Abstract
In the present study, we analyzed a unique phytophysiognomy in the Amazon region, which is formed by savanna-like vegetation on iron-rich soil (known locally as canga) located within an iron-ore mining region. We used the habitat template theory to test the hypothesis that changes in the physical-chemical properties of streams and the physical structure of their habitats at in-stream and micro-basin (landscape) levels affect the taxonomic and trophic composition of immature aquatic insects. For this, we used a local environmental matrix composed of nine physical-chemical and structural habitat variables, together with the Habitat Integrity Index. We also calculated landscape metrics based on the area of the micro-basin, such as relief, slope, mean current flow, and vegetation cover. We divided the aquatic insects into five functional feeding groups based on their diet and food sources. Our results indicate that changes in the trophic level of the insects of the orders Ephemeroptera, Plecoptera, and Trichoptera are more easily observed than the taxonomic structure of communities. The loss of environmental integrity and vegetation cover were responsible for 84% of the variation observed in the composition of functional feeding groups (FFGs). Our study shows that aquatic insect communities in the canga and in the Amazon regions dominated by forest require specific in-stream and landscape conditions. These findings reinforce the need for the preservation of areas of canga vegetation, which not only have a unique levels of biological diversity, but are also targeted for the exploitation of their economically valuable natural resources.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Allan JD, Castillo MM (2007) Stream ecology: structure and function of running waters. Springer Science & Business Media
Alvares CA, Stape JL, Sentelhas PC, Moraes Gonçalves JL, Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Antunes MAH, Debiasi P, Siqueira JCS (2014) Avaliação espectral e geométrica das imagens Rapideye e seu potencial para o mapeamento e monitoramento agrícola e ambiental. Rev Bras Cartogr 66(1):105–113
Ardente NC, Ferreguetti AC, Gettinger D, Leal P, Mendes-Oliveira AC, Martins-Hatano F, Bergallo HG (2016) Diversity and impacts of mining on the non-volant small mammal communities of two vegetation types in the Brazilian Amazon. PLoS One 11(11):e0167266. https://doi.org/10.1371/journal.pone.0167266
Astudillo MR, Novelo-Gutiérrez R, Vázquez G, García-Franco JG, Ramírez G (2016) Relationships between land cover, riparian vegetation, stream characteristics, and aquatic insects in cloud forest streams, Mexico. Hydrobiologia 768:167–181. https://doi.org/10.1007/s10750-015-2545-1
Baptista DF, Buss DF, Dorvillé LFM, Nessimian JL (2001) Diversity and habitat preference of aquatic insects along the longitudinal gradient of the Macaé river basin, Rio de Janeiro, Brazil. Rev Bras Biol 61(2):249–258
Barbosa DDA, Brasil LS, Azevêdo CASD, Lima LRC (2020) The role of spatial and environmental variables in shaping aquatic insect assemblages in two protected areas in the transition area between Cerrado and Amazônia. Biota Neotropica 20(3). https://doi.org/10.1590/1676-0611-bn-2019-0923
Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632. https://doi.org/10.1890/07-0986
Borges SH, Santos MPD, Soares LMS, da Silva AS (2017) Avian communities in the Amazonian cangas vegetation: biogeographic affinities, components of beta diversity and conservation. Ann Braz Acad Sci 89(3):2167–2180. https://doi.org/10.1590/0001-3765201720160048
Brand C, Miserendino ML (2014) Biological traits and community patterns of Trichoptera at two Patagonian headwater streams affected by volcanic ash deposition. Zool Stud 53(1):72. https://doi.org/10.1186/s40555-014-0072-9
Brasil LS, Juen L, Giehl NFS, Cabette HSR (2017) Effect of environmental and temporal factors on patterns of rarity of Ephemeroptera in stream of the Brazilian Cerrado. Neotrop Entomol 46(1):29–35
Brasil LS, Luiza-Andrade A, Calvão LB, Dias-Silva K, Faria APJ, Shimano Y, Oliveira-Júnior JMB, Cardoso MN, Juen L (2020a) Aquatic insects and their environmental predictors: a scientometric study focused on environmental monitoring in lotic environmental. Environ Monit Assess 192:194. https://doi.org/10.1007/s10661-020-8147-z
