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Evaluation of the environmental quality monitoring protocol for Amazonian streams: a systematic review

Avaliação da eficácia do protocolo de monitoramento da qualidade ambiental para riachos amazônicos: uma revisão sistemática

Abstract

The Amazon Rainforest is renowned for its extraordinary biodiversity and the ravages of pervasive deforestation. The removal of natural vegetation significantly affects Amazonian streams, leading to alterations in their environmental conditions. In the United States, the Environmental Protection Agency has devised a comprehensive protocol to monitor changes in the environmental quality of streams. Since 2011, the Sustainable Amazon Network has implemented this protocol in Amazonian streams. Our systematic review aimed to address the following questions: i) How widely has the protocol been employed in Amazonian streams?; ii) Is the utilization of this protocol well-distributed across the Amazon Basin?; iii) Which types of land use have been assessed using this protocol?; iv) Which components of the aquatic biota have been studied in conjunction with the protocol?; and, v) Which metrics of the protocol are most crucial for elucidating aquatic biota distribution? We conducted searches using the Web of Science and Google Scholar databases, identifying 34 studies that directly aligned with our objectives. It was observed that the Eastern Amazon had the highest number of streams evaluated. Additionally, aquatic insects emerged as an effective tool when utilized alongside the protocol for evaluating the impacts of changes in land use. Ultimately, the most important metrics for assessing impacts on aquatic biota were shelter availability in the channels, the preservation status of riparian forests, and water quality. We recommend developing a simplified version of this protocol to facilitate its application for research teams with limited personnel and financial resources available for fieldwork.

Keywords:
aquatic conservation; biomonitoring; land use change; sampling efficiency; stream ecology

Resumo

A Floresta Amazônica é renomada por sua extraordinária biodiversidade e pelo difundido desmatamento. A remoção da vegetação natural impacta significativamente os riachos amazônicos, levando a alterações em suas condições ambientais. Nos Estados Unidos, a Agência de Proteção Ambiental desenvolveu um protocolo abrangente para monitorar mudanças na qualidade ambiental dos rios. Desde 2011, a Rede Amazônica Sustentável implementou esse protocolo em riachos amazônicos. Nossa revisão sistemática teve como objetivo abordar as seguintes questões: i) Quão amplamente o protocolo foi utilizado em riachos amazônicos? ii) A utilização desse protocolo está bem distribuída na bacia amazônica? iii) Quais tipos de uso da terra foram avaliados com esse protocolo? iv) Quais componentes da biota aquática foram estudados em conjunto com o protocolo? v) Quais métricas do protocolo são mais cruciais para elucidar a distribuição da biota aquática? Conduzimos buscas nas bases de dados Web of Science e Google Scholar, identificando 34 estudos que se alinharam diretamente com nossos objetivos. Observou-se que a Amazônia Oriental teve o maior número de rios avaliados. Além disso, insetos aquáticos surgiram como uma ferramenta eficaz quando utilizados junto ao protocolo para avaliar os impactos das mudanças no uso da terra. Por fim, as métricas mais importantes para avaliar os impactos na biota aquática foram a disponibilidade de abrigo nos canais, o estado de preservação das florestas ripárias e a qualidade da água. Recomendamos o desenvolvimento de uma versão simplificada desse protocolo para facilitar sua aplicação em equipes de pesquisa com recursos financeiros limitados e um número restrito de pessoal disponível para trabalho de campo.

Palavras-chave:
biomonitoramento; conservação aquática; ecologia de riachos; eficiência de amostragem; mudança de uso da terra

1. INTRODUCTION

Amazon has the largest hydrographic basin in the world. Its water network is mainly composed of numerous first- and third-order streams, which harbor a rich aquatic biodiversity (Junk et al., 2007JUNK, W. J.; SOARES, M. G. M.; BAYLEY, P. B. Freshwater fishes of the Amazon River basin: their biodiversity, fisheries, and habitats. Aquatic Ecosystem Health & Management, v. 10, p. 153-173, 2007. https://doi.org/10.1080/14634980701351023
https://doi.org/10.1080/1463498070135102...
) that depends on the riparian vegetation and allochthonous material (Vannote et al., 1980VANNOTE, R. L.; MINSHALL, G. W.; CUMMINS, K. W.; SEDELL, J. R.; CUSHING, C. E. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, v. 37, n. 1, p. 130-137, 1980. https://doi.org/10.1139/f80-017
https://doi.org/10.1139/f80-017...
). However, the expansion of different land use and land covers over Amazonia represents a constant threat to the maintenance of its environmental conditions and biodiversity (Gardner et al., 2013GARDNER, T. A.; FERREIRA, J.; BARLOW, J.; LEES, A. C.; PARRY, L.; VIEIRA, I. C. G. et al. A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philosophical Transactions of the Royal Society B: Biological Sciences, v. 368, n. 1619, p. 20120166-20120166, 2013. https://doi.org/10.1098/rstb.2012.0166
https://doi.org/10.1098/rstb.2012.0166...
). Some of the main land uses in Amazon are livestock (Barona et al., 2010BARONA, E. et al. The role of pasture and soybean in deforestation of the Brazilian Amazon. Environmental Research Letters, v. 5, n. 2, p. 024002, 2010. http://dx.doi.org/10.1088/1748-9326/5/2/024002
http://dx.doi.org/10.1088/1748-9326/5/2/...
), monocultures (Juen et al., 2016JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al. Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
https://doi.org/10.1002/rra.3050...
), selective and non-selective logging (Calvão et al., 2016CALVÃO, L. B.; NOGUEIRA, D. S.; de ASSIS MONTAG, L. F.; LOPES, M. A.; JUEN, L. Are Odonata communities impacted by conventional or reduced impact logging? Forest Ecology and Management, v. 382, p. 143-150, 2016. https://doi.org/10.1016/j.foreco.2016.10.013
https://doi.org/10.1016/j.foreco.2016.10...
) and mining (Sonter et al., 2017SONTER, L. J. et al. Mining drives extensive deforestation in the Brazilian Amazon. Nature Communications, v. 8, n. 1, 2017. https://doi.org/10.1038/s41467-017-00557-w
https://doi.org/10.1038/s41467-017-00557...
; Paiva et al. 2021PAIVA, C. K. S.; FARIA, A. P. J.; CALVAO, L. B.; JUEN, L. The anthropic gradient determines the taxonomic diversity of aquatic insects in Amazonian streams. Hydrobiologia, v. 848, p. 1073-1085, 2021. https://doi.org/10.1007/s10750-021-04515-y
https://doi.org/10.1007/s10750-021-04515...
). These activities cause the total or partial removal of the riparian vegetation (Teresa and Casatti, 2017TERESA, F. B.; CASATTI, L. Trait-based metrics as bioindicators: Responses of stream fish assemblages to a gradient of environmental degradation. Ecological Indicators, v. 75, p. 249-258, 2017. https://doi.org/10.1016/j.ecolind.2016.12.041
https://doi.org/10.1016/j.ecolind.2016.1...
), and the transformation of natural forests into agriculture (Leal et al., 2017LEAL, C. G. et al. Is environmental legislation conserving tropical stream faunas? A large-scale assessment of local, riparian and catchment-scale influences on Amazonian fish. Journal of Applied Ecology, v. 55, n. 3, p. 1312-1326, 2017. https://doi.org/10.1111/1365-2664.13028
https://doi.org/10.1111/1365-2664.13028...
), pasture (Cederberg et al., 2011CEDERBERG, C.; PERSSON, U. M.; NEOVIUS, K.; MOLANDER, S.; CLIFT, R. Including Carbon Emissions from Deforestation in the Carbon Footprint of Brazilian Beef. Environmental Science & Technology, v. 45, n. 5, p. 1773-1779, 2011. https://doi.org/10.1021/es103240z
https://doi.org/10.1021/es103240z...
), or urban areas (Faria et al., 2017FARIA, A. P. J.; LIGEIRO, R.; CALLISTO, M.; JUEN, L. Response of aquatic insect assemblages to the activities of traditional populations in eastern Amazonia. Hydrobiologia, v. 802, n. 1, p. 39-51, 2017. https://doi.org/10.1007/s10750-017-3238-8
https://doi.org/10.1007/s10750-017-3238-...
; Brito et al., 2021BRITO, J. S.; MICHELAN, T. S.; JUEN, L. Aquatic macrophytes are important substrates for Libellulidae (Odonata) larvae and adults. Limnology, v. 22, n. 1, p. 139-149, 2021. https://doi.org/10.1007/s10201-020-00643-x
https://doi.org/10.1007/s10201-020-00643...
) potentially impacting biodiversity.

Environmental agencies are aware of these and other potential anthropic impacts. For this reason, they seek to standardize consistent methodologies for laboratory and field activities, to better monitor streams’ environmental quality (Buss et al., 2014BUSS, D. F.; CARLISLE, D.; CHON, T. S.; CULP, J.; HARDING, J. S.; KEIZER-VLEK, H. E. et al. Stream biomonitoring using macroinvertebrates around the globe: a comparison of large-scale programs. Environmental Monitoring and Assessment, v. 187, p. 4132, 2014. https://doi.org/10.1007/S10661-014-4132-8
https://doi.org/10.1007/S10661-014-4132-...
). In the United States, the Environmental Protection Agency (US-EPA) developed a protocol for field operations, which evaluates the conservation status of streams in forest regions (Peck et al., 2006PECK, D. V. et al. Environmental monitoring and assessment program - surface waters western pilot study: field operations manual for wadeable streams. EPA 600/R-06/003. Washington, DC: USEPA, 2006.). This extensive protocol includes around 240 environmental variables that describe characteristics of the physical habitat like: i) stream morphology; ii) substrate types; iii) hydrodynamics; iv) riparian vegetation; v) wood debris; vi) refuge to aquatic biota; vii) anthropogenic disturbance; and viii) water variables (physical-chemical) (Peck et al., 2006PECK, D. V. et al. Environmental monitoring and assessment program - surface waters western pilot study: field operations manual for wadeable streams. EPA 600/R-06/003. Washington, DC: USEPA, 2006.). This protocol is relatively cheap to apply, requiring only a team of approximately four members, a millimeter pipe, a compass and some visual estimates to obtain the vast majority of variables (except for the water variables that are measured with expensive multiparameter probes) (Kaufmann et al., 1999KAUFMANN, P. R.; LEVINE, P.; ROBISON, E. G.; SEELIGER, C.; PECK, D. V. Quantifying Physical Habitat in Wadeable Streams. EPA/620/R-99/003. Washington, D.C., 1999.; Peck et al., 2006PECK, D. V. et al. Environmental monitoring and assessment program - surface waters western pilot study: field operations manual for wadeable streams. EPA 600/R-06/003. Washington, DC: USEPA, 2006.). This makes the set of variables provided by the US-EPA protocol, associated with different biological groups, a useful tool for ecological and biomonitoring studies.

