South America. Corbicula spp. and L. fortunei were first recorded in the Paraguay River during the 1990s (Callil & Mansur, 2002Callil, C.T., & Mansur, M.C.D., 2002. Corbiculidae in the Pantanal: history of invasion in southeast and central South America and biometrical data. Amazoniana 17(1-2), 153-167.; Oliveira et al., 2006Oliveira, M.D., Takeda, A.M., de Barros, L.F., Barbosa, D.S., & de Resende, E.K., 2006. Invasion by Limnoperna fortunei (Dunker, 1857) (Bivalvia, Mytilidae) of the Pantanal wetland, Brazil. Biol. Invasions 8(1), 97-104. http://dx.doi.org/10.1007/s10530-005-0331-0.
http://dx.doi.org/10.1007/s10530-005-033...
), and there are few records of invasive bivalves in the country, most of them from areas shared with Argentina or Brazil (Peso et al., 2011Peso, J.G., Pérez, D.C., & Vogler, R.E., 2011. The invasive snail Melanoides tuberculata in Argentina and Paraguay. Limnologica 41(4), 281-284. http://dx.doi.org/10.1016/j.limno.2010.12.001.
http://dx.doi.org/10.1016/j.limno.2010.1...
; Oliveira et al., 2015Oliveira, M.D., Campos, M.C., Paolucci, E.M., Mansur, M.C., & Hamilton, S.K., 2015. Colonization and spread of Limnoperna fortunei in South America. In: Boltovskoy, D., ed. Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Switzerland: Springer International, 333-355, 1 ed.; Hermes-Silva et al., 2021Hermes-Silva, S., Ribolli, J., Ávila-Simas, S.D., Zaniboni-Filho, E., Cardoso, G.F.M., & Nuñer, A.P.D.O., 2021. Limnoperna fortunei-Updating the geographic distribution in the Brazilian watersheds and mapping the regional occurrence in the Upper Uruguay River basin. Biota Neotrop. 21(3), e20201175. http://dx.doi.org/10.1590/1676-0611-bn-2020-1175.
http://dx.doi.org/10.1590/1676-0611-bn-2...
). A comprehensive revision of the golden mussel invasion in La Plata Basin was done recently by Oliveira et al. (2015)Oliveira, M.D., Campos, M.C., Paolucci, E.M., Mansur, M.C., & Hamilton, S.K., 2015. Colonization and spread of Limnoperna fortunei in South America. In: Boltovskoy, D., ed. Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Switzerland: Springer International, 333-355, 1 ed. and Ludwig et al. (2021)Ludwig, S., Sari, E.H.R., Paixão, H., Montresor, L.C., Araújo, J., Alves de Brito, C., Darrigran, G., Pepato, A.P., Barreira Martinez, C., & Vidigal, T.H.D.A., 2021. High connectivity and migration potentiate the invasion of Limnoperna fortunei (Mollusca: Mytilidae) in South America. Hydrobiologia 842(2), 499-513. http://dx.doi.org/10.1007/s10750-020-04458-w.
http://dx.doi.org/10.1007/s10750-020-044...
, however, with scarce records from Paraguay and several occurrences upstream (Brazil) and downstream (Brazil, Argentina and Uruguay). Thus, there are records upstream and downstream to Paraguay, but any in Paraguayan area. Moreover, the understanding of the invasion process of bivalves in the La Plata Basin was probably biased due this lack of information.

The main goal of this study was to present an updated distribution of invasive bivalves in Paraguay, relying on new records and museum data, relating this to freshwater and terrestrial ecoregions, as also presenting physical and environmental variables (pH, conductivity, TDS). The occurrence of invasive species in protected areas are discussed, and comments on the possible impacts of invasive on native species.

