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

Vitor L. A. Rodrigues1 , Helder C. Guabiroba1, Ciro C. Vilar1, Ryan Andrades1, Alexandre Villela2, Maurício Hostim-Silva3 and Jean-Christophe Joyeux1

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Abstract​


EN

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 werethe 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.

PT

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, 2004). Despite their economic and social value (e.g., providing fishing grounds, water supply, aquaculture and navigation) (Basset et al., 2013), estuaries have been sorely exposed to human-driven habitat loss, the introduction of non-native species and water contamination (Lotze et al., 2006).

The Doce River is among the major fluvial systems of southeastern Brazil and flows over 850 km (Lins et al., 2012) through the states of Minas Gerais and Espírito Santo. It runs through the Neotropical Atlantic Forest, a hotspot biome (Ribeiro et al., 2011) 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, 1870; Saint-Hilaire, 1936; Wied-Neuwied, 1940; Baviera, 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, 2007; Saldanha, 2018). Knowledge about the river’s ichthyofauna composition (Vieira, 2009; Sarmento-Soares et al., 2017; Vilar et al., 2022) and its conservation status (Su et al., 2021) has improved in recent years. However, estuarine fish assemblages remain poorly characterized in the Doce River estuary (DRE) (Jankowsky et al., 2021) despite the area being recognized as of ‘extremely high’ biological importance (MMA, 2007).

Impacts caused by mining have been known for centuries (Saint-Hilaire, 1938, 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., 2014; Espindola, 2015). In this sense, biodiversity and ecological services have been threatened by habitat fragmentation, loss of basin and riparian vegetation, introduction of exotic species (Ruschi, 1965; Fragoso-Moura et al., 2016; Bueno et al., 2021; Su et al., 2021) and widespread pollution (Agostinho et al., 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., 2017; Bonecker et al., 2019; Cordeiro et al., 2019; Gabriel et al., 2021).

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, 2018; Richard et al., 2020; Longhini et al., 2022). Conversely, the lack of faunal assemblages baselines (such as Gomes et al., 2017; Andrades et al., 2020; Bueno et al., 2021; Condini et al., 2022) 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., 2022; Vilar et al., 2022) and trophic ecology (Andrades et al., 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, 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., 2006; França et al., 2013). The climate is tropical, with the dry season extending from April to September and the rainy season from October to March (Nimer, 1989; Alvares et al., 2013). Despite a decreasing trend in the Doce River hydrological regime (Coelho, 2006), median streamflow during the wet season reaches up to 900 m3/s (Oliveira, Quaresma, 2017), which explains the very low salinity near the river mouth (Gomes et al., 2017; Vilar et al., 2022). According to the geomorphological context, the Doce River mouth is a submerged deltaic system dominated by waves (Dominguez, Wanless, 1991). 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., 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, 2015).

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., 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.

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.

Taxa

Euryhalinity

Trophic group

Origin

Brazilian Red List

Endemism

PRISTIFORMES

 

 

 

 

 

Pristidae

 

 

 

 

 

Pristis pristis (Linnaeus, 1758)* ?

Per

PV

NV

CR

NE

ELOPIFORMES

 

 

 

 

 

Elopidae

 

 

 

 

 

Elops cf. smithi McBride, Rocha, Ruiz-Carus & Bowen, 2010*

Per

GC

NV

LC

NE

ANGUILLIFORMES

 

 

 

 

 

Ophichthidae

 

 

 

 

 

Myrophis punctatus Lütken, 1852

Per

ZB

NV

LC

NE

CLUPEIFORMES

 

 

 

 

 

Clupeidae

 

 

 

 

 

Lilie piquitinga (Schreiner & Miranda Ribeiro, 1903)

Per

ZP

NV

LC

NE

Engraulidae

 

 

 

 

 

Anchoa januaria (Steindachner, 1879)

Per

ZP

NV

LC

ED

Anchoa spinifer (Valenciennes, 1848)

Per

ZP

NV

LC

NE

Anchoa tricolor (Spix & Agassiz, 1829)

Per

ZP

NV

LC

ED

Anchovia clupeoides (Swainson, 1839)

Per

ZP

NV

LC

NE

Anchoviella cayennensis (Puyo, 1946)

Per

ZP

NV

LC

NE

Anchoviella lepidentostole (Fowler, 1911)