Several studies have used diversity metrics of biological communities associated with environmental variables from the protocol to produce a complete diagnosis of the environmental and ecological quality of streams (Karr, 1991KARR, J. R. Biological Integrity: A Long-Neglected Aspect of Water Resource Management. Ecological Applications, v. 1, n. 1, p. 66-84, 1991. https://doi.org/10.2307/1941848
https://doi.org/10.2307/1941848...
; Allan, 2004ALLAN, J. D. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology, Evolution, and Systematics, v. 35, p. 257-284, 2004. http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122 .
http://dx.doi.org/10.1146/annurev.ecolsy...
; Ochocka and Pasztaleniec, 2016OCHOCKA, A.; PASZTALENIEC, A. Sensitivity of plankton indices to lake trophic conditions. Environmental Monitoring and Assessment, v. 188, n. 11, 2016. https://doi.org/10.1007/s10661-016-5634). In these studies, fish and aquatic insects are among the most relevant components of the aquatic biota in environmental monitoring programs (Plafkin, 1989PLAFKIN, J. L. Rapid bioassessment protocols for use in streams and rivers: benthic macroinvertebrates and fish. Washington, DC: USEPA, 1989.; Hughes et al., 1998HUGHES, R. M.; KAUFMANN, P. R.; HERLIHY, A. T.; KINCAID, T. M.; REYNOLDS, L.; LARSEN, D. P. A process for developing and evaluating indices of fish assemblage integrity. Canadian Journal of Fisheries and Aquatic Sciences, v. 55, n. 7, p. 1618-1631, 1998. https://doi.org/10.1139/f98-060
https://doi.org/10.1139/f98-060...
; Buss et al., 2014BUSS, D. F.; CARLISLE, D.; CHON, T. S.; CULP, J.; HARDING, J. S.; KEIZER-VLEK, H. E. et al. Stream biomonitoring using macroinvertebrates around the globe: a comparison of large-scale programs. Environmental Monitoring and Assessment, v. 187, p. 4132, 2014. https://doi.org/10.1007/S10661-014-4132-8
https://doi.org/10.1007/S10661-014-4132-...
). Fish live exclusively in aquatic environments and some species are sensitive to changes in the habitat. Structural alterations, for example, may lead to changes in biological communities because fish use stream channels to feed and shelter (Montag et al., 2019MONTAG, L. F. A. et al. Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia, v. 826, 2019. https://doi.org/10.1007/s10750-018-3738-1
https://doi.org/10.1007/s10750-018-3738-...
). Aquatic insects are also sensitive to changes in the characteristics of streams like riparian vegetation, physical integrity and substrate types, both in their adult (and in some cases terrestrial) (e.g., Oliveira-Junior et al., 2019aOLIVEIRA-JUNIOR, J. M. B.; JUEN, L. Structuring of Dragonfly Communities (Insecta: Odonata) in Eastern Amazon: Effects of Environmental and Spatial Factors in Preserved and Altered Streams. Insects, v. 10, n. 10, p. 322, 2019a. https://doi.org/10.3390/insects10100322
https://doi.org/10.3390/insects10100322...
; Bastos et al., 2021BASTOS, R. C. et al. Morphological and phylogenetic factors structure the distribution of damselfly and dragonfly species (Odonata) along an environmental gradient in Amazonian streams. Ecological Indicators, v. 122, p. 107257, 2021. https://doi.org/10.1016/j.ecolind.2020.107257
https://doi.org/10.1016/j.ecolind.2020.1...
) or immature phase (generally strictly aquatic) (e.g., Mendes et al., 2020MENDES, T. P.; AMADO, L. L.; JUEN, L. Glutathione S-transferase activity in Mnesarete aenea (Odonata), Campylocia anceps (Ephemeroptera), and Cylindrostethus palmaris (Hemiptera) from forest and oil palm plantation areas in the Eastern Amazon. Ecological Indicators, v. 118, p. 106770, 2020. https://doi.org/10.1016/j.ecolind.2020.106770
https://doi.org/10.1016/j.ecolind.2020.1...
; Cruz et al., 2022CRUZ, G. M.; FARIA, A. P. J.; JUEN, L. Patterns and metacommunity structure of aquatic insects (Trichoptera) in Amazonian streams depend on the environmental conditions. Hydrobiologia, v. 849, n. 12, p. 2831-2843, 2022. https://doi.org/10.1007/s10750-022-04901-0
https://doi.org/10.1007/s10750-022-04901...
). But these groups can also respond to changes including pesticide contamination (Mendes et al., 2020MENDES, T. P.; AMADO, L. L.; JUEN, L. Glutathione S-transferase activity in Mnesarete aenea (Odonata), Campylocia anceps (Ephemeroptera), and Cylindrostethus palmaris (Hemiptera) from forest and oil palm plantation areas in the Eastern Amazon. Ecological Indicators, v. 118, p. 106770, 2020. https://doi.org/10.1016/j.ecolind.2020.106770
https://doi.org/10.1016/j.ecolind.2020.1...
; Sumudumali and Jayawardana, 2021SUMUDUMALI, R. G. I.; JAYAWARDANA, J. M. C. K. A Review of Biological Monitoring of Aquatic Ecosystems Approaches: with Special Reference to Macroinvertebrates and Pesticide Pollution. Environmental Management, v. 67, n. 2, p. 263-276, 2021. https://doi.org/10.1007/s00267-020-01423-0
https://doi.org/10.1007/s00267-020-01423...
), temperature increase and oxygen depletion (Martins et al., 2017MARTINS, R. T. et al. Effects of urbanization on stream benthic invertebrate communities in Central Amazon. Ecological Indicators, v. 73, p. 480-491, 2017. https://doi.org/10.1016/j.ecolind.2016.10.013
https://doi.org/10.1016/j.ecolind.2016.1...
).

The US-EPA protocol has been used in countries of all continents, except Antarctica, (Borja et al., 2008BORJA, A. et al. Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. Marine Pollution Bulletin, v. 56, n. 9, p. 1519-1537, 2008. https://doi.org/10.1016/j.marpolbul.2008.07.005
https://doi.org/10.1016/j.marpolbul.2008...
; Karr and Chu, 2000KARR, J. R.; CHU, E. W. Introduction: Sustaining living rivers. In: JUNGWIRTH, M.; MUHAR, S.; SCHMUTZ, S. (eds.). Assessing the Ecological Integrity of Running Waters. Dordrecht: Springer, 2000. https://doi.org/10.1007/978-94-011-4164-2_1
https://doi.org/10.1007/978-94-011-4164-...
; Xu et al., 2013XU, M. et al. Effects of pollution on macroinvertebrates and water quality bio-assessment. Hydrobiologia, v. 729, n. 1, p. 247-259, 2013. https://doi.org/10.1007/s10750-013-1504-y
https://doi.org/10.1007/s10750-013-1504-...
), and in Brazil it has been used in Cerrado (e.g., Silva et al., 2018SILVA, D. R. O. et al. Assessing the extent and relative risk of aquatic stressors on stream macroinvertebrate assemblages in the neotropical savanna. Science of the Total Environment, v. 633, p. 179-188, 2018. https://doi.org/10.1016/j.scitotenv.2018.03.127
https://doi.org/10.1016/j.scitotenv.2018...
; Alvarenga et al., 2021ALVARENGA, L. R. P. et al. Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna. Neotropical Ichthyology, v. 19, 2021. https://doi.org/10.1590/1982-0224-2021-0035
https://doi.org/10.1590/1982-0224-2021-0...
; Silva et al., 2022SILVA, L. F. R. et al. Ecological thresholds of Odonata larvae to anthropogenic disturbances in neotropical savanna headwater streams. Hydrobiologia, p. 1-14, 2022. https://doi.org/10.1007/s10750-022-05097-z
https://doi.org/10.1007/s10750-022-05097...
), and Amazon biomes (e.g., Juen et al., 2016JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al. Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
https://doi.org/10.1002/rra.3050...
; Faria et al., 2017FARIA, A. P. J.; LIGEIRO, R.; CALLISTO, M.; JUEN, L. Response of aquatic insect assemblages to the activities of traditional populations in eastern Amazonia. Hydrobiologia, v. 802, n. 1, p. 39-51, 2017. https://doi.org/10.1007/s10750-017-3238-8
https://doi.org/10.1007/s10750-017-3238-...
; Leal et al., 2017LEAL, C. G. et al. Is environmental legislation conserving tropical stream faunas? A large-scale assessment of local, riparian and catchment-scale influences on Amazonian fish. Journal of Applied Ecology, v. 55, n. 3, p. 1312-1326, 2017. https://doi.org/10.1111/1365-2664.13028
https://doi.org/10.1111/1365-2664.13028...
). In the Amazon Rainforest, though, until the year 2000 there were no relevant programs for monitoring streams. This contrasts with the importance of this biome, which is the largest tropical forest with the highest biodiversity of the world. Only in 2001, a project named Igarapés was created in Brazil with research teams that started researching small lotic environments. Later, in 2008, a group of scientists from different institutions and nationalities created the Sustainable Amazon Network (RAS - Rede Amazônia Sustentável, in Portuguese). These researchers aimed to assess the sustainability of land-use systems in two regions of the Brazilian Amazon, and for this, they applied the US-EPA protocol to 100 streams in these areas (Gardner et al., 2013GARDNER, T. A.; FERREIRA, J.; BARLOW, J.; LEES, A. C.; PARRY, L.; VIEIRA, I. C. G. et al. A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philosophical Transactions of the Royal Society B: Biological Sciences, v. 368, n. 1619, p. 20120166-20120166, 2013. https://doi.org/10.1098/rstb.2012.0166
https://doi.org/10.1098/rstb.2012.0166...
). Since then, this protocol has been widely used in scientific research to evaluate the ecological conditions of streams that have been altered by different types of land use in the Amazon (Leitão et al., 2017LEITÃO, R. P. et al. Disentangling the pathways of land use impacts on the functional structure of fish assemblages in Amazon streams. Ecography, v. 41, n. 1, p. 219-232, 2017. https://doi.org/10.1111/ecog.02845
https://doi.org/10.1111/ecog.02845...
; Chen et al., 2017CHEN, K.; HUGHES, R. M.; BRITO, J. G.; LEAL, C. G.; LEITÃO, R. P.; de OLIVEIRA-JUNIOR, J. M. B. et al. A multi-assemblage, multi-metric biological condition index for eastern Amazonia streams. Ecological Indicators, v. 78, p. 48-61, 2017. https://doi.org/10.1016/j.ecolind.2017.03.003
https://doi.org/10.1016/j.ecolind.2017.0...
; Pereira et al., 2019PEREIRA, D. F. G. et al. Environmental changes promote larger species of Odonata (Insecta) in Amazonian streams. Ecological Indicators, v. 98, 2019. https://doi.org/10.1016/j.ecolind.2018.09.020
https://doi.org/10.1016/j.ecolind.2018.0...
).