The records of invasive bivalves came from a recent field expedition conducted in Paraguay (September 2021). The field surveys encompassed 41 collecting stations, in seven Departments (Concepción, Guairá, Misiones, Ñeembucú, Paraguari, Presidente Hayes and San Pedro) and the Capital District (Asunción), where bivalves were searched using bare hands and feet. Almost all surveyed sites were never sampled before for freshwater mussels. At all collecting stations, georeferenced coordinates were obtained using a GPS Garmin 64s; and conductivity, pH and TDS (Total Dissolved Solids) using a Hanna HI98129 Multiparameter. Following Brasil (1997)Brasil, 1997. Plano de Conservação da Bacia do Alto Paraguai (PCBAP) - Pantanal. Diagnóstico do Meio Físico e Biótico. Brasilia: Ministério do Meio Ambiente, dos Recursos Hídricos e da Amazônia Legal., the Paraguay River can be divided into three parts, Upper Paraguay from the headwaters to Jauru River; Middle Paraguay from Cáceres (state of Mato Grosso, Brazil) to Apa River (border of Brazil and Paraguay); and Lower Paraguay from Apa River to the mouth at Paraná River (border of Paraguay and Argentina). All collecting stations at Paraguay River Basin were carried out at the lower part of the basin but covered an important portion of Paraguay, including tributaries from the western and eastern regions of the country. There is scarce information about native freshwater mussels of Paraguay, but based in this piece of information, the sampled area can be pointed as a high diversity area (Schade, 1965Schade, F.H., 1965. Lista de los moluscos del Guaíra (Villarica - Paraguay) conocidos hasta la presente. Comun Soc. Malacol. Urug. 7(62-63), 209-221.; Quintana, 1982Quintana, M.G., 1982. Catálogo preliminar de la malacofauna del Paraguay. Rev. Mus. Argent. Cienc. Nat. Zoologia 11(3), 61-158.). The data from field surveys were complemented with a review from the collection of the Museo Nacional de Historia Natural del Paraguay.

The study was carried out with the authorization of the Ministerio del Ambiente y Desarrollo Sostenible of Paraguay (Permission number 028/2021) and all the specimens obtained were deposited at the Invertebrates Collection of the Museo Nacional de Historia Natural del Paraguay under field trip code PY-21-01 to PY-21-40.

Paraguay is divided into four freshwater ecoregions (Abell et al., 2008Abell, R., Thieme, M., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Contreras-Balderas, S., Bussing, W., Stiassny, M.L.J., Skelton, P., Allen, G.R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J., Heibel, T.J., Wikramanayake, E., Olson, D., López, H.L., Reis, R.E., Lundberg, J.G., Sabaj Perez, M.H., & Petry, P., 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58(5), 403-414. http://dx.doi.org/10.1641/B580507.
http://dx.doi.org/10.1641/B580507...
) and these were used for analyzing the invasive species distribution. The Paraguay River divides the country on a north-south axis, at the West, one large ecoregion (Chaco) that drain a huge dry area, and in the East, a more humid area with perennial rivers (Paraguay, Lower Paraná and Upper Paraná ecoregions) (Abell et al., 2008Abell, R., Thieme, M., Revenga, C., Bryer, M., Kottelat, M., Bogutskaya, N., Coad, B., Mandrak, N., Contreras-Balderas, S., Bussing, W., Stiassny, M.L.J., Skelton, P., Allen, G.R., Unmack, P., Naseka, A., Ng, R., Sindorf, N., Robertson, J., Armijo, E., Higgins, J., Heibel, T.J., Wikramanayake, E., Olson, D., López, H.L., Reis, R.E., Lundberg, J.G., Sabaj Perez, M.H., & Petry, P., 2008. Freshwater ecoregions of the world: a new map of biogeographic units for freshwater biodiversity conservation. Bioscience 58(5), 403-414. http://dx.doi.org/10.1641/B580507.
http://dx.doi.org/10.1641/B580507...
; Koerber et al., 2017Koerber, S., Vera-Alcaraz, H.S., & dos Reis, R.E., 2017. Checklist of the fishes of Paraguay (CLOFPY). Ichthyological Contrib. Peces Criollos 53, 1-99.). We also analyzed the distribution of bivalves in terrestrial ecoregions (Olson et al., 2001Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., D’Amico, J.A., Itoua, I., Strand, H.E., Morrison, J.C., Loucks, T., Allnutt, C.J.F., Ricketts, T.H., Kura, Y., Lamoreux, J.F., Wettengel, W.W., Hedao, P., & Kassem, K.R., 2001. Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51(11), 933-938. http://dx.doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2.
http://dx.doi.org/10.1641/0006-3568(2001...
), which retain some information about the nearby environment. There are five main terrestrial ecoregions in Paraguay: Cerrado, Dry Chaco, Upper Paraná Atlantic Forest, Pantanal and Humid Chaco. There are also small portions of the Paraná flooded savanna and Southern Cone Mesopotamian savanna that was considered along with the surrounding Humid Chaco in our analysis. The terrestrial ecoregions were also evaluated because add different division of Paraguayan territory that bring environmental information that cannot be perceived at freshwater ecoregions analysis. The georeferenced data of protected areas in Paraguay were obtained from World Database on Protected Areas (WDPA, 2021World Database on Protected Areas - WDPA, 2021. Protected Planet: The World Database on Protected Areas (WDPA) and World Database on Other Effective Area-based Conservation Measures (WD-OECM) [online]. Cambridge: UNEP-WCMC and IUCN. Retrieved in 2021, November 5, from www.protectedplanet.net
www.protectedplanet.net...
). The percentage of invasive species occurrences was calculated with a 1km buffer around each occurrence to discount any inaccuracy in the GPS measurements.

Three non-native invasive bivalves species were found in Paraguay, two species of Asiatic clams, Corbicula fluminea and C. largillierti; and the golden mussel, Limnoperna fortunei (Figure 1). The invasive species occurred in 33 localities (21 from field survey and 12 from museum collection), and in 20 localities no invasive bivalves were found (Figure 2A-C). Only C. fluminea was found at the museum survey, the other two species were found at field survey.

Figure 1
. Invasive bivalves in Paraguay. A - Clusters of Limnoperna fortunei in an exposed rock. B - Specimen of Corbicula fluminea collected in Paraguay. Scale bar = 1cm.
Figure 2
. Distribution of invasive bivalves in Paraguay. The circles are the records from sampled sites and the squares the records from the Museo Nacional de Historia Natural del Paraguay. A - Freshwater ecoregions, B - Terrestrial ecoregions, C - Protected areas.

Corbicula fluminea was the species with wider distribution, occurring in 33 localities and all four freshwater ecoregions of Paraguay (Chaco, Paraguay, Upper Paraná and Lower Paraná). The other Asiatic clam, C. largillierti, occurred in one locality in the Lower Paraná ecoregion. Limnoperna fortunei occurred in six localities in three freshwater ecoregions (Chaco, Lower Paraná and Paraguay) (Figure 2A). The invasive bivalves occurred together six times, always with the combination of Corbicula fluminea and Limnoperna fortunei in sympatry, except for one locality where the three invasive bivalves occurred together (Table 1).

Table 1
Species of invasive bivalves found occurring in sympatry in Paraguay.

Considering terrestrial ecoregions of Paraguay, there were 31 records of invasive bivalves at Humid Chaco (24 of Corbicula fluminea, one of C. largillierti and six of Limnoperna fortunei), eight at Upper Paraná Atlantic forests (C. fluminea) and one at Cerrado (C. fluminea). The field survey did not include areas of Pantanal and Dry Chaco ecoregions, however, we revised local museum specimens and found no records from these regions at Museo Nacional de Historia Natural de Paraguay (Figure 2B).

Invasive bivalves occurred in three protected areas of Paraguay. In the protected area Carrizales del Paraná National Park the three invasive bivalves (Corbicula fluminea, C. largillierti and Limnoperna fortunei) were recorded in two sites (south of Paraguay; coordinates in Table 1); in the Ecological Reserve Banco San Miguel y Bahía de Asunción (on the banks of Paraguay River in Asunción; -25.271149, -57.618595), and in the Managed Resources Reserve Lago Ypacaraí y el sistema de humedales adyacentes were found the species C. fluminea in two sites (near Asunción; -25.153036, -57.382539 and -25.252658, -57.341042) (Figure 2C).

Corbicula fluminea was more flexible in environmental preferences, occurring in waters with a lower pH, and also with higher conductivity and TDS (Table 2).

