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Assessing the occurrence of alien species on Brazilian freshwater ecosystems: insights from a comprehensive survey

Avaliando a ocorrência de espécies exóticas nos ecossistemas de água doce brasileiros: percepções de uma pesquisa abrangente

Abstract:

Aim

Assessing the damage caused to natural environments and native biodiversity by alien species is challenging. We tested whether the number of detections of alien species is affected by total alien or total invader alien species richness, considering the importance of predicting which species are more probable future invaders.

Methods

We summarized a research information survey conducted on alien amphibians, annelids, aquatic macrophytes, cnidarians, crustaceans, fish, microorganisms, mollusks, nemathelminths, platyhelminths, and reptiles, and for Brazilian watersheds. We used linear regressions between detections and total alien species richness and between detections and invader species richness.

Results

We obtained 1,896 alien detections of 183 aquatic species in Brazil. Fish and mollusk species were the commonest invaders due to their detections being more frequent than expected by chance, considering all the alien species occurring in Brazilian freshwater ecosystems. We also found positive and robust linear relationships between alien species detections and alien species richness.

Conclusions

Our results illustrate how Brazilian freshwater systems are fragile to alien invasions and highlight the need for effective action to address this question. Scientific uncertainty in Brazil regarding the status of some alien species and their potential harm is high, highlighting the need for a cautionary overview of invaders. Despite this scenario, new policies create opportunities for aquatic parks with exotic organisms to spread further in Brazil, which, in actual Brazilian conditions, is likely to increase the pressure on natural ecosystems and native species. This reinforces the already expressed need by the scientific community for greater attention to the issue.

Keywords:
biological conservation; exotic species; inland waters; watersheds

Resumo:

Objetivo

Inventariar os danos causados aos ambientes naturais ou à biodiversidade nativa por por espécies exóticas é desafiador. Nós testamos se o número de detecções de espécies exóticas é afetado pelo número total de espécies exóticas ou pela riqueza de exóticas invasoras, com o intuito de predizer que grupos de espécies são mais prováveis futuros invasores.

Métodos

Nós apresentamos informações obtidas de um senso nacional conduzido sobre organismos exóticos anelídeos, anfíbios, cnidários, crustáceos, macrófitas aquáticas, microrganismos, moluscos, nematelmintos, peixes, platelmintos e répteis para todas as bacias hidrográficas do país. Utilizamos o número de detecções como variável dependente da riqueza de espécies exóticas, por grupo taxonômico e da riqueza de espécies exóticas invasoras.

Resultados

Nós obtivemos 1.896 detecções de diferentes 183 espécies aquáticas. Peixes e moluscos foram os invasores comuns já que suas detecções são mais frequentes do que o esperado ao acaso, considerando todas as espécies ocorrendo nos ecossistemas de água doce do país. Nós também encontramos relações positivas e robustas entre as detecções por grupo taxonômico e a riqueza em espécies por grupo.

Conclusões

Os resultados ilustram como o ambiente de água doce brasileiro é frágil a invasões biológicas e destacam a necessidade de ações efetivas direcionadas à questão. A incerteza científica a respeito do status de espécies exóticas e seu podencial invasor é grande, o que leva à necessidade de precaução a respeito destas espécies. Apesar do cenário atual, novas políticas abrem opotunidades para que parques aquáticos com organismos exóticos se dispersem mais no Brasil o que deve aumentar ainda mais a pressão sobre ecossistemas naturais e espécies nativas, reforçando a necessidade já manifestada pela comunidade científica, de maior atenção ao tema.

Palavras-chave:
conservação da biodiversidade; espécies exóticas; ecossistemas continentais de água doce; bacias hidrográficas

1. Introduction

Over the last few decades, alien species dispersal has allowed economic benefits and extensive damage to biodiversity and society worldwide (Boddy et al., 2012Boddy, L.G., Bradford, K.J., & Fischer, A.J., 2012. Population-based threshold models describe weed germination and emergence patterns across varying temperature, moisture, and oxygen conditions. J. Appl. Ecol. 49(6), 1225-1236. http://doi.org/10.1111/j.1365-2664.2012.02206.x.
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). After many studies on alien species (Elton, 1958Elton, C.S., 1958. The ecology of invasions by animals and plants. United Kingdom: Chapman and Hall. http://doi.org/10.1007/978-1-4899-7214-9.
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), knowledge regarding their dispersal, range, and damage to biodiversity and society is still inconclusive (Chivers et al., 2017Chivers, C., Drake, D.A.R., & Leung, B., 2017. Economic effects and the efficacy of intervention: exploring unintended effects of management and policy on the spread of non-indigenous species. Biol. Invasions 19(6), 1795-1810. http://doi.org/10.1007/s10530-017-1391-7.
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). Some studies have indicated the contribution of alien species (Gozlan, 2008Gozlan, R.E., 2008. Introduction of non-native freshwater fish: is it all bad? Fish Fish. 9(1), 106-115. http://doi.org/10.1111/j.1467-2979.2007.00267.x.
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), while others reinforced the negative impacts of these species in natural ecosystems (Vitule et al., 2019Vitule, J.R.S., Occhi, T.V.T., Kang, B., & Ichiro, S., 2019. Intra‑country introductions unraveling global hotspots of alien fish species. Biodivers. Conserv. 28(11), 3037-3043. http://doi.org/10.1007/s10531-019-01815-7.
http://doi.org/10.1007/s10531-019-01815-...
; Magalhães et al., 2020Magalhães, A.L.B., Daga, V.S., Bezerra, L.A.V., Vitule, J.R.S., Jacobi, C.M., & Silva, L.G.M., 2020. All the colors of the world: biotic homogenization-differentiation dynamics of freshwater fish communities on demand of the Brazilian aquarium trade. Hydrobiologia 847(18), 3897-3915. http://doi.org/10.1007/s10750-020-04307-w.
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; Magalhães et al., 2021Magalhães, A.L.B., Bezerra, L.A.V., Daga, V.S., Pelicice, F.M., Vitule, J.R.S., & Brito, M.F.G., 2021. Biotic differentiation in headwater creeks after the massive introduction of non-native freshwater aquarium fish in the Paraíba do Sul River basin, Brazil. Neotrop. Ichthyol. 19(3), e200147. http://doi.org/10.1590/1982-0224-2020-0147.
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) and on the worldwide economy (Diagne et al., 2021Diagne, C., Leroy, B., Vaissière, A.C., Gozlan, R.E., Roiz, D., Jarić, I., Salles, J., Bradshaw, C.J.A., & Courchamp, F., 2021. High and rising economic costs of biological invasions worldwide. Nature. 592, 571-576. http://doi.org/10.1038/s41586-021-03405-6.
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). Short surveys for early detection and procedures on alien species dispersal are recognized as an opportunity to prevent social, economic, and environmental damage, especially in large areas (Beric & MacIsaac, 2015Beric, B., & MacIsaac, H.J., 2015. Determinants of rapid response success for alien invasive species in aquatic ecosystems. Biol. Invasions 17(11), 3327-3335. http://doi.org/10.1007/s10530-015-0959-3.
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; Early et al., 2016Early, R., Bradley, B.A., Dukes, J.S., Lawler, J.J., Olden, J.D., Blumenthal, D.M., Gonzalez, P., Grosholz, E.D., Ibañez, I., Miller, L.P., Sorte, C.J.B., & Tatem, A.J., 2016. Global threats from invasive alien species in the twenty-first century and national response capacities. Nat. Commun. 7(1), 12485. PMid:27549569. http://doi.org/10.1038/ncomms12485.
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; Latini and Petrere Junior, 2018Latini, A.O., & Petrere Junior, M., 2018. Efficiency of rapid field methods for detecting non-native fish in Eastern Brazilian Lakes. Hydrobiologia 817(1), 85-96. http://doi.org/10.1007/s10750-018-3624-x.
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; Anastácio et al., 2019Anastácio, P.M., Ribeiro, F., Capinha, C., Banha, F., Gama, M., Filipe, A.F., Rebelo, R., & Sousa, R., 2019. Non-native freshwater fauna in Portugal: a review. Sci. Total Environ. 650(Pt 2), 1923-1934. PMid:30286358. http://doi.org/10.1016/j.scitotenv.2018.09.251.
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; Hughes et al., 2020Hughes, K.A., Pescott, O.L., Peyton, J., Adriaens, T., Cottier-Cook, E.J., Key, G., Rabitsch, W., Tricarico, E., Barnes, D.K.A., Baxter, N., Belchier, M., Blake, D., Convey, P., Dawson, W., Frohlich, D., Gardiner, L.M., González-Moreno, P., James, R., Malumphy, C., Martin, S., Martinou, A.F., Minchin, D., Monaco, A., Moore, N., Morley, S.A., Ross, K., Shanklin, J., Turvey, K., Vaughan, D., Vaux, A.G.C., Werenkraut, V., Winfield, I.J., & Roy, H.E., 2020. Invasive non-native species likely to threaten biodiversity and ecosystems in the Antarctic Peninsula region. Glob. Chang. Biol. 26(4), 2702-2716. PMid:31930639. http://doi.org/10.1111/gcb.14938.
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). However, climate, environmental impacts, fisheries, and inadequate environmental policies may also increase threats to biodiversity (Gonçalves et al., 2020Gonçalves, P.R., Di Dario, F., Petry, A.C., Martins, R.L., da Fonseca, R.N., Henry, M.D., de Assis Esteves, F., Ruiz-Miranda, C.R., Monteiro, L.R., & Nascimento, M.T., 2020. Brazil undermines parks by relocating staff. Science 368(6496), 1199. PMid:32527824. http://doi.org/10.1126/science.abc8297.
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; Charvet et al., 2021Charvet, P., Occhi, T.V.T., Faria, L., Carvalho, B., Pedroso, C.R., Carneiro, L., Freitas, M., Petrere-Junior, M., & Vitule, J.R.S., 2021. Tilapia farming threatens Brazil’s waters. Science 371(6527), 356. PMid:33479145. http://doi.org/10.1126/science.abg1346.
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; Latini et al., 2021Latini, A.O., Mormul, R.P., Giacomini, H.C., Di Dario, F., Vitule, J.R.S., Reis, R.E., Tonella, L., Polaz, C.N.M., Lucifora, L.O., Lima, L.B., Teixeira-de-Mello, F., Lima-Júnior, D.P., Magalhães, A.L.B., Charvet, P., Jimenez-Segura, L.F., Azevedo-Santos, V.M., Carvalho, F.R., D’Anatro, A., Malabarba, L.R., Mandelburger, D., Orsi, M.L., González-Bergonzoni, I., Cunico, A.M., Petrere-Júnior, M., Scarabotti, P., & Vidal, N., 2021. Brazil’s new fish farming decree threatens freshwater conservation in South America. Biol. Conserv. 263, 109353. http://doi.org/10.1016/j.biocon.2021.109353.
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).

Many Brazilian basins and wetlands surround one of the most diverse freshwater aquatic communities worldwide (Richards et al., 2015Richards, R.C., Rerolle, J., Aronson, J., Pereira, P.H., Gonçalves, H., & Brancalion, P.H.S., 2015. Governing a pioneer program on payment for watershed services: stakeholder involvement, legal frameworks and early lessons from the Atlantic forest of Brazil. Ecosyst. Serv. 16, 23-32. http://doi.org/10.1016/j.ecoser.2015.09.002.
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). However, this also makes it extraordinarily complicated to know which species are near to invade or occur there. Furthermore, escaping alien species from aquaculture and damaging freshwaters threaten Brazilian international compromises, as established in the Conference of the Parties of the Convention on Biological Diversity (Lima-Junior et al., 2018Lima-Junior, D.P., Magalhães, A.L.B., Pelicice, F.M., Vitule, J.R.S., Azevedo-Santos, V.M., Orsi, M.L., Simberloff, D., & Agostinho, A.A., 2018. Aquaculture expansion in Brazilian freshwaters against the Aichi Biodiversity Targets. Ambio 47(4), 427-440. PMid:29306998. http://doi.org/10.1007/s13280-017-1001-z.
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; Latini et al., 2021Latini, A.O., Mormul, R.P., Giacomini, H.C., Di Dario, F., Vitule, J.R.S., Reis, R.E., Tonella, L., Polaz, C.N.M., Lucifora, L.O., Lima, L.B., Teixeira-de-Mello, F., Lima-Júnior, D.P., Magalhães, A.L.B., Charvet, P., Jimenez-Segura, L.F., Azevedo-Santos, V.M., Carvalho, F.R., D’Anatro, A., Malabarba, L.R., Mandelburger, D., Orsi, M.L., González-Bergonzoni, I., Cunico, A.M., Petrere-Júnior, M., Scarabotti, P., & Vidal, N., 2021. Brazil’s new fish farming decree threatens freshwater conservation in South America. Biol. Conserv. 263, 109353. http://doi.org/10.1016/j.biocon.2021.109353.
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).

Considering the extensive network of hydrographic basins in Brazil, many aquatic species, and the risk that alien invasions represent to biodiversity and society, this work aimed to summarize and analyze the results of the first Brazilian survey on alien species in freshwater ecosystems. Judging the importance of predicting which species are more probable future invaders (Fournier et al., 2019Fournier, A., Penone, C., Pennino, M.G., & Courchamp, F., 2019. Predicting future invaders and future invasions. Proc. Natl. Acad. Sci. USA 116(16), 7905-7910. PMid:30926662. http://doi.org/10.1073/pnas.1803456116.
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), the inventory data were useful for testing whether the number of detections of alien amphibians, annelids, aquatic macrophytes, cnidarians, crustaceans, fish, microorganisms, mollusks, nemathelminths, platyhelminths, and reptiles species groups is affected by alien or invasive alien species richness.

2. Material and Methods

A survey was conducted physically and digitally using a questionnaire that addressed questions on alien amphibians, annelids, aquatic macrophytes, cnidarians, crustaceans, fish, microorganisms, mollusks, nemathelminths, platyhelminths, and reptile species for Brazilian watersheds from 2006 to 2012. We communicated with researchers via mail and gathered information on alien species residing in inland waters by utilizing the Plataforma Lattes (CNPq, 2023Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq, 2023. Currículo Lattes [online]. Retrieved in 2023, April 11, from https://www.lattes.cnpq.br/.
https://www.lattes.cnpq.br/...
; Lane, 2010Lane, J., 2010. Let’s make science metrics more scientific. Nature 464(7288), 488-489. PMid:20336116. http://doi.org/10.1038/464488a.
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), a comprehensive researcher catalog containing the credentials of approximately 200,000 Brazilian researchers. The researchers were chosen based on their scientific productivity, as documented by Plataforma Lattes, and their affiliation with the investigated taxonomic group. In addition, we sent a questionnaire to governmental and private institutions with a significant economic, social, or academic impact. These institutions were selected based on a combination of formal and informal databases, including commercial and government sources. For illustration, we obtained a list of hydroelectric plants from the websites of the Agência Nacional das Águas e Saneamento Básico (ANA) and Agência Nacional de Energia Elétrica (ANEEL), and we collected data related to aquatic organism breeders from the website of the Ministério de Aquacultura e Pesca. At some level, all these were related or potentially related to any alien species in continental aquatic ecosystems, and all of them were informed about the possibility of answering the survey by an internet link where some additional questions related to the biome and the basin were requested.

The questionnaire, sent by mail to 6,000 recipients, requested the name of the person responsible for filling them out (optional), the completion date, and responses to the following questions: a) Do you know of any exotic species?, b) What is the name of the species (common or scientific or both), c) How do you believe the species reached the location?, d) Is the organism contained in some artificial place or the natural environment?, e) Do you know why the species reached the region?, f) Could you describe the type of environment?, g) Do you have any measure of counting of the organism?, h) How do you describe the organism?, i) What is the exact location of occurrence?, j) Are you able to identify some economic importance?, k) Are there visible consequences?, l) Do you know any control methods?, m) Do you work with the organism?, and n) Do you know any publication about it?

The survey also used a bibliographic revision done in databases and digital libraries. The Web of Science (Clarivate, 2023Clarivate, 2023. Web of Science [online]. Retrieved in 2023, April 10, from https://www.webofscience.com/wos.
https://www.webofscience.com/wos...
), the Scopus Preview (Elsevier, 2023Elsevier, 2023. Scopus Preview [online]. Retrieved in 2023, April 11, from https://www.scopus.com/.
https://www.scopus.com/...
), the SciELO (SciELO, 2023Scientific Electronic Library Online - SciELO, 2023. Scientific Electronic Library Online [online]. Retrieved in 2023, April 13, from https://scielo.org/.
https://scielo.org/...
), and the thesis database from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, 2023Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES, 2023. Catálogo de Teses e Dissertações [online]. Retrieved in 2023, April 11, from http://catalogodeteses.capes.gov.br/catalogo-teses.
http://catalogodeteses.capes.gov.br/cata...
) were used searching for publications about alien species incidence. We also searched for alien species in aquatic environments in published books, nonindexed journals, technical reports, regional species datasets, scientific meeting proceedings, and gray literature, such as journal articles or books. All data were used to build a dataset with freshwater alien species occurrence in Brazil.

After concluding the survey, the Plataforma Lattes was used again to invite some of the leading Brazilian specialists and was carefully chosen by the importance of their scientific production. Two specialists were invited for each surveyed taxonomic group. The specialists could check the data for failures and help improve the final dataset in an in-person workshop.

Alien species occurrences were obtained, and a list of alien species of amphibians, annelids, aquatic macrophytes, cnidarians, crustaceans, fish, microorganisms, mollusks, nemathelminths, platyhelminths, and reptile groups was achieved. The species were classified into one of the categories: i) isolated alien species (IAS) – species confined in artificial environments; ii) detected alien species (DAS) – who were just detected in natural environments; iii) established alien species (EAS) – species with all life stages in natural environments, but without recognized impacts on the environment; and iv) invasive alien species (InAS) – established species, with at least one scientifically proven damage to a native species, native community, or aquatic environment. Sometimes it was impossible to discern whether a given species was a native species with high growth rates or an alien species when it was associated with preexisting impacts in the aquatic environment. Therefore, this last situation classified the species as cryptic (CRY).

Linear regressions between detections and total alien species richness and between detections and invader species richness (InAS) were performed by considering the number of alien species as a surrogate of their dispersal potential and discussing this result regarding Brazilian inland waters. We used Statistica v.13 (StatSoft; license: 201804-41993) for these analyses.

3. Results

In total, 1,148 Brazilian institutions were contacted to obtain information on alien species, of which 52 were companies responsible for hydroelectric power generation, 657 non-governmental organizations related to environmental issues, 205 colleges and universities with professionals potentially involved with alien species, and 234 governmental (e.g., federal, state, and municipal) autarchies. Additionally, we obtained the collaboration of 333 researchers and managers involved in environmental issues and some influence of alien species in Brazilian inland waters.

The survey detected 1,896 occurrences of 183 alien species in Brazilian inland waters (Table 1). Of these, 40 (21.86%) cause social, economic, or environmental problems, allowing us to characterize them as invasive alien species (InAS) (ISSG, 2018Invasive Species Specialist Group - ISSG, 2018. 100 of the world’s worst invasive alien species [online]. Retrieved in 2023, July 1, from https://portals.iucn.org/library/sites/library/files/documents/2000-126.pdf
https://portals.iucn.org/library/sites/l...
). Among all the invasive taxonomic groups found, there was one nemathelminth, one annelid, two reptiles, two platyhelminthes, two cnidarians, four amphibians, seven mollusks, 11 crustaceans, 12 aquatic macrophytes, 12 microorganisms (including microcrustacean) and 1,029 fish (Table 2). A large number of the alien species in Brazilian freshwater ecosystems (e.g., 58% for aquatic macrophytes, 36% for crustaceans, and 57% for fishes) are translocated and are primarily related to aquaculture use (Table 3 and Table 1).

Table 1
Taxonomic group, species name, native range, and classification of alien species in Brazilian inland waters. The classification refers to origin (another country or translocated) and invasion categories (IAS, isolated alien species; DAS - detected alien species; EAS, established alien species; InAS, invasive alien species, and CRY, cryptic species).
Table 2
The number of detected species by category of alien species in Brazilian inland waters. The richness of alien species and the number of cases by group of species. Codes indicate: IAS, isolated alien species; DAS - detected alien species; EAS, established alien species; InAS, invasive alien species, and CRY, cryptic species.
Table 3
The number of alien species in Brazilian inland waters originated from another country or as translocated domestic species. The ‘n.i.’ (not identified) status was assigned for species with no confirmed origin.

Fish species were in the group with the highest number of occurrences of introduced species and InAS in Brazilian inland waters. Despite the few introduced species of aquatic macrophytes and mollusks, they also reached many species classified as InAS: 100% and 71%, respectively. By considering the number of alien species detections as a surrogate of their dispersal potential, we found positive and robust linear relationships between alien species detections and alien species richness (Figure 1; R2 = 80%) and with InAS richness (Figure 2; R2 = 60%).

Figure 1
Relationship between the richness of alien species and detections for each alien species group in Brazilian inland waters.
Figure 2
Relationship between the invaders of alien species richness and detections for each group of alien species in Brazilian inland waters.

4. Discussion

Despite the time of the survey (data was gathered only until 2012), alien species richness in Brazilian freshwater environments (N=183) is important in establishing an essential measure for subsequent comparisons. The same consideration may be made for the number of confirmed cases (1,896). According to the results for the species groups, the detections of microorganisms, mollusks, and fish outperform the alien species pool, which can be visualized both in the relationship between detections and the richness of alien species (Figure 1) and in the relationship between detections and the richness of alien invasive species (Figure 2).

Some features may favor these groups: pollution primarily benefits microorganisms (e.g., cyanobacterial species), commonly associated with decreasing water quality (Crooks et al., 2010Crooks, J.A., Chang, A.L., & Ruiz, G.M., 2010. Aquatic pollution increases the relative success of invasive species. Biol. Invasions 13(1), 165-176. http://doi.org/10.1007/s10530-010-9799-3.
http://doi.org/10.1007/s10530-010-9799-3...
), but also benefits fish species, such as the guppy Poecilia reticulata (Peters, 1859) that assimilate carbon directly from sewage (Carvalho et al., 2019Carvalho, D.R., Flecker, A.S., Alves, C.B.M., Sparks, J.P., & Pompeu, P.S., 2019. Trophic responses to aquatic pollution of native and exotic livebearer fishes. Sci. Total Environ. 681, 503-515. PMid:31128341. http://doi.org/10.1016/j.scitotenv.2019.05.092.
http://doi.org/10.1016/j.scitotenv.2019....
). Mollusks, such as Limnoperna fortunei (Dunker 1857), have improved dispersal abilities since fixing on boats and have long-term survival out of the water (Oliveira et al., 2010Oliveira, M.D., Hamilton, S.K., Calheiros, D.F., Jacobi, C.M., & Latini, R.O., 2010. Modeling the potential distribution of the invasive golden mussel Limnoperna fortunei in the Upper Paraguay River system using limnological variables. Braz. J. Biol. 70(3, Suppl.), 831-840. PMid:21085788. http://doi.org/10.1590/S1519-69842010000400014.
http://doi.org/10.1590/S1519-69842010000...
). Fish have dispersal potentialized by fishing (Daga et al., 2016Daga, V.S., Debona, T., Abilhoa, V., Gubiani, E.A., & Vitule, J.R.S., 2016. Non-native fish invasions of a Neotropical ecoregion with high endemism: a review of the Iguaçú River. Aquat. Invasions 11(2), 209-223. http://doi.org/10.3391/ai.2016.11.2.10.
http://doi.org/10.3391/ai.2016.11.2.10...
), inland aquaculture (Lima-Junior et al., 2018Lima-Junior, D.P., Magalhães, A.L.B., Pelicice, F.M., Vitule, J.R.S., Azevedo-Santos, V.M., Orsi, M.L., Simberloff, D., & Agostinho, A.A., 2018. Aquaculture expansion in Brazilian freshwaters against the Aichi Biodiversity Targets. Ambio 47(4), 427-440. PMid:29306998. http://doi.org/10.1007/s13280-017-1001-z.
http://doi.org/10.1007/s13280-017-1001-z...
; Forneck et al., 2020Forneck, S.C., Dutra, F.M., Camargo, M.P., Vitule, J.E.S., & Cunico, A.M., 2020. Aquaculture facilities drive the introduction and establishment of non-native Oreochromis niloticus populations in Neotropical streams. Hydrobiologia 848(9), 1955-1966. http://doi.org/10.1007/s10750-020-04430-8.
http://doi.org/10.1007/s10750-020-04430-...
), and ornamental cultivation and dumping in natural habitats (Magalhães et al., 2017Magalhães, A.L.B., Orsi, M.L., Pelicice, F.M., Azevedo-Santos, V.M., Vitule, J.R.S., Lima-Junior, P.D., & Brito, M.F.G., 2017. Small size today, aquarium dumping tomorrow: sales of juvenile non-native large fish as an important threat in Brazil. Neotrop. Ichthyol. 15(4), e170033. https://doi.org/10.1590/1982-0224-20170033., 2021Magalhães, A.L.B., Bezerra, L.A.V., Daga, V.S., Pelicice, F.M., Vitule, J.R.S., & Brito, M.F.G., 2021. Biotic differentiation in headwater creeks after the massive introduction of non-native freshwater aquarium fish in the Paraíba do Sul River basin, Brazil. Neotrop. Ichthyol. 19(3), e200147. http://doi.org/10.1590/1982-0224-2020-0147.
http://doi.org/10.1590/1982-0224-2020-01...
). Explanations came from a bibliographic review and were corroborated by the invited specialists who validated the survey.

A recent and significant publication on alien species provided a systematic discussion of the vectors influencing the introduction, establishment, and spread of alien species in Brazil (Bergallo et al., 2024Bergallo, H.G., dos Santos, L.N., Barros, F., Petruzzella, A., Figueiredo, B.R.S., Pereira, A.D., Latini, A.O., Lopes, A.V., Rosa, C., Vieira Filho, E.A., Evangelista, E.F., Dias, G.M., Ortega, J.C.G., Capel, K.C.C., & Abreu, R.C.R., 2024. Vetores de mudança diretos e indiretos que afetam a introdução, o estabelecimento e a disseminação de espécies exóticas invasoras. In: Dechoum, M.S., Junqueira, A. O. R., Orsi, M.L., orgs. Relatório temático sobre espécies exóticas invasoras, biodiversidade e serviços ecossistêmicos. São Carlos: Editora Cubo, 92-132, Cap. 3. http://doi.org/10.4322/978-65-00-87228-6.cap3.
http://doi.org/10.4322/978-65-00-87228-6...
). The changes in aquatic ecosystems, organism trade, and navigation are considered some of the most important direct vectors. There is evidence of organism trade benefiting fish (e.g., Magalhães & Jacobi, 2017Magalhães, A.L.B., & Jacobi, C.M. 2013. Invasion risks posed by ornamental freshwater fish trade to southeastern Brazilian rivers. Neotrop. Ichthyol. 11(2), 433–441.), environmental impacts benefiting microorganisms (e.g., Saulino & Trivinho-Strixino, 2017Saulino, H.H.L., & Trivinho-Strixino, S., 2017. Forecasting the impact of an invasive macrophyte species in the littoral zone through aquatic insect species composition. Iheringia Sér. Zool.. 107, e2017043. https://doi.org/10.1590/1678-4766e2017043.), and navigation benefiting mollusks (e.g., 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://doi.org/10.1590/1676-0611-bn-2020-1175.
http://doi.org/10.1590/1676-0611-bn-2020...
). These vectors are likely responsible for the response that these taxa, fish, microorganisms, and mollusks have, allowing us to identify, among them, an average response superior to the expected in our models.

In addition to constituting a dangerous scenario, alien species in Brazilian inland waters may be a surrogate vision of what has occurred, since they represent specialists and documented alien species occurrence in Brazilian watersheds. It helps to show how fragile and threatened these freshwater ecosystems are, given the pervasive effects on biodiversity loss worldwide (Bellard et al., 2016Bellard, C., Leroy, B., Thuiller, W., Rysman, J.F., & Courchamp, F., 2016. Major drivers of invasion risks throughout the world. Ecosphere 7(3), e01241. http://doi.org/10.1002/ecs2.1241.
http://doi.org/10.1002/ecs2.1241...
), mainly in megadiverse countries such as Brazil (Pelicice et al., 2017Pelicice, F.M., Azevedo-Santos, V.M., Vitule, J.R.S., Orsi, M.L., Lima-Junior, D.P., Magalhães, A.L.B., Pompeu, P.S., Petrere Junior, M., & Agostinho, A.A., 2017. Neotropical freshwater fishes imperilled by unsustainable policies. Fish Fish. 18(6), 1119-1133. http://doi.org/10.1111/faf.12228.
http://doi.org/10.1111/faf.12228...
). However, the survey also represents a primordial step to knowing about the establishment of alien species.

It is essential to note that a large number of the alien species in Brazilian freshwater ecosystems (e.g., 58% for aquatic macrophytes, 36% for crustaceans, and 57% for fishes) are translocated (i.e., species introduced from another river basin or freshwater ecoregion within Brazil) and are primarily related to aquaculture use (Tables 1, 2) what corroborates with previous studies that showed that aquaculture is the leading vector or pathway of introduced species in Brazil (Ortega et al., 2015Ortega, J.C.G., Júlio Junior, H.F., Gomes, L.C., & Agostinho, A.A., 2015. Fish farming as the main driver of fish introductions in Neotropical reservoirs. Hydrobiologia 746(1), 147-158. http://doi.org/10.1007/s10750-014-2025-z.
http://doi.org/10.1007/s10750-014-2025-z...
), China (Kang et al., 2023 Kang, B., Vitule, J.R.S., Li, S., Shuai, F., Huang, L., Huang, X., Fang, J., Shi, X., Zhu, Y., Xu, D., Yan, Y., & Lou, F., 2023. Introduction of non-native fish for aquaculture in China: a systematic review. Rev. Aquacult. 15(2), 676-703. http://doi.org/10.1111/raq.12751.
http://doi.org/10.1111/raq.12751...
) and in the world (Casal, 2006Casal, C.M.V., 2006. Global documentation of fish introductions: the growing crisis and recommendations for action. Biol. Invasions 8(1), 3-11. http://doi.org/10.1007/s10530-005-0231-3.
http://doi.org/10.1007/s10530-005-0231-3...
). Therefore, this scenario is worrisome once it is difficult to control the transport and introduction of species among the national river basin. A direct consequence is the increasing number of alien species in freshwater ecosystems in Brazil (Magalhães et al., 2021Magalhães, A.L.B., Bezerra, L.A.V., Daga, V.S., Pelicice, F.M., Vitule, J.R.S., & Brito, M.F.G., 2021. Biotic differentiation in headwater creeks after the massive introduction of non-native freshwater aquarium fish in the Paraíba do Sul River basin, Brazil. Neotrop. Ichthyol. 19(3), e200147. http://doi.org/10.1590/1982-0224-2020-0147.
http://doi.org/10.1590/1982-0224-2020-01...
; Rocha et al., 2023Rocha, B.S., García-Berthou, E., & Cianciaruso, M.V., 2023. Non-native fishes in Brazilian freshwaters: identifying biases and gaps in ecological research. Biol. Invasions 25(5), 1643-1658. http://doi.org/10.1007/s10530-023-03002-w.
http://doi.org/10.1007/s10530-023-03002-...
), including pristine regions like the Amazon River basin (Doria et al., 2021Doria, C.R.C., Agudelo, E., Akama, A., Barros, B., Bonfim, M., Carneiro, L., Briglia-Ferreira, S.R., Nobre Carvalho, L., Bonilla-Castillo, C.A., Charvet, P., dos Santos Catâneo, D.T.B., da Silva, H.P., Garcia-Dávila, C.R., dos Anjos, H.D.B., Duponchelle, F., Encalada, A., Fernandes, I., Florentino, A.C., Guarido, P.C.P., de Oliveira Guedes, T.L., Jimenez-Segura, L., Lasso-Alcalá, O.M., Macean, M.R., Marques, E.E., Mendes-Júnior, R.N.G., Miranda-Chumacero, G., Nunes, J.L.S., Occhi, T.V.T., Pereira, L.S., Castro-Pulido, W., Soares, L., Sousa, R.G.C., Torrente-Vilara, G., Van Damme, P.A., Zuanon, J., & Vitule, J.R.S., 2021. The silent threat of non-native fish in the Amazon: ANNF database and review. Front. Ecol. Evol. 9, 646702. http://doi.org/10.3389/fevo.2021.646702.
http://doi.org/10.3389/fevo.2021.646702...
). An emblematic example is the invasion of giant arapaima Arapaima gigas (Schinz, 1822). This species was introduced in the Madeira River (in the Amazon River basin) and Grande River (in the Paraná River basin) due to the escape of aquaculture facilities (Catâneo et al., 2022Catâneo, D.T.B., Ximenes, A.M., Garcia-Davila, C.R., Van Damme, P.A., Pagotto, R.C., Vitule, J.R.S., Hrbek, T., Farias, I.P., & Doria, C.R.C., 2022. Elucidating a history of invasion: population genetics of pirarucu (Arapaima gigas, Actinopterygii, Arapaimidae) in the Madeira River. Hydrobiologia 849(16), 3617-3632. http://doi.org/10.1007/s10750-022-04977-8.
http://doi.org/10.1007/s10750-022-04977-...
; Sousa et al., 2022Sousa, R.G.C., Pereira, L.S., Cintra, M.A., de Carvalho Freitas, C.E., de Almeida Mereles, M., Zacardi, D.M., Faria Júnior, C.H., Castello, L., & Vitule, J.R.S., 2022. Status of Arapaima spp. in Brazil: threatened in its places of origin, a rapidly spreading invader elsewhere. Manag. Biol. Invasions 13(4), 631-643. http://doi.org/10.3391/mbi.2022.13.4.03.
http://doi.org/10.3391/mbi.2022.13.4.03...
).

Despite the well-known crisis of freshwater ecosystems worldwide (Albert et al., 2021Albert, J.S., Destouni, G., Duke‐Sylvester, S.M., Magurran, A.E., Oberdorff, T., Reis, R.E., Winemiller, K.O., & Ripple, W.J., 2021. Scientists’ warning to humanity on the freshwater biodiversity crisis. Ambio 50(1), 85-94. PMid:32040746. http://doi.org/10.1007/s13280-020-01318-8.
http://doi.org/10.1007/s13280-020-01318-...
), freshwater biodiversity and its benefits persist in decline. Water supply, wild-caught fishing, recreation, flood control, and gene biodiversity are just examples of the reduced benefits of nature that alien invasions and dispersal can reduce (Flood et al., 2020Flood, P.J., Duran, A., Barton, M., Mercado-Molina, A.E., & Trexler, J.C., 2020. Invasion impacts on functions and services of aquatic ecosystems. Hydrobiologia 847(7), 1571-1586. http://doi.org/10.1007/s10750-020-04211-3.
http://doi.org/10.1007/s10750-020-04211-...
). Unfortunately, the general opinion of Brazilians about this problem is poor. Changing this scenario is imperative and requires enhancing the quality of environmental regulatory policies and considering a cautionary overview regarding alien species and biodiversity and benefit maintenance.

In Brazil, some other factors worsen alien species. For instance, the Forest Code amendments relax natural area preservation and affect water quality and community stability (Magalhães et al., 2010Magalhães, A.L.B., Casatti, L., & Vitule, J.R.S., 2010. Changes in the Brazilian Forest Law will promote non-native species of freshwater fish. Nat. Conserv. 9, 121-124. http://doi.org/10.4322/natcon.2011.017.
http://doi.org/10.4322/natcon.2011.017...
; Tollefson, 2011Tollefson, J., 2011. Brazil revisits forest code. Nature 476(7360), 259-260. PMid:21850076. http://doi.org/10.1038/476259a.
http://doi.org/10.1038/476259a...
). Additionally, the expansion of dams/reservoirs around all river basins impact negatively the integrity of local ecological communities and favors the establishment of alien species (Johnson et al. 2008Johnson, P.T.J., Olden, J.D., & Vander Zande, M.J., 2008. Dam invaders – impoundments facilitate biological invasions into freshwaters. Front. Ecol. Environ. 6(7), 357-363. http://doi.org/10.1890/070156.
http://doi.org/10.1890/070156...
; Muniz et al. 2021Muniz, C.M., García-Berthou, E., Ganassin, M.J.M., Agostinho, A.A., & Gomes, L.C., 2021. Alien fish in Neotropical reservoirs: assessing multiple hypotheses in invasion biology. Ecol. Indic. 121, 107034. http://doi.org/10.1016/j.ecolind.2020.107034.
http://doi.org/10.1016/j.ecolind.2020.10...
). The aquaculture expansion with alien species, a key introduction vector, spreads across regions (Pelicice et al., 2017Pelicice, F.M., Azevedo-Santos, V.M., Vitule, J.R.S., Orsi, M.L., Lima-Junior, D.P., Magalhães, A.L.B., Pompeu, P.S., Petrere Junior, M., & Agostinho, A.A., 2017. Neotropical freshwater fishes imperilled by unsustainable policies. Fish Fish. 18(6), 1119-1133. http://doi.org/10.1111/faf.12228.
http://doi.org/10.1111/faf.12228...
; Lima-Junior et al., 2018Lima-Junior, D.P., Magalhães, A.L.B., Pelicice, F.M., Vitule, J.R.S., Azevedo-Santos, V.M., Orsi, M.L., Simberloff, D., & Agostinho, A.A., 2018. Aquaculture expansion in Brazilian freshwaters against the Aichi Biodiversity Targets. Ambio 47(4), 427-440. PMid:29306998. http://doi.org/10.1007/s13280-017-1001-z.
http://doi.org/10.1007/s13280-017-1001-z...
; Charvet et al., 2021Charvet, P., Occhi, T.V.T., Faria, L., Carvalho, B., Pedroso, C.R., Carneiro, L., Freitas, M., Petrere-Junior, M., & Vitule, J.R.S., 2021. Tilapia farming threatens Brazil’s waters. Science 371(6527), 356. PMid:33479145. http://doi.org/10.1126/science.abg1346.
http://doi.org/10.1126/science.abg1346...
), while the crisis in science investments impacting biodiversity (Overbeck et al., 2018Overbeck, G.E., Bergallo, H.G., Grelle, C.E.V., Akama, A., Bravo, F., Colli, G.R., Magnusson, W.E., Tomas, W.M., & Fernandes, G.W., 2018. Global biodiversity threatened by science budget cuts in Brazil. Bioscience 68(1), 11-12. PMid:29599546. http://doi.org/10.1093/biosci/bix130.
http://doi.org/10.1093/biosci/bix130...
; Escobar, 2019Escobar, H., 2019. Brazilian scientists lament “freeze” on research budget. Science 364(6436), 111. PMid:30975866. http://doi.org/10.1126/science.364.6436.111.
http://doi.org/10.1126/science.364.6436....
; Gonçalves et al., 2020Gonçalves, P.R., Di Dario, F., Petry, A.C., Martins, R.L., da Fonseca, R.N., Henry, M.D., de Assis Esteves, F., Ruiz-Miranda, C.R., Monteiro, L.R., & Nascimento, M.T., 2020. Brazil undermines parks by relocating staff. Science 368(6496), 1199. PMid:32527824. http://doi.org/10.1126/science.abc8297.
http://doi.org/10.1126/science.abc8297...
; Kowaltowski, 2021Kowaltowski, A.J., 2021. Brazil’s scientists face 90% budget cut. Nature 598(7882), 566. PMid:34697474. http://doi.org/10.1038/d41586-021-02882-z.
http://doi.org/10.1038/d41586-021-02882-...
) and new laws threaten freshwater biodiversity in neighboring countries, promoting alien fish farming (Latini et al., 2021Latini, A.O., Mormul, R.P., Giacomini, H.C., Di Dario, F., Vitule, J.R.S., Reis, R.E., Tonella, L., Polaz, C.N.M., Lucifora, L.O., Lima, L.B., Teixeira-de-Mello, F., Lima-Júnior, D.P., Magalhães, A.L.B., Charvet, P., Jimenez-Segura, L.F., Azevedo-Santos, V.M., Carvalho, F.R., D’Anatro, A., Malabarba, L.R., Mandelburger, D., Orsi, M.L., González-Bergonzoni, I., Cunico, A.M., Petrere-Júnior, M., Scarabotti, P., & Vidal, N., 2021. Brazil’s new fish farming decree threatens freshwater conservation in South America. Biol. Conserv. 263, 109353. http://doi.org/10.1016/j.biocon.2021.109353.
http://doi.org/10.1016/j.biocon.2021.109...
). Like what happens worldwide, scientific uncertainty in Brazil regarding the status of alien species is high and their potential harm, highlighting the need for a cautionary overview of invaders.

Acknowledgements

This work was supported by the Ministério do Meio Ambiente e Mudança do Clima and Projeto de Conservação e Utilização Sustentável da Diversidade Biológica Brasileira – PROBIO (grant number 68.0012/04-4). Thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research grants awarded to D. P. Lima-Junior (Grant Number: 305923/2020-0).

  • Cite as: Latini, A.O. et al. Assessing the occurrence of alien species on Brazilian freshwater ecosystems: insights from a comprehensive survey. Acta Limnologica Brasiliensia, 2024, vol. 36, e19. https://doi.org/10.1590/S2179-975X6423

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Edited by

Associate Editor: Andre Andrian Padial.

Publication Dates

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

History

  • Received
    01 July 2023
  • Accepted
    07 May 2024
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