Per

ZP

NV

LC

NE

Cetengraulis edentulus (Cuvier, 1829)

Per

ZP

NV

LC

NE

Lycengraulis grossidens (Spix & Agassiz, 1829)

Per

GC

NV

LC

NE

Odontognathus mucronatus Lacepède, 1800

Per

ZP

NV

LC

NE

SILURIFORMES

 

 

 

 

 

Callichthyidae

 

 

 

 

 

Callichthys callichthys (Linnaeus, 1758)

1st

ZB

NV

LC

NE

Loricariidae

 

 

 

 

 

Hypostomus scabriceps (Eigenmann & Eigenmann, 1888)

1st

DT

EX-B

LC

ED

Ariidae

 

 

 

 

 

Cathorops cf. arenatus (Valenciennes, 1840)

Per

ZB

NV

LC

NE

Cathorops spixii (Agassiz, 1829)

Per

ZB

NV

LC

ED

Genidens barbus (Lacepède, 1803)

Per

ZB

NV

EN

NE

Genidens genidens (Cuvier, 1829)

Per

ZB

NV

LC

ED

Paragenidens grandoculis (Steindachner, 1877)

Per

ZB

NV

CR

ED

Sciades herzbergii (Bloch, 1794)

Per

ZB

NV

LC

NE

Auchenipteridae

 

 

 

 

 

Pseudauchenipterus affinis (Steindachner, 1877)

1st

OV

NV

LC

ED

Pimelodidae

 

 

 

 

 

Pimelodus maculatus Lacepède, 1803

1st

OV

EX-B

LC

NE

Pseudopimelodidae

 

 

 

 

 

Microglanis pataxo Sarmento-Soares, Martins-Pinheiro, Aranda & Chamon, 2006

1st

OV

EX-B

LC

NE

CHARACIFORMES

 

 

 

 

 

Characidae

 

 

 

 

 

Astyanax cf. lacustris (Lütken, 1875)

1st

OV

NV

LC

ED

Deuterodon cf. intermedius Eigenmann, 1908

1st

OV

NV

LC

ED

Knodus cf. moenkhausii (Eigenmann & Kennedy, 1903)

1st

OV

EX-B

LC

NE

Bryconidae

 

 

 

 

 

Salminus brasiliensis (Cuvier, 1816)

1st

PV

EX-B

LC

NE

Erythrinidae

 

 

 

 

 

Hoplias intermedius (Günther, 1864)

1st

PV

NV

LC

ED

Hoplias cf. malabaricus (Bloch, 1794)

1st

PV

NV

LC

ED

Serrasalmidae

 

 

 

 

 

Pygocentrus nattereri Kner, 1858

1st

PV

EX-B

LC

NE

Prochilodontidae

 

 

 

 

 

Prochilodus argenteus Spix & Agassiz, 1829

1st

DT

EX-B

LC

ED

Prochilodus costatus Valenciennes, 1850

1st

DT

EX-B

LC

ED

Anostomidae

 

 

 

 

 

Megaleporinus conirostris (Steindachner, 1875)

1st

OV

NV

LC

ED

AULOPIFORMES

 

 

 

 

 

Synodontidae

 

 

 

 

 

Synodus foetens (Linnaeus, 1766)

Per

PV

NV

LC

NE

SCOMBRIFORMES

 

 

 

 

 

Scombridae

 

 

 

 

 

Scomberomorus brasiliensis Collette, Russo & Zavala-Camin, 1978

Per

PV

NV

LC

NE

SYNGNATHIFORMES

 

 

 

 

 

Syngnathidae

 

 

 

 

 

Microphis lineatus (Kaup, 1856)

Per

ZB

NV

LC

NE

GOBIIFORMES

 

 

 

 

 

Eleotridae

 

 

 

 

 

Butis koilomatodon (Bleeker, 1849)

Per

GC

EX-C

NA

NE

Dormitator maculatus (Bloch, 1792)

Per

OV

NV

NT

NE

Eleotris pisonis (Gmelin, 1789)

Per

GC

NV

LC

NE

Gobiidae

 

 

 

 

 

Awaous tajasica (Lichtenstein, 1822)

Per

OV

NV

LC

NE

Bathygobius soporator (Valenciennes, 1837)

Per

OV

NV

LC

NE

Ctenogobius boleosoma (Jordan & Gilbert, 1882)

Per

OV

NV

LC

NE

Ctenogobius shufeldti (Jordan & Eigenmann, 1887)

Per

OV

NV

LC

NE

Evorthodus lyricus (Girard, 1858)

Per

DT

NV

LC

NE

Gobionellus oceanicus (Pallas, 1770)

Per

DT

NV

LC

NE

Microgobius meeki Evermann & Marsh, 1899

Per

ZB

NV

LC

NE

SYNBRANCHIFORMES

 

 

 

 

 

Synbranchidae

 

 

 

 

 

Synbranchus marmoratus Bloch, 1795

Per

PV

NV

LC

NE

CARANGIFORMES

 

 

 

 

 

Centropomidae

 

 

 

 

 

Centropomus parallelus Poey, 1860

Per

GC

NV

LC

NE

Centropomus undecimalis (Bloch, 1792)

Per

GC

NV

LC

NE

Polynemidae

Per

 

 

 

 

Polydactylus oligodon (Günther, 1860)

Per

GC

NV

LC

NE

Polydactylus virginicus (Linnaeus, 1758)

Per

GC

NV

LC

NE

Carangidae

 

 

 

 

 

Caranx crysos (Mitchill, 1815)

Per

PV

NV

LC

NE

Caranx hippos (Linnaeus, 1766)

Per

PV

NV

LC

NE

Caranx latus Agassiz, 1831

Per

ZB

NV

LC

NE

Chloroscombrus chrysurus (Linnaeus, 1766)*

Per

OV

NV

LC

NE

Oligoplites saliens (Bloch, 1793)

Per

PV

NV

LC

NE

Selene vomer (Linnaeus, 1758)

Per

GC

NV

LC

NE

Trachinotus goodei Jordan & Evermann, 1896

Per

GC

NV

LC

NE

Echeneidae

 

 

 

 

 

Echeneis naucrates Linnaeus, 1758

Per

UD

NV

LC

NE

Paralichthyidae

 

 

 

 

 

Citharichthys arenaceus Evermann & Marsh, 1900

Per

GC

NV

LC

NE

Citharichthys macrops Dresel, 1885

Per

ZB

NV

LC

NE

Citharichthys spilopterus Günther, 1862

Per

ZB

NV

LC

NE

Etropus crossotus (Jordan & Gilbert, 1882)*

Per

ZB

NV

LC

NE

Achiridae

 

 

 

 

 

Achirus declivis Chabanaud, 1940

Per

ZB

NV

LC

NE

Achirus lineatus (Linnaeus, 1758)

Per

ZB

NV

LC

NE

Catathyridium garmani (Jordan, 1889)

Per

ZB

NV

LC

NE

Trinectes microphthalmus (Chabanaud, 1928)

Per

ZB

NV

LC

ED

Trinectes paulistanus (Miranda Ribeiro, 1915)

Per

ZB

NV

LC

NE

Cynoglossidae

 

 

 

 

 

Symphurus tessellatus (Quoy & Gaimard, 1824)

Per

ZB

NV

LC

NE

CICHLIFORMES

 

 

 

 

 

Cichlidae

 

 

 

 

 

Cichla cf. kelberi Kullander & Ferreira, 2006

2nd

PV

EX-B

LC

NE

Cichla monoculus Spix & Agassiz, 1831*

2nd

PV

EX-B

LC

NE

Cichlasoma dimerus Heckel, 1840

2nd

OV

EX-B

LC

ED

Coptodon rendalli (Boulenger, 1897)

2nd

HB

EX-C

NA

NE

Crenicichla cf. lacustris (Castelnau, 1855)

2nd

GC

NV

LC

NE

Geophagus cf. brasiliensis (Quoy & Gaimard, 1824)

2nd

OV

NV

LC

NE

Oreochromis niloticus (Linnaeus, 1758)

2nd

HB

EX-C

NA

NE

BELONIFORMES

 

 

 

 

 

Belonidae

 

 

 

 

 

Strongylura marina (Walbaum, 1792)

Per

GC

NV

LC

NE

CYPRINODONTIFORMES

 

 

 

 

 

Poeciliidae

 

 

 

 

 

Poecilia vivipara Bloch & Schneider, 1801

2nd

OV

NV

LC

NE

ATHERINIFORMES

 

 

 

 

 

Atherinopsidae

 

 

 

 

 

Atherinella brasiliensis (Quoy & Gaimard, 1825)

Per

ZP

NV

LC

NE

MUGILIFORMES

 

 

 

 

 

Mugilidae

 

 

 

 

 

Mugil brevirostris Miranda Ribeiro, 1915

Per

DT

NV

DD

NE

Mugil curema Valenciennes, 1836

Per

DT

NV

DD

NE

Mugil curvidens Valenciennes, 1836

Per

DT

NV

DD

NE

Mugil incilis Hancock, 1830

Per

DT

NV

LC

NE

Mugil liza Valenciennes, 1836

Per

DT

NV

NT

NE

BLENNIIFORMES

 

 

 

 

 

Blenniidae

 

 

 

 

 

Lupinoblennius paivai (Pinto, 1958)

Per

ZB

NV

LC

ED

GERREIFORMES

 

 

 

 

 

Gerreidae

 

 

 

 

 

Diapterus auratus Ranzani, 1842

Per

ZB

NV

LC

NE

Diapterus rhombeus (Cuvier, 1829)

Per

ZB

NV

LC

NE

Eucinostomus argenteus Baird & Girard, 1855

Per

ZB

NV

LC

NE

Eucinostomus melanopterus (Bleeker, 1863)

Per

ZB

NV

LC

NE

Eugerres brasilianus (Cuvier, 1830)

Per

ZB

NV

LC

NE

EUPERCARIA incertae sedis

 

 

 

 

 

Sciaenidae

 

 

 

 

 

Bairdiella goeldi Marceniuk, Molina, Caires, Rotundo, Wosiacki & Oliveira, 2019

Per

ZB

NV

LC

NE

Cynoscion acoupa (Lacepède, 1801)

Per

GC

NV

NT

NE

Cynoscion microlepidotus (Cuvier, 1830)

Per

GC

NV

LC

NE

Larimus breviceps Cuvier, 1830

Per

GC

NV

LC

NE

Menticirrhus americanus (Linnaeus, 1758)

Per

ZB

NV

DD

NE

Micropogonias furnieri (Desmarest, 1823)

Per

ZB

NV

LC

NE

Pachyurus adspersus Steindachner, 1879

Per

ZB

NV

DD

ED

Stellifer brasiliensis (Schultz, 1945)

Per

ZB

NV

LC

ED

Stellifer naso (Jordan, 1889)

Per

GC

NV

LC

NE

Stellifer punctatissimus (Meek & Hildebrand, 1925)

Per

ZB

NV

DD

NE

Stellifer rastrifer (Jordan, 1889)

Per

ZB

NV

LC

NE

Stellifer stellifer (Bloch, 1790)

Per

ZB

NV

LC

NE

LUTJANIFORMES

 

 

 

 

 

Haemulidae

 

 

 

 

 

Conodon nobilis (Linnaeus, 1758)*

Per

ZB

NV

LC

NE

Haemulopsis corvinaeformis (Steindachner, 1868)

Per

ZB

NV

LC

NE

Pomadasys ramosus (Poey, 1860)

Per

ZB

NV

LC

NE

Rhonciscus cf. crocro (Cuvier, 1830)

Per

ZB

NV

LC

NE

Lutjanidae

 

 

 

 

 

Lutjanus cyanopterus (Cuvier, 1828)

Per

GC

NV

VU

NE

Lutjanus jocu (Bloch & Schneider, 1801)

Per

GC

NV

NT

NE

Lutjanus synagris (Linnaeus, 1758)

Per

GC

NV

NT

NE

CENTRARCHIFORMES

 

 

 

 

 

Kyphosidae

 

 

 

 

 

Kyphosus sectatrix (Linnaeus, 1758)

Per

HB

NV

LC

NE

SPARIFORMES

 

 

 

 

 

Sparidae

 

 

 

 

 

Archosargus probatocephalus (Walbaum, 1792)*

Per

OV

NV

DD

NE

TETRAODONTIFORMES

 

 

 

 

 

Tetraodontidae

 

 

 

 

 

Lagocephalus laevigatus (Linnaeus, 1766)