Table 2
Environmental variables range in the site with invasive bivalves in Paraguay, except for C. largillierti which occurred in one area.

Previous data only included some scattered records in the rivers shared with nearby countries (mainly Brazil and Argentina), with the contribution of this manuscript the distribution of invasive bivalves in Paraguay is now more detailed, with new records inside the country, including large rivers and small tributaries. Most of the records were to the east of Paraguay River, except by two sites in Confuso River near to the mouth of this river in Paraguay River. The gap in invasive species distribution in Paraguay is not a real absence of these species, but a lack of sampling effort. The works done before in Paraguay were isolated efforts (Schade, 1965Schade, F.H., 1965. Lista de los moluscos del Guaíra (Villarica - Paraguay) conocidos hasta la presente. Comun Soc. Malacol. Urug. 7(62-63), 209-221.; Quintana, 1982Quintana, M.G., 1982. Catálogo preliminar de la malacofauna del Paraguay. Rev. Mus. Argent. Cienc. Nat. Zoologia 11(3), 61-158.) and was never established continuous research in malacology at Paraguay. Therefore, the recent records of invasive species at Paraguay were done at the borders (e.g. Oliveira et al., 2015Oliveira, M.D., Campos, M.C., Paolucci, E.M., Mansur, M.C., & Hamilton, S.K., 2015. Colonization and spread of Limnoperna fortunei in South America. In: Boltovskoy, D., ed. Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Switzerland: Springer International, 333-355, 1 ed.). Our records indicate that invasive bivalves were also widespread in this part of the La Plata Basin which corresponds to the lower portion of the Paraguay River.

The occurrence of invasive species was concentrated at the east of the Paraguay River. The large freshwater ecoregion of Chaco dominates the area west of the Paraguay River, and despite the sampling effort in our survey was concentrated at south (Humid Chaco), is probably that this ecoregion is really poor in bivalve occurrences. We raise this hypothesis considering that the collecting stations done by us at the south portion of the freshwater ecoregion of Chaco returned no invasive bivalves (Figure 2A-B). The north portion of Chaco (which corresponds to the terrestrial ecoregion of Dry Chaco) was an area not sampled by us, however, data from the literature indicates that the environmental conditions became even harsher (Lemenkova, 2021Lemenkova, P., 2021. Comparative analysis of climate and topography in Chaco and Oriental, Paraguay. Cad. Geogr. 31(66), 865-888. http://dx.doi.org/10.5752/P.2318-2962.2021v31n66p865.
http://dx.doi.org/10.5752/P.2318-2962.20...
) and suggests to us that should be unsuitable for most invasive bivalves. Although can be possible to find some species of Sphaeriidae that resist extreme dry climates (e.g., Vila et al., 2020Vila, I., Hermosilla, V., Gonzalez, F., Sobarzo, G., & Rojas, P., 2020. Macroinvertebrate community structure in an extreme altiplanic environment from Chile: the Ascotán salt pan. Glob. Ecol. Conserv. 24, e01260. http://dx.doi.org/10.1016/j.gecco.2020.e01260.
http://dx.doi.org/10.1016/j.gecco.2020.e...
), this is not usual for invasive bivalves (i.e. Corbicula and Limnoperna) and large native freshwater mussels (Unionida). Guareschi & Wood (2020)Guareschi, S., & Wood, P.J., 2020. Exploring the desiccation tolerance of the invasive bivalve Corbicula fluminea (Müller 1774) at different temperatures. Biol. Invasions 22(9), 2813-2824. http://dx.doi.org/10.1007/s10530-020-02291-9.
http://dx.doi.org/10.1007/s10530-020-022...
showed a massive die-off of C. fluminea in water temperatures higher than 25°C. Limnoperna fortunei can survive in higher temperatures than C. fluminea (Oliveira et al., 2015Oliveira, M.D., Campos, M.C., Paolucci, E.M., Mansur, M.C., & Hamilton, S.K., 2015. Colonization and spread of Limnoperna fortunei in South America. In: Boltovskoy, D., ed. Limnoperna fortunei: the ecology, distribution and control of a swiftly spreading invasive fouling mussel. Switzerland: Springer International, 333-355, 1 ed.), although extreme water level variation during the year as occurs at Chaco is also a limitation. Annual variation in water level associated with water acidification at Pantanal was suggested as a limitation to the establishment of large populations of golden mussel in this region (Pessotto & Nogueira, 2018Pessotto, M.A., & Nogueira, M.G., 2018. More than two decades after the introduction of Limnoperna fortunei (Dunker 1857) in La Plata Basin. Braz. J. Biol. 78(4), 773-784. PMid:29340533. http://dx.doi.org/10.1590/1519-6984.180789.
http://dx.doi.org/10.1590/1519-6984.1807...
). Therefore, the combination of dry climates and extreme water variation makes almost half of Paraguayan territory unsuitable for freshwater bivalves (native and invasive).

The species of Corbicula were widely distributed in South America, and in Paraguay the situation is similar. These species, especially C. fluminea, occur virtually in all basins of South America (e.g., Darrigran et al., 2020Darrigran, G., Agudo-Padrón, I., Baez, P., Belz, C., Cardoso, F., Carranza, A., Collado, G., Correoso, M., Cuezzo, M.G., Fabres, A., Gregoric, D.E., Letelier, S., Ludwig, S., Mansur, M.C.D., Pastorino, G., Penchaszadeh, P., Peralta, C., Rebolledo, A., Rumi, A., Santos, S., Thiengo, S., Vigidal, T., & Damborenea, C., 2020. Non-native mollusks throughout South America: emergent patterns in an understudied continent. Biol. Invasions 22(3), 853-871. http://dx.doi.org/10.1007/s10530-019-02178-4.
http://dx.doi.org/10.1007/s10530-019-021...
; Miyahira et al., 2020Miyahira, I.C., Pereira, L.S., & dos Santos, L.N., 2020. Non-native freshwater molluscs in the Neotropics: what can be learned from Brazilian reservoirs? Aquat. Invasions 15(3), 455-472. http://dx.doi.org/10.3391/ai.2020.15.3.06.
http://dx.doi.org/10.3391/ai.2020.15.3.0...
). Corbicula fluminea occurred from small to large rivers in Paraguay, suggesting some flexibility in environmental requirements. There is also a wide range of environmental variables (Table 2) in the sites where this species occurs. However, more information is needed to test the relationship of the occurrence of C. fluminea with environmental variables in Paraguay. Corbicula fluminea was the only invasive species to occur in interior basins. Corbicula largillierti presented a restricted distribution in Paraguay, and this species is usually displaced by C. fluminea in invaded sites (Reshaid et al., 2017Reshaid, Y., Cao, L., Brea, F., Blanche, M.O., Torres, S., & Darrigran, G., 2017. Variation in the distribution of Corbicula species (Mollusca: Bivalvia: Corbiculidae) after 25 years of its introduction in the Río de la Plata, Argentina. Zoologia 34, e22181. http://dx.doi.org/10.3897/zoologia.34.22181.
http://dx.doi.org/10.3897/zoologia.34.22...
). Thus, a narrow distribution is expected for C. largillierti compared to C. fluminea. Noteworthy, is that the Confuso River recorded dead shells of C. fluminea and L. fortunei at really high conductivity values, above 4000µS, probably unappropriated for these species. Shells of other native and more sensible mussels were found at the same collecting station. Despite the Corbicula fluminea can survive in estuarine conditions (higher salinity and conductivity than freshwaters), the Confuso River can sporadically receive water from the Pilcomayo River becoming an almost salt river, a type of river that is common in the Chaco ecoregion (Karatayev et al., 2007Karatayev, A.Y., Boltovskoy, D., Padilla, D.K., & Burlakova, L.E., 2007. The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: parallels, contrasts, potential spread and invasion impacts. J. Shellfish Res. 26(1), 205-213. http://dx.doi.org/10.2983/0730-8000(2007)26[205:TIBDPA]2.0.CO;2.
http://dx.doi.org/10.2983/0730-8000(2007...
; Facetti- Masulli et al., 2009Facetti- Masulli, J.F., Flores-Ocampo, F.D. & Cáceres-Dueñas, F., 2009. Estudios hidroquímicos en el Río Confuso. Rev. Soc. Cient. Py 14(219), 219-228.; Ferreira-Rodríguez & Pardo, 2016Ferreira-Rodríguez, N., & Pardo, I., 2016. An experimental approach to assess Corbicula fluminea (Müller, 1774) resistance to osmotic stress in estuarine habitats. Estuar. Coast. Shelf Sci. 176, 110-116. http://dx.doi.org/10.1016/j.ecss.2016.04.017.
http://dx.doi.org/10.1016/j.ecss.2016.04...
; Crespo et al., 2017Crespo, D., Leston, S., Martinho, F., Pardal, M.A., & Dolbeth, M., 2017. Survival of Corbicula fluminea (Müller, 1774) in a natural salinity and tempreature gradient: a field experiment in a temperate estuary. Hydrobiologia 784(1), 337-347. http://dx.doi.org/10.1007/s10750-016-2887-3.
http://dx.doi.org/10.1007/s10750-016-288...
). Those bivalves (invasive and native) probably colonize the Confuso River seasonally from the Paraguay River, during the period of floods, and were extirpated during dry periods of higher influence of the Pilcomayo River. Our collecting survey was conducted during a period of low level of the Paraguay River waters. As we considered that these species do not truly occur under these conditions, these values were not considered in Table 2. Darrigran et al. (2011)Darrigran, G., Damborenea, C., Drago, E., Ezcurra de Drago, I., & Paira, A., 2011. Environmental factors restrict the invasion process of Limnoperna fortunei (Mytilidae) in the Neotropical Region: a case study from the Andean tributaries. Ann. Limnol. - Int. J. Lim. 47(3), 221-229. http://dx.doi.org/10.1051/limn/2011025.
http://dx.doi.org/10.1051/limn/2011025...
already proposed the Pilcomayo River as a salinity barrier for the dispersion of L. fortunei to the Andean tributaries of La Plata Basin.