The US-EPA protocol has been used as a predictor of changes in taxonomic (Oliveira-Junior et al., 2015OLIVEIRA-JUNIOR, J. M. B. et al. Neotropical dragonflies (Insecta: Odonata) as indicators of ecological condition of small streams in the eastern Amazon. Austral Ecology, v. 40, n. 6, p. 733-744, 2015. https://doi.org/10.1111/aec.12242
https://doi.org/10.1111/aec.12242...
), functional (Pereira et al., 2019PEREIRA, D. F. G. et al. Environmental changes promote larger species of Odonata (Insecta) in Amazonian streams. Ecological Indicators, v. 98, 2019. https://doi.org/10.1016/j.ecolind.2018.09.020
https://doi.org/10.1016/j.ecolind.2018.0...
; Luiza-Andrade et al., 2017LUIZA-ANDRADE, A.; MONTAG, L. F. de A.; JUEN, L. Functional diversity in studies of aquatic macroinvertebrates community. Scientometrics, v. 111, n. 3, p. 1643-1656, 2017. https://doi.org/10.1007/s11192-017-2315-0
https://doi.org/10.1007/s11192-017-2315-...
), phylogenetic (Bastos et al., 2021BASTOS, R. C. et al. Morphological and phylogenetic factors structure the distribution of damselfly and dragonfly species (Odonata) along an environmental gradient in Amazonian streams. Ecological Indicators, v. 122, p. 107257, 2021. https://doi.org/10.1016/j.ecolind.2020.107257
https://doi.org/10.1016/j.ecolind.2020.1...
), morphological (Mendes et al., 2019aMENDES, T. P. et al. Morphological diversity of Odonata larvae (Insecta) and abiotic variables in oil palm plantation areas in the Eastern Amazon. Hydrobiologia, v. 847, n. 1, p. 161-175, 2019a. https://doi.org/10.1007/s10750-019-04079-y
https://doi.org/10.1007/s10750-019-04079...
) and behavioral (Resende et al., 2021RESENDE, B. O. et al. Impact of environmental changes on the behavioral diversity of the Odonata (Insecta) in the Amazon. Scientific Reports, v. 11, n. 1, 2021. https://doi.org/10.1038/s41598-021-88999-7
https://doi.org/10.1038/s41598-021-88999...
) diversity of several aquatic organisms. For this reason, this protocol has been useful to quantify natural variation in Amazonian streams (Benone et al., 2017BENONE, N. L. et al. Regional controls on physical habitat structure of Amazon streams. River Research and Applications, v. 33, n. 5, p. 766-776, 2017. https://doi.org/10.1002/rra.3137
https://doi.org/10.1002/rra.3137...
; Shimano et al., 2021SHIMANO, Y. et al. Environmental variation in Amazonian interfluves and its effects on local mayfly assemblages. Hydrobiologia, v. 848, n. 17, p. 4075-4092, 2021. https://doi.org/10.1007/s10750-021-04626-6
https://doi.org/10.1007/s10750-021-04626...
), as well as for monitoring environmental quality of streams in altered regions. The already mentioned land-use and land-cover changes are some of the multiple stressors that impact Amazonian streams (Albert et al., 2021ALBERT, J. S. et al. Scientists’ warning to humanity on the freshwater biodiversity crisis. Ambio, v. 50, n. 1, p. 85-94, 2021. https://doi.org/10.1007/s13280-020-01318-8
https://doi.org/10.1007/s13280-020-01318...
; He et al., 2017HE, F.; ZARFL, C.; BREMERICH, V.; HENSHAW, A.; DARWALL, W.; TOCKNER, K. et al. Disappearing giants: a review of threats to freshwater megafauna. Wiley Interdisciplinary Reviews: Water, v. 4, n. 3, p. e1208, 2017. https://doi.org/10.1002/wat2.1208
https://doi.org/10.1002/wat2.1208...
) and cause changes in habitat structure and loss of biodiversity (Juen et al., 2016JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al. Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
https://doi.org/10.1002/rra.3050...
; Leal et al., 2016LEAL, C. G.; POMPEU, P. S.; GARDNER, T. A.; LEITÃO, R. P.; HUGHES, R. M.; KAUFMANN, P. R. et al. Multi-scale assessment of human-induced changes to Amazonian instream habitats. Landscape Ecology, v. 31, p. 1725-1745, 2016. https://doi.org/10.1007/s10980-016-0358-x
https://doi.org/10.1007/s10980-016-0358-...
). As such, evaluating whether and how environmental changes impact Amazonian streams is crucial for ecosystem conservation (Leal et al., 2016LEAL, C. G.; POMPEU, P. S.; GARDNER, T. A.; LEITÃO, R. P.; HUGHES, R. M.; KAUFMANN, P. R. et al. Multi-scale assessment of human-induced changes to Amazonian instream habitats. Landscape Ecology, v. 31, p. 1725-1745, 2016. https://doi.org/10.1007/s10980-016-0358-x
https://doi.org/10.1007/s10980-016-0358-...
; Martins et al., 2018MARTINS, I. et al. Regionalisation is key to establishing reference conditions for neotropical savanna streams. Marine and Freshwater Research, v. 69, p. 82-94, 2018. https://doi.org/10.1071/mf16381
https://doi.org/10.1071/mf16381...
). Tropical countries still need great improvements in freshwater systems’ research (Brasil et al., 2020BRASIL, L. S.; de LIMA, E. L.; SPIGOLONI, Z. A.; RIBEIRO-BRASIL, D. R. G.; JUEN, L. The habitat integrity index and aquatic insect communities in tropical streams: A meta-analysis. Ecological Indicators, v. 116, p. 106495, 2020. https://doi.org/10.1016/j.ecolind.2020.106495
https://doi.org/10.1016/j.ecolind.2020.1...
), so it is important to identify the main knowledge gaps and indicate directions for future studies to be efficient (Diniz-Filho et al., 2010DINIZ- FILHO, J. A. F.; DE MARCO JR, P.; HAWKINS, B. A. Defying the curse of ignorance: perspectives in insect macroecology and conservation biogeography. Insect Conservation and Diversity, v. 3, 2010. https://dx.doi.org/10.1111/j.1752-4598.2010.0009
https://dx.doi.org/10.1111/j.1752-4598.2...
).

Considering this scenario, we aimed to answer several questions related to the use of the US-EPA protocol in Amazonian streams: 1) In how many Amazonian streams has the US-EPA protocol been used?; 2) Is the use of this protocol well distributed across the Amazonian Basin?; 3) Which types of land use have been evaluated using the protocol?; 4) Which components of the aquatic biota have been used together with the protocol to assess environmental quality of Amazonian streams?; and, 5) Which metrics of this protocol were the most important to explain aquatic biota distribution?

2. MATERIAL AND METHODS

We used the Web of Science (WoS) database to search for scientific papers related to our objectives. This platform contains about 21,100 studies from different areas of knowledge and a wide database from the global scientific literature. It also has indexed journals of reliable quality and a rigorous selection process to include studies in its database (Clarivate, 2021CLARIVATE. Web of Science. 2021. Available at: Available at: https://clarivate-com.translate.goog/webofsciencegroup/solutions/webofscience/?_x_tr_sl=en&_x_tr_tl=pt&_x_tr_hl=pt-BR&_x_tr_pto=op,sc Access: Mar. 21, 2021.
https://clarivate-com.translate.goog/web...
). We also searched for scientific papers on Google Scholar (GS), which is a web search engine that enables simple access to academic literature. It contains relevant studies from all over the world, published as articles, theses, books, abstracts, among other resources (Google Scholar, 2021GOOGLE SCHOLAR. Webpage. 2021. Available at: Available at: https://scholar.google.com.br/?hl=pt Access: Jun. 17, 2021.
https://scholar.google.com.br/?hl=pt...
).

