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The midday sun reveals what the waters hide: Podocnemis unifilis Troschel, 1848 (Testudines, Podocnemididae), another exotic species in the Pantanal of Mato Grosso state

O sol do meio-dia revela o que as águas escondem: Podocnemis unifilis Troschel, 1848 (Testudines, Podocnemididae), outra espécie exótica no Pantanal mato-grossense

Abstract

The process of exotic species introduction is recognized as one of the greatest threats to the ecology and economy of the planet, due to changes in interactions in native biological communities. In this sense, reporting bioinvasions is the first step to understanding its introduction process and creating strategies to mitigate possible socio-environmental damages. Here we report the first records of Podocnemis unifilis introduced in the Northern Pantanal, Mato Grosso, Brazil. We obtained the species’ first records occasionally during 2014 and 2015. In the following years from 2016 to 2019, we carried out systematic observations through nautical incursions on the Paraguay River, between the Sepotuba River mouth and the Taiamã Ecological Station (TES). We also included third part records, when it was possible to prove the species identification and registration sites. Podocnemis unifilis adults, hatchling and nests were recorded at different points along the Paraguay River. Our results indicate that P. unifilis was introduced close to the urban nucleus of Cáceres about 30 years ago. Currently, it has an established population, recording nests and hatchling for years in a row. A particular one is its occurrence at the TES, an important natural fish nursery and refuge for the wetland fauna. Thus, continuous monitoring is suggested from P.unifilis, since the Pantanal’s environment with several different aquatic environments, offers favorable conditions for the species population increase in the Northern Pantanal.

Keywords
Chelonian distribution; Conservation Unit; Floodplain; Invasive fauna; Tracajá

Resumo

O processo de introdução de espécies exóticas é reconhecido como uma das maiores ameaças à ecologia e economia do planeta, devido às mudanças nas interações em comunidades biológicas nativas. Nesse sentido, relatar as bioinvasões é o primeiro passo para entender seu processo de implantação e criar estratégias para mitigar possíveis danos socioambientais. Aqui relatamos os primeiros registros de P. unifilis introduzidos no Pantanal Norte, Mato Grosso, Brasil. Obtivemos os primeiros registros das espécies ocasionalmente durante 2014 e 2015. Nos anos seguintes, de 2016 a 2019, realizamos observações sistemáticas por meio de incursões náuticas no rio Paraguai, entre a foz do rio Sepotuba e a Estação Ecológica Taiamã (TES). Incluímos também registros de terceiros, quando foi possível comprovar os locais de identificação e registro das espécies. Adultos de Podcnemis unifilis, filhotes e ninhos foram registrados em diferentes pontos ao longo do rio Paraguai. Nossos resultados indicam que P. unifilis foi introduzido próximo ao núcleo urbano de Cáceres há cerca de 30 anos. Atualmente, ela tem uma população estabelecida, registrando ninhos e filhotes por anos consecutivos. Uma em particular é a sua ocorrência no TES, importante viveiro natural de peixes e refúgio da fauna pantaneira. Assim, sugere-se o monitoramento contínuo de P.unifilis, uma vez que o ambiente do Pantanal com diversos ambientes aquáticos distintos, oferece condições favoráveis para o aumento da população da espécie no Pantanal Norte.

Palavras-chave
Distribuição de quelônios; Unidade de Conservação; Várzea; Fauna invasora; Tracajá

Introduction

The process of exotic species introduction is recognized as one of the greatest threats to the ecology of species and the economy of the planet (Gisp 2005GISP. 2005. Programa Global de Espécies Invasoras. América do Sul invadida. A crescente ameaça das espécies exóticas invasoras, p80. ISBN 1-919684-48-4., Doherty et al. 2016DOHERTY, T.S., GLEN, A.S., NIMMO, D.G., RITCHIE, E.G. & DICKMAN, C.R. 2016. Invasive predators and global biodiversity loss. Proc. Natl. Acad. Sci. 113(40):11261–11265. www.pnas.org/lookup/suppl/doi:10.1073/pnas.1602480113/-/DCSupplemental
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). Its impacts, in a given environment, can vary in different degrees of severity, which has led researchers to seek to understand the relationship dynamics of invasive species with the native biological community of the invaded areas (Crystal-Ornelas & Lockwood 2020CRYSTAL-ORNELAS, R. & LOCKWOOD, J.L. 2020. The ‘known unknowns’ of invasive species impact measurement. Biol. Invasions. 22(4):1513–1525. https://doi.org/10.1007/s10530-020-02200-0
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). From a harmful perspective to biodiversity, it concerns the interactions change of the of native biological communities, such as competition, predation, parasitism, changes in the food web, hybridization, which can lead to changes in the community structure and even local extinctions (Mack et al. 2000MACK, R.N., SIMBERLOFF, D., LONSDALE, W.M., EVANS, H., CLOUT, M., BAZZAZ, F.A. 2000. Biological Invasions: causes, epidemiology, global consequences and control. Ecol. Applic. 10:689–710. https://doi.org/10.1890/10510761(2000)010[0689:BICEGC]2.0.CO;2
https://doi.org/10.1890/10510761(2000)01...
, Simberloff & Rejmáne 2011SIMBERLOFF, D. & REJMÁNEK, M. 2011. Encyclopedia of Biological Invasions. University of California Press, Oakland, California, U.S.A., Doherty et al. 2016DOHERTY, T.S., GLEN, A.S., NIMMO, D.G., RITCHIE, E.G. & DICKMAN, C.R. 2016. Invasive predators and global biodiversity loss. Proc. Natl. Acad. Sci. 113(40):11261–11265. www.pnas.org/lookup/suppl/doi:10.1073/pnas.1602480113/-/DCSupplemental
www.pnas.org/lookup/suppl/doi:10.1073/pn...
, Frehse et al. 2016FREHSE, F.A., BRAGA, R.R., NOCERA, G.A. & VITULE, J.R.S. 2016. Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biol. Invasions.18(12):3713–3725.).

Reviewing publications on biological invasions in Brazil, Frehse et al. (2016FREHSE, F.A., BRAGA, R.R., NOCERA, G.A. & VITULE, J.R.S. 2016. Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biol. Invasions.18(12):3713–3725.) describe the introduction of 980 animal species in the country and point out that almost a third of these were intentionally introduced for some economic purpose. Regarding vertebrates, the occurrence of 137 invasive species in Brazil is reported, which represents about two percent of the non-marine vertebrate fauna, registered for the country (Rocha et al. 2011ROCHA, C.F.D., BERGALLO, H.G. & MAZZONI, R. 2011. Invasive vertebrates in Brazil. In: Pimentel D (Ed.). Economic and Environmental Costs of Alien Plant, Animal, and Microbe Species. 2nd. ed. New York: CRC Press. p53–103.). Have also to consider the existence of internal bioinvasions, that is, environments occupations by national species, but not native to that environment.

Despite the increasing number of studies, aquatic bioinvasion systems are still little reported in Latin America (Pysek et al. 2008PYSEK, P., RICHARDSON, D.M., PERGL, J., JAROSIK, V., SIXTOVA, Z. & WEBER, E. 2008. Geographical and taxonomic biases in invasion ecology. Trends Ecol. Evol. 23(5):237–244. https://doi.org/10.1016/j.tree.2008.02.002
https://doi.org/10.1016/j.tree.2008.02.0...
). In Brazil, from the end of the last century, scientific research on bioinvasion in aquatic systems has been intensified, increasing the introduced exotic species registration (Sousa et al. 2009SOUZA, R.C.C.L., CALAZANS, S.H. & SILVA, E.P. 2009. Impacto das espécies invasoras no ambiente aquático. Ciênc. Cult. 61(1):35–41.). However, available data on aquatic bioinvasions are still sparse and restricted to certain species or regions (Sousa et al. 2009SOUZA, R.C.C.L., CALAZANS, S.H. & SILVA, E.P. 2009. Impacto das espécies invasoras no ambiente aquático. Ciênc. Cult. 61(1):35–41.), which results in concern about the biodiversity of Brazilian aquatic systems.

The Pantanal biome is no exception to the occurrence of exotic species, since after human occupation, non-native plants and animals were introduced, either intentionally or accidentally, altering the natural ecological communities (Alho et al. 2011ALHO, C.J.R., MAMEDE, S., BITENCOURT, K. & BENITES, M. 2011. Introduced species in the Pantanal: implications for conservation. Braz. J. Biol. 71:321–325. https://doi.org/10.1590/S1519-69842011000200011
https://doi.org/10.1590/S1519-6984201100...
). This biome has the largest continuous wetland on the planet, with approximately 140,000 km2, distributed along the Paraguay River basin (Harris et al. 2005HARRIS, M.B., TOMAS, W.M., MOURÃO, G., SILVA, C.J., GUIMARÃES, E., SONODA, F. & FACHIM, E. 2005. Desafios para proteger o Pantanal brasileiro: ameaças e iniciativas em conservação. Megadiversidade 1(1):56–164.). The main Pantanal characteristic is its alternation of habitats between flooded and dry periods, causing the lateral overflow of rivers and lakes (Alho 2008ALHO, C.J.R. 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmental degradation. Braz. J. Biol. 68(4):957–996. https://doi.org/10.1590/S1519-69842008000500005
https://doi.org/10.1590/S1519-6984200800...
). These characteristics mainly favor the establishment of aquatic or semi-aquatic species. This biome is still poorly studied and has only two federal conservation units in the territory, the Taiamã Ecological Station (TES) and the Pantanal National Park. Therefore, the occurrence of an invasive species in these protected areas in the Pantanal is worrying, and the introduction and species reproduction in a conservation unit area is prohibited by Federal Law Nº. 9985/00 Art. 31 (Sampaio & Schmidt 2013SAMPAIO, A.B. & SCHMIDT, I.B. 2013. Espécies exóticas invasoras em Unidades de Conservação federais do Brasil. Biodivers. Bras. 3(2):32–49.).

Several taxonomic groups have the potential for bioinvasion including reptiles (Gisp 2005GISP. 2005. Programa Global de Espécies Invasoras. América do Sul invadida. A crescente ameaça das espécies exóticas invasoras, p80. ISBN 1-919684-48-4.). Among reptiles, turtles are an important invasive fauna, because many species of this group are capable to adapt to a wide variety of environments and are easily established in different aquatic environments (Gisp 2005GISP. 2005. Programa Global de Espécies Invasoras. América do Sul invadida. A crescente ameaça das espécies exóticas invasoras, p80. ISBN 1-919684-48-4.). Currently, Brazil has records of invasive turtle species, including introductions from other countries or even native species in non-native environments, as is the case with Trachemys scripta, an United States native species that was introduced in Brazil and today can be found for example in the central-west, northeast and south regions of the country (see Vieira & Costa 2006VIEIRA, C.S. & COSTA, E.M.M. 2006. Análise da estrutura populacional de Trachemys scripta elegans (Chelonia) no Parque Ecológico Olhos D’Água – Brasília-DF. Universitas: Cien Saude. 4(1–2):1–8. DOI: https://doi.org/10.5102/ucs.v4i1.18
https://doi.org/10.5102/ucs.v4i1.18...
, Leão et al. 2011LEÃO, T.C.C., ALMEIDA, W.R., DECHOUM, M. & ZILLER, S.R. 2011. Espécies exóticas invasoras no Nordeste do Brasil: contextualização, manejo e políticas públicas: 1–99. CEPAN/Instituto Hórus, Recife., Tortato et al. 2014TORTATO, M.A., BRESSAN, R.F. & KUNZ, T.S. 2014. Reproduction of two exotic species of Trachemys Agassiz, 1857 (Testudines, Emydidae) at Parque Estadual da Serra do Tabuleiro, state of Santa Catarina, southern Brazil. Herpetol Notes. 7:11–15., Ferreira et al. 2016FERREIRA, V.L., TERRA, J.S., PIATTI, L., DELATORRE, M., STRÜSSMANN, C., BÉDA, A.F., KAWASHITA-RIBEIRO, R.A., LANDGREF-FILHO, P., AOKI, C., CAMPOS, Z., SOUZA, F.L., ÁVILA, R.W., DULEBA, S., MARTINS, K.S., RITA, P.H.S. & ALBUQUERQUE, N.R. 2016. Répteis do Mato Grosso do Sul, Brasil. Iherringia 107: 13. https://doi.org/10.1590/1678-4766e2017153
https://doi.org/10.1590/1678-4766e201715...
). Trachemys dorbigni, whose original distribution is Uruguay, Northeast Argentina and the central southern portion of Rio Grande do Sul, Brazil, was recently registered as introduced of Santa Catarina and São Paulo states (see Santos et al. 2009, Tortato et al. 2014TORTATO, M.A., BRESSAN, R.F. & KUNZ, T.S. 2014. Reproduction of two exotic species of Trachemys Agassiz, 1857 (Testudines, Emydidae) at Parque Estadual da Serra do Tabuleiro, state of Santa Catarina, southern Brazil. Herpetol Notes. 7:11–15.). Trachemys scripta and T. dorbigni are species officially listed as invasive in Santa Catarina state (Consema 2010CONSEMA. 2010. Conselho Estadual de Meio Ambiente de Santa Catariana. Resolução CONSEMA Nº 11, de 17 de dezembro de 2010. Disponivel em: http://www.institutohorus.org.br/download/marcos_legais/Resolucao_CONSEMA_ SC_11_2010.pdf
http://www.institutohorus.org.br/downloa...
). Podocnemis expansa and P. unifilis are originally described for the Orinoco, Amazonas and Araguaia-Tocantins river basins, (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., Santos & Blamires 2012SANTOS, D.R. & BLAMIRES, D. 2012. Relação entre data de descrição, tamanho corporal e área de distribuição geográfica dos quelônios Sulamericanos. Bio. J. 28:439–444.; van Dijk et al. 2014VAN DIJK, P.P., INVERSON, J.B., RHODIN, A.G.J., SHAFTER, B.H. & BOUR, R. 2014. Turtles of the World, 7th Edition: Annotated Checklist of Taxonomy, Synonymy, Distribution with Maps, and Conservation Status. Chelonian Conserv. Biol. 7:329–479., Cantarelli et al. 2014CANTARELLE, V.H., MALVASIO, A. & VERDADE, L.M. 2014. Brazil’s Podocnemis expansa Conservation Program: Retrospective and Future. Chelonian Conserv. Biol. 13:124–128. https://doi.org/10.2744/CCB-0926.1
https://doi.org/10.2744/CCB-0926.1...
), however, both species have already been found in Pernambuco state (Santos et al. 2016SANTOS, E., RAMEH-DE-ALBUQUERQUE, L.C., ZANOTTI, A.P., PEREIRA, E.M. & SANTOS, E.M. 2016. Podocnemis expansa (Schweigger, 1812) (Reptilia, Testudines, Podocnemidae): espécie exótica no estado de Pernambuco, Nordeste, Brasil. Boletim do Museu Paraense Emílio Goeldi. Ciências Naturais 10(2):261–265., Souza et al. 2019SOUZA, D.T.M.T.O., CORREIA, J.M.S., RAMEH-DE-ALBUQUERQUE, L.C. & SANTOS, E.M. 2019. Record of exotic species Yellow-spotted river turtle (Podocnemis unifilis Podocnemididae) in a Conservation Unit in Northeastern Brazil. Herpetol Notes. 12:87–89.) and P. unifilis also in Mato Grosso do Sul state (Ferreira et al. 2016FERREIRA, V.L., TERRA, J.S., PIATTI, L., DELATORRE, M., STRÜSSMANN, C., BÉDA, A.F., KAWASHITA-RIBEIRO, R.A., LANDGREF-FILHO, P., AOKI, C., CAMPOS, Z., SOUZA, F.L., ÁVILA, R.W., DULEBA, S., MARTINS, K.S., RITA, P.H.S. & ALBUQUERQUE, N.R. 2016. Répteis do Mato Grosso do Sul, Brasil. Iherringia 107: 13. https://doi.org/10.1590/1678-4766e2017153
https://doi.org/10.1590/1678-4766e201715...
, Caramaschi 2020CARAMASCHI, U. 2020. Podocnemis unifilis Troschel, 1848 (Testudines, Podocnemididae) – distribution extension and new state record in Brazil. Herpetol. Bras. 9(3):140–145.). These are some works that demonstrate the invasive potential of the Chelonians, including species native to Brazil introduced outside their natural origin areas.

Podocnemis unifilis, popularly known as “tracajá”, is one of the most widely distributed species of the genus Podocnemis (see Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.). It has high plasticity, occupying a wide variety of aquatic habitats, such as large rivers, lakes, meandering lakes, swamps, marshes, white, black or clear water rivers (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p.). Females of this species can reach a little more than 50 cm in length with an approximate weight of 12 kg and can spawn in several places, such as beaches and river banks (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p.). Their nests can be dug either in the sand, in the clay or a mixture of soil with plant remains (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.). A female can spawn 15 to 30 eggs (Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.), and the offspring born after a period of 48 to 89 days (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., MMA 2016MMA. 2016. Ministério do Meio Ambiente: Manejo Conservacionista e Monitoramento Populacional de Quelônios Amazônicos. Brasília. p138.).

The species P. unifilis occurs naturally in the Amazon, Oniroco and Araguaia-Tocantins basins, covering Brazil, Colombia, Venezuela, Peru, Equator, Bolivia, Guyana, French Guiana and Suriname (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., Schneider et al. 2012SCHNEIDER, L., IVERSON, J.B. & VOGT, R.C. 2012. Podocnemis unifilis. Catalogue of American Amphibians and Reptiles (CAAR) 890:3–33., Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3., Rhodin et al. 2017RHODIN, A.G.J., IVERSON, J.B., BOUR, R., FRITZ, U., GEORGES, A., SHAFFER, H.B. & VAN DIJK, P.P. 2017. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. (8th ed.) Chelonian Res. Monogr. 7(8):1–292. ISBN: 978-1-5323-5026-9.). However, in none of Testudines’ assessments, (Vogt et al. 2015VOGT, R.C., FAGUNDES, C.K., BATAUS, Y.S.L., BALESTRA, R.A.M., BATISTA, F.R.W., UHLIG, V.M., SILVEIRA, A.L., BAGER, A., BATISTELLA, A.M., SOUZA, F.L., DRUMMOND, G.M., REIS, I.J., BERNHARD, R., MENDONÇA, S.H.S.T. & LUZ, V.L.F. 2015. Avaliação do Risco de Extinção de Podocnemis expansa (Schweigger, 1812) no Brasil. Processo de avaliação do risco de extinção da fauna brasileira. ICMBio. http://www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/estado-de-conservacao/7431-repteis-podocnemis-expansa-tartaruga-da-amazonia2.html
http://www.icmbio.gov.br/portal/biodiver...
, Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3., Rhodin et al. 2017RHODIN, A.G.J., IVERSON, J.B., BOUR, R., FRITZ, U., GEORGES, A., SHAFFER, H.B. & VAN DIJK, P.P. 2017. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. (8th ed.) Chelonian Res. Monogr. 7(8):1–292. ISBN: 978-1-5323-5026-9.) or studies with reptiles in the Northern Pantanal (see Strüssmann et al. 2011STRÜSSMANN, C., PRADO, C.P., FERREIRA, V.L. & KAWASHITA-RIBEIRO, R. 2011. Diversity, ecology, management and conservation of amphibians and reptiles of the Brazilian Pantanal: a review. The Pantanal: Ecology, biodiversity ad sustainable management of a large neotropical seasonal wetland (WJ Junk, CJ Da Silva & KM Wantzen eds.). Pensoft Publishers. Sofia-Moscow 497–521., ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.) reports the species P. unifilis or any congener to this portion of the Pantanal. Furthermore, the records of the introduction of P. unifilis in the Paraguay River in the state of Mato Grosso do Sul are punctual and the structure of the population species is still unknown to the Pantanal.

Thus, the present work aims to report the first records populations of P. unifilis for the Northern Pantanal, Mato Grosso state, Brazil, considering a case of introduction and presenting the species first records at the Taiamã Ecological Station (TES), one of two federal conservation areas in the Pantanal biome.

Material and Methods

1. Species identification

To identify the specimes we used it as a base taxonomic key of Amazonian chelonians (Ferrara 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.). Voucher specimens deposited in the herpetological collection of the Limnology, Biodiversity, Ethnobiology of Pantanal Research Center (CELBE), of the State University of Mato Grosso (UNEMAT) were also used to identify the species. We carried out morphological characteristics analyzes of adult specimens, hatchling turtles and eggs, found in the Paraguay River. We also got the help of Dr. Richard C. Vogt, a researcher with extensive experience in South American turtles, who confirmed the identification of the specimens through pictures.

2. Study area

The study area comprises a stretch of the Paraguay River of approximately 440 km long, located between the confluence of the Sepotuda and Paraguay rivers (15° 55'26.51" S and 57° 39'8.69" W), and approximately 15 km to the downstream of the Taiamã Ecological Station (17° 1'37.07" S 57° 22'38.77" W) (Figure 1). Within this stretch, the largest beach found is “Furo do touro” (16° 11'02.87" S and 57° 46'55" W), approximately 25 km, downstream from the Cáceres-MT city center. The “Furo do touro” beach is formed by white sand, with an approximate 400 m length × 105 m wide, parallel to the Paraguay River, which forms between the months of July and November with the water level reduction, in the dry season. This region constitutes the Upper Course of the Paraguay River and is described as Pantanal of Cáceres (Silva and Abdon 1998SILVA, J.S.V. & ABDON, M.M. 1998. Delimitação do Pantanal brasileiro e suas sub-regiões. Revista PAB 33:1703–1711., Leandro & Souza 2012LEANDRO, G.R.S. & SOUZA, C.A. 2012. Pantanal de Cáceres: composição granulométrica dos sedimentos de fundo no rio Paraguai entre a foz do rio Cabaçal e a cidade de Cáceres, Mato Grosso, Brasil. Rev. Ambient. Água. 7:263–276.) consisting of the beginning of the Pantanal floodplain.