In Paraguay, the golden mussel Limnoperna fortunei was restricted to the main channel of large rivers (Paraguay and Paraná) and nearby areas. However, not only on the borders with Brazil and Argentina but also on the Paraguay River inside the country. Limnoperna fortunei is usually restricted to large rivers and rarely attains small tributaries (Barbosa et al., 2016Barbosa, N.P., Silva, F.A., de Oliveira, M.D., dos Santos Neto, M.A., de Carvalho, M.D., & Cardoso, A.V., 2016. Limnoperna fortunei (Dunker, 1857) (Mollusca, Bivalvia, Mytilidae): first record in the São Francisco river basin, Brazil. Check List 12(1), 1846. http://dx.doi.org/10.15560/12.1.1846.
http://dx.doi.org/10.15560/12.1.1846...
). The faster dispersion of the golden mussel throughout the La Plata Basin is usually linked to commercial navigation (Pessotto & Nogueira, 2018Pessotto, M.A., & Nogueira, M.G., 2018. More than two decades after the introduction of Limnoperna fortunei (Dunker 1857) in La Plata Basin. Braz. J. Biol. 78(4), 773-784. PMid:29340533. http://dx.doi.org/10.1590/1519-6984.180789.
http://dx.doi.org/10.1590/1519-6984.1807...
). This can also explain the distribution observed in Paraguay (i.e. in large rivers with more ships), although a dispersion in large tributaries of the Paraguay River can be possible, as, in Aquidabán and Tebicuary rivers, the golden mussel has not achieved those basins yet. In our study, L. fortunei was found in higher pH values than in previous studies (Pessotto & Nogueira, 2018Pessotto, M.A., & Nogueira, M.G., 2018. More than two decades after the introduction of Limnoperna fortunei (Dunker 1857) in La Plata Basin. Braz. J. Biol. 78(4), 773-784. PMid:29340533. http://dx.doi.org/10.1590/1519-6984.180789.
http://dx.doi.org/10.1590/1519-6984.1807...
), but with lower values of conductivity. Despite being less flexible to environmental conditions than Corbicula fluminea; L. fortunei also presented a wide range of tolerance to different conditions.