Per

GC

NV

LC

NE

Sphoeroides greeleyi Gilbert, 1900*

Per

OV

NV

LC

NE

Sphoeroides testudineus (Linnaeus, 1758)

Per

ZB

NV

DD

NE

 

Data analysis. All species were identified to the lowest possible taxonomic level with the aid of classical and current literature (e.g., Figueiredo, Menezes, 1978; Menezes, 1980; Menezes, Figueiredo, 1980, 1985, 2000; Carvalho-Filho, 1999; Munroe, Nizinski, 2002; Nizinski, Munroe, 2002; Marceniuk, 2005; Kullander, Ferreira, 2006; Moura, Lindeman, 2007; Vieira et al., 2014, 2015; Marceniuk et al., 2019). Scientific names and phylogenetic arrangement of orders and families follow Betancur-R et al. (2017) and The Catalog of Fishes (Fricke et al., 2022).

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, 2018; Froese, Pauly, 2020). Fish tolerance to salinity was classified into three categories following Myers (1938) and Berra (2001): 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, 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.

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: Paragenidensgrandoculis (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, 2020), 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., 2014; Vilar et al., 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, 1966; Kaatz, 2002).

The DRE fish fauna is dominated by zoobenthivores in both richness and biomass (Vilar et al., 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, 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, 2006; Aprile et al., 2016; Rudorff et al., 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, 2007; Keesen et al., 2016; Swarça et al., 2018; Roberto et al., 2020). Beyond the immeasurable value of biodiversity loss, ecological consequences related to habitat homogenization are plentiful (Layman et al., 2007; Andrades et al., 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., 2017; Fernandes et al., 2022; Rocha et al., 2022). As shown by Andrades et al. (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, 2015; Aprile et al., 2016; Fragoso-Moura et al., 2016). However, the DRE fish biodiversity is surprisingly higher than in geographically close estuaries, including one wave-dominated delta (Neto, 2009; Hostim-Silva et al., 2013; Vilar et al., 2013, Catelani et al., 2014). 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, 2007) while the latter was considered restricted to deep lakes adjacent to the lower Doce River (Marceniuk et al., 2019). 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., 2020; Andrades et al., 2021; Costa et al., 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., 2017). 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) 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., 2021 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., 2010; Jere et al., 2021). 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, 2004; Pinto-Coelho et al., 2008).

The Doce River and its estuary have been affected by multiple human‑induced 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).

Acknowledgments​


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.

References​


Agostinho 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

Alexander 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

Alvares 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

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

Andrades 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

Aprile 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

Basset 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

Baviera PT. Viagem pelo Espírito Santo (1888): Viagem pelos trópicos brasileiros. Vitória: Arquivo Público do Estado do Espírito Santo, Brasil; 2013.

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

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

Bonecker 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

Bueno 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

Carvalho-Filho A. Peixes: Costa brasileira. São Paulo: Melro; 1999.

Catelani 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

Coelho 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.

Condini 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

Cordeiro 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

Costa 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

Diniz 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

Dominguez 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

Espindola 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

Espindola 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

Fernandes 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

Figueiredo JL, Menezes NA. Manual de peixes marinhos do sudeste do Brasil. II. Teleostei (1). São Paulo: Museu de Zoologia: USP; 1978.

Fragoso-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

França 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

Fricke 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

Froese R, Pauly D. FishBase. World Wide Web electronic publication. 2020. Available from: https://www.fishbase.se/search.php

Gabriel 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

Gabriel 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

GEOBASES. Sistema Integrado de Bases Geoespaciais do Estado do Espírito Santo. 2015. Available from: https://geobases.es.gov.br/

Girard 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

Gomes 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

Hartt 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.

Hatje 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

Hostim-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

Instituto Brasileiro de Geografia e Estatística (IBGE). Manual técnico da vegetação brasileira. Rio de Janeiro. IBGE – Coordenação de Recursos Naturais e Estudos Ambientais; 2012.

Ministério 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.

Instituto 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.

Jankowsky 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

Jere 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

Kaatz 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

Keesen 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

Kullander 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.

Latini 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

Layman 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

Lins 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

Longhini 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

Lotze 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

Machado FS, Carvalho-Filho A, Giarrizzo T. Redescription and range extension of the endangered Paiva’s blenny Lupinoblennius paivai (Percif