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Special Article of Flora perifítica • Hoehnea 48 • 2021 • https://doi.org/10.1590/2236-8906-18/2021   copy

Periphytic algal flora of the lower Doce river basin after ore tailings flow, Espírito Santo State, Brazil: Sampling design and methods

Flora de algas perifíticas da bacia do baixo rio Doce, após a passagem de rejeitos de minério, Estado do Espírito Santo, Brasil: Delineamento amostral e métodos

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

The present work aims to describe the sampling design and the methods used in the series “Periphytic algal flora of the Lower Doce River basin (Espírito Santo State, Brazil) after ore tailings flow”. This series will present the biodiversity of periphytic algae registered during the Aquatic Biodiversity Monitoring Program, Environmental Area I, carried out in the Lower Doce River basin three years after the passage of the ore tailings from Fundão dam (Mariana, Minas Gerais). Samples from the periphytic community were collected monthly, between October/2018 and February/2020, at five sampling stations in lotic environments and seven in lentic environments of the basin. These samples were fixed and the taxa will be identified and described, following specific methods. These taxa will be presented in sequential fascicles, split according to their taxonomic and morphological classification. More than 900 taxa have been recorded in this survey. This is the first taxonomic study about inland algae carried out in the Lower Doce River basin.

Keywords:
epilithon; epiphyton; freshwater diversity; lakes; rivers

RESUMO

O presente trabalho tem como objetivo descrever o delineamento amostral e os métodos utilizados na série “Flora de algas perifíticas da bacia do baixo rio Doce, após a passagem de rejeitos de minério, Estado do Espírito Santo, Brasil”. Esta série apresentará a biodiversidade de algas perifíticas registradas durante o Programa de Monitoramento da Biodiversidade Aquática, Área Ambiental I, realizado na bacia do baixo rio Doce três anos após a passagem do rejeito de minério da barragem de Fundão, Mariana, Estado de Minas Gerais. Foram coletadas mensalmente mensalmente, entre outubro/2018 e fevereiro/2020, amostras da comunidade perifítica em cinco estações amostrais em ambientes lóticos e sete em ambientes lênticos da bacia. Essas amostras foram fixadas e os táxons serão identificados e descritos, seguindo métodos específicos. Esses táxons serão apresentados em fascículos sequenciais, divididos de acordo com sua classificação taxonômica e morfológica. Mais de 900 táxons foram registrados no levantamento. Este é o primeiro trabalho taxonômico sobre algas continentais realizado na bacia do baixo rio Doce.

Palavras-chave:
epilíton; epifíton; diversidade de água doce; lagos; rios

Introduction

Phycofloristic studies are important for the local and regional biodiversity knowledge (Bicudo 2020Bicudo, C.E.M. 2020. PEFI algal flora: a half-century of investigation. Hoehnea 47: e232019.), for species autecology, and also to correct identification of these organisms when they are used in biomonitoring programs (Hamada & Ferreira-Keppler 2012Hamada, N. & Ferreira-Keppler, R.L. 2012. Guia ilustrado de insetos aquáticos e semiaquáticos da Reserva Florestal Ducke, Editora da Universidade Federal do Amazonas, Manaus.). Menezes et al. (2015)Menezes, M. et al. 2015. Update of the Brazilian floristic list of Algae and Cyanobacteria. Rodriguésia 66: 1047-1062. recorded 4,747 species of algae and cyanobacteria for Brazil. This number is increasing even more with several study efforts, such as the algae flora of streams in the Parnaíba River basin (Auricchio et al. 2019Auricchio, M.R., Lambrecht, R.W. & Peres, C.K. 2019. Stream macroalgal flora from Parnaíba River Basin, Brazil: reducing Wallacean shortfall. Biota Neotropica 19: e20180685.), checklist of the Cosmarium in Brazil (Biolo & Bicudo 2018Biolo S. & Bicudo C.E.M. 2018. Checklist of the genus Cosmarium (Zygnematophyceae, Streptophyta) from Brazil. Biodiversity International Journal 2: 452-454.), floristic survey of urban parks (D’alessandro & Nogueira 2017D’Alessandro, E.B. & Nogueira, I.S. 2017. Algas planctônicas flageladas e cocoides verdes de um lago no Parque Beija-Flor, Goiânia, GO, Brasil. Hoehnea 44: 415-430.), and descriptions of new species (Ramos et al. 2017Ramos, G.J.P., Bicudo, C.E.M. & Moura, C.W.D.N. 2017. Cosmarium bahianum, sp. nov. (Desmidiaceae), a new desmid species from a phytotelm habitat in the Brazilian restinga. Phytotaxa 291: 66., Lehmkuhl et al. 2019Lehmkuhl, E.A., Morales, E.A., Tremarin, P.I., Bartozek, E.C.R., Zorzal-Almeida, S., Ludwig, T. A.V., & Bicudo, C.E.M. 2019. Two new species of Nitzschia (Bacillariaceae, Bacillariophyta) from tropical reservoirs of southeastern Brazil. Phytotaxa 399: 83., Ramos et al. 2019Ramos, G.J.P., Bicudo, C.E.M. & Moura, C.W.D.N. 2019. Cosmarium bromelicola sp. nov. (Desmidiaceae, Zygnematophyceae), a new desmid species from Northeast Brazil. Brazilian Journal of Biology 79: 410-413., Zorzal-Almeida et al. 2020Zorzal-Almeida, S., Rodrigues Bartozek, E.C., Morales, E. & Bicudo, C. 2020. Brachysira aristidesii sp. nov. (Bacillariophyceae, Brachysiraceae): a new species from oligotrophic and mesotrophic tropical reservoirs in southeastern Brazil. Phytotaxa 456: 105-113.). One of the most relevant studies about Brazilian microalgae flora is the survey of the ‘Algal Flora of the Parque Estadual das Fontes do Ipiranga (PEFI)’, which started in 1962 and registered 869 taxa in 42 fascicles (Bicudo 2020Bicudo, C.E.M. 2020. PEFI algal flora: a half-century of investigation. Hoehnea 47: e232019.).

Algal flora of inland waters in Espírito Santo State, considering peer-reviewed works with illustration and description, is represented by Delazari-Barroso et al. (2007)Delazari-Barroso, A., Sant’Anna, C.L. & Senna, P.A.C. 2007. Phytoplankton from Duas Bocas Reservoir, Espírito Santo State, Brazil (except diatoms). Hoehnea 34: 211-229., recording phytoplankton community (except diatoms) from a dam, and the description of new cyanobacteria species (Senna et al. 1999). Thus, considering the high density of aquatic ecosystems in the State (Barroso 2007Barroso, G. F. 2007. Lagoas costeiras do Espírito Santo: perspectivas para conservação. In: Menezes, L.F. et al., (orgs). Ecossistemas costeiros do Espírito Santo: conservação e restauração. Vitória, EDUFES, pp: 71-86.), the knowledge about the continental algae flora is practically null. This fact is aggravated by the threats to aquatic ecosystems that are increasing in frequency (Dudgeon et al. 2006, Reid et al. 2019Reid, A.J., Carlson, A.K., Creed, I.F., Eliason, E.J., Gell, P.A., Johnson, P.T.J., Kidd, K.A., MacCormack, T.J., Olden, J.D., Ormerod, S.J., Smol, J.P., Taylor, W.W., Tockner, K., Vermaire, J.C., Dudgeon, D. & Cooke, S.J. 2019. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews 94: 849-873.), which lead to a decreasing in algal diversity (Wengrat et al. 2018Wengrat, S., Padial, A.A., Jeppesen, E., Davidson, T.A., Fontana, L., Costa-Böddeker, S. & Bicudo, D.C. 2018. Paleolimnological records reveal biotic homogenization driven by eutrophication in tropical reservoirs. Journal of Paleolimnology 60: 299-309.) before they could be observed by researchers. For Espírito Santo State, it can be mentioned the case of Fundão dam rupture, in 2015, which released more than 43 million square meters of iron ore tailings in Rio Doce basin waters (Renova 2016Renova, 2016. Atualização do Plano de Recuperação Ambiental Integrado, PRAI. Available at: https://www.fundacaorenova.org/wp-content/uploads/2017/01/prai_renova_jan17_rev03.pdf
https://www.fundacaorenova.org/wp-conten... ). The tailings load drastically affected the Doce river, which has been historically contaminated by mining, causing a substantial increase in the loading of suspended sediments and transported various dissolved metals, such as iron and aluminium (Hatje et al. 2017Hatje, V., Pedreira, R.M.A., Rezende, C.E., Schettini, C.A.F, Souza, G.C., Marin, D.C. & Hackspacher, P.C. 2017. The environmental impacts of one of the largest tailing dam failures worldwide. Scientific Reports 7: 1-13.). Besides the contamination of the main channel of Doce River, some adjacent lake ecosystems in the basin were also affected by the tailings. Although data about the effects in periphytic community integrity has not yet been published, it is important to highlight that surveys of the flora of microalgae (both periphyton and phytoplankton) were non-existent. For this reason, the real species pool in the region before the tailings pass is unknown, making it difficult to understand the real impact on the algae flora.