The presence of invasive bivalves in protected areas is a silent threat in Paraguay. The occurrence of the two most invasive bivalves of South America (Corbicula fluminea and Limnoperna fortunei) in three protected areas of Paraguay is an indication that these areas are not fully efficient to protect the freshwater fauna. The invasive bivalves affect not only their native counterparts but may also affect the whole environment, affecting transparency and plankton dynamics (e.g., Boltovskoy et al., 2009Boltovskoy, D., Karatayev, A., Burlakova, L., Cataldo, D., Karatayev, V., Sylvester, F., & Marinelarena, A., 2009. Significant ecosystem-wide effects of the swiftly spreading invasive freshwater bivalve Limnoperna fortunei. Hydrobiologia 636(1), 271-284. http://dx.doi.org/10.1007/s10750-009-9956-9.
http://dx.doi.org/10.1007/s10750-009-995...
; Darrigran & Damborenea, 2011Darrigran, G., & Damborenea, C., 2011. Ecosystem engineering impacts of Limnoperna fortunei in South America. Zool. Sci. 28(1), 1-7. PMid:21186940. http://dx.doi.org/10.2108/zsj.28.1.
http://dx.doi.org/10.2108/zsj.28.1...
; Sousa et al., 2014Sousa, R., Novais, A., Costa, R., & Strayer, D.L., 2014. Invasive bivalves in fresh waters: impacts from individuals to ecosystems and possible control strategies. Hydrobiologia 735(1), 233-251. http://dx.doi.org/10.1007/s10750-012-1409-1.
http://dx.doi.org/10.1007/s10750-012-140...
; Ferreira-Rodríguez et al., 2018Ferreira-Rodríguez, N., Sousa, R., & Pardo, I., 2018. Negative effects of Corbicula fluminea over native freshwater mussels. Hydrobiologia 810(1), 85-95. http://dx.doi.org/10.1007/s10750-016-3059-1.
http://dx.doi.org/10.1007/s10750-016-305...
). Protected areas are usually developed based on the needs of plants and terrestrial vertebrate animals (Fagundes et al., 2016Fagundes, C.K., Vogt, R.C., & Marco Júnior, P., 2016. Testing the efficiency of protected areas in the Amazon for conserving freshwater turtles. Divers. Distrib. 22(2), 123-135. http://dx.doi.org/10.1111/ddi.12396.
http://dx.doi.org/10.1111/ddi.12396...
; Frederico et al., 2018Frederico, R.G., Zuanon, J., & Marco Junior, P., 2018. Amazon protected areas and its ability to protect stream dwelling fish fauna. Biol. Conserv. 219, 12-19. http://dx.doi.org/10.1016/j.biocon.2017.12.032.
http://dx.doi.org/10.1016/j.biocon.2017....
), and freshwater species usually have different requirements. Thus, the existing protected areas are not always suitable for freshwater animals and environments. Our surveys were not directed to protected areas, and probably the invasive bivalves occur in other areas of Paraguay. The management plans of those areas must be updated to consider the presence of invasive species and develop strategies to mitigate their impacts on native fauna. Moreover, the occurrence of invasive bivalves in sympatry (Table 1) can potentialize their negative effects.