Brasil LS, Lima EL, Spigoloni ZA, Ribeiro-Brasil DRG, Juen L (2020b) The habitat integrity index and the aquatic insects communities in tropical streams: a meta-analysis. Ecol Indic 116:106495. https://doi.org/10.1016/j.ecolind.2020.106495
Brito EF, Moulton TP, De Souza ML, Bunn SE (2006) Stable isotope analysis indicates microalgae as the predominant food source of fauna in a coastal forest stream, south-east Brazil. Austral Ecol 31(5):623–633. https://doi.org/10.1111/j.1442-9993.2006.01610.x
Brito JG, Martins RT, Oliveira VC, Hamada N, Nessimian JL, Hughes RM, de Paula FR (2018) Biological indicators of diversity in tropical streams: congruence in the similarity of invertebrate assemblages. Ecol Indic 85:85–92. https://doi.org/10.1016/j.ecolind.2017.09.001
Callisto M, Esteves FA (1998) Caracterização funcional dos macroinvertebrados bentônicos em quatro ecossistemas lóticos sob influência das atividades de uma mineração de bauxita na Amazônia central (Brasil). Oecol bras 5(1):15
Capparelli MV, Moulatlet GM, Abessa DMS, Lucas-Solis O, Rosero B, Galarza E, Tuba D, Carpintero N, Ochoa-Herrera V, Cipriani-Avila I (2020) An integrative approach to identify the impacts of multiple metal contamination sources on the eastern Andean foothills of the Ecuadorian Amazonia. Sci Total Environ 709:136088. https://doi.org/10.1016/j.scitotenv.2019.136088
Carvalho A, Martins-Hatano F, Martins F, Gettinger D, Dutra F, Bergallo H (2014) Large and medium-sized mammals of Carajás National Forest, Pará state, Brazil. Check List 10(1):1–10
Castro DMP, Dolédec S, Callisto M (2018) Land cover disturbance homogenizes aquatic insect functional structure in neotropical savanna streams. Ecol Indic 84:573–582. https://doi.org/10.1016/j.ecolind.2017.09.030
Compin A, Céréghino R (2007) Spatial patterns of macroinvertebrate functional feeding groups in streams in relation to physical variables and land-cover in Southwestern France. Landsc Ecol 22(8):1215–1225
Core Team R (2018) R: a language and environment for statistical computing. In: R Foundation for statistical computing. Austria. URL, Vienna https://www.R-project.org/
Crisci-Bispo VL, Bispo PC, Froehlich CG (2007) Ephemeroptera, Plecoptera and Trichoptera assemblages in litter in a mountain stream of the Atlantic rainforest from southeastern Brazil. Rev Bras Zool 24(3):545–551. https://doi.org/10.1590/S0101-81752007000200007
Cummins KW, Merritt RW, Andrade PCN (2005) The use of invertebrate functional groups to characterize ecosystem attributes in selected streams and rivers in South Brazil. Stud Neotropical Fauna Environ 40:69–89. https://doi.org/10.1080/01650520400025720
Dala-Corte RB, Melo AS, Siqueira T, Bini LM, Martins RT, Cunico AM, Monteiro-Júnior CS et al (2020) Thresholds of freshwater biodiversity in response to riparian vegetation loss in the Neotropical region. J Appl Ecol 57(7):1391–1402. https://doi.org/10.1111/1365-2664.13657
Dedieu N, Rhone M, Vigouroux R, Céréghino R (2015) Assessing the impact of gold mining in headwater streams of eastern Amazonia using Ephemeroptera assemblages and biological traits. Ecol Indic 52:332–340. https://doi.org/10.1016/j.ecolind.2014.12.012
Deegan LA, Neill C, Haupert CL, Ballester MVR, Krusche AV, Victoria RL, de Moor E (2011) Amazon deforestation alters small stream structure, nitrogen biogeochemistry and connectivity to larger rivers. Biogeochemistry 105:53–74. https://doi.org/10.1007/s10533-010-95404)
Domínguez E (2006) Ephemeroptera de América del sur (Vol. 2). Pensoft Publishers. Fernandes GW, Vale MM, Overbeck GE, Bustamante MM, Grelle CE, Bergallo HG., ... & Araújo, J. (2017). Dismantling Brazil's science threatens global biodiversity heritage. Perspect Ecol Conserv 15(3): 239–243
Dray S, Bauman D, Blanchet G, Borcard D, Clappe S, Guenard G, Jombart T, Larocque G, Legendre P, Madi N, Wagner HH (2018). adespatial: multivariate multiscale spatial analysis. R package version 0.2–0. https://CRAN.R-project.org/package=adespatial
Firmiano KR, Ligeiro R, Macedo DR, Juen L, Hughes RM, Callisto M (2017) Mayfly bioindicator thresholds for several anthropogenic disturbances in neotropical savanna streams. Ecol Indic 74:276–284. https://doi.org/10.1016/j.ecolind.2016.11.033
Frimpong EA, Sutton TM, Lim KJ, Hrodey PJ, Engel BA, Simon TP, Le Master DC (2005) Determination of optimal riparian forest buffer dimensions for stream biota-landscape association models using multimetric and multivariate responses. Can J Fish Aquat Sci 62(1):1–6. https://doi.org/10.1139/f05-020