We searched the studies at WoS using the words and the Boolean operators: (“Physical Habitat” OR “Environmental Protection Agency” OR EPA) AND (Amazon* OR Brazil*) AND (stream* OR river*). During the selection process, we noticed that most scientific papers cited the studies of Kaufmann et al. (1999)KAUFMANN, P. R.; LEVINE, P.; ROBISON, E. G.; SEELIGER, C.; PECK, D. V. Quantifying Physical Habitat in Wadeable Streams. EPA/620/R-99/003. Washington, D.C., 1999. and Peck et al. (2006)PECK, D. V. et al. Environmental monitoring and assessment program - surface waters western pilot study: field operations manual for wadeable streams. EPA 600/R-06/003. Washington, DC: USEPA, 2006.. For this reason, we searched for articles that cited these specific studies considering that these works were those that described the calculations of variables and the method of measurement in the field, respectively and fitted our searching terms (Amazon* OR Brazil* AND Stream* OR river*) at Google Scholar.

We searched the articles at WoS and GS from April 5th to July 20th, 2021, and selected articles published between 2013 (year when the US-EPA protocol was used in Amazon by Gardner et al., 2013GARDNER, T. A.; FERREIRA, J.; BARLOW, J.; LEES, A. C.; PARRY, L.; VIEIRA, I. C. G. et al. A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philosophical Transactions of the Royal Society B: Biological Sciences, v. 368, n. 1619, p. 20120166-20120166, 2013. https://doi.org/10.1098/rstb.2012.0166
https://doi.org/10.1098/rstb.2012.0166...
) and 2020 because it corresponded to the last year of our searching process. We only considered documents that effectively used the US-EPA protocol in Amazonian streams. We selected only studies published as “article” type, because these publications are peer reviewed by the editorial group of a scientific journal, and hence, they are not considered gray literature (such as monographies, dissertations, and theses). Finally, we accepted articles published in any language (e.g., English, Portuguese, and Spanish).

We organized the selected studies in a spreadsheet editor software to produce graphs and tables. We inserted the studies as rows and the basic information, such as title, year of publication, journal and first author, as columns. After reading the articles, we included other data as columns in the spreadsheet. These included: number of streams in each study, geographic coordinates of each stream where the US-EPA was applied, main land-use type in the study, the protocol metrics most affected by changes in land use, and the taxonomic groups used together with the US-EPA protocol. Finally, to answer our questions, we quantified the data obtained from the selected studies and used graphs and tables to represent the results. We also produced a map to spatially represent the geographic distribution of the Amazonian streams where the US-EPA protocol was applied. For this, we used the software Quantum GIS.

3. RESULTS AND DISCUSSION

3.1. General description of the scientometrics

Initially, we obtained 243 articles from the WoS and GS database, but after the selection process, 36 remained, as they were the only studies in accordance with our objectives. The first study that described RAS activities was published in 2013 (Gardner et al., 2013GARDNER, T. A.; FERREIRA, J.; BARLOW, J.; LEES, A. C.; PARRY, L.; VIEIRA, I. C. G. et al. A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philosophical Transactions of the Royal Society B: Biological Sciences, v. 368, n. 1619, p. 20120166-20120166, 2013. https://doi.org/10.1098/rstb.2012.0166
https://doi.org/10.1098/rstb.2012.0166...
), but the first studies that used the US-EPA protocol in Amazonian streams were only published in 2015 (Oliveira-Junior et al., 2015OLIVEIRA-JUNIOR, J. M. B. et al. Neotropical dragonflies (Insecta: Odonata) as indicators of ecological condition of small streams in the eastern Amazon. Austral Ecology, v. 40, n. 6, p. 733-744, 2015. https://doi.org/10.1111/aec.12242
https://doi.org/10.1111/aec.12242...
) (Figure 1).

Figure 1.
Number of scientific productions that used the US-EPA protocol for environmental monitoring Amazonian streams, and that were indexed to WoS and GS between 2015 and 2020.

3.2. In how many Amazonian streams has the US-EPA protocol been used?

In our study, we found that the US-EPA protocol was used in 889 Amazonian streams. However, many of the filtered papers share the same databases, so the actual number of sampled streams identified in our search is 380; but still, this number may be overestimated. When we plotted the coordinates, we found that some points were less than 100 meters apart, which may be related to the accuracy of the coordinates provided by papers that share the same data. In contrast, according to public data from US-EPA, in 2014 this protocol had already been applied to 91,975 North American streams to assess their environmental quality (USEPA, 2021USEPA. Data from the National Aquatic Resource Surveys. 2021. Available at: Available at: https://www.epa.gov/national-aquatic-resource-surveys/data-national-aquatic-resource-surveys . Access: Dec. 20, 2021.
https://www.epa.gov/national-aquatic-res...
). All these numbers show that the coverage of Amazonian streams where this protocol is still small compared to the US. But considering the period in which it began to be applied and the logistical difficulties in Amazon, especially in relation to access, the US-EPA protocol has been applied successfully.

It is important that Brazilian federal and state governments, environmental and funding agencies, and private companies use this tool for monitoring environmental quality of Amazonian streams, as well as to achieve a representative evaluation of these habitats. These institutions can create specific agencies to evaluate aquatic systems, or fund studies, environmental companies, Non-Governmental Organizations (NGOs), universities and research institutions to widen the use of the US-EPA protocol in Amazonian streams. Only with these incentives, we will be able to obtain an expansion of environmental monitoring and have a good projection of the environmental quality of Amazonian streams. Scenarios of fire, deforestation, and use of natural areas for anthropic purposes make this agenda even more urgent.

3.3. Is the use of the US-EPA protocol well distributed across the Amazonian Basin?

We found that the use of the US-EPA protocol was restricted to five of the nine Amazon endemism areas: Belém (231), Xingú (75), Tapajós (69), Guiana (10) and Imeri (1) (Figure 2). Most of the streams were in Pará state, and Acará Basin (in Belém endemism area) had the highest concentration of streams evaluated by scientific studies in comparison to other basins.

We do not find application records of the US-EPA protocol to streams in the Northern and Western Amazon or in the states of Roraima and Acre. These areas differ greatly in limnological characteristics, as they present upland forests (Pires and Prance, 1985PIRES, J. M.; PRANCE, G. T. The vegetation types of the Brazilian Amazon. In: PRANCE, G. T.; LOVEJOY, T. E. (eds.). Key Environments: Amazonia. Oxford: Pergamon Press, 1985. p. 109-145.; Pazin et al., 2006PAZIN, V. F. V. et al. Fish assemblages in temporary ponds adjacent to “terra-firme” streams in Central Amazonia. Freshwater Biology, v. 51, n. 6, p. 1025-1037, 2006. https://doi.org/10.1111/j.1365-2427.2006.01
https://doi.org/10.1111/j.1365-2427.2006...
) and floodplains of 8.4 x105 km2. During the rainy period, plains become flooded, and lakes get connected to each other and to the mainstream, producing a diversity of trophic environments (Hess et al., 2015HESS, L. L. et al. Wetlands of the Lowland Amazon Basin: Extent, Vegetative Cover, and Dual-season Inundated Area as Mapped with JERS-1 Synthetic Aperture Radar. Wetlands, v. 35, n. 4, p. 745-756, 2015. https://doi.org/10.1007/s13157-015-0666-y
https://doi.org/10.1007/s13157-015-0666-...
). These regions also differ in climate, soil, and hydrographic characteristics due to the Amazon evolutionary history. Thus, each region has specific physicochemical characteristics, which create an important environmental heterogeneity in the Amazon biome (Shimano et al., 2021SHIMANO, Y. et al. Environmental variation in Amazonian interfluves and its effects on local mayfly assemblages. Hydrobiologia, v. 848, n. 17, p. 4075-4092, 2021. https://doi.org/10.1007/s10750-021-04626-6
https://doi.org/10.1007/s10750-021-04626...
).

Figure 2.
Spatial distribution of the streams with EPA-protocol applications in Amazonian streams between 2015 and 2020.

3.4. Which types of land use have been evaluated using the protocol?

The analyzed streams were surrounded by different types of land use and occupation, which included forest (37.23%), agriculture (27.66%), logging (15.96%), livestock (12.77%) and urbanization (6.38%). The data obtained in forest streams provide a good base to describe the expected characteristics of morphology, structure, and water quality for Amazonian streams in the sampled area. Streams in preserved regions present considerable natural variation between plain areas with low-flow water bodies and upland areas, with fast-flowing waters (Benone et al., 2017BENONE, N. L. et al. Regional controls on physical habitat structure of Amazon streams. River Research and Applications, v. 33, n. 5, p. 766-776, 2017. https://doi.org/10.1002/rra.3137
https://doi.org/10.1002/rra.3137...
; Shimano et al., 2021SHIMANO, Y. et al. Environmental variation in Amazonian interfluves and its effects on local mayfly assemblages. Hydrobiologia, v. 848, n. 17, p. 4075-4092, 2021. https://doi.org/10.1007/s10750-021-04626-6
https://doi.org/10.1007/s10750-021-04626...
). Such environmental variation contributes to the diversity of fish (Benone et al., 2017BENONE, N. L. et al. Regional controls on physical habitat structure of Amazon streams. River Research and Applications, v. 33, n. 5, p. 766-776, 2017. https://doi.org/10.1002/rra.3137
https://doi.org/10.1002/rra.3137...
) and aquatic insects of the Order Ephemeroptera (Shimano et al., 2021SHIMANO, Y. et al. Environmental variation in Amazonian interfluves and its effects on local mayfly assemblages. Hydrobiologia, v. 848, n. 17, p. 4075-4092, 2021. https://doi.org/10.1007/s10750-021-04626-6
https://doi.org/10.1007/s10750-021-04626...
) in Amazon, in an evolutionary history context.

In 2020, the MapBiomas platform registered that 15% of Amazonian areas had been transformed into other types of land use, among which livestock and agriculture were the most common activities (Souza et al., 2020SOUZA, C. M. et al. Reconstructing Three Decades of Land Use and Land Cover Changes in Brazilian Biomes with Landsat Archive and Earth Engine. Remote Sensing, v. 12, n. 17, 2020. https://doi.org/10.3390/rs12172735
https://doi.org/10.3390/rs12172735...
). Evidence shows that the expansion of soybean crops and beef production in Brazil cause the decrease of rainfall in these areas (Leite-Filho et al. 2021LEITE-FILHO, A. T. et al. Deforestation reduces rainfall and agricultural revenues in the Brazilian Amazon. Nature Communications, v. 12, n. 1, 2021. https://doi.org/10.1038/s41467-021-22840-7
https://doi.org/10.1038/s41467-021-22840...
). As such, measuring and monitoring the effect of anthropic disturbances in forest streams, especially those in different Amazonian regions, can be challenging, but they are crucial to protect the remaining natural vegetation and to maintain rainfall patterns.

3.5. Which components of the aquatic biota have been used together with the protocol to assess environmental quality of Amazonian streams?

We found that most studies (n=20) used aquatic insects from the orders Ephemeroptera, Plecoptera, Trichoptera, Hemiptera and Odonata to complement the US-EPA protocol, followed by studies that used fish (n=10), and a minority of studies that used aquatic insects and fish together (n=4) (Figure 3). Many aquatic insect groups are sensitive to environmental changes or are bioindicators from some specific impact and, in addition, occupy different microhabitats on stream ecosystems, which allows them to be used to assess impacts on different aspects of the physical structure of Amazonian streams. For example, Odonata (adults) are associated to riparian vegetation, while Heteroptera and Trichoptera (larvae) are associated with surface and substrates, respectively (Juen et al., 2016JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al. Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
https://doi.org/10.1002/rra.3050...
; Cunha et al., 2022CUNHA, E. J. et al. Urban development and industrialization impacts on semi aquatic bugs diversity: A case study in eastern Amazonian streams. Water Biology and Security, v. 1, n. 4, p. 100061, 2022. https://doi.org/10.1016/j.watbs.2022.100061
https://doi.org/10.1016/j.watbs.2022.100...
; Cruz et al., 2022CRUZ, G. M.; FARIA, A. P. J.; JUEN, L. Patterns and metacommunity structure of aquatic insects (Trichoptera) in Amazonian streams depend on the environmental conditions. Hydrobiologia, v. 849, n. 12, p. 2831-2843, 2022. https://doi.org/10.1007/s10750-022-04901-0
https://doi.org/10.1007/s10750-022-04901...
), so they are widely used for monitoring environmental impacts. This explains why we found a high number of articles using these organisms (Oliveira-Junior and Juen, 2019aOLIVEIRA-JUNIOR, J. M. B.; JUEN, L. Structuring of Dragonfly Communities (Insecta: Odonata) in Eastern Amazon: Effects of Environmental and Spatial Factors in Preserved and Altered Streams. Insects, v. 10, n. 10, p. 322, 2019a. https://doi.org/10.3390/insects10100322
https://doi.org/10.3390/insects10100322...
; Mendes et al., 2019bMENDES, T. P.; BENONE, N. L.; JUEN, L. To what extent can oil palm plantations in the Amazon support assemblages of Odonata larvae? Insect Conservation and Diversity, 2019b. https://doi.org/10.1111/icad.12357
https://doi.org/10.1111/icad.12357...
; Brasil et al., 2020BRASIL, L. S.; de LIMA, E. L.; SPIGOLONI, Z. A.; RIBEIRO-BRASIL, D. R. G.; JUEN, L. The habitat integrity index and aquatic insect communities in tropical streams: A meta-analysis. Ecological Indicators, v. 116, p. 106495, 2020. https://doi.org/10.1016/j.ecolind.2020.106495
https://doi.org/10.1016/j.ecolind.2020.1...
). The low number of studies using fish and aquatic insects together is likely due to the long time necessary to sort and identify species in the laboratory, in addition to difficulties of finding specialists in the taxonomy of these groups. For these reasons, it is more usual to find studies that work with these groups separately. Recent studies have used the environmental variables analyzed in the US-protocol together with the diversity and distribution of aquatic macrophytes (Fares et al., 2020FARES, A. L. B. et al. Environmental factors affect macrophyte diversity on Amazonian aquatic ecosystems inserted in an anthropogenic landscape. Ecological Indicators, v. 113, p. 106231, 2020. https://doi.org/10.1016/j.ecolind.2020.106231
https://doi.org/10.1016/j.ecolind.2020.1...
; Carmo et al., 2023CARMO, R. S. et al. Does the structure of riparian vegetation affect the diversity of macrophytes in eastern Amazonian streams? Biologia, v. 78, n. 1, p. 79-89, 2023. https://doi.org/10.1007/s11756-022-01181-w
https://doi.org/10.1007/s11756-022-01181...
).

Figure 3.
Quantity of studies and biological groups that were used together with the US-EPA protocol for monitoring Amazonian streams.

3.6. Which metrics of the protocol were the most important to explain aquatic biota distribution?

Among the 239 metrics analyzed in the US-EPA protocol, five repeatedly presented significant statistical relationships with fish and aquatic insect communities in the studies. These were: canopy cover or density (1), presence of wood in the channel (2), anthropic impacts in the riparian zone or in the landscape (3), width and depth of the channel (4), and water temperature (5). We also observed other variables in the studies, such as type of substrate, which included sand, leaves and roots in the stream channel, and physicochemical characteristics of the water such as pH, oxidation/reduction potential (ORP) and dissolved oxygen in the water (Figure 4 A, B and C).

Such relationships between the metrics of the protocol with fish and aquatic insects have some specificities. For both, the most important metric found repeatedly in the studies was the canopy cover. Low percentages of canopy cover reflect deforestation surrounding the stream, which is composed of forests in the case of Amazon. For fish, canopy cover can positively affect the species richness, as observed by Montag et al. (2019)MONTAG, L. F. A. et al. Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia, v. 826, 2019. https://doi.org/10.1007/s10750-018-3738-1
https://doi.org/10.1007/s10750-018-3738-...
in the surroundings of Conservation Units. However, canopy cover loss negatively affects the composition of fish communities (Prudente et al., 2016PRUDENTE, B. S. et al. Effects of reduced-impact logging on physical habitat and fish assemblages in streams of Eastern Amazonia. Freshwater Biology, v. 62, n. 2, p. 303-316, 2016. https://doi.org/10.1111/fwb.12868 .
https://doi.org/10.1111/fwb.12868...
). Considering aquatic insects, especially Odonata adults, both loss of canopy cover and anthropic impacts in the riparian zone increase the entrance of sunlight into forest streams (Juen et al., 2016JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al. Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
https://doi.org/10.1002/rra.3050...
). The species richness of Zygoptera and Anisoptera, for example, is restricted to sunlight availability, which determines their environmental gradient of distribution (Calvão et al., 2016CALVÃO, L. B.; NOGUEIRA, D. S.; de ASSIS MONTAG, L. F.; LOPES, M. A.; JUEN, L. Are Odonata communities impacted by conventional or reduced impact logging? Forest Ecology and Management, v. 382, p. 143-150, 2016. https://doi.org/10.1016/j.foreco.2016.10.013
https://doi.org/10.1016/j.foreco.2016.10...
; Oliveira-Junior and Juen, 2019bOLIVEIRA-JUNIOR, J. M. B.; JUEN, L. The Zygoptera/Anisoptera ratio (Insecta: Odonata): a new tool for habitat alterations assessment in Amazonian streams. Neotropical entomology, v. 48, n. 4, p. 552-560, 2019b. https://doi.org/10.1007/s13744-019-00672-x
https://doi.org/10.1007/s13744-019-00672...
). Anisoptera species occur mainly in deforested areas, where Zygoptera corresponds to the minority of species. As such, these groups are commonly used as bioindicators of environmental quality in Amazonian streams (Oliveira-Junior and Juen, 2019bOLIVEIRA-JUNIOR, J. M. B.; JUEN, L. The Zygoptera/Anisoptera ratio (Insecta: Odonata): a new tool for habitat alterations assessment in Amazonian streams. Neotropical entomology, v. 48, n. 4, p. 552-560, 2019b. https://doi.org/10.1007/s13744-019-00672-x
https://doi.org/10.1007/s13744-019-00672...
). This pattern is so consistent that the Brazilian Environmental Agency (Chico Mendes Institute for Biodiversity Conservation, ICMBio) uses it as a protocol for monitoring environmental conditions of streams within Amazonian Conservation Units (Brasil et al., 2020BRASIL, L. S.; de LIMA, E. L.; SPIGOLONI, Z. A.; RIBEIRO-BRASIL, D. R. G.; JUEN, L. The habitat integrity index and aquatic insect communities in tropical streams: A meta-analysis. Ecological Indicators, v. 116, p. 106495, 2020. https://doi.org/10.1016/j.ecolind.2020.106495
https://doi.org/10.1016/j.ecolind.2020.1...
).

Figure 4.
Most important metrics of the US-EPA protocol for the aquatic biota, represented by (A) fish and/or aquatic insects, (B) fish, and (C) aquatic insects. The colors represent the block of variables.

Stream morphology variables, like width and depth, are also important for fish and aquatic insect communities, but anthropic changes in the landscape can change these characteristics. Consequently, local populations of specialist species can be made extinct or replaced by generalist species. This may not affect species richness but can change the composition of fish in these habitats (Prudente et al., 2016PRUDENTE, B. S. et al. Effects of reduced-impact logging on physical habitat and fish assemblages in streams of Eastern Amazonia. Freshwater Biology, v. 62, n. 2, p. 303-316, 2016. https://doi.org/10.1111/fwb.12868 .
https://doi.org/10.1111/fwb.12868...
; Ilha et al., 2019ILHA, P.; ROSSO, S.; SCHIESARI, L. Effects of deforestation on headwater stream fish assemblages in the Upper Xingu River Basin, Southeastern Amazonia. Neotropical Ichthyology, v. 17, n. 1, 2019. https://doi.org/10.1590/1982-0224-20180099
https://doi.org/10.1590/1982-0224-201800...
). Differently from this pattern, Leão et al. (2020)LEÃO, H.; SIQUEIRA, T.; TORRES, N. R.; MONTAG, L. F. de A. Ecological uniqueness of fish communities from streams in modified landscapes of Eastern Amazonia. Ecological Indicators, v. 111, p. 106039, 2020. https://doi.org/10.1016/j.ecolind.2019.106039
https://doi.org/10.1016/j.ecolind.2019.1...
found a higher diversity of fish in streams of pasture areas than in those of forest areas. However, their results were associated with different levels of environmental heterogeneity, and riparian vegetation around the sampled streams.

In addition to the incidence of light, the removal of riparian vegetation also causes the increase of water temperature in the stream, and the decrease of available oxygen for immature insect communities, such as Ephemeroptera, Plecoptera and Trichoptera (Juen et al., 2016JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al. Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
https://doi.org/10.1002/rra.3050...
; Shimano and Juen, 2016SHIMANO, Y.; JUEN, L. How oil palm cultivation is affecting mayfly assemblages in Amazon streams. International Journal of Limnology, v. 52, p. 35-45, 2016. https://doi.org/10.1051/limn/2016004
https://doi.org/10.1051/limn/2016004...
; Mendes et al., 2019bMENDES, T. P.; BENONE, N. L.; JUEN, L. To what extent can oil palm plantations in the Amazon support assemblages of Odonata larvae? Insect Conservation and Diversity, 2019b. https://doi.org/10.1111/icad.12357
https://doi.org/10.1111/icad.12357...
). As such, we can expect that alterations in the riparian zone reduce species richness of sensitive aquatic macroinvertebrates. Consequently, generalist species richness increases, whereas populations of specialist species, which depend on high environmental quality, decrease or are extinct (Martins et al., 2017MARTINS, R. T. et al. Effects of urbanization on stream benthic invertebrate communities in Central Amazon. Ecological Indicators, v. 73, p. 480-491, 2017. https://doi.org/10.1016/j.ecolind.2016.10.013
https://doi.org/10.1016/j.ecolind.2016.1...
). This makes it clear that the riparian vegetation is an important aspect of the stream's physical habitat.

Additionally, the presence of wood and other organic substrates in the stream channel can be important for fish and insect communities by providing refuge, food resources and habitat heterogeneity. Fish of the genus Characidium, for example, use leaves, stems, and branches to hide and capture prey (Montag et al., 2019MONTAG, L. F. A. et al. Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia, v. 826, 2019. https://doi.org/10.1007/s10750-018-3738-1
https://doi.org/10.1007/s10750-018-3738-...
). Insects from the Trichoptera order, like Phylloicus and Triplectides, depend on these substrates for refuge construction and feeding and are excluded from the streams under high levels of deforestation (Lima et al., 2022LIMA, M. et al. Land use changes disrupt streams and affect the functional feeding groups of aquatic insects in the Amazon. Journal of Insect Conservation, v. 26, n. 2, p. 137-148, 2022. https://doi.org/10.1007/s10841-022-00375-6
https://doi.org/10.1007/s10841-022-00375...
). Furthermore, the reduction in the availability of allochthonous organic resources affects not only the organisms that directly benefit from them, but also the entire food chain in stream ecosystems (Vannote et al., 1980VANNOTE, R. L.; MINSHALL, G. W.; CUMMINS, K. W.; SEDELL, J. R.; CUSHING, C. E. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, v. 37, n. 1, p. 130-137, 1980. https://doi.org/10.1139/f80-017
https://doi.org/10.1139/f80-017...
; Teresa et al., 2015TERESA, F. B.; CASATTI, L.; CIANCIARUSO, M. V. Functional differentiation between fish assemblages from forested and deforested streams. Neotropical Ichthyology, v. 13, n. 2, p. 361-370, 2015. https://doi.org/10.1590/1982-0224-20130229
https://doi.org/10.1590/1982-0224-201302...
; Lima et al., 2022LIMA, M. et al. Land use changes disrupt streams and affect the functional feeding groups of aquatic insects in the Amazon. Journal of Insect Conservation, v. 26, n. 2, p. 137-148, 2022. https://doi.org/10.1007/s10841-022-00375-6
https://doi.org/10.1007/s10841-022-00375...
).

4. CONCLUSIONS

Our study shows that the US-EPA protocol is an important tool for characterizing streams, monitoring environmental impacts, and predicting the aquatic biota. However, this protocol is not homogeneously used across the Amazon Basin. The Western, Northern and Southern Amazon Basin still need a greater sampling effort using this protocol so we can obtain a complete environmental characterization of Amazonian streams. The use of the US-EPA protocol for monitoring the environmental quality of streams should be expanded to enable the evaluation of different types of land-use impacts. Also, whenever possible, it should be used together with a component of the aquatic biota, especially fish and aquatic insects, which have proven to be efficient tools to detect impacts and for monitoring the aquatic environment.

In Brazil, scientific research still lacks financial resources and environmental changes in the Amazon Rainforest are accelerated. As such, we suggest the development of a simplified version of the US-EPA protocol, based on the most important metrics for the aquatic biota, to be used in Amazonian streams. This would enable the evaluation of a greater number of Amazonian streams, even those of difficult access. It would also be an important initiative for research teams with low funding, which cannot gather enough fieldworkers to apply the complete protocol.

5. ACKNOWLEDGMENTS

We are also grateful to Brazilian National Council for Scientific and Technological Development (CNPq) for granting a research productivity fellowship to LSB (process 305929/2022-4) and to JMBOJ (process 307808/2022-0).