Detailed distribution is important to establish proper strategies to deal with invasive species and for the conservation of native species. Several species of native mussels occur in Paraguay and Paraná basins (Cuezzo et al., 2020Cuezzo, M.G., Gregoric, D.E.G., Pointier, J.P., Vázquez, A.A., Ituarte, C., Mansur, M.C.D., Arruda, J.O., Baker, G., Santos, S.B., Ovando, X.M., Fernandez, M.A., Thiengo, S.C., Mattos, A.C., Silva, E.F., Berning, M.I., Collado, G.A., Miyahira, I.C., Antoniazzi, T.N., Pimpão, D.M., & Damborenea, C., 2020. Phylum Mollusca. In: Damborenea, C., Rogers, D.C. & Thorp, J.H., eds. Thorp and Covich’s Freshwater Invertebrates. London: Academic Press, 261-430, 4 ed., vol. 5: Keys to Neotropical and Antartic Fauna. http://dx.doi.org/10.1016/B978-0-12-804225-0.00011-3.
http://dx.doi.org/10.1016/B978-0-12-8042...
), although the information is still limited to old records (Schade, 1965Schade, F.H., 1965. Lista de los moluscos del Guaíra (Villarica - Paraguay) conocidos hasta la presente. Comun Soc. Malacol. Urug. 7(62-63), 209-221.; Quintana, 1982Quintana, M.G., 1982. Catálogo preliminar de la malacofauna del Paraguay. Rev. Mus. Argent. Cienc. Nat. Zoologia 11(3), 61-158.). Recent efforts done in the state of Mato Grosso, upstream of Paraguay, showed a rich and ecologically important fauna of native freshwater mussels (e.g., Colle & Callil, 2012Colle, A.C., & Callil, C.T., 2012. Environmental influences on the composition and structure of the freshwater mussels in shallow lakes in the Cuiabá River floodplain. Braz. J. Biol. 72(2), 249-256. PMid:22735131. http://dx.doi.org/10.1590/S1519-69842012000200004.
http://dx.doi.org/10.1590/S1519-69842012...
; Olivera-Hyde et al., 2020Olivera-Hyde, M., Hallerman, E., Santos, R., Jones, J., Varnerin, B., Santos Neto, G.C., Mansur, M.C.D., Moraleco, P., & Callil, C., 2020. Phylogenetic assessment of freshwater mussels Castalia ambigua and C. inflata at an ecotone in the Paraguay River Basin, Brazil shows that inflated and compressed shell morphotypes are the same species. Diversity (Basel) 12(12), 481. http://dx.doi.org/10.3390/d12120481.
http://dx.doi.org/10.3390/d12120481...
; Santos et al., 2020Santos, R.C.L., Callil, C.T., & Landeiro, V.L., 2020. Unraveling the effects of water-sediment conditions and spatial patterns on Unionida assemblages in seasonally connected floodplain lakes. Hydrobiologia 847(13), 2909-2922. http://dx.doi.org/10.1007/s10750-020-04290-2.
http://dx.doi.org/10.1007/s10750-020-042...
, 2021Santos, R. C., Michiura, A. W. & Callil, C. T., 2021. Host attraction behaviour: the red exhalent aperture extension of the Neotropical freshwater mussel Castalia ambigua. J. Moll. Stud. 87(3), eyab025. http://dx.doi.org/10.1093/mollus/eyab025.
http://dx.doi.org/10.1093/mollus/eyab025...
). Pereira et al. (2014)Pereira, D., Mansur, M.C.D., Duarte, L.D.S., Oliveira, A.S., Pimpão, D.M., Callil, C.T., Ituarte, C., Parada, E., Peredo, S., Darrigran, G., Scarabino, F., Clavijo, C., Lara, G., Miyahira, I.C., & Lasso, C., 2014. Bivalve distribution in hydrographic regions in South America: historical overview and conservation. Hydrobiologia 735(1), 15-44. http://dx.doi.org/10.1007/s10750-013-1639-x.
http://dx.doi.org/10.1007/s10750-013-163...
considered the Paraguay Basin at Mato Grosso as of high diversity, but the Paraguayan portion as of medium richness. However, it is probably an artifact of low sampling effort as were observed for invasive species, but further investigation is needed to reveal the real diversity of native freshwater mussels in Paraguay.

Acknowledgments

Our gratitude goes to Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ E-26/201.347/2021) for the grant to ICM; to Agencia Nacional de Investigación e Innovación (ANII), Programa de Desarrollo de las Ciencias Básicas (PEDECIBA), and Mohamed bin Zayed species conservation fund (MBZ 202524562) for the financial support for CC.

  • Cite as: Miyahira, I.C. et al. Distribution of invasive bivalves in Paraguay: filling the gaps in the heart of South America. Acta Limnologica Brasiliensia, 2024, vol. 36, e2

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Edited by

Associate Editor: André Andrian Padial.

Publication Dates

  • Publication in this collection
    05 Feb 2024
  • Date of issue
    2024

History

  • Received
    13 June 2023
  • Accepted
    24 Nov 2023
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