Figure 1.
Distribution map of P. unifilis. Green polygon represents the species natural distribution as compiled by data from Ferrara et al. (2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.); Red star corresponds to Santos et al. (2016SANTOS, E., RAMEH-DE-ALBUQUERQUE, L.C., ZANOTTI, A.P., PEREIRA, E.M. & SANTOS, E.M. 2016. Podocnemis expansa (Schweigger, 1812) (Reptilia, Testudines, Podocnemidae): espécie exótica no estado de Pernambuco, Nordeste, Brasil. Boletim do Museu Paraense Emílio Goeldi. Ciências Naturais 10(2):261–265.); The orange star corresponds to Ferreira et al. (2016FERREIRA, V.L., TERRA, J.S., PIATTI, L., DELATORRE, M., STRÜSSMANN, C., BÉDA, A.F., KAWASHITA-RIBEIRO, R.A., LANDGREF-FILHO, P., AOKI, C., CAMPOS, Z., SOUZA, F.L., ÁVILA, R.W., DULEBA, S., MARTINS, K.S., RITA, P.H.S. & ALBUQUERQUE, N.R. 2016. Répteis do Mato Grosso do Sul, Brasil. Iherringia 107: 13. https://doi.org/10.1590/1678-4766e2017153
https://doi.org/10.1590/1678-4766e201715...
); The blue star corresponds to Caramaschi (2020)CARAMASCHI, U. 2020. Podocnemis unifilis Troschel, 1848 (Testudines, Podocnemididae) – distribution extension and new state record in Brazil. Herpetol. Bras. 9(3):140–145.; and the black stars corresponds to the new records of P. unifilis in the Paraguay River, Northern Pantanal, Mato Grosso state, Brazil.

According to Alvares et al. (2014ALVARES, C.A., STAPE, J.L., SENTELHAS, P.C., MORAES, G., LEONARDO, J. & SPAROVEK, G. 2014. Köppen’s climate classification map for Brazil. Meteorol. Z. 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
), the region’s climate is of the Aw type (wet and dry tropical, or of savanna climate). The average annual precipitation is 1,330 mm with temperatures ranging from 10ºC in June to 38ºC in December (Resende et al. 1994RESENDE, M.S., SANDANIELO, A. & COUTO, E.G. 1994. Zoneamento agroecológico do sudoeste do estado de Mato Grosso. Documentos 4. EMPAER/EMBRAPA. p130.). The vegetation in this area diverges, with the transition area between the Cerrado and the Amazon Forest biomes in its upstream portion (Silva-Júnior et al. 2019SILVA-JUNIOR, C.A., COSTA, G.M., ROSSI, F.S., VALE, J.C.E., LIMA, R.B., LIMA, M., OLIVEIRA-JUNIOR, J.F., TEODORA, P.E. & SANTOS, R.C. 2019. Remote sensing for updating the boundaries between the Brazilian Cerrado-Amazonia biomes. Environ Sci Policy. 101:383–392. https://doi.org/10.1016/j.envsci.2019.04.006
https://doi.org/10.1016/j.envsci.2019.04...
). In its intermediate portion, between the urban centre of Cáceres and further downstream, in TES the vegetation is characterized by typical tree formations of riparian forest, with trees belonging to the Cerrado biome or the semideciduous forest and covered fields composed of grasses, both seasonally flooded (ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.).

3. Taiamã Ecological Station (TES)

TES is located in the Mato Grosso state, in its northern portion, within the limits of the municipality of Cáceres, between the meridians W 57º 24' and W 45° 40' and parallels S 16° 48' and W 16° 58' (ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.). It has a total area of 11,555 ha strongly influenced by the marked seasonality of the Paraguay River hydrological regime, which leads to the structuring of a wide variety of aquatic environments such as permanent, temporary lagoons, meandering lagoons and small channels that connect lakes and river (ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.). TES has an important role in protecting the Pantanal biodiversity, as it is one of the few areas, institutionally, protected within the Pantanal. The station presents a series of measures that provide for the control of the impact of invasive alien species on the biological diversity of native species. However, until now P. unifilis is not one of the invasive species for the Northern Pantanal region and occurs in TES (ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.).

4. Field data collection

The P. unifilis species’ first records in the Paraguay River occurred occasionally, during sport fishing activity, carried out by the researchers in the years 2014 and 2015. During the following years, from 2016 to 2019, systematic observations were made through nautical incursions courses along the Paraguay River, in the studied stretch. The incursions were carried out during the drought period between July and November. Sampling took place using the direct observation method when the specimens were found lounging on beaches. This method consists of counting animals that are exposed to the sun on logs or the river banks and lakes. This strategy has been used successfully by authors such as Pluto and Bellis (1986)PLUTO, T.G. & BEELIS, E.D. 1986. Habitat utilization by the turtle, Graptemys geographica, along a river. J. Herpet. 20:22–3. https://doi.org/10.2307/1564121
https://doi.org/10.2307/1564121...
, Conway-Gómez (2007)CONWAY-GÓMEZ, K. 2017. Effects of human settlements on abundance of Podocnemis unifilis and P. expansa turtles in northeastern Bolivia. Chelonian Conserv. Biol. 6:199–205. https://doi.org/10.2744/1071-8443(2007)6[199:EOHSOA]2.0.CO;2
https://doi.org/10.2744/1071-8443(2007)6...
and Segurado and Figueiredo (2007)SEGURADO, P. & FIGUEIREDO, D. 2007. Coexistence of two freshwater turtle species along a Mediterranean stream: The role of spatial and temporal heterogeneity. Acta Oecol. 32:134–144. https://doi.org/10.1016/j.actao.2007.03.015
https://doi.org/10.1016/j.actao.2007.03....
.

We also include records made on occasional or opportunistic collections, which occurred during the conduct of other research or fishing activity by professional fishermen and/or amateurs. These records were confirmed utilizing photos and the location of the visualization. Subsequently, these points were located on maps and the geographic coordinate was obtained.

We collected some hatchling that were found dead after birth. The collected animals were deposited in the herpetological collection at Centro de Pesquisa em Limnologia, Biodiversidade, Etnobiologia do Pantanal (CELBE), of State University of Mato Grosso (UNEMAT), (permanent license from Sistema of Autorização and Informações on Biodiversidade – SISBIO – número 8849-1).

We also carried out a historical bibliographic review in scientific articles and relief maps, observing the main natural barriers that separate the watersheds with the natural occurrence of P. unifilis and the Paraguay river basin, to verify a possible natural migration of the species. Finally, we analyzed historical records related to the municipality of Cáceres. Through historical documents, historians, official websites such as the city hall website, International Fishing Festival (Festival Internacional de Pesca esportiva – FIPe) and the Institute of National Artistic Historical Patrimony (Instituto of Patrimônio Histórico Artístico Nacional – IPHAN). We also obtained information from fishermen from pioneer families in the city of Cáceres.

Results

1. Records

In October 2014, seven nests of P. unifilis were observed, with eggs already hatched (Figure 2a, b and c), and 18 hatchling turtles on the “Furo do touro” beach (Figure 3).

Figure 2.
(a) “Furo do Touro” beach, on the Paraguay River, in the Pantanal of Cáceres, Mato Grosso state; (b and c) Traces and nest of P. unifilis, found on the “Furo do touro” beach in October 2014. Photographs by Dionei J. Silva.
Figure 3.
(a) Nest with eggs, (b, c) Live baby P. unifilis e (d) dead baby turtles of P. unifilis on “Furo do touro” beach, in the Pantanal of Cáceres, Mato Grosso state, Brazil. Photographs by Amabilen Furlan; Claumir For Review Only Muniz and Dionei Silva.

In September 2015, 22 adult individuals were sighted near the confluence of the Sepotuba River with the Paraguay River. In October 2017, two young specimens of P. unifilis were accidentally collected from fishing nets, while researchers from the State University of Mato Grosso collected fish in a bay downstream from the beach “Furo do touro”, these animals were collected and deposited in the herpetology collection at the CELBE (CELBE-Q-0001; CELBE-Q-0002). At the end of August 2019, we registered four nests, with about 26 eggs each, on a beach 2 km upstream of the “Furo do touro” beach. In October 2019, the largest number of nests was observed, where we observed traces of 85 nests with eggs already hatched on the “Furo do touro” beach. In that same month, we recorded an adult specimen of P. unifilis looming on a dirt and clay beach downstream from TES. Besides, between 2016 and 2019, adult and young specimens were regularly observed in bays and on beaches along the “Furo do touro” beach and the mouth of the Sepotuba river, along the course of the Paraguay river, (Figure4). In November 2019, two specimens were recorded lounging on a beach within the perimeters of TES. Four nests were also recorded, which indicates that the species is established and reproducing within the conservation unit.

Figure 4.
(a–d) Records of specimens of P. unifilis, young and adult on logs and beaches along the study area in the Pantanal de Cáceres, Mato Grosso, Brazil. Photographs by Claumir Muniz and Dionei J. Silva.

2. Historical surveys

According to information from residents, the specimens were introduced into the Paraguay River in the 1970s, released near the urban center of the municipality of Cáceres. The first specimens were reportedly brought from the Amazonas state by the Fanaia family patriarch (family report). These animals remained close to the urban nucleus, where there are reports from residents that around 1985 some specimens were recaptured and placed in a fountain, located in the Major João Carlos square, where they remained for years (residents’ report).

Discussion

1. Migration hypothesis

The hypothesis of P. unifilis specimens migration to this portion of the Paraguay River from the Guaporé River, which belongs to the Amazon basin where the species presence is recorded (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., Schneider et al. 2012SCHNEIDER, L., IVERSON, J.B. & VOGT, R.C. 2012. Podocnemis unifilis. Catalogue of American Amphibians and Reptiles (CAAR) 890:3–33., Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3., Rhodin et al. 2017RHODIN, A.G.J., IVERSON, J.B., BOUR, R., FRITZ, U., GEORGES, A., SHAFFER, H.B. & VAN DIJK, P.P. 2017. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. (8th ed.) Chelonian Res. Monogr. 7(8):1–292. ISBN: 978-1-5323-5026-9.), is initially discarded. The possibility is unlikely considering that there is no direct connection between the Paraguay and Guaporé rivers and that the distance between them, at the nearest record point, is approximately 160 km.

Due to the residual plateaus, it is not considered that the Paraguay River basin is connected to the Guaporé River basin (MMA 2006MMA. 2006. Ministério do Meio Ambiente: Caderno da Região Hidrográfica do Paraguai/Ministério do Meio Ambiente, Secretaria de Recursos Hídricos. Brasília. p140.). However, the Upper Paraguay-Guaporé depressions are indirectly connected by a slightly sloping segment, where the distance between the Guaporé River and the Upper Jauru River basins is approximately 5 km (Ross 1985ROSS, J. 1985. Relevo brasileiro: uma nova proposta de classificação. Revista do Departamento de Geografia 4:25–39.), where Jauru River is an important tributary of the Paraguay River.

By the aforementioned connection, a remote possibility of transposing the species from the Guaporé basin to the Paraguay River basin could be considered, however, there are no species occurrence records in these regions (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., Schneider et al. 2012SCHNEIDER, L., IVERSON, J.B. & VOGT, R.C. 2012. Podocnemis unifilis. Catalogue of American Amphibians and Reptiles (CAAR) 890:3–33., Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3., Rhodin et al. 2017RHODIN, A.G.J., IVERSON, J.B., BOUR, R., FRITZ, U., GEORGES, A., SHAFFER, H.B. & VAN DIJK, P.P. 2017. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. (8th ed.) Chelonian Res. Monogr. 7(8):1–292. ISBN: 978-1-5323-5026-9.). Likewise, there are no records of any floods that have established water contact between the two basins. Another point that rules out natural migration is the fact that our P. unifilis records in the Paraguay River are concentrated close to the urban nucleus of the municipality of Cáceres and the record closest points of P. unifilis in the Guaporé River (Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.) are about 425 km away from our records (see Figure 1). Migration from another basin is also ruled out, since the closest occurrence point of P. unifilis, in our records, besides the Guaporé River, is in the Araguaia River, in locations that are about 650 km from this portion of the Paraguay River.

2. Introduction hypothesis

The municipality of Cáceres was formed from a small village named Vila Maria do Paraguay, founded in 1778, in the Pantanal of the Mato Grosso state (IPHAN 2020IPHAN. 2020. Instituto do Patrimônio Histórico Artístico Nacional. Disponível em http://portal.iphan.gov.br/pagina/detalhes/367/, acesso em 08 Maio de 2020
http://portal.iphan.gov.br/pagina/detalh...
). At the end of the 19th century, Cáceres played a prominent role in the state economy mainly because of its location, on the banks of the Paraguay River, whereby many means of transport, exported and imported varied commodities (Pinho 2013PINHO, R.T. 2013. Entre monumentos e documentos: Reflexões sobre os tombamentos de Cáceres-MT. XXVII Simpósio nacional de história. https://anpuh.org.br/uploads/anais-simposios/pdf/2019-01/1548875179_1ed5cd12806b2287e46310fe80cc76a5.pdf
https://anpuh.org.br/uploads/anais-simpo...
). However, with improvements in the construction of the road network, especially with the construction of the “Marechal Rondon” bridge over the Paraguay River in the 1950s (Almeida 2014ALMEIDA, L. 2014. A Avenida sete de setembro em Cáceres-MT: História e memória. História, Natureza e Espaço, 3(1):p19.) connecting Cáceres to the western region of the state and part of the northern region of Brazil (Silva et al. 2007SILVA, A., SOUZA, C. A. & ZANI, H. 2007. Avaliação da erosão na margem direita do rio Paraguai a jusante da praia do Julião município de Cáceres-MT. Revista Geográfica Acadêmica, 1(1):5–19.), made it possible to increase land transport to the city. Subsequently, the construction of the bus terminal in the center of Cáceres, as well as the improvement of the old airport called “Manoel Cuiabano” (Almeida 2014ALMEIDA, L. 2014. A Avenida sete de setembro em Cáceres-MT: História e memória. História, Natureza e Espaço, 3(1):p19.) provided Cáceres with a greater flow of people and objects.

So, considering that: (1) the majority of P. unifilis nest and adult records in the Northern Pantanal, are close to the urban center of Cáceres and; (2) taking into account the fact that tracajás return to the same nesting sites and feeding lakes (Andrade et al. 2015ANDRADE, P.C.M., AZEVEDO, S.H., DUARTE, J.A.M., GARCEZ, J.R., OLIVEIRA, P.H.G., PINTO, J.R.S. & ALMEIDA, JR.C.D. 2015. Projeto Pé-de-pincha: Conservação e manejo de quelônios – Manual para Gestores Ambientais – N.2 Editor/Organizador: Paulo César Machado Andrade – Manaus: UNISOL/UFAM. ISBN 978-85-9510-009-1.), and; (3) distance and geographical barriers in its area of occurrence and; (4) the historical reports of residents, it is palpable to assume that P. unifilis was introduced close to the urban center of Cáceres, in the recent past.

This hypothesis is reinforced by the fact that in conversations with fishermen and riverside dwellers and residents, we did not obtain reports of turtle registration before the 1950s. The recent introduction is also reinforced by studies with the distribution of turtles (Van Dikj et al. 2014VAN DIJK, P.P., INVERSON, J.B., RHODIN, A.G.J., SHAFTER, B.H. & BOUR, R. 2014. Turtles of the World, 7th Edition: Annotated Checklist of Taxonomy, Synonymy, Distribution with Maps, and Conservation Status. Chelonian Conserv. Biol. 7:329–479., Vogt et al. 2015VOGT, R.C., FAGUNDES, C.K., BATAUS, Y.S.L., BALESTRA, R.A.M., BATISTA, F.R.W., UHLIG, V.M., SILVEIRA, A.L., BAGER, A., BATISTELLA, A.M., SOUZA, F.L., DRUMMOND, G.M., REIS, I.J., BERNHARD, R., MENDONÇA, S.H.S.T. & LUZ, V.L.F. 2015. Avaliação do Risco de Extinção de Podocnemis expansa (Schweigger, 1812) no Brasil. Processo de avaliação do risco de extinção da fauna brasileira. ICMBio. http://www.icmbio.gov.br/portal/biodiversidade/fauna-brasileira/estado-de-conservacao/7431-repteis-podocnemis-expansa-tartaruga-da-amazonia2.html
http://www.icmbio.gov.br/portal/biodiver...
, Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3., Rhodin et al. 2017RHODIN, A.G.J., IVERSON, J.B., BOUR, R., FRITZ, U., GEORGES, A., SHAFFER, H.B. & VAN DIJK, P.P. 2017. Turtles of the world: annotated checklist and atlas of taxonomy, synonymy, distribution, and conservation status. (8th ed.) Chelonian Res. Monogr. 7(8):1–292. ISBN: 978-1-5323-5026-9.), and studies with herpetofauna in the Pantanal (Strüssmann et al. 2011STRÜSSMANN, C., PRADO, C.P., FERREIRA, V.L. & KAWASHITA-RIBEIRO, R. 2011. Diversity, ecology, management and conservation of amphibians and reptiles of the Brazilian Pantanal: a review. The Pantanal: Ecology, biodiversity ad sustainable management of a large neotropical seasonal wetland (WJ Junk, CJ Da Silva & KM Wantzen eds.). Pensoft Publishers. Sofia-Moscow 497–521., ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.) there is no indication of the species for the Northern Pantanal so far. This may be related to the fact that the species took several years to reach a population size in which individuals could be noticed by the population.

3. Podocnemis unifilis in the Taiamã Ecological Station

After the species records in November 2019, we no longer obtained records of it within the ecological station. However, taking into account its high displacement capacity (IBAMA 2016IBAMA. 2016. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis: Manejo conservacionista e monitoramento populacional de quelônios amazônicos. Balestra RAM (Org). Ibama, Brasília, p136.), and our species records both downstream and upstream of the ecological station, it is reasonable to assume that P. unifilis occurs, even in low density, in the Paraguay River in the entire extension of the Taiamã Ecological Station. The fact that the species is reproducing inside the conservation unit is worrying, as it is an area intended for the reproduction and conservation of typical Pantanal species. The presence of an invasive species can directly generate competition with native species within the conservation unit, such as the aquatic Testudines Acanthochelys macrocephala and Phrynops geoffroanus and the pacu fish Piaractus mesopotamicus, which has a diet similar to P. unifilis and finds an important natural nursery in Taiamã (ICMBIO 2017ICMBIO. 2017. Instituto Chico Mendes de Conservação da Biodiversidade: Plano de Manejo da Estação Ecológica de Taiamã. 1o ed. Brasília, DF: Ministério do Meio Ambiente/ICMBIO, p174.).

4. Introduction problem

Chelonians have been used as an important food source by traditional Amazonian peoples for hundreds of years (Vogt 1994VOGT, R.C. 1994. Temperature controlled sex-determination as a tool for turtle conservation. Chelonian Conserv. Biol. 1(2):159–162., Eisemberg et al. 2019EISEMBERG, C.C., VOGT, R.C., BALESTRA, R.A.M., REYNOLDS, S.J. & CHRISTIAN, K. A. 2019. Don’t put all your eggs in one basket–Lessons learned from the largest-scale and longest-term wildlife conservation program in the Amazon Basin. Biol. Conserv. 238. https://doi.org/10.1016/j.biocon.2019.07.027
https://doi.org/10.1016/j.biocon.2019.07...
, Stanford et al. 2020STANFORD, C,B., IVERSON, J.B., RHODIN, A.G.J., VAN DIJK, P.P., MITTERMEIER, R.A., KUCHLING, G., BERRY, K.H., BERTOLERO, A., BJORNDAL, K.A., BLANCK, T.E.G., BUHLMANN, K.A., BURKE, R.L., CONGDON, J.D., DIAGNE, T., EDWARDS, T., EISEMBERG, C.C., ENNEN, J.R., FORERO-MEDINA, G., FRANKEL, M., FRITZ, U., GALLEGO-GARCI, N., GEORGES, A., GIBBONS, J.W., GONG, S., GOODE, E.V., SHI, H.T., HOANG, H., HOFMEYR, M.D., HORNE, B.D., HUDSON, R., JUVIK, J.O., KIESTER, R.A., KOVAL, P., LE, M., LINDEMAN, P.V., LOVICH, J.E., LUISELLI, L., MCCORMACK, T.E.M., MEYER, G.A., PAÉZ, V.P., PLATT, K., PLATT, S.G., PRITCHARD, P.C.H., QUINN, H.R., ROOSENBURG, W.M., SEMINOFF, J.A., SHAFFER, H.B., SPENCER, R., VAN DYKE, J.U., VOGT, R.C. & WALDE, A.D. 2020. Turtles and Tortoises Are in Trouble. Curr. Biol. 30(12), R721–R735. https://doi.org/10.1016/j.cub.2020.04.088
https://doi.org/10.1016/j.cub.2020.04.08...
). Turtle and eggs consumption is part of the Amazon culture (Andrade et al. 2015ANDRADE, P.C.M., AZEVEDO, S.H., DUARTE, J.A.M., GARCEZ, J.R., OLIVEIRA, P.H.G., PINTO, J.R.S. & ALMEIDA, JR.C.D. 2015. Projeto Pé-de-pincha: Conservação e manejo de quelônios – Manual para Gestores Ambientais – N.2 Editor/Organizador: Paulo César Machado Andrade – Manaus: UNISOL/UFAM. ISBN 978-85-9510-009-1.). These explorations have aimed not only at sustainable consumption of turtles but also at illegal trade in large urban centers (Fachín-Terán 1999FACHIN-TERÁN, A. 1999. Ecologia de Podocnemis sextuberculata (Testudines, Pelomedusidae), na Reserva de Desenvolvimento Sustentável Mamirauá, Amazonas, Brasil. Tese de Doutorado. Manaus: INPA/UFAM., Fachín-Terán et al. 2000FACHIN-TERÁN, A. 2000. Padrões de caça e uso de quelônios na Reserva de Desenvolvimento Sustentável Mamirauá, Amazonas, Brasil. In: Cabrera, E., Marcolli, C., Resquin R (Eds.). Manejo de fauna silvestre em Amazonia y Latinoamericana. Asunción, Paraguay, p323–337., Stanford et al. 2020STANFORD, C,B., IVERSON, J.B., RHODIN, A.G.J., VAN DIJK, P.P., MITTERMEIER, R.A., KUCHLING, G., BERRY, K.H., BERTOLERO, A., BJORNDAL, K.A., BLANCK, T.E.G., BUHLMANN, K.A., BURKE, R.L., CONGDON, J.D., DIAGNE, T., EDWARDS, T., EISEMBERG, C.C., ENNEN, J.R., FORERO-MEDINA, G., FRANKEL, M., FRITZ, U., GALLEGO-GARCI, N., GEORGES, A., GIBBONS, J.W., GONG, S., GOODE, E.V., SHI, H.T., HOANG, H., HOFMEYR, M.D., HORNE, B.D., HUDSON, R., JUVIK, J.O., KIESTER, R.A., KOVAL, P., LE, M., LINDEMAN, P.V., LOVICH, J.E., LUISELLI, L., MCCORMACK, T.E.M., MEYER, G.A., PAÉZ, V.P., PLATT, K., PLATT, S.G., PRITCHARD, P.C.H., QUINN, H.R., ROOSENBURG, W.M., SEMINOFF, J.A., SHAFFER, H.B., SPENCER, R., VAN DYKE, J.U., VOGT, R.C. & WALDE, A.D. 2020. Turtles and Tortoises Are in Trouble. Curr. Biol. 30(12), R721–R735. https://doi.org/10.1016/j.cub.2020.04.088
https://doi.org/10.1016/j.cub.2020.04.08...
) leading to super exploration. This is one of the main factors that make turtles be considered one of the most threatened animal groups on the planet (Vogt 2008VOGT, R.C. 2008. Tartarugas da Amazônia. Lima, Peru, 104p., IBAMA 2016IBAMA. 2016. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis: Manejo conservacionista e monitoramento populacional de quelônios amazônicos. Balestra RAM (Org). Ibama, Brasília, p136., Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3., Stanford et al. 2020STANFORD, C,B., IVERSON, J.B., RHODIN, A.G.J., VAN DIJK, P.P., MITTERMEIER, R.A., KUCHLING, G., BERRY, K.H., BERTOLERO, A., BJORNDAL, K.A., BLANCK, T.E.G., BUHLMANN, K.A., BURKE, R.L., CONGDON, J.D., DIAGNE, T., EDWARDS, T., EISEMBERG, C.C., ENNEN, J.R., FORERO-MEDINA, G., FRANKEL, M., FRITZ, U., GALLEGO-GARCI, N., GEORGES, A., GIBBONS, J.W., GONG, S., GOODE, E.V., SHI, H.T., HOANG, H., HOFMEYR, M.D., HORNE, B.D., HUDSON, R., JUVIK, J.O., KIESTER, R.A., KOVAL, P., LE, M., LINDEMAN, P.V., LOVICH, J.E., LUISELLI, L., MCCORMACK, T.E.M., MEYER, G.A., PAÉZ, V.P., PLATT, K., PLATT, S.G., PRITCHARD, P.C.H., QUINN, H.R., ROOSENBURG, W.M., SEMINOFF, J.A., SHAFFER, H.B., SPENCER, R., VAN DYKE, J.U., VOGT, R.C. & WALDE, A.D. 2020. Turtles and Tortoises Are in Trouble. Curr. Biol. 30(12), R721–R735. https://doi.org/10.1016/j.cub.2020.04.088
https://doi.org/10.1016/j.cub.2020.04.08...
).

In this new introduction area of P. unifilis in the Northern Pantanal, the consumption of tracajás and their eggs is not cultural, therefore, there is a tendency for the population to grow higher than those recorded in native habitats. Also, species’ natural characteristics, such as high longevity and displacement capacity (IBAMA 2016IBAMA. 2016. Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis: Manejo conservacionista e monitoramento populacional de quelônios amazônicos. Balestra RAM (Org). Ibama, Brasília, p136.), and its reproductive capacity, laying 15 to 30 eggs per year (Ferrara et al. 2017FERRARA, C.R., FAGUNDES, C.K., MORCATTY, T.Q. & VOGT, R.C. 2017. Quelônios Amazônicos: Guia de identificação e distribuição. Manaus, Brazil: Wildlife Conservation Society Brasil, p182. ISBN 978-85-93844-00-3.), favor the population increase. The favoring of the establishment and population increase of P. unifilis in the studied region is also due to the Pantanal environmental characteristics, which has several aquatic habitats suited to the characteristics of the species. In this way, areas of the Pantanal may allow good adaptation of this species in the northern portion of the Pantanal. In addition, its ability to move is also a cause for concern, as a recent record of P. unifilis for the Serra do Amolar region, Paraguay river basin (Caramaschi 2020CARAMASCHI, U. 2020. Podocnemis unifilis Troschel, 1848 (Testudines, Podocnemididae) – distribution extension and new state record in Brazil. Herpetol. Bras. 9(3):140–145.), might be the result of migration of this population described here, given that this record is located about 120 km downstream of the points at the Taiamã Ecological Station.

Thus, the occurrence of P. unifilis in the Pantanal brings ecological concerns since, in most cases, exotic species constitute threats to biodiversity, as they can modify the structure of the local community, changing the habitat and restructuring the community through new interspecific interactions (CrystalOrnelas & Lockwood 2020CRYSTAL-ORNELAS, R. & LOCKWOOD, J.L. 2020. The ‘known unknowns’ of invasive species impact measurement. Biol. Invasions. 22(4):1513–1525. https://doi.org/10.1007/s10530-020-02200-0
https://doi.org/10.1007/s10530-020-02200...
, Frehse et al. 2016FREHSE, F.A., BRAGA, R.R., NOCERA, G.A. & VITULE, J.R.S. 2016. Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biol. Invasions.18(12):3713–3725.). In this way, it can cause extinctions of native species (Cadi and Joly 2004CADI, A. & JOLY, P. 2004. Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodivers. Conserv. 13:2511–2518. https://doi.org/10.1023/B:BIOC.0000048451.07820.9c
https://doi.org/10.1023/B:BIOC.000004845...
, Alho & Gonçalves 2005ALHO, C.J.R. & GONÇALVES, H.C. 2005. Biodiversidade do Pantanal: ecologia e conservação. Campo Grande, Brazil: Uniderp, p142., Alho 2008ALHO, C.J.R. 2008. Biodiversity of the Pantanal: response to seasonal flooding regime and to environmental degradation. Braz. J. Biol. 68(4):957–996. https://doi.org/10.1590/S1519-69842008000500005
https://doi.org/10.1590/S1519-6984200800...
, Alho et al. 2011ALHO, C.J.R., MAMEDE, S., BITENCOURT, K. & BENITES, M. 2011. Introduced species in the Pantanal: implications for conservation. Braz. J. Biol. 71:321–325. https://doi.org/10.1590/S1519-69842011000200011
https://doi.org/10.1590/S1519-6984201100...
, Garcia-Diaz et al. 2015GARCIA-DIAZ, P., ROSS, J.V., AYRES, C. & CASSEY, P. 2015. Understanding the biological invasion risk posed by the global wildlife trade: propagule pressure drives the introduction and establishment of Nearctic turtles. Glob. Change Biol. 21:1078–1091. https://doi.org/10.1111/gcb.12790
https://doi.org/10.1111/gcb.12790...
).

Although the results of an introduction are difficult to predict, the most predictable consequences are competition with closely related species (Frehse et al. 2016FREHSE, F.A., BRAGA, R.R., NOCERA, G.A. & VITULE, J.R.S. 2016. Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biol. Invasions.18(12):3713–3725.). In studies with the introduction of turtles, Cadi & Joly (2003CADI, A. & JOLY, P. 2003. Competition for basking places between the endangered European pond turtle (Emys orbicularis galloitalica) and the introduced red-eared turtle (Trachemys scripta elegans). Can. J. Zool. 81:1392–1398. https://doi.org/10.1139/z03-108
https://doi.org/10.1139/z03-108...
) observed that Emys orbicularis ended up changing its thermoregulation habits, giving the best places for sunbathing to the species Trachemys scripta elegans, which is an introduced species. Finally, Cadi and Joly (2004CADI, A. & JOLY, P. 2004. Impact of the introduction of the red-eared slider (Trachemys scripta elegans) on survival rates of the European pond turtle (Emys orbicularis). Biodivers. Conserv. 13:2511–2518. https://doi.org/10.1023/B:BIOC.0000048451.07820.9c
https://doi.org/10.1023/B:BIOC.000004845...
) observed that the introduction of T. s. elegans caused weight loss and high mortality in the populations of E. orbicularis. Extensions of results like these can be aggravated for the Pantanal, as the Testudines constitute one of the most poorly sampled groups in this biome (Strüssmann et al. 2011STRÜSSMANN, C., PRADO, C.P., FERREIRA, V.L. & KAWASHITA-RIBEIRO, R. 2011. Diversity, ecology, management and conservation of amphibians and reptiles of the Brazilian Pantanal: a review. The Pantanal: Ecology, biodiversity ad sustainable management of a large neotropical seasonal wetland (WJ Junk, CJ Da Silva & KM Wantzen eds.). Pensoft Publishers. Sofia-Moscow 497–521.) and there are still many doubts and disagreements about the distribution of aquatic Testudines in the Pantanal. However, when considering the different approaches to invasive species (Frehse et al. 2016FREHSE, F.A., BRAGA, R.R., NOCERA, G.A. & VITULE, J.R.S. 2016. Non-native species and invasion biology in a megadiverse country: scientometric analysis and ecological interactions in Brazil. Biol. Invasions.18(12):3713–3725.), it is reasonable to predict that P. unifilis can cause direct competition with species of aquatic Testudines occurring in the Pantanal biome such as Acanthochelys macrocephala and Phrynops geoffroanus. Since with the introduction of P. unifilis there was a densification of individuals, competing for food and spawning grounds, since, for example, the diet of P. unifilis and P. geoffroanus are similar and we have already recorded P. unifilis and P. geoffroanus in a radius of 1 meter on a beach of the Paraguay River (personal communication), thus suggesting that P. unifilis can compete with native species in the wetland.

Several invasive species are registered in the Pantanal, such as the “Porco do mato” Sus scrofa (Linnaeus, 1758), the golden mussel Limnoperna fortunei (Dunker 1857), the “tucunaré”, Amazonian fish, Cichla cf. ocellaris Bloch and Schneider 1801, the “tambaqui from the Amazon”, Colossoma macropomum Cuvier, 1816, in addition to the various domesticated animals and grasses (Alho et al. 2011ALHO, C.J.R., MAMEDE, S., BITENCOURT, K. & BENITES, M. 2011. Introduced species in the Pantanal: implications for conservation. Braz. J. Biol. 71:321–325. https://doi.org/10.1590/S1519-69842011000200011
https://doi.org/10.1590/S1519-6984201100...
). Podocnemis unifilis starts to constitute the first exotic chelonian known to the Pantanal, whose ecological interactions may cause effects that are quickly visible to the biodiversity of the Pantanal. However, many of them will only be observed in the long term, which requires continuous monitoring of this species in the region.

Our records are the first of this kind for the Northern Pantanal, including Taiamã Ecological Station. We found that the species was introduced in this region of the Pantanal in the recent past and is currently established since it has been reproducing in the place for several years. The typical environment structure with large rivers, where forests are flooded during the flood season, the presence of large meanders, lakes and white sand beaches during the dry season are characteristics of suitable habitats for the species, ensuring conditions of the permanent establishment in the region.

If the presence of the species Podocnemis unifilis in this area of the Pantanal constitutes, in fact, an impact factor on the structure of the local communities, the registration of the species and its reproduction at the Taiamã Ecological Station, which is considered a nursery for several species of fish, is worrying. These facts point to the necessity for proposing research and studies seeking to understand how P. unifilis is structured in the Pantanal, seeking to understand its ecological aspects, such as reproduction, main predators, competition with native species and reproduction. Local monitoring programs are also essential to detect the evolution of the species’ occupation and distribution and to avoid possible damages.

Acknowledgements

This work was carried out with the support of the Coordenação of Aperfeiçoamento of Pessoal of Nível Superior – Brazil (CAPES) – financing code 001. We thank Richard Carl Vogt “in memorian” (Instituto Nacional de Pesquisas da Amazônia), for confirming the species identification; to the team of the Erosão da Biodiversidade project (UNEMAT/FAPEMAT/UFMT/UEA-UK), which has financial support from FAPEMAT (notice nº. 037/2016 – Redes de Pesquisa em Mato Grosso with concession term under no. 0589188/2016). We are also thankful for the records of the years 2016 and 2017; to the fishermen Jânio and Reis for their logistical support; to ICMBIO through the local coordination for the logistical support given to the research, to Taiamã Ecological Station in the person of Daniel Kantek. We also thank the team from the book “Quelônios Amazônicos: Guia de identificação e distribuição”, whose authors’ Camila Rudge Ferrara, Camila Kurzmann Fagundes, Thais Queiroz Marcatty and Richard C. Vogt work resulted in the database and historical natural distribution of P. unifilis, kindly provided by Camila Kurzmann Fagundes. We also thank Anamélia de Sousa Jesus for making the map and Richard C. Vogt “in memorian” for assisting in the species identification.

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Edited by

Associate Editor

Pedro Nunes

Publication Dates

  • Publication in this collection
    05 Aug 2022
  • Date of issue
    2022

History

  • Received
    13 Sept 2021
  • Accepted
    12 July 2022
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