6. REFERENCES

  • ALBERT, J. S. et al Scientists’ warning to humanity on the freshwater biodiversity crisis. Ambio, v. 50, n. 1, p. 85-94, 2021. https://doi.org/10.1007/s13280-020-01318-8
    » https://doi.org/10.1007/s13280-020-01318-8
  • ALLAN, J. D. Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology, Evolution, and Systematics, v. 35, p. 257-284, 2004. http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122 .
    » http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122
  • ALVARENGA, L. R. P. et al Land-use changes affect the functional structure of stream fish assemblages in the Brazilian Savanna. Neotropical Ichthyology, v. 19, 2021. https://doi.org/10.1590/1982-0224-2021-0035
    » https://doi.org/10.1590/1982-0224-2021-0035
  • BARONA, E. et al The role of pasture and soybean in deforestation of the Brazilian Amazon. Environmental Research Letters, v. 5, n. 2, p. 024002, 2010. http://dx.doi.org/10.1088/1748-9326/5/2/024002
    » http://dx.doi.org/10.1088/1748-9326/5/2/024002
  • BASTOS, R. C. et al Morphological and phylogenetic factors structure the distribution of damselfly and dragonfly species (Odonata) along an environmental gradient in Amazonian streams. Ecological Indicators, v. 122, p. 107257, 2021. https://doi.org/10.1016/j.ecolind.2020.107257
    » https://doi.org/10.1016/j.ecolind.2020.107257
  • BENONE, N. L. et al Regional controls on physical habitat structure of Amazon streams. River Research and Applications, v. 33, n. 5, p. 766-776, 2017. https://doi.org/10.1002/rra.3137
    » https://doi.org/10.1002/rra.3137
  • BORJA, A. et al Overview of integrative tools and methods in assessing ecological integrity in estuarine and coastal systems worldwide. Marine Pollution Bulletin, v. 56, n. 9, p. 1519-1537, 2008. https://doi.org/10.1016/j.marpolbul.2008.07.005
    » https://doi.org/10.1016/j.marpolbul.2008.07.005
  • BRASIL, L. S.; de LIMA, E. L.; SPIGOLONI, Z. A.; RIBEIRO-BRASIL, D. R. G.; JUEN, L. The habitat integrity index and aquatic insect communities in tropical streams: A meta-analysis. Ecological Indicators, v. 116, p. 106495, 2020. https://doi.org/10.1016/j.ecolind.2020.106495
    » https://doi.org/10.1016/j.ecolind.2020.106495
  • BRITO, J. S.; MICHELAN, T. S.; JUEN, L. Aquatic macrophytes are important substrates for Libellulidae (Odonata) larvae and adults. Limnology, v. 22, n. 1, p. 139-149, 2021. https://doi.org/10.1007/s10201-020-00643-x
    » https://doi.org/10.1007/s10201-020-00643-x
  • BUSS, D. F.; CARLISLE, D.; CHON, T. S.; CULP, J.; HARDING, J. S.; KEIZER-VLEK, H. E. et al Stream biomonitoring using macroinvertebrates around the globe: a comparison of large-scale programs. Environmental Monitoring and Assessment, v. 187, p. 4132, 2014. https://doi.org/10.1007/S10661-014-4132-8
    » https://doi.org/10.1007/S10661-014-4132-8
  • CALVÃO, L. B.; NOGUEIRA, D. S.; de ASSIS MONTAG, L. F.; LOPES, M. A.; JUEN, L. Are Odonata communities impacted by conventional or reduced impact logging? Forest Ecology and Management, v. 382, p. 143-150, 2016. https://doi.org/10.1016/j.foreco.2016.10.013
    » https://doi.org/10.1016/j.foreco.2016.10.013
  • CARMO, R. S. et al Does the structure of riparian vegetation affect the diversity of macrophytes in eastern Amazonian streams? Biologia, v. 78, n. 1, p. 79-89, 2023. https://doi.org/10.1007/s11756-022-01181-w
    » https://doi.org/10.1007/s11756-022-01181-w
  • CEDERBERG, C.; PERSSON, U. M.; NEOVIUS, K.; MOLANDER, S.; CLIFT, R. Including Carbon Emissions from Deforestation in the Carbon Footprint of Brazilian Beef. Environmental Science & Technology, v. 45, n. 5, p. 1773-1779, 2011. https://doi.org/10.1021/es103240z
    » https://doi.org/10.1021/es103240z
  • CHEN, K.; HUGHES, R. M.; BRITO, J. G.; LEAL, C. G.; LEITÃO, R. P.; de OLIVEIRA-JUNIOR, J. M. B. et al A multi-assemblage, multi-metric biological condition index for eastern Amazonia streams. Ecological Indicators, v. 78, p. 48-61, 2017. https://doi.org/10.1016/j.ecolind.2017.03.003
    » https://doi.org/10.1016/j.ecolind.2017.03.003
  • CLARIVATE. Web of Science. 2021. Available at: Available at: https://clarivate-com.translate.goog/webofsciencegroup/solutions/webofscience/?_x_tr_sl=en&_x_tr_tl=pt&_x_tr_hl=pt-BR&_x_tr_pto=op,sc Access: Mar. 21, 2021.
    » https://clarivate-com.translate.goog/webofsciencegroup/solutions/webofscience/?_x_tr_sl=en&_x_tr_tl=pt&_x_tr_hl=pt-BR&_x_tr_pto=op,sc
  • CRUZ, G. M.; FARIA, A. P. J.; JUEN, L. Patterns and metacommunity structure of aquatic insects (Trichoptera) in Amazonian streams depend on the environmental conditions. Hydrobiologia, v. 849, n. 12, p. 2831-2843, 2022. https://doi.org/10.1007/s10750-022-04901-0
    » https://doi.org/10.1007/s10750-022-04901-0
  • CUNHA, E. J. et al Urban development and industrialization impacts on semi aquatic bugs diversity: A case study in eastern Amazonian streams. Water Biology and Security, v. 1, n. 4, p. 100061, 2022. https://doi.org/10.1016/j.watbs.2022.100061
    » https://doi.org/10.1016/j.watbs.2022.100061
  • DINIZ- FILHO, J. A. F.; DE MARCO JR, P.; HAWKINS, B. A. Defying the curse of ignorance: perspectives in insect macroecology and conservation biogeography. Insect Conservation and Diversity, v. 3, 2010. https://dx.doi.org/10.1111/j.1752-4598.2010.0009
    » https://dx.doi.org/10.1111/j.1752-4598.2010.0009
  • FARES, A. L. B. et al Environmental factors affect macrophyte diversity on Amazonian aquatic ecosystems inserted in an anthropogenic landscape. Ecological Indicators, v. 113, p. 106231, 2020. https://doi.org/10.1016/j.ecolind.2020.106231
    » https://doi.org/10.1016/j.ecolind.2020.106231
  • FARIA, A. P. J.; LIGEIRO, R.; CALLISTO, M.; JUEN, L. Response of aquatic insect assemblages to the activities of traditional populations in eastern Amazonia. Hydrobiologia, v. 802, n. 1, p. 39-51, 2017. https://doi.org/10.1007/s10750-017-3238-8
    » https://doi.org/10.1007/s10750-017-3238-8
  • GARDNER, T. A.; FERREIRA, J.; BARLOW, J.; LEES, A. C.; PARRY, L.; VIEIRA, I. C. G. et al A social and ecological assessment of tropical land uses at multiple scales: the Sustainable Amazon Network. Philosophical Transactions of the Royal Society B: Biological Sciences, v. 368, n. 1619, p. 20120166-20120166, 2013. https://doi.org/10.1098/rstb.2012.0166
    » https://doi.org/10.1098/rstb.2012.0166
  • GOOGLE SCHOLAR. Webpage. 2021. Available at: Available at: https://scholar.google.com.br/?hl=pt Access: Jun. 17, 2021.
    » https://scholar.google.com.br/?hl=pt
  • HE, F.; ZARFL, C.; BREMERICH, V.; HENSHAW, A.; DARWALL, W.; TOCKNER, K. et al Disappearing giants: a review of threats to freshwater megafauna. Wiley Interdisciplinary Reviews: Water, v. 4, n. 3, p. e1208, 2017. https://doi.org/10.1002/wat2.1208
    » https://doi.org/10.1002/wat2.1208
  • HESS, L. L. et al Wetlands of the Lowland Amazon Basin: Extent, Vegetative Cover, and Dual-season Inundated Area as Mapped with JERS-1 Synthetic Aperture Radar. Wetlands, v. 35, n. 4, p. 745-756, 2015. https://doi.org/10.1007/s13157-015-0666-y
    » https://doi.org/10.1007/s13157-015-0666-y
  • HUGHES, R. M.; KAUFMANN, P. R.; HERLIHY, A. T.; KINCAID, T. M.; REYNOLDS, L.; LARSEN, D. P. A process for developing and evaluating indices of fish assemblage integrity. Canadian Journal of Fisheries and Aquatic Sciences, v. 55, n. 7, p. 1618-1631, 1998. https://doi.org/10.1139/f98-060
    » https://doi.org/10.1139/f98-060
  • ILHA, P.; ROSSO, S.; SCHIESARI, L. Effects of deforestation on headwater stream fish assemblages in the Upper Xingu River Basin, Southeastern Amazonia. Neotropical Ichthyology, v. 17, n. 1, 2019. https://doi.org/10.1590/1982-0224-20180099
    » https://doi.org/10.1590/1982-0224-20180099
  • JUEN, L.; CUNHA, E. J.; CARVALHO, F. G.; FERREIRA, M. C.; BEGOT, T. O.; ANDRADE, A. L. et al Effects of Oil Palm Plantations on the Habitat Structure and Biota of Streams in Eastern Amazon. River Research and Applications, v. 32, n. 10, p. 2081-2094, 2016. https://doi.org/10.1002/rra.3050
    » https://doi.org/10.1002/rra.3050
  • JUNK, W. J.; SOARES, M. G. M.; BAYLEY, P. B. Freshwater fishes of the Amazon River basin: their biodiversity, fisheries, and habitats. Aquatic Ecosystem Health & Management, v. 10, p. 153-173, 2007. https://doi.org/10.1080/14634980701351023
    » https://doi.org/10.1080/14634980701351023
  • KARR, J. R. Biological Integrity: A Long-Neglected Aspect of Water Resource Management. Ecological Applications, v. 1, n. 1, p. 66-84, 1991. https://doi.org/10.2307/1941848
    » https://doi.org/10.2307/1941848
  • KARR, J. R.; CHU, E. W. Introduction: Sustaining living rivers. In: JUNGWIRTH, M.; MUHAR, S.; SCHMUTZ, S. (eds.). Assessing the Ecological Integrity of Running Waters. Dordrecht: Springer, 2000. https://doi.org/10.1007/978-94-011-4164-2_1
    » https://doi.org/10.1007/978-94-011-4164-2_1
  • KAUFMANN, P. R.; LEVINE, P.; ROBISON, E. G.; SEELIGER, C.; PECK, D. V. Quantifying Physical Habitat in Wadeable Streams. EPA/620/R-99/003. Washington, D.C., 1999.
  • LEAL, C. G. et al Is environmental legislation conserving tropical stream faunas? A large-scale assessment of local, riparian and catchment-scale influences on Amazonian fish. Journal of Applied Ecology, v. 55, n. 3, p. 1312-1326, 2017. https://doi.org/10.1111/1365-2664.13028
    » https://doi.org/10.1111/1365-2664.13028
  • LEAL, C. G.; POMPEU, P. S.; GARDNER, T. A.; LEITÃO, R. P.; HUGHES, R. M.; KAUFMANN, P. R. et al Multi-scale assessment of human-induced changes to Amazonian instream habitats. Landscape Ecology, v. 31, p. 1725-1745, 2016. https://doi.org/10.1007/s10980-016-0358-x
    » https://doi.org/10.1007/s10980-016-0358-x
  • LEÃO, H.; SIQUEIRA, T.; TORRES, N. R.; MONTAG, L. F. de A. Ecological uniqueness of fish communities from streams in modified landscapes of Eastern Amazonia. Ecological Indicators, v. 111, p. 106039, 2020. https://doi.org/10.1016/j.ecolind.2019.106039
    » https://doi.org/10.1016/j.ecolind.2019.106039
  • LEITÃO, R. P. et al Disentangling the pathways of land use impacts on the functional structure of fish assemblages in Amazon streams. Ecography, v. 41, n. 1, p. 219-232, 2017. https://doi.org/10.1111/ecog.02845
    » https://doi.org/10.1111/ecog.02845
  • LEITE-FILHO, A. T. et al Deforestation reduces rainfall and agricultural revenues in the Brazilian Amazon. Nature Communications, v. 12, n. 1, 2021. https://doi.org/10.1038/s41467-021-22840-7
    » https://doi.org/10.1038/s41467-021-22840-7
  • LIMA, M. et al Land use changes disrupt streams and affect the functional feeding groups of aquatic insects in the Amazon. Journal of Insect Conservation, v. 26, n. 2, p. 137-148, 2022. https://doi.org/10.1007/s10841-022-00375-6
    » https://doi.org/10.1007/s10841-022-00375-6
  • LUIZA-ANDRADE, A.; MONTAG, L. F. de A.; JUEN, L. Functional diversity in studies of aquatic macroinvertebrates community. Scientometrics, v. 111, n. 3, p. 1643-1656, 2017. https://doi.org/10.1007/s11192-017-2315-0
    » https://doi.org/10.1007/s11192-017-2315-0
  • MARTINS, I. et al Regionalisation is key to establishing reference conditions for neotropical savanna streams. Marine and Freshwater Research, v. 69, p. 82-94, 2018. https://doi.org/10.1071/mf16381
    » https://doi.org/10.1071/mf16381
  • MARTINS, R. T. et al Effects of urbanization on stream benthic invertebrate communities in Central Amazon. Ecological Indicators, v. 73, p. 480-491, 2017. https://doi.org/10.1016/j.ecolind.2016.10.013
    » https://doi.org/10.1016/j.ecolind.2016.10.013
  • MENDES, T. P. et al Morphological diversity of Odonata larvae (Insecta) and abiotic variables in oil palm plantation areas in the Eastern Amazon. Hydrobiologia, v. 847, n. 1, p. 161-175, 2019a. https://doi.org/10.1007/s10750-019-04079-y
    » https://doi.org/10.1007/s10750-019-04079-y
  • MENDES, T. P.; BENONE, N. L.; JUEN, L. To what extent can oil palm plantations in the Amazon support assemblages of Odonata larvae? Insect Conservation and Diversity, 2019b. https://doi.org/10.1111/icad.12357
    » https://doi.org/10.1111/icad.12357
  • MENDES, T. P.; AMADO, L. L.; JUEN, L. Glutathione S-transferase activity in Mnesarete aenea (Odonata), Campylocia anceps (Ephemeroptera), and Cylindrostethus palmaris (Hemiptera) from forest and oil palm plantation areas in the Eastern Amazon. Ecological Indicators, v. 118, p. 106770, 2020. https://doi.org/10.1016/j.ecolind.2020.106770
    » https://doi.org/10.1016/j.ecolind.2020.106770
  • MONTAG, L. F. A. et al Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia, v. 826, 2019. https://doi.org/10.1007/s10750-018-3738-1
    » https://doi.org/10.1007/s10750-018-3738-1
  • OCHOCKA, A.; PASZTALENIEC, A. Sensitivity of plankton indices to lake trophic conditions. Environmental Monitoring and Assessment, v. 188, n. 11, 2016. https://doi.org/10.1007/s10661-016-5634
  • OLIVEIRA-JUNIOR, J. M. B. et al Neotropical dragonflies (Insecta: Odonata) as indicators of ecological condition of small streams in the eastern Amazon. Austral Ecology, v. 40, n. 6, p. 733-744, 2015. https://doi.org/10.1111/aec.12242
    » https://doi.org/10.1111/aec.12242
  • OLIVEIRA-JUNIOR, J. M. B.; JUEN, L. Structuring of Dragonfly Communities (Insecta: Odonata) in Eastern Amazon: Effects of Environmental and Spatial Factors in Preserved and Altered Streams. Insects, v. 10, n. 10, p. 322, 2019a. https://doi.org/10.3390/insects10100322
    » https://doi.org/10.3390/insects10100322
  • OLIVEIRA-JUNIOR, J. M. B.; JUEN, L. The Zygoptera/Anisoptera ratio (Insecta: Odonata): a new tool for habitat alterations assessment in Amazonian streams. Neotropical entomology, v. 48, n. 4, p. 552-560, 2019b. https://doi.org/10.1007/s13744-019-00672-x
    » https://doi.org/10.1007/s13744-019-00672-x
  • PAIVA, C. K. S.; FARIA, A. P. J.; CALVAO, L. B.; JUEN, L. The anthropic gradient determines the taxonomic diversity of aquatic insects in Amazonian streams. Hydrobiologia, v. 848, p. 1073-1085, 2021. https://doi.org/10.1007/s10750-021-04515-y
    » https://doi.org/10.1007/s10750-021-04515-y
  • PAZIN, V. F. V. et al Fish assemblages in temporary ponds adjacent to “terra-firme” streams in Central Amazonia. Freshwater Biology, v. 51, n. 6, p. 1025-1037, 2006. https://doi.org/10.1111/j.1365-2427.2006.01
    » https://doi.org/10.1111/j.1365-2427.2006.01
  • PECK, D. V. et al Environmental monitoring and assessment program - surface waters western pilot study: field operations manual for wadeable streams. EPA 600/R-06/003. Washington, DC: USEPA, 2006.
  • PEREIRA, D. F. G. et al Environmental changes promote larger species of Odonata (Insecta) in Amazonian streams. Ecological Indicators, v. 98, 2019. https://doi.org/10.1016/j.ecolind.2018.09.020
    » https://doi.org/10.1016/j.ecolind.2018.09.020
  • PIRES, J. M.; PRANCE, G. T. The vegetation types of the Brazilian Amazon. In: PRANCE, G. T.; LOVEJOY, T. E. (eds.). Key Environments: Amazonia. Oxford: Pergamon Press, 1985. p. 109-145.
  • PLAFKIN, J. L. Rapid bioassessment protocols for use in streams and rivers: benthic macroinvertebrates and fish. Washington, DC: USEPA, 1989.
  • PRUDENTE, B. S. et al Effects of reduced-impact logging on physical habitat and fish assemblages in streams of Eastern Amazonia. Freshwater Biology, v. 62, n. 2, p. 303-316, 2016. https://doi.org/10.1111/fwb.12868 .
    » https://doi.org/10.1111/fwb.12868
  • RESENDE, B. O. et al Impact of environmental changes on the behavioral diversity of the Odonata (Insecta) in the Amazon. Scientific Reports, v. 11, n. 1, 2021. https://doi.org/10.1038/s41598-021-88999-7
    » https://doi.org/10.1038/s41598-021-88999-7
  • SHIMANO, Y. et al Environmental variation in Amazonian interfluves and its effects on local mayfly assemblages. Hydrobiologia, v. 848, n. 17, p. 4075-4092, 2021. https://doi.org/10.1007/s10750-021-04626-6
    » https://doi.org/10.1007/s10750-021-04626-6
  • SHIMANO, Y.; JUEN, L. How oil palm cultivation is affecting mayfly assemblages in Amazon streams. International Journal of Limnology, v. 52, p. 35-45, 2016. https://doi.org/10.1051/limn/2016004
    » https://doi.org/10.1051/limn/2016004
  • SILVA, D. R. O. et al Assessing the extent and relative risk of aquatic stressors on stream macroinvertebrate assemblages in the neotropical savanna. Science of the Total Environment, v. 633, p. 179-188, 2018. https://doi.org/10.1016/j.scitotenv.2018.03.127
    » https://doi.org/10.1016/j.scitotenv.2018.03.127
  • SILVA, L. F. R. et al Ecological thresholds of Odonata larvae to anthropogenic disturbances in neotropical savanna headwater streams. Hydrobiologia, p. 1-14, 2022. https://doi.org/10.1007/s10750-022-05097-z
    » https://doi.org/10.1007/s10750-022-05097-z
  • SONTER, L. J. et al Mining drives extensive deforestation in the Brazilian Amazon. Nature Communications, v. 8, n. 1, 2017. https://doi.org/10.1038/s41467-017-00557-w
    » https://doi.org/10.1038/s41467-017-00557-w
  • SOUZA, C. M. et al Reconstructing Three Decades of Land Use and Land Cover Changes in Brazilian Biomes with Landsat Archive and Earth Engine. Remote Sensing, v. 12, n. 17, 2020. https://doi.org/10.3390/rs12172735
    » https://doi.org/10.3390/rs12172735
  • SUMUDUMALI, R. G. I.; JAYAWARDANA, J. M. C. K. A Review of Biological Monitoring of Aquatic Ecosystems Approaches: with Special Reference to Macroinvertebrates and Pesticide Pollution. Environmental Management, v. 67, n. 2, p. 263-276, 2021. https://doi.org/10.1007/s00267-020-01423-0
    » https://doi.org/10.1007/s00267-020-01423-0
  • TERESA, F. B.; CASATTI, L. Trait-based metrics as bioindicators: Responses of stream fish assemblages to a gradient of environmental degradation. Ecological Indicators, v. 75, p. 249-258, 2017. https://doi.org/10.1016/j.ecolind.2016.12.041
    » https://doi.org/10.1016/j.ecolind.2016.12.041
  • TERESA, F. B.; CASATTI, L.; CIANCIARUSO, M. V. Functional differentiation between fish assemblages from forested and deforested streams. Neotropical Ichthyology, v. 13, n. 2, p. 361-370, 2015. https://doi.org/10.1590/1982-0224-20130229
    » https://doi.org/10.1590/1982-0224-20130229
  • USEPA. Data from the National Aquatic Resource Surveys. 2021. Available at: Available at: https://www.epa.gov/national-aquatic-resource-surveys/data-national-aquatic-resource-surveys Access: Dec. 20, 2021.
    » https://www.epa.gov/national-aquatic-resource-surveys/data-national-aquatic-resource-surveys
  • VANNOTE, R. L.; MINSHALL, G. W.; CUMMINS, K. W.; SEDELL, J. R.; CUSHING, C. E. The river continuum concept. Canadian Journal of Fisheries and Aquatic Sciences, v. 37, n. 1, p. 130-137, 1980. https://doi.org/10.1139/f80-017
    » https://doi.org/10.1139/f80-017
  • XU, M. et al Effects of pollution on macroinvertebrates and water quality bio-assessment. Hydrobiologia, v. 729, n. 1, p. 247-259, 2013. https://doi.org/10.1007/s10750-013-1504-y
    » https://doi.org/10.1007/s10750-013-1504-y

Publication Dates

  • Publication in this collection
    22 Mar 2024
  • Date of issue
    2024

History

  • Received
    18 Oct 2023
  • Accepted
    15 Jan 2024
Instituto de Pesquisas Ambientais em Bacias Hidrográficas Instituto de Pesquisas Ambientais em Bacias Hidrográficas (IPABHi), Estrada Mun. Dr. José Luis Cembranelli, 5000, Taubaté, SP, Brasil, CEP 12081-010 - Taubaté - SP - Brazil
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