Works with periphytic algae community in Espírito Santo State are restricted to ecological approaches (e.g. Cavati & Fernandes 2007Cavati, B. & Fernandes, V.O. 2007. Algas perifíticas em dois ambientes do baixo rio Doce (lagoa Juparanã e rio Pequeno - Linhares, Estado do Espírito santo, Brasil): variação espacial e temporal. Acta Scientiarum. BIological Sciences 30: 439-448., Almeida & Fernandes 2013Almeida, S.Z. & Fernandes, V.O. 2013. Effects of intensive fish-farming and domestic wastewater on the periphytic algal community in a tropical coastal lagoon (Juara, Brazil). Acta Scientiarum. Biological Sciences 35: 335-342.). This community is an important component of aquatic biodiversity (Lowe & Pan 1996Lowe, R.L. & Pan, Y. 1996. Benthic algal communities as biological indicators. In Stevenson, R.J., Bothwell, M.L., & Lowe, R.L. (Eds.). Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, pp. 705-739.) playing important roles in ecological processes, such as trophic chain (Vadeboncoeur & Steinman 2002Vadeboncoeur, Y., Steinman, A.D. 2002. Periphyton Function in Lake Ecosystems. The Scientific World Journal 2: 1449-1468.) and biogeochemical cycles (Hagerthey et al. 2011Hagerthey, S.E., Bellinger, B.J., Wheeler, K., Gantar, M., Gaiser, E. 2011. Everglades Periphyton: A Biogeochemical Perspective. Critical Reviews in Environmental Science and Technology 41: 309-343.), and it is considered an important bioindicator of the integrity of aquatic ecosystems (Lobo et al. 2014Lobo, E.A., Wetzel, C.E., Schuch, M., Ector, L. 2014. Diatomáceas epilíticas como indicadores da qualidade da água em Sistemas Lóticos subtropicais e temperados brasileiros. EDUNISC, Santa Cruz do Sul.). Then, it is crucial to know which species make up the current regional pool of the Lower Doce River basin. This paper aims to describe the sample design and methods for the development of the series “Periphytic algal flora of the Lower Doce River basin (Espírito Santo State, Brazil) after ore tailings flow”. This series will be divided into fascicles according to taxonomic groups found in the periphytic community of the lentic and lotic aquatic ecosystems of the Lower Doce river studied in the Aquatic Biodiversity Monitoring Program, Environmental Area I, Periphyton project, carried out by the research group “Rede Rio Doce-Mar”, starting to unravel their algae biodiversity.

Material and Methods

Study area - Lower Doce River basin is fully located in the State of Espírito Santo, southeast Brazil (41º30’ to 39º30’W and 19º30’ to 20º30’S) in the Tertiary plateaus formed by Barreiras Formation and the Quaternary Coastal Plain (Salinas et al. 2020Salinas, J.B.G., Eggerth, M.K.P., Miller, M.E., Meza, R.R.B., Chacaltana, J.T.A., Acuña, J.R., Barroso, G.F. 2020. Wetland mapping with Multitemporal Sentinel Radar Remote Sensing in the Southeast region of Brazil. IEEE Latin American GRSS & ISPRS Remote Sensing Conference (LAGIRS), pp. 669-674.). Its drainage area covers about 11,921 km2 and contains about 90 smaller lakes, including the second largest Brazilian freshwater lake (Juparanã) (Barroso et al. 2012Barroso, G. F., Garcia, F. D. C., Gonçalves, M. A., Martins, F. D. O., Venturini, J. C., Sabadini, S. & Bertoldi, L. 2012. Estudos integrados no sistema lacustre do baixo rio Doce (Espírito Santo). I Seminário Nacional de Gestão Sustentável de Ecossistemas Aquáticos: Complexidade, Interatividade e Ecodesenvolvimento, COPPE/UFRJ.). According to the Köppen classification, region climate is Aw (humid tropical with dry winter) (Nóbrega et al. 2008Nóbrega, N.E.F., Silva, J.G.F., Ramos, H.E.A. & Pagung, F.S. 2008. Balanço hídrico climatológico e classificação climática de Thornthwaite e Köippen para o município de Linhares - ES. In: Congresso Nacional de Irrigação e Drenagem: O equilíbrio do fluxo hídrico para uma agricultura irrigada sustentável, São Mateus, ABID.) and seasonality can be divided into dry (April to September) and rainy (October to March) seasons (RRDM 2019RRDM - Rede Rio Doce-Mar. 2019. Relatório Anual - Anexo 3 Dulcícola. Disponível em https://www.ibama.gov.br/cif/notas-tecnicas/ct-bio/relatorios-da-rede-rio-doce-mar
https://www.ibama.gov.br/cif/notas-tecni... ), with 1,123 mm of average annual rainfall (Salinas et al. 2020Salinas, J.B.G., Eggerth, M.K.P., Miller, M.E., Meza, R.R.B., Chacaltana, J.T.A., Acuña, J.R., Barroso, G.F. 2020. Wetland mapping with Multitemporal Sentinel Radar Remote Sensing in the Southeast region of Brazil. IEEE Latin American GRSS & ISPRS Remote Sensing Conference (LAGIRS), pp. 669-674.). Lakes and lagoons in Lower Doce River, due to their formation, are often connected with Doce River in a bidirectional flow that varies according to the level of the river. Lower Doce River riparian area is highly degraded, with a large portion with more than 80% deforested (Pires et al. 2017Pires, A.P.F., Rezende, C.L., Assad, E.D., Loyola, R., Scarano, F.R. 2017. Forest restoration can increase the Rio Doce watershed resilience. Perspective in Ecology and Conservation 15: 187-193.), one of the causes of the intense silting up of rivers. Discharge of untreated domestic sewage in most municipalities in the basin has also caused the degradation of the water quality of the Doce River and its tributaries (ANA 2016ANA (Agência Nacional de Águas). 2016. Encarte especial sobre a Bacia do Rio Doce - rompimento da barragem de Mariana/MG. Conjuntura do Recursos Hídricos no Brasil, Informe 2015. Brasília.).

Figure 1
Sampling stations in the lower Doce river basin, Espírito Santo State, Brazil. Development by Gilberto F. Barroso.

Sampling design and material preparing - Samples were collected in four sampling sites in shallow lakes (Areão - E23, Areal - E24, and Monsarás - E25 and E25a), three in deep lakes (Limão - E18, Nova - E19, and Juparanã - E20), four in Doce River (E0, E21, E22, E26), and one in its affluent (Guandu river - E17) (figure 1). Our choices of the sampling sites were based on environmental kind (river, lake, lagoon) and the possible impact of the ore tailing. Samplings were carried out monthly between October 2018 and February 2020 (except for October 2019 due to logistic problems). Periphytic material was collected from different substrates in littoral zone, such as pebbles and macrophytes. Whenever possible, the same kind of substrate was collected at each sampling station throughout the campaign. Substrates were transported to the laboratory in refrigerated recipients containing a small amount of distilled water to keep samples humid. At the laboratory, periphytic material was scrapped from the substrates with a smooth bristle brush and small jets of distilled water (following recommendations in Ferragut et al. 2013Ferragut, C., Bicudo, D.C. & Vercellino, I.S. 2013. Amostragem e medidas de estrutura da comunidade perifítica. In: A. Schwarzbold, A. Burliga & L.C. Torgan (eds.). Ecologia do perifíton. RiMa, São Carlos, pp. 157-177.). All biological material was fixed and preserved with 3-5% formalin solution. For diatoms, organic materials were removed using hydrogen peroxide (H2O2 35%) and hydrochloric acid (HCl 10%), following Battarbee et al. (2001)Battarbee, R.W. et al. 2001. Diatoms. In: Smol, J.P; Birks, H.J.B.; Last, W.M. (eds.). Tracking Environmental Change Using Lake Sediments. Kluwer Academic Publishers, London, pp. 155-203., and permanent slides were mounted using Naphrax® (IR = 1.73) as the inclusion medium. Samples were deposited at the Herbário VIES at Federal University of Espírito Santo. We created for each herbarium sample a code that will be used to represent all information about the deposited sample (such as locality, sampling date, herbarium number, and substrate), as shown in table 2. For this purpose, we considered that all periphytic samples were collected in Espírito Santo State, Brazil.

Conductivity and pH were measured in the field (YSI Horiba U-53 or Exo2 multiparameter) and superficial water samples were taken to determine total iron (Inductively Coupled Plasma Atomic Spectrometry with detection by Spectrometry of Masses - ICP-MS), total phosphorous (Valderrama 1981Valderrama, J.C. 1981. The simultaneous analysis of total nitrogen and total phosphorus in natural waters. Marine Chemistry 10: 109-122.), and chlorophyll-a (fluorimetric method; Barroso & Littlepage 1998Barroso, G. F., & Littlepage, J. 1998 Protocolo para análise de clorofila a e feopigmentos pelo método fluorimétrico (Fluorímetro TD-700). Brazilian Mariculture Linkage Program. Vitória.). Trophic state index was calculated following Lamparelli (2004)Lamparelli, M. C. 2004. Graus de trofia em corpos d\’água do estado de São Paulo: avaliação dos métodos de monitoramento. Tese de Doutorado, Universidade de São Paulo, São Paulo.. For more details about abiotic variables, see RRDM (2019)RRDM - Rede Rio Doce-Mar. 2019. Relatório Anual - Anexo 3 Dulcícola. Disponível em https://www.ibama.gov.br/cif/notas-tecnicas/ct-bio/relatorios-da-rede-rio-doce-mar
https://www.ibama.gov.br/cif/notas-tecni... . These variables were selected since they represent ecosystem metabolism, eutrophication, and metal content in water.

Taxonomic and ecological analysis - For non-diatom species, a minimum of five non-permanent slides were prepared for each sample for the taxonomic survey and specimens were observed and photographed. For diatoms species, the analysis were conducted in a full permanent slide per sampling site. Observed taxonomic features and the bibliography used in identification will be described in each fascicule, as it is specific to each algae group. Autecology will be based on the environmental variables range in which the species were found. Yet, taxa distribution was assess using the frequency of occurrence and will be calculated to classify them according to the categories in Matteucci & Colma (1982)Matteucci, S.D., Colma, A. 1982. Metodologia para el estúdio de la vegetación. The General Secretarial of The Organization of American States, Washington.: Very Frequent: VF (> 70%), Frequent: F (≤ 70% and > 40%), Little Frequent: LF (≤ 40% and > 10%), and Rare: R (≤ 10%).

Results and Discussion

During the survey, 185 samples were collected along the Lower Doce River basin. Some samples could not be collected due to difficulty in accessing the sample station, or loss of the sample during transport. Sampling stations coordinates and environmental characterization (based on the variables used for the autecology of the species) are shown in table 1. The environments were characterized by a wide range of conductivity, total iron, and trophic states (from ultraoligotrophic to supereutrophic). Only the sampling stations of the lagoons could be classified as slight acid in some campaigns, while pH in other sampling stations never were less than 7. For more details on the ecosystem characteristics, see RRDM (2019)RRDM - Rede Rio Doce-Mar. 2019. Relatório Anual - Anexo 3 Dulcícola. Disponível em https://www.ibama.gov.br/cif/notas-tecnicas/ct-bio/relatorios-da-rede-rio-doce-mar
https://www.ibama.gov.br/cif/notas-tecni... . Table 2 shows the herbarium numbers and other related features and substrates from which periphytic material was scraped in each sampling site.

More than 900 taxa (~ 17 Classes) have already been registered and, “even though not all taxa identification have been finished”, we found that the most representative Classes were Bacillariophyceae (~300 taxa), Zygnematophycae (~185 taxa), Cyanophyceae (~145 taxa), and Chlorophyceae (~125 taxa). After identification and description, these taxa will be grouped according to taxonomic groups (e.g., genus Cosmarium) and/or their morphology (e.g., coccoid Cyanophyceae), according to the number of species. Each group will compose a fascicule of the series about periphytic flora of the Lower Doce River basin, which will be submitted non-periodically. This series is the first effort to describe periphytic algae flora from this region.

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Table 1
Sampling sites location and range of environmental conditions, Espirito Santo State, Brazil. Cond: conductivity. Fe: total iron. Trophic state - Ult: Ultraoligotrophic. Oli: oligotrophic. Mes: Mesotrophic. Eut: Eutrophic. Sup: Supereutrophic.
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Table 2
Sample codes, herbarium numbers and attached information about locality, date, substrate and collector, lower Doce river basin after ore tailings flow, Espírito Santo State, Brazil.

Acknowledgment

We thank Prof. Dr. Vânya Márcia Duarte Pasa (UFMG), for analyzing total iron and to Prof. Dr. Gilberto Fonseca Barroso (UFES), for analyzing pH, conductivity, chlorophyll-a and total phosphorus, and for the development of the map. This research was developed under the Aquatic Biodiversity Monitoring Program, Environmental Area I, established by the Technical-Scientific Cooperation Agreement nº 30/2018 between Espírito Santo Foundation of Technology (FEST) and Renova Foundation, published in Brazil’s Official Gazette (Diário Oficial da União).

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Edited by

Associate Editor: Maria Margarida da Rocha Fiuza de Melo

Publication Dates

  • Publication in this collection
    17 Dec 2021
  • Date of issue
    2021

History

  • Received
    02 Mar 2021
  • Accepted
    26 June 2021
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