Gonçalves JFL, Martins RT, Ottoni BMP, Couceiro SRM (2013) Uma visão sobre a decomposição foliar em sistemas aquáticos brasileiros. Páginas 89-117 in Insetos Aquáticos na Amazônia Brasileira: taxonomia, biologia e ecologia. Editora do INPA, 2014. Manaus. 724 p. ISBN 978-85-211-0123-9
Henriques-Oliveira AL, Nessimian JL (2010) Aquatic macroinvertebrate diversity and composition in streams along an altitudinal gradient in southeastern Brazil. Biota Neotropica 10(3):115–128
IBAMA (2003) Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais. PLANO DE MANEJO PARA USO MÚLTIPLO DA FLORESTA NACIONAL DE CARAJÁS. Brasília
Kovalenko KE, Brady VJ, Ciborowski JJH, Ilyushkin S, Johnson LB (2014) Functional changes in littoral macroinvertebrate communities in response to watershed-level anthropogenic stress. PLoS One 9(7):e101499. https://doi.org/10.1371/journal.pone.0101499
Leal CG, Pompeu PS, Gardner TA, Leitão RP, Hughes RM, Kaufmann PR, Zuanon Z, Paula FR, Ferraz SFB, Tomson JR, Mac Nally R, Ferreira J, Barlow J (2016) Multi-scale assessment of human-induced changes to Amazonian instream habitats. Landsc Ecol 31(8):1725–1745. https://doi.org/10.1007/s10980-016-0358-x
Lecci LS, Froehlich CG (2007) Plecoptera. In: Froehlich, C.G. (Ed.), Guia On-line: Identificação de Larvas de Insetos Aquáticos do Estado de São Paulo. http://sites.ffclrp.usp.br/aguadoce/Guia_online/
Legendre P, Legendre LFJ (2012) Numerical ecology. Elsevier, USA
Luiza-Andrade A, Brasil LS, Benone N, Shimano Y, Farias APJ, Montag LF, Juen L (2017a) Influence of oil palm monoculture on the taxonomic and functional composition of aquatic insect communities in eastern Brazilian Amazonia. Ecol Indic 82:478–483. https://doi.org/10.1016/j.ecolind.2017.07.006
Luiza-Andrade A, Montag LFA, Juen L (2017b) Functional diversity in studies of aquatic macroinvertebrates community. Scientometrics 111(3):1643–1656. https://doi.org/10.1007/s11192-017-2315-0
Merritt RW, Cummins KW (eds) (1996) An introduction to the aquatic insects of North America. Kendall Hunt 15:401–403. https://doi.org/10.2307/1467288
Merritt RW, Cummins KW, Berg MB (2017) Trophic relationships of macroinvertebrates. Methods Stream Ecol 1:413–433. https://doi.org/10.1016/b978-0-12-416558-8.00020-2
Montag LFA, Leão H, Benone NL, Monteiro-JúniorCS, FariaAPJ, Nicacio G, Ferreira CP, Garcia DHA, Santos CRM, Pompeu PS, Winemiller KO, Juen L (2019) Contrasting associations between habitat conditions and stream aquatic biodiversity in a forest reserve and its surrounding area in the Eastern Amazon. Hydrobiologia 826(1): 263–277.https://doi.org/10.1007/s10750-018-3738-1
Mota NFDO, Watanabe MTC, Zappi DC, Hiura AL, Pallos J, Viveros RS, Giulietti AM, Viana PL (2018) Amazon canga: the unique vegetation of Carajás revealed by the list of seed plants. Rodriguésia 69(3): 1435-1488.
Nessimian JL, Venticinque EM, Zuanon J, De Marco JP, Gordo M, Fidelis L, Batista JD, Juen L (2008) Land use, habitat integrity, and aquatic insect assemblages in Central Amazonian streams. Hydrobiologia 614(1):117. https://doi.org/10.1007/s10750-008-9441-x
Nogueira DS, Calvão LB, Montag LFS, Juen L, De Marco-Jr P (2016) Little effects of reduced-impact logging on insect communities in eastern Amazonia. Environ Monit Assess 188:441. https://doi.org/10.1007/s10661-016-5431-z3
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Stevens MHH, (2015) vegan: Community Ecology Package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. Version 2.3–3.2016
Paiva CKS, de Faria APJ, Calvão LB, Juen L (2017) Effect of oil palm on the Plecoptera and Trichoptera (Insecta) assemblages in streams of eastern Amazon. Environ Monit Assess 189(8):393
Pearson RG (2014) Dynamics of invertebrate diversity in a tropical stream. Diversity 6(4):771–791. https://doi.org/10.3390/d6040771
Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Koppen Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644. https://doi.org/10.5194/hess-11-1633-2007
Pes AM, Moreira Santos AP, Barcelos-Silva P, Camargos LM, (2014) Ordem Trichoptera. In Hamada N, Nessimian JL, Querino RB (Ed) Insetos Aquáticos na Amazônia Brasileira: taxonomia, biologia e ecologia. Editora do INPA, Manaus.724 p. ISBN 978-85-211-0123-9
Poff NL, Ward JV (1990) Physical habitat template of lotic systems: recovery in the context of historical pattern of spatiotemporal heterogeneity. Environ Manag 14(5):629–645
Poff NL, Olden JD, