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Original Article • Neotrop. ichthyol. 20 (03) • 2022 • https://doi.org/10.1590/1982-0224-2022-0022   copy

Fish biodiversity of a tropical estuary under severe anthropic pressure (Doce River, Brazil)

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

The Doce River has undergone severe changes over the last centuries (e.g., flow regulation, pollution, habitat and species loss). Here, we present the first comprehensive fish biodiversity assessment of the Doce River estuary and a summary of the main impacts and their drivers for the whole river since the early 18th century. Carangiformes, Siluriformes and Eupercaria incertae sedis were the most representative orders for the 115 species recorded. Most species are native (87.8%), euryhaline/peripheral (80%) and zoobenthivorous (33.9%). Threatened (Paragenidens grandoculis, Genidens barbus, and Lutjanus cyanopterus) and near threatened (Cynoscion acoupa, Dormitator maculatus, Lutjanus jocu, Lutjanus synagris, and Mugil liza) species are peripheral. Thirteen species are exotic at the country (Butis koilomatodon, Coptodon rendalli, and Oreochromis niloticus) or the basin level (e.g., Pygocentrus nattereri and Salminus brasiliensis). The catfish Cathorops cf. arenatus is reported for the first time on the eastern coast of Brazil and Paragenidens grandoculis, considered extinct in the Doce River, was discovered in the estuary.

Keywords:
Environmental impact; Estuarine; Ichthyofauna; Mining; Species richness

Resumo

O rio Doce tem passado por mudanças drásticas ao longo dos últimos séculos (e.g., alterações na vazão, poluição, perda de espécies e habitats). Neste trabalho, apresentamos a primeira avaliação abrangente da biodiversidade de peixes no estuário do rio Doce além de um resumo dos principais impactos e suas forçantes em toda a extensão do rio desde o início do século vinte. Carangiformes, Siluriformes e Eupercaria incertae sedis foram as ordens mais representativas considerando as 115 espécies registradas. A maioria das espécies são nativas (87,8%), eurialinas/periféricas (80%) e zoobentívoras (33,9%). As espécies ameaçadas (Paragenidens grandoculis, Genidens barbus e Lutjanus cyanopterus) e quase ameaçadas (Cynoscion acoupa, Dormitator maculatus, Lutjanus jocu, Lutjanus synagris e Mugil liza) são periféricas. Treze espécies são exóticas a nivel de país (Butis koilomatodon, Coptodon rendalli e Oreochromis niloticus) ou bacia (e.g., Pygocentrus nattereri e Salminus brasiliensis). O bagre Cathorops cf. arenatus é reportado pela primeira vez na costa leste do Brasil e Paragenidens grandoculis, considerado extinto no rio Doce, foi descoberto no estuário.

Palavras-chave:
Estuarino; Ictiofauna; Impactos ambientais; Mineração; Riqueza de espécies

INTRODUCTION

Estuaries are habitat-rich, highly productive ecotones between riverine and marine environments with diverse subsystems (e.g., mud and sand flats, seagrass meadows and mangrove forests) that shelter complex benthic and pelagic communities (McLusky, Elliott, 2004McLusky DS, Elliott M. The estuarine ecosystem. 3rd ed. New York: Oxford University Press; 2004. https://doi.org/10.1093/acprof:oso/9780198525080.001.0001
https://doi.org/10.1093/acprof:oso/97801... ). Despite their economic and social value (e.g., providing fishing grounds, water supply, aquaculture and navigation) (Basset et al., 2013Basset A, Elliott M, West RJ, Wilson JG. Estuarine and lagoon biodiversity and their natural goods and services. Estuar Coast Shelf Sci. 2013; 132:1–04. https://doi.org/10.1016/j.ecss.2013.05.018
https://doi.org/10.1016/j.ecss.2013.05.0... ), estuaries have been sorely exposed to human-driven habitat loss, the introduction of non-native species and water contamination (Lotze et al., 2006Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC et al. Depletion, degradation, and recovery potential of estuaries and coastal seas. Science. 2006; 312(5781):1806–09. https://doi.org/10.1126/science.1128035
https://doi.org/10.1126/science.1128035... ).

The Doce River is among the major fluvial systems of southeastern Brazil and flows over 850 km (Lins et al., 2012Lins RC, Mendes CAB, Agra SG, Carvalho AE, Fragoso Junior CR. Integração de um modelo hidrológico a um SIG para avaliação da qualidade da agua na bacia do Rio Doce. Rev Bras Recur Hídricos. 2012; 17(4):171–81. https://doi.org/10.21168/rbrh.v17n4.p171-181
https://doi.org/10.21168/rbrh.v17n4.p171... ) through the states of Minas Gerais and Espírito Santo. It runs through the Neotropical Atlantic Forest, a hotspot biome (Ribeiro et al., 2011Ribeiro MC, Martensen AC, Metzger JP, Tabarelli M, Scarano F, Fortin M-J. The Brazilian Atlantic Forest: A shrinking biodiversity hotspot. Biodiversity Hotspots. Berlin, Heidelberg: Springer Berlin Heidelberg; 2011. p.405–34. https://doi.org/10.1007/978-3-642-20992-5_21
https://doi.org/10.1007/978-3-642-20992-... ) whose luxuriant vegetation and biodiversity was described by early European naturalists in the 19th century – Prince Maximilian in 1815; Saint-Hilaire in 1822; the Thayer Expedition in 1865 and Princess Therese in 1888 (Hartt, Agassiz, 1870Hartt CF, Agassiz L. Scientific results of a journey in Brazil by Louis Agassiz and his travelling companions: Geology and physical geography of Brazil. Boston: Fields, Osgood & Co; 1870. p.620.; Saint-Hilaire, 1936Saint-Hilaire A. Segunda viagem ao interior do Brasil : Espirito Santo. Série V: 7. São Paulo: Companhia Editora Nacional; 1936.; Wied-Neuwied, 1940Wied-Neuwied M. Viagem ao Brasil. Série V: 1. São Paulo: Companhia Editora Nacional; 1940.; Baviera, 2013Baviera PT. Viagem pelo Espírito Santo (1888): Viagem pelos trópicos brasileiros. Vitória: Arquivo Público do Estado do Espírito Santo, Brasil; 2013.). These pioneering expeditions also produced the first reports on the fishes of the Doce River that, in particular, cite the locally extinct sawfish Pristis pristis (Linnaeus, 1758) (Vieira, Gasparini, 2007Vieira F, Gasparini JL. Os peixes ameaçados de extinção no estado do Espírito Santo. In: Passamani M, Mendes SL, editors. Espécies da Fauna Ameaçada Extinção no Estado do Espírito Santo. 1st ed. Vitória: Instituto de Pesquisas da Mata Atlântica; 2007.; Saldanha, 2018Saldanha MC. Do sistema tripolar GTP – geossistema, território e paisagem à geografia transversal e de travessias: Uma abordagem geográfica do distrito de Regência Augusta – Linhares (ES). Master Thesis in Geography, Universidade Federal do Espírito Santo. 2018. http://repositorio.ufes.br/bitstream/10/10670/1/tese_12667_MIGUEL CHAVES SALDANHA.pdf
http://repositorio.ufes.br/bitstream/10/... ). Knowledge about the river’s ichthyofauna composition (Vieira, 2009Vieira F. Distribuição, impactos ambientais e conservação da fauna de peixes da bacia do rio Doce. MGBiota. 2009; 2(5):5–22.; Sarmento-Soares et al., 2017Sarmento-Soares LM, Pinheiro RM, Rodrigues LN. Peixes do Rio Doce segundo as coleções. Bol Soc Bras Ictiol. 2017; 123(3):9–25.; Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ) and its conservation status (Su et al., 2021Su G, Logez M, Xu J, Tao S, Villéger S, Brosse S. Human impacts on global freshwater fish biodiversity. Science. 2021; 371(6531):835–38. https://doi.org/10.1126/science.abd3369
https://doi.org/10.1126/science.abd3369... ) has improved in recent years. However, estuarine fish assemblages remain poorly characterized in the Doce River estuary (DRE) (Jankowsky et al., 2021Jankowsky M, Carvalho RM, Gomes VAP, Freitas RR. Peixes e pesca na bacia do Rio Doce, uma análise bibliométrica. Brazilian J Prod Eng - BJPE. 2021:14–40. https://doi.org/10.47456/bjpe.v6i8.33769
https://doi.org/10.47456/bjpe.v6i8.33769... ) despite the area being recognized as of ‘extremely high’ biological importance (MMA, 2007Ministério do Meio Ambiente (MMA). Áreas prioritárias para conservação, uso sustentável e repartição de benefícios da diversidade biológica brasileira. Portaria n°. 9, de 23 de janeiro de 2007. Diário Oficial da União, seção 1, edição 17 (23 de janeiro de 2007). Brasília: 2007.).

Impacts caused by mining have been known for centuries (Saint-Hilaire, 1938Saint-Hilaire A. Viagem pelas províncias de Rio de Janeiro e Minas Gerais. Série V: 1. São Paulo: Companhia Editora Nacional; 1938., 1936Saint-Hilaire A. Segunda viagem ao interior do Brasil : Espirito Santo. Série V: 7. São Paulo: Companhia Editora Nacional; 1936.). However, the past decades were marked by a rapid and severe degradation due to urban growth and unsustainable use of resources (e.g., wood-cycle deforestation, agriculture, industry and mining, dam construction) (Diniz et al., 2014Diniz JMFS, Reis AA, Acerbi Junior FW, Gomide LR. Detecção da expansão da área minerada no Quadrilátero Ferrífero, Minas Gerais, no período de 1985 a 2011 através de técnicas de sensoriamento remoto. Bol Ciênc Geod. 2014; 20(3):683–700. https://doi.org/http://dx.doi.org/10.1590/S1982-21702014000300039
https://doi.org/http://dx.doi.org/10.159... ; Espindola, 2015Espindola HS. Vale do rio Doce: Fronteira, industrialização e colapso socioambiental. Front J Soc Technol Environ Sci. 2015; 4(1):160. https://doi.org/10.21664/2238-8869.2015v4i1.p160-206
https://doi.org/10.21664/2238-8869.2015v... ). In this sense, biodiversity and ecological services have been threatened by habitat fragmentation, loss of basin and riparian vegetation, introduction of exotic species (Ruschi, 1965Ruschi A. Lista dos tubarões, raias e peixes de água doce e salgada do estado do Espírito Santo e uma observação sobre a introdução do dourado no Rio Doce. Bol do Mus Biol Prof Mello-Leitão. 1965; 25(A):1–24.; Fragoso-Moura et al., 2016Fragoso-Moura EN, Oporto LT, Maia-Barbosa PM, Barbosa FAR. Perda de biodiversidade em uma unidade de conservação da mata atlântica brasileira: Efeitos da introdução de espécies não nativas de peixes. Braz J Biol. 2016; 76(1):18–27. https://doi.org/10.1590/1519-6984.07914
https://doi.org/10.1590/1519-6984.07914... ; Bueno et al., 2021Bueno ML, Magalhães ALB, Andrade Neto FR, Alves CBM, Rosa DM, Junqueira NT et al. Alien fish fauna of southeastern Brazil: species status, introduction pathways, distribution and impacts. Biol Invasions. 2021; 23(10):3021–34. https://doi.org/10.1007/s10530-021-02564-x
https://doi.org/10.1007/s10530-021-02564... ; Su et al., 2021Su G, Logez M, Xu J, Tao S, Villéger S, Brosse S. Human impacts on global freshwater fish biodiversity. Science. 2021; 371(6531):835–38. https://doi.org/10.1126/science.abd3369
https://doi.org/10.1126/science.abd3369... ) and widespread pollution (Agostinho et al., 2005Agostinho AA, Thomaz SM, Gomes LC. Conservation of the biodiversity of Brazil’s inland waters. Conserv Biol. 2005; 19(3):646–52. https://doi.org/10.1111/j.1523-1739.2005.00701.x
https://doi.org/10.1111/j.1523-1739.2005... ). In November 2015, the collapse of the Fundão dam (controlled by Samarco Mineração SA.) in the state of Minas Gerais, released about 40 million tons of iron ore tailings into the Doce River watershed. Environmental consequences varied from acute (such as immediate mass mortality of aquatic fauna) to chronic effects that still are under investigation (Hatje et al., 2017Hatje V, Pedreira RMA, Rezende CE, Schettini CAF, Souza GC, Marin DC et al. The environmental impacts of one of the largest tailing dam failures worldwide. Sci Rep. 2017; 7:10706. https://doi.org/10.1038/s41598-017-11143-x
https://doi.org/10.1038/s41598-017-11143... ; Bonecker et al., 2019Bonecker ACT, Castro MS, Costa PG, Bianchini A, Bonecker SLC. Larval fish assemblages of the coastal area affected by the tailings of the collapsed dam in southeast Brazil. Reg Stud Mar Sci. 2019; 32:100848. https://doi.org/https://doi.org/10.1016/j.rsma.2019.100848
https://doi.org/https://doi.org/10.1016/... ; Cordeiro et al., 2019Cordeiro MC, Garcia GD, Rocha AM, Tschoeke DA, Campeão ME, Appolinario LR et al. Insights on the freshwater microbiomes metabolic changes associated with the world’s largest mining disaster. Sci Total Environ. 2019; 654:1209–17. https://doi.org/https://doi.org/10.1016/j.scitotenv.2018.11.112
https://doi.org/https://doi.org/10.1016/... ; Gabriel et al., 2021Gabriel FÂ, Ferreira AD, Queiroz HM, Vasconcelos ALS, Ferreira TO, Bernardino AF. Long-term contamination of the rio Doce estuary as a result of Brazil’s largest environmental disaster. Perspect Ecol Conserv. 2021; 19(4):417–28. https://doi.org/10.1016/j.pecon.2021.09.001
https://doi.org/10.1016/j.pecon.2021.09.... ).

After the dam breach, most studies carried in the Doce River have focused on socio-political, geochemistry and water quality issues (e.g., Espindola, Guerra, 2018Espindola HS, Guerra CB. The ongoing danger of large-scale mining on the rio Doce: An account of Brazil’s largest biocultural disaster. In: From Biocultural Homogenization to Biocultural Conservation. Ecology and Ethics, vol 3. Springer, Cham. 2018. p.97–108. https://doi.org/10.1007/978-3-319-99513-7_6
https://doi.org/10.1007/978-3-319-99513-... ; Richard et al., 2020Richard EC, Estrada GCD, Bechtold J-P, Duarte Jr. HA, Maioli BG, Freitas AHA et al. Water and sediment quality in the coastal zone around the mouth of Doce River after the Fundão tailings dam failure. Integr Environ Assess Manag. 2020; 16(5):643–54. https://doi.org/10.1002/ieam.4309
https://doi.org/10.1002/ieam.4309... ; Longhini et al., 2022Longhini CM, Rodrigues SK, Costa ES, Silva CA, Cagnin RC, Gripp M et al. Environmental quality assessment in a marine coastal area impacted by mining tailing using a geochemical multi-index and physical approach. Sci Total Environ. 2022; 803:149883. https://doi.org/10.1016/j.scitotenv.2021.149883
https://doi.org/10.1016/j.scitotenv.2021... ). Conversely, the lack of faunal assemblages baselines (such as Gomes et al., 2017Gomes LEO, Correa LB, Sá F, Neto RR, Bernardino AF. The impacts of the Samarco mine tailing spill on the Rio Doce estuary, Eastern Brazil. Mar Pollut Bull. 2017; 120(1–2):28–36. https://doi.org/10.1016/j.marpolbul.2017.04.056
https://doi.org/10.1016/j.marpolbul.2017... ; Andrades et al., 2020Andrades R, Guabiroba HC, Hora MSC, Martins RF, Rodrigues VLA, Vilar CC et al. Early evidences of niche shifts in estuarine fishes following one of the world’s largest mining dam disasters. Mar Pollut Bull. 2020; 154:111073. https://doi.org/10.1016/j.marpolbul.2020.111073
https://doi.org/10.1016/j.marpolbul.2020... ; Bueno et al., 2021Bueno ML, Magalhães ALB, Andrade Neto FR, Alves CBM, Rosa DM, Junqueira NT et al. Alien fish fauna of southeastern Brazil: species status, introduction pathways, distribution and impacts. Biol Invasions. 2021; 23(10):3021–34. https://doi.org/10.1007/s10530-021-02564-x
https://doi.org/10.1007/s10530-021-02564... ; Condini et al., 2022Condini MV, Pichler HA, Oliveira-Filho RR, Cattani AP, Andrades R, Vilar CC et al. Marine fish assemblages of Eastern Brazil: An update after the world’s largest mining disaster and suggestions of functional groups for biomonitoring long-lasting effects. Sci Total Environ. 2022; 807(2):150987. https://doi.org/10.1016/j.scitotenv.2021.150987
https://doi.org/10.1016/j.scitotenv.2021... ) hinders a comprehensive analysis of the effects of the released mining tailing on biodiversity.

Here we present the first ichthyofaunal inventory of the Doce River estuary. This work is inserted within a larger effort to detect and understand the assemblage structure (Condini et al., 2022Condini MV, Pichler HA, Oliveira-Filho RR, Cattani AP, Andrades R, Vilar CC et al. Marine fish assemblages of Eastern Brazil: An update after the world’s largest mining disaster and suggestions of functional groups for biomonitoring long-lasting effects. Sci Total Environ. 2022; 807(2):150987. https://doi.org/10.1016/j.scitotenv.2021.150987
https://doi.org/10.1016/j.scitotenv.2021... ; Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ) and trophic ecology (Andrades et al., 2020Andrades R, Guabiroba HC, Hora MSC, Martins RF, Rodrigues VLA, Vilar CC et al. Early evidences of niche shifts in estuarine fishes following one of the world’s largest mining dam disasters. Mar Pollut Bull. 2020; 154:111073. https://doi.org/10.1016/j.marpolbul.2020.111073
https://doi.org/10.1016/j.marpolbul.2020... , 2021) of the estuarine and coastal fishes of the Doce River.

MATERIAL AND METHODS

Study area. The surveys were conducted in the lower reaches of the Doce River, located on the central coast of the state of Espírito Santo (Fig. 1; 19°39’S 39°49’W). This region belongs to the Atlantic Forest domain (IBGE, Instituto Brasileiro de Geografia e Estatística (IBGE). Manual técnico da vegetação brasileira. Rio de Janeiro. IBGE, - Coordenação de Recursos Naturais e Estudos Ambientais; 2012.2012), with the riparian vegetation a mosaic of pioneering freshwater plants (e.g., Araceae, Cyperaceae, Poaceae), native tree-shaded cocoa farms and remnants of tropical rainforest (Rolim et al., 2006Rolim SG, Ivanauskas NM, Rodrigues RR, Nascimento MT, Gomes JML, Folli DA et al. Composição florística do estrato arbóreo da floresta estacional semidecidual na planície aluvial do rio Doce, Linhares, ES, Brasil. Acta Bot Bras. 2006; 20(3):549–61. https://doi.org/10.1590/S0102-33062006000300005
https://doi.org/10.1590/S0102-3306200600... ; França et al., 2013França MC, Cohen MCL, Pessenda LCR, Rossetti DF, Lorente FL, Buso Junior AÁ et al. Mangrove vegetation changes on Holocene terraces of the Doce River, southeastern Brazil. Catena. 2013; 110:59–69. https://doi.org/10.1016/j.catena.2013.06.011
https://doi.org/10.1016/j.catena.2013.06... ). The climate is tropical, with the dry season extending from April to September and the rainy season from October to March (Nimer, 1989Nimer E. Climatologia do Brasil. Rio de Janeiro: IBGE, - Departamento de Recursos Naturais e Estudos Ambientais; 1989.; Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift. 2013; 22(6):711–28. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0... ). Despite a decreasing trend in the Doce River hydrological regime (Coelho, 2006Coelho ALN. Situação hídrico-geomorfológica da bacia do rio doce com base nos dados da série histórica de vazões da estação de colatina - ES. Caminhos Geogr. 2006; 6(19):56–79.), median streamflow during the wet season reaches up to 900 m3/s (Oliveira, Quaresma, 2017Oliveira KSS, Quaresma VS. Temporal variability in the suspended sediment load and streamflow of the Doce River. J South Am Earth Sci. 2017; 78:101–15. https://doi.org/10.1016/j.jsames.2017.06.009
https://doi.org/10.1016/j.jsames.2017.06... ), which explains the very low salinity near the river mouth (Gomes et al., 2017Gomes LEO, Correa LB, Sá F, Neto RR, Bernardino AF. The impacts of the Samarco mine tailing spill on the Rio Doce estuary, Eastern Brazil. Mar Pollut Bull. 2017; 120(1–2):28–36. https://doi.org/10.1016/j.marpolbul.2017.04.056
https://doi.org/10.1016/j.marpolbul.2017... ; Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ). According to the geomorphological context, the Doce River mouth is a submerged deltaic system dominated by waves (Dominguez, Wanless, 1991Dominguez JML, Wanless HR. Facies architecture of a falling sea-level strandplain, Doce River coast, Brazil. In: Swift DJP, Oertel GF, Tillman RW, Thorne JA, editors. Shelf sand and sandstone bodies: Geometry, facies and sequence stratigraphy. Blackwell Publishing Ltd.; 1991. p.257–81. https://doi.org/10.1002/9781444303933.ch7
https://doi.org/10.1002/9781444303933.ch... ). However, for the purpose of this study, we call this region the Doce River estuary (DRE) given the tidal influence on the river sedimentation and hydrodynamics and the perennial occurrence of marine fish species (Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ).

FIGURE 1 |
Location of the study area in Eastern Brazil with some features detailed: A. Sandy banks; B. Marginal creek; and C. Main channel of the Doce River estuary (DRE). Photos: Helder C. Guabiroba (A; C), Alexandre Villela (B). Aerial image source: (GEOBASES, 2015GEOBASES. Sistema Integrado de Bases Geoespaciais do Estado do Espírito Santo. 2015. Available from: https://geobases.es.gov.br/
https://geobases.es.gov.br/... ).

Data acquisition. Most data presented here come from two different monitoring programs. The first comprises nine expeditions conducted in November 2015 (before the mud reached the estuary), June 2016, June and November 2019, July/August and November/December 2020, June 2021, November/December 2021 and June 2022, totalizing 23 days of sampling in the marginal creeks and adjacencies of the sandbanks. Specimens were collected in both lotic and lentic environments by exhaustive sampling with the aid of multiple fishing gears (cast net, beach seine, dip net, and gillnets). The second sampling program was performed using a standardized bottom trawl towed by a 5-m-boat during 5-min at a speed of 2 to 3 knots (Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ). Six sites distributed along the main channel of the DRE were monitored monthly from October 2018 to September 2019, and every three months from December 2019 to April 2022; sampling was interrupted between March and December of 2020 due to the COVID-19 pandemy. The present work also builds upon collection records available in the ‘SpeciesLink’ network database (http://splink.cria.org.br) that presented valid coordinates and a detailed description of the sampling area.

All collected fishes were euthanized in an ice-water slurry, kept on ice for a maximum of 48h, then frozen. After thawing and identification, representants of most species were fixed in formalin 10% and finally preserved in alcohol 70%. Selected lots were deposited at the Coleção Ictiológica da Universidade Federal do Espírito Santo, Vitória (CIUFES), see vouchers in Tab. S1.

Data analysis. All species were identified to the lowest possible taxonomic level with the aid of classical and current literature (e.g., Figueiredo, Menezes, 1978Figueiredo JL, Menezes NA. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo: Museu de Zoologia: USP; 1978.; Menezes, 1980Menezes NA. Manual de peixes marinhos do sudeste do Brasil III Teleostei (2). São Paulo: Museu de Zoologia USP; 1980.; Menezes, Figueiredo, 1980Menezes NA, Figueiredo JL. Manual de peixes marinhos do Sudeste do Brasil IV Teleostei (3). São Paulo: Museu de Zoologia USP; 1980., 1985Menezes NA, Figueiredo JL. Manual de peixes marinhos do sudeste do Brasil V Teleostei (4). São Paulo: Museu de Zoologia USP; 1985., 2000Menezes NA, Figueiredo JL. Manual de peixes marinhos do sudeste do Brasil VI Teleostei (5). São Paulo: Museu de Zoologia USP; 2000.; Carvalho-Filho, 1999Carvalho-Filho A. Peixes: Costa brasileira. São Paulo: Melro; 1999.; Munroe, Nizinski, 2002Munroe TA, Nizinski MS. Clupeidae. In The living marine resources of the Western Central Atlantic Volume 2: Bony fishes part 1 (Acipenseridae to Grammatidae). In: Carpenter KE, editor. FAO Species Identification Guide for Fishery Purposes, Am Soc Ichthyol Herpetol Spec. Publ. 5.; 2002.; Nizinski, Munroe, 2002Nizinski MS, Munroe TA. Engraulidae, in The living marine resources of the Western Central Atlantic Volume 2: Bony fishes part 1 (Acipenseridae to Grammatidae). In: Carpenter KE, editor. FAO Species Identification Guide for Fishery Purposes, Am Soc Ichthyol Herpetol Spec. Publ. 5; 2002.; Marceniuk, 2005Marceniuk AP. Chave para identificação das espécies de bagres marinhos (Siluriformes, Ariidae) da costa brasileira. B Inst Pesca. 2005; 31(2):89–101.; Kullander, Ferreira, 2006Kullander SO, Ferreira EJG. A review of the South American cichlid genus Cichla, with descriptions of nine new species (Teleostei: Cichlidae). Ichthyol Explor Freshw. 2006; 17(4):289–398.; Moura, Lindeman, 2007Moura RL, Lindeman KC. A new species of snapper (Perciformes: Lutjanidae) from Brazil, with comments on the distribution of Lutjanus griseus and L. apodus. Zootaxa. 2007; 1442(1):31–43. https://doi.org/http://doi.org/10.11646/zootaxa.1422.1.2
https://doi.org/http://doi.org/10.11646/... ; Vieira et al., 2014Vieira F, Gasparini JL, Macieira RM. Guia ilustrado dos peixes da bacia do rio Benevente - ES. Vitória: ACQUA Consultoria e Recuperação de Ambientes Aquáticos Ltda/São Joaquim Energia S.A.; 2014., 2015Vieira F, Gomes JPC, Maia BP, Silva LGM. Peixes do Quadrilátero Ferrífero: Guia de identificação (Fish of the Iron Quadrangle: Identification guide). Belo Horizonte: Fundação Biodiversitas; 2015.; Marceniuk et al., 2019Marceniuk AP, Ingenito LFS, Lima FCT, Gasparini JLR, Oliveira C. Systematics, biogeography and conservation of Paragenidens grandoculis n. gen. and n. comb. (Siluriformes; Ariidae), a critically endangered species from southeastern Brazil. Zootaxa. 2019; 4586(3):425–44. https://doi.org/10.11646/zootaxa.4586.3.2
https://doi.org/10.11646/zootaxa.4586.3.... ). Scientific names and phylogenetic arrangement of orders and families follow Betancur-R et al., (2017)Betancur-R R, Wiley EO, Arratia G, Acero A, Bailly N, Miya M et al. Phylogenetic classification of bony fishes. BMC Evol Biol. 2017; 17(162). https://doi.org/http://doi.org/10.1186/s12862-017-0958-3
https://doi.org/http://doi.org/10.1186/s... and The Catalog of Fishes (Fricke et al., 2022Fricke R, Eschmeyer WN, van der Laan R. Eschmeyer's catalog of fishes: Genera, species, references [Internet]. Sna Francisco: California Academy of Sciences; 2022. Available from: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
http://researcharchive.calacademy.org/re... ).

Fishes were classified as ‘native’ or ‘exotic’. The latter category was composed by ‘exotic at the country-level’, for non-Brazilian species and ‘exotic at basin-level’ for fishes native of other Brazilian river basins (ICMBio, 2018Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio). Livro vermelho da fauna brasileira ameaçada de extinção: Volume VI - Peixes. 1 ed. Brasília, DF: ICMBio/MMA, 2018.; Froese, Pauly, 2020Froese R, Pauly D. FishBase. World Wide Web electronic publication. 2020. Available from: https://www.fishbase.se/
https://www.fishbase.se/... ). Fish tolerance to salinity was classified into three categories following Myers, (1938)Myers GS. Fresh water fishes and West Indian zoogeography. 1937th ed. Annual Report of the Board of Regents of the Smithsonian Institution; 1938. p.339–64. and Berra, (2001)Berra TM, editor. Introduction. In: Freshwater Fish Distribution. San Diego: Academic Press; 2001. https://doi.org/https://doi.org/10.1016/B978-012093156-9/50026-3
https://doi.org/https://doi.org/10.1016/... : primary (freshwater fishes with low salinity tolerance); secondary (freshwater fishes with some salinity tolerance) and peripheral (marine fishes that occasionally occur in freshwater ecosystems). The current Brazilian Red List of Threatened Species (MMA, 2022Ministério do Meio Ambiente (MMA). Atualização da lista nacional de espécies ameaçadas de extinção. Portaria nº 148, de 7 de junho de 2022. Diário Oficial da União, seção 1, edição 108 (7 de junho de 2022). Brasília: MMA; 2022.) was considered for the assessment of the conservation status of native fishes. Status of exotic species from other countries was not assessed. Fish species were grouped into seven trophic categories according to literature (see Tab. S1): Zoobenthivore (feed primarily on benthic mobile invertebrates); Zooplanktivore (feed primarily on zooplankton); Piscivore (feed only or mostly on live fishes); Generalist carnivore (feed on both mobile invertebrates and fishes); Omnivore (feed on both plant and animal food sources); Detritivore (the main food sources are detritus and sediment); and Herbivore (feed primarily on vegetal material).

RESULTS

A total of 115 fish species, belonging to 24 orders, 44 families and 84 genera was recorded (Tab. 1). The order Carangiformes was the most speciose, with 22 species, followed by Eupercaria incertae sedis (12 species) and Siluriformes (11 species) (Fig. 2). The most representative families were Sciaenidae (12 species), Engraulidae (8), Carangidae, Cichlidae, and Gobiidae (7 each). Euryhaline or peripheral fishes were predominant in the DRE (92, or 80%), followed by primary (13%) and secondary fishes (7%). In terms of trophic guilds, zoobenthivores were dominant (33.9%), followed by generalist carnivores (19.1%), omnivores (14.8%), piscivores (11.3%), detritivores and zooplanktivores (8.7%). Herbivores comprised only 2.6% of species recorded.

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TABLE 1 |
Fishes of the Doce River estuary. Euryhalinity: Per, Peripheral; 1st, Primary; 2nd, Secondary. Trophic group: GC, Generalist carnivore; ZB, Zoobenthivore; ZP, Zooplanktivore; PV, Piscivore; OV, Omnivore; DT, Detritivore; HB, Herbivore; UD, Undefined. Origin: NV, Native; EX-B, Exotic at the basin level; EX-C, Exotic at the country level. Brazilian Red List: NA, Not Applied; DD, Data Deficient; LC, Least Concern; NT, Near Threatened; VU, Vulnerable; EN, Endangered; CR, Critically Endangered. Endemism: ED, Endemic of Brazil; NE, Non endemic of Brazil, fishing gear, vouchers and references for trophic guild are available in Tab. S1. *Specimens not caught in this study; † Locally extinct.

FIGURE 2 |
Number of species, genera and families for fish orders in the Doce River estuary. The following orders were represented by a single species and were omitted in the figure: Anguilliformes, Atheriniformes, Aulopiformes, Beloniformes, Blenniiformes, Centrarchiformes, Cyprinodontiformes, Elopiformes, Scombriformes, Spariformes, Symbranchiformes and Syngnathiformes (illustrative taxa images from Phylopic.org).

Most species are native (101, or 87.8%), three species (2.6%) are exotic at the country level: Coptodon rendalli (Boulenger, 1897), Oreochromis niloticus (Linnaeus, 1758) and Butis koilomatodon (Bleeker, 1849) (Figs. 3C,D), and 11 species (9.6%) are from other Brazilian basins: Cichla cf. kelberi, Cichla monoculus Spix & Agassiz, 1831, Cichlasoma dimerus (Heckel, 1840), Knodus cf. moenkhausii, Hypostomus scabriceps (Eigenmann & Eigenmann, 1888), Microglanis pataxo Sarmento-Soares, Martins-Pinheiro, Aranda & Chamon, 2006, Pimelodus maculatus Lacepède, 1803, Prochilodus argenteus Spix & Agassiz, 1829, Prochilodus costatus Valenciennes, 1850, Pygocentrus nattereri Kner, 1858 and Salminus brasiliensis (Cuvier, 1816) (Figs. 3A,B). Brazilian endemics represent 19 species (16.5%); no species endemic to the Doce River basin was sampled. According to the Brazilian Red List, four species (3.5%) are currently threatened: Paragenidens grandoculis (Steindachner, 1877) (Critically Endangered), Pristis pristis (Critically Endangered and locally extinct), Genidens barbus (Lacepède, 1803) (Endangered) and Lutjanus cyanopterus (Cuvier, 1828) (Vulnerable; Fig. 3E). Among non-threatened species, 94 (81.7%) are considered as Least Concern, seven (6.1%) as Data Deficient, and five (4.3%) are Near Threatened: Cynoscion acoupa (Lacepède, 1801), Dormitator maculatus (Bloch, 1792), Lutjanus jocu (Bloch & Schneider, 1801), Lutjanus synagris (Linnaeus, 1758), and Mugil liza Valenciennes, 1836.

FIGURE 3 |
Examples of fishes recorded for the first time in the Doce River estuary. A. Cichlasoma dimerus; B. Pygocentrus nattereri; C. Coptodon rendalli; D. Butis koilomatodon; E. Lutjanus cyanopterus; F. Genidens barbus; G. Pimelodus maculatus; H. Catathyridium garmani. Photos: Helder C. Guabiroba (A, B, C, E, H), Flávio T. Szablak (D, F, G).

DISCUSSION

This is the first comprehensive fish inventory of the Doce River estuary, with 115 recorded species being Carangiformes, Eupercaria incertae sedis and Siluriformes the most speciose orders. Here, we followed the most recent classification of the Carangiformes (Girard et al., 2020Girard MG, Matthew PD, Smith WL. The phylogeny of carangiform fishes: Morphological and genomic investigations of a new fish clade. Copeia. 2020; 108(2):265–98. https://doi.org/10.1643/CI-19-320
https://doi.org/10.1643/CI-19-320... ), that nests a series of subclades with many estuarine representants. Among the recorded Carangiformes species are the snooks (Centropomidae), the flatfishes (e.g., Paralichthyidae and Achiridae), and the jacks (Carangidae). The Eupercaria incertae sedis order was only represented by the croakers (Sciaenidae) that, like the catfishes (Siluriformes), usually occur in high abundance and richness in tropical estuaries (e.g., Catelani et al., 2014Catelani PA, Petry AC, Di Dario F, Santos VLM, Mincarone MM. Fish composition (Teleostei) of the estuarine region of the Macaé River, southeastern Brazil. Check List. 2014; 10(4):927–35. https://doi.org/10.15560/10.4.927
https://doi.org/10.15560/10.4.927... ; Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ). Among the diverse adaptative processes that favor the success of these two last groups in turbid brackish waters are the Weberian apparatus (Siluriformes), mechanosensory barbels and sound-producing mechanisms (Alexander, 1966Alexander RMcN. Structure and function in the catfish. J Zool. 1966; 148(1):88–152. https://doi.org/10.1111/j.1469-7998.1966.tb02943.x
https://doi.org/10.1111/j.1469-7998.1966... ; Kaatz, 2002Kaatz IM. Multiple sound-producing mechanisms in teleost fishes and hypotheses regarding their behavioural significance. Bioacoustics. 2002; 12(2–3):230–33. https://doi.org/10.1080/09524622.2002.9753705
https://doi.org/10.1080/09524622.2002.97... ).

The DRE fish fauna is dominated by zoobenthivores in both richness and biomass (Vilar et al., 2022Vilar CC, Andrades R, Szablak FT, Guabiroba HC, Pichler HA, Lima LRS et al. Variability in nearshore fish biodiversity indicators after a mining disaster in eastern Brazil. Mar Environ Res. 2022; 175:105565. https://doi.org/10.1016/j.marenvres.2022.105565
https://doi.org/10.1016/j.marenvres.2022... ) and the rarity of piscivores may reflect ill-suited water characteristics for this group (e.g., shallow and turbid). The low depth, high turbidity and frequent floods in the low reaches of the Doce River are known since the 19th century expeditions (Saint-Hilaire, 1938Saint-Hilaire A. Viagem pelas províncias de Rio de Janeiro e Minas Gerais. Série V: 1. São Paulo: Companhia Editora Nacional; 1938.). However, with the rapid expansion of agriculture, industry, urbanization and the construction of hydropower and mining dams, sedimentation and hydrological processes have been severely affected (Coelho, 2006Coelho ALN. Situação hídrico-geomorfológica da bacia do rio doce com base nos dados da série histórica de vazões da estação de colatina - ES. Caminhos Geogr. 2006; 6(19):56–79.; Aprile et al., 2016Aprile F, Lorandi R, Siqueira G. Influence of natural and anthropogenic processes in the coastline evolution at the Doce River mouth (Espírito Santo, Brazil). Br J Environ Clim Chang. 2016; 6(1):18–27. https://doi.org/10.9734/bjecc/2016/25454
https://doi.org/10.9734/bjecc/2016/25454... ; Rudorff et al., 2018Rudorff N, Rudorff CM, Kampel M, Ortiz G. Remote sensing monitoring of the impact of a major mining wastewater disaster on the turbidity of the Doce River plume off the eastern Brazilian coast. ISPRS J Photogramm Remote Sens. 2018; 145:349–61. https://doi.org/10.1016/j.isprsjprs.2018.02.013
https://doi.org/10.1016/j.isprsjprs.2018... ). The 19th and 20th centuries were also marked by the decline or extirpation of apex-predators in the lower (or the entirety of the) Doce River such as the largetooth sawfish Pristis pristis, the giant endemic catfish Steindachneridion doceanum (Eigenmann & Eigenmann, 1889), an endemic lineage of broad-snouted alligator Caiman latirostris (Daudin, 1802) and the giant otter Pteronura brasiliensis (Gmelin, 1788) (Vieira, Gasparini, 2007Vieira F, Gasparini JL. Os peixes ameaçados de extinção no estado do Espírito Santo. In: Passamani M, Mendes SL, editors. Espécies da Fauna Ameaçada Extinção no Estado do Espírito Santo. 1st ed. Vitória: Instituto de Pesquisas da Mata Atlântica; 2007.; Keesen et al., 2016Keesen F, Nunes AV, Scoss LM. Updated list of mammals of Rio Doce State Park, Minas Gerais, Brazil. Bol Mus Biol Mello Leitão. 2016; 38(2):139–62. http://boletim.sambio.org.br/pdf/38_2_06.pdf
http://boletim.sambio.org.br/pdf/38_2_06... ; Swarça et al., 2018Swarça AC, Orsi ML, Takagui FH, Dias AL, Dergam JA, Fenocchio AS. First chromosome data on Steindachneridion doceanum (Siluriformes: Pimelodidae): A critically endangered catfish endemic of the doce river basin, Brazil. Neotrop Ichthyol. 2018; 16(4):3–07. https://doi.org/10.1590/1982-0224-20180066
https://doi.org/10.1590/1982-0224-201800... ; Roberto et al., 2020Roberto IJ, Bittencourt PS, Muniz FL, Hernández-Rangel SM, Nóbrega YC, Ávila RW et al. Unexpected but unsurprising lineage diversity within the most widespread Neotropical crocodilian genus Caiman (Crocodylia, Alligatoridae). Syst Biodivers. 2020; 18(4):377–95. https://doi.org/10.1080/14772000.2020.1769222
https://doi.org/10.1080/14772000.2020.17... ). Beyond the immeasurable value of biodiversity loss, ecological consequences related to habitat homogenization are plentiful (Layman et al., 2007Layman CA, Quattrochi JP, Peyer CM, Allgeier JE. Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol Lett. 2007; 10(10):937–44. https://doi.org/10.1111/j.1461-0248.2007.01087.x
https://doi.org/10.1111/j.1461-0248.2007... ; Andrades et al., 2021Andrades R, Martins RF, Guabiroba HC, Rodrigues VLA, Szablak FT, Bastos KV et al. Effects of seasonal contaminant remobilization on the community trophic dynamics in a Brazilian tropical estuary. Sci Total Environ. 2021; 801:149670. https://doi.org/10.1016/j.scitotenv.2021.149670
https://doi.org/10.1016/j.scitotenv.2021... ).

Changes in richness and composition of basal organisms communities after the arriving of the tailing mud in the estuarine and coastal areas of Doce River have been reported (Gomes et al., 2017Gomes LEO, Correa LB, Sá F, Neto RR, Bernardino AF. The impacts of the Samarco mine tailing spill on the Rio Doce estuary, Eastern Brazil. Mar Pollut Bull. 2017; 120(1–2):28–36. https://doi.org/10.1016/j.marpolbul.2017.04.056
https://doi.org/10.1016/j.marpolbul.2017... ; Fernandes et al., 2022Fernandes L, Jesus H, Almeida P, Sandrini J, Bianchini A, Santos H. The influence of the Doce River mouth on the microbiome of nearby coastal areas three years after the Fundão Dam failure, Brazil. Sci Total Environ. 2022; 807:151777. https://doi.org/10.1016/J.SCITOTENV.2021.151777
https://doi.org/10.1016/J.SCITOTENV.2021... ; Rocha et al., 2022Rocha GM, Salvador B, Laino PS, Santos GHC, Demoner LE, Conceição LR et al. Responses of marine zooplankton indicators after five years of a dam rupture in the Doce River, Southeastern Brazil. Sci Total Environ. 2022; 806:151249. https://doi.org/10.1016/j.scitotenv.2021.151249
https://doi.org/10.1016/j.scitotenv.2021... ). As shown by Andrades et al., (2020)Andrades R, Guabiroba HC, Hora MSC, Martins RF, Rodrigues VLA, Vilar CC et al. Early evidences of niche shifts in estuarine fishes following one of the world’s largest mining dam disasters. Mar Pollut Bull. 2020; 154:111073. https://doi.org/10.1016/j.marpolbul.2020.111073
https://doi.org/10.1016/j.marpolbul.2020... the ecological niches of some estuarine fishes of the Doce River were also affected by the pollution caused by ore tailings. Here we warns for risks that chronic contamination in the DRE poses to the ichthyofauna given the high number of bottom-feeding species that occurs in this ecosystem (Tab. S1).

Human-induced changes along the whole Doce River length have been severe (Espindola, 2015Espindola HS. Vale do rio Doce: Fronteira, industrialização e colapso socioambiental. Front J Soc Technol Environ Sci. 2015; 4(1):160. https://doi.org/10.21664/2238-8869.2015v4i1.p160-206
https://doi.org/10.21664/2238-8869.2015v... ; Aprile et al., 2016; Fragoso-Moura et al., 2016Fragoso-Moura EN, Oporto LT, Maia-Barbosa PM, Barbosa FAR. Perda de biodiversidade em uma unidade de conservação da mata atlântica brasileira: Efeitos da introdução de espécies não nativas de peixes. Braz J Biol. 2016; 76(1):18–27. https://doi.org/10.1590/1519-6984.07914
https://doi.org/10.1590/1519-6984.07914... ). However, the DRE fish biodiversity is surprisingly higher than in geographically close estuaries, including one wave-dominated delta (Neto, 2009Neto FR de A. Estado atual do conhecimento sobre a fauna de peixes da bacia do Jequitinhonha. MGBiota. 2009; 2(5):23–35.; Hostim-Silva et al., 2013Hostim-Silva M, Lima AC, Spach HL, Passos AC, Souza JD. Estuarine demersal fish assemblage from a transition region between the tropics and the subtropics of the South Atlantic. Biotemas. 2013; 26(3):153–61. https://doi.org/10.5007/2175-7925.2013v26n3p153
https://doi.org/10.5007/2175-7925.2013v2... ; Vilar et al., 2013Vilar CC, Joyeux J-C, Giarrizzo T, Spach HL, Vieira JP, Vaske-Junior T. Local and regional ecological drivers of fish assemblages in Brazilian estuaries. Mar Ecol Prog Ser. 2013; 485:181–97. https://doi.org/10.3354/meps10343
https://doi.org/10.3354/meps10343... , Catelani et al., 2014Catelani PA, Petry AC, Di Dario F, Santos VLM, Mincarone MM. Fish composition (Teleostei) of the estuarine region of the Macaé River, southeastern Brazil. Check List. 2014; 10(4):927–35. https://doi.org/10.15560/10.4.927
https://doi.org/10.15560/10.4.927... ). This finding should, however, be parsimoniously interpreted due to distinct sampling effort, catch methods, and the uniqueness of each estuary.

Some records deserve special attention as the Ariidae Cathorops cf. arenatus and Paragenidens grandoculis that were not expected to occur in the DRE. The former is described from the northern Brazilian coast (Marceniuk, 2007Marceniuk AP. Revalidação de Cathorops arenatus e Cathorops agassizii (Siluriformes, Ariidae), bagres marinhos das regiões norte e nordeste da América do Sul. Iheringia Sér Zool. 2007; 97(4):360–75. https://doi.org/10.1590/S0073-47212007000400002
https://doi.org/10.1590/S0073-4721200700... ) while the latter was considered restricted to deep lakes adjacent to the lower Doce River (Marceniuk et al., 2019Marceniuk AP, Ingenito LFS, Lima FCT, Gasparini JLR, Oliveira C. Systematics, biogeography and conservation of Paragenidens grandoculis n. gen. and n. comb. (Siluriformes; Ariidae), a critically endangered species from southeastern Brazil. Zootaxa. 2019; 4586(3):425–44. https://doi.org/10.11646/zootaxa.4586.3.2
https://doi.org/10.11646/zootaxa.4586.3.... ). The occurrence of the critically endangered P. grandoculis in DRE should be monitored given the threats of chronic exposure to toxic ore tailings (Gabriel et al., 2020Gabriel FÂ, Silva AG, Queiroz HM, Ferreira TO, Hauser-Davis RA, Bernardino AF. Ecological risks of metal and metalloid contamination in the Rio Doce estuary. Integr Environ Assess Manag. 2020; 16(5):655–60. https://doi.org/10.1002/ieam.4250
https://doi.org/10.1002/ieam.4250... ; Andrades et al., 2021Andrades R, Martins RF, Guabiroba HC, Rodrigues VLA, Szablak FT, Bastos KV et al. Effects of seasonal contaminant remobilization on the community trophic dynamics in a Brazilian tropical estuary. Sci Total Environ. 2021; 801:149670. https://doi.org/10.1016/j.scitotenv.2021.149670
https://doi.org/10.1016/j.scitotenv.2021... ; Costa et al., 2021Costa ES, Cagnin RC, Silva CA, Longhini CM, Sá F, Lima AT et al. Iron ore tailings as a source of nutrients to the coastal zone. Mar Pollut Bull. 2021; 171:112725. https://doi.org/10.1016/j.marpolbul.2021.112725
https://doi.org/10.1016/j.marpolbul.2021... ) and the lack of information on its population status.

Some unexpected records for estuaries, such as Scomberomorus brasiliensis Collette, Russo & Zavala-Camin, 1978, Kyphosus sectatrix (Linnaeus, 1758) and Echeneis naucrates Linnaeus, 1758, clearly refer to vagrant marine individuals that occasionally enter these ecosystems. Another noteworthy record is that of the cryptic blenny Lupinoblennius paivai (Pinto, 1958), a species that tolerates low salinity and is usually found in mangroves branches cavities or other submerged vegetation (Machado et al., 2017Machado FS, Carvalho-Filho A, Giarrizzo T. Redescription and range extension of the endangered Paiva’s blenny Lupinoblennius paivai (Perciformes: Blenniidae). J Fish Biol. 2017; 90(6):2394–401. https://doi.org/10.1111/JFB.13322
https://doi.org/10.1111/JFB.13322... ). Despite the multiple fishing gears and the high effort employed in this study, we have captured only one specimen in 2015 (i.e., before the ore tailings reached the estuary). Sazima, Carvalho-Filho, (2003)Sazima I, Carvalho-Filho A. Natural history of the elusive blenny Lupinoblennius paivai (Perciformes: Blenniidae) in coastal streams of southeast Brazil. Ichthyol Explor Freshw. 2003; 14(2):175–84. warned about the extinction risks for this species due to increasing human pressure over coastal ecosystems.

The presence of exotic fishes in the DRE is another relevant issue (see Bueno et al., 2021Bueno ML, Magalhães ALB, Andrade Neto FR, Alves CBM, Rosa DM, Junqueira NT et al. Alien fish fauna of southeastern Brazil: species status, introduction pathways, distribution and impacts. Biol Invasions. 2021; 23(10):3021–34. https://doi.org/10.1007/s10530-021-02564-x
https://doi.org/10.1007/s10530-021-02564... for non-estuarine environments). Some of those species have been widely spread for aquaculture purposes (e.g., Oreochromis niloticus) and the risks they present for the native fish community structure and the supporting trophic web are well known (Zambrano et al., 2010Zambrano L, Valiente E, Zanden MJV. Food web overlap among native axolotl (Ambystoma mexicanum) and two exotic fishes: carp (Cyprinus carpio) and tilapia (Oreochromis niloticus) in Xochimilco, Mexico City. Biol Invasions. 2010; 12(9):3061–69. https://doi.org/10.1007/S10530-010-9697-8
https://doi.org/10.1007/S10530-010-9697-... ; Jere et al., 2021Jere A, Jere WWL, Mtethiwa A, Kassam D. Impact of Oreochromis niloticus (Linnaeus, 1758) (Pisces: Cichlidae) invasion on taxonomic and functional diversity of native fish species in the upper Kabompo River, northwest of Zambia. Ecol Evol. 2021; 11(18):12845–57. https://doi.org/10.1002/ECE3.8031
https://doi.org/10.1002/ECE3.8031... ). We are also concerned about native Brazilian species exotic to the Doce River basin (e.g., Pygocentrus nattereri, Salminus brasiliensis, and Cichla spp.). Studies conducted in Doce River lakes show evidence of loss in native species richness and changes in the structure of basal resources after the introduction of exotic predatory species such as the red-piranha P. nattereri and Peacock bass Cichla spp., among others (Latini, Petrere, 2004Latini AO, Petrere Jr. M. Reduction of a native fish fauna by alien species: An example from Brazilian freshwater tropical lakes. Fish Manag Ecol. 2004; 11(2):71–79. https://doi.org/10.1046/J.1365-2400.2003.00372.X
https://doi.org/10.1046/J.1365-2400.2003... ; Pinto-Coelho et al., 2008Pinto-Coelho RM, Bezerra-Neto JF, Miranda F, Mota TG, Resck R, Santos AM et al. The inverted trophic cascade in tropical plankton communities: Impacts of exotic fish in the middle Rio Doce lake district, Minas Gerais, Brazil. Braz J Biol. 2008; 68(4):1025–37. https://doi.org/10.1590/S1519-69842008000500010
https://doi.org/10.1590/S1519-6984200800... ).

The Doce River and its estuary have been affected by multiple humaninduced stressors during the 20­th and 21st centuries (Fig. 4; Tab. S2). In this context, the present study serves as a valuable baseline of the local ichthyofauna –even though the system is far from pristine. We emphasize the importance of long-term monitoring of fishery target resources, vulnerable species (e.g., endangered and rheophilic fishes) and high-level consumers (generalist carnivores and piscivores) for a better understanding of the consequences of human impacts on the local ichthyofauna and its social-economic unfoldings.

FIGURE 4 |
Main human-driven impacts after the 19th century and their consequences on the Doce River basin. Photos by A. Villela (Exotic species) and E. Nascimento (Mining dam collapse); the other pictures belong to the public domain (Tab. S2).

ACKNOWLEDGEMENTS

The present work would not have been possible without the immense help of Flávio Szablak, Rebeka Martins, Kathiani Bastos, Layza de Lima and Pedro Bastos in field and laboratory activities. We also thank Luiza Sarmento-Soares and João Luiz Gasparini for helping with the taxonomic identification of some freshwater fishes and Alexandre Marceniuk for catfish species.We are indebted with Felipe Buloto, Maik Da Hora, Nelson Barcelos, Jonathas Barreto, Cristielli Rotta, Miguel Saldanha, Lucas Caliman, Fernanda Guimarães, Bianca Cruz, Nefertiti Rojas and all the fishermen of Regência village for their help in sampling and for sharing their knowledge about the fish community of the Doce River; special thanks are due to Arnoilto Alcântara, Josenildo “Frango”, Clavelanio “Preto” and Leônidas. We also would like to thank TAMAR/ICMBio and Associação de Pescadores de Regência for logistic support for field activities. Data acquisition for this research was partially done in the scope of the Aquatic Biodiversity Monitoring Program, Environmental Area I, established by the Technical-Scientific Cooperation Agreement nº 30/2018 between Fundação Espírito-Santense de Tecnologia (FEST) and Fundação Renova, published in Brazil’s Official Gazette (Diário Oficial da União). Neither agency played any role in result interpretation or manuscript preparation.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Rodrigues VLA, Guabiroba HC, Vilar CC, Andrades R, Villela A, Hostim-Silva M, Joyeux J-C. Fish biodiversity of a tropical estuary under severe anthropic pressure (Doce River, Brazil). Neotrop Ichthyol. 2022; 20(3):e220022. https://doi.org/10.1590/1982-0224-2022-0022

Edited-by

Osmar Luiz

Publication Dates

  • Publication in this collection
    14 Oct 2022
  • Date of issue
    2022

History

  • Received
    23 Mar 2022
  • Accepted
    24 Aug 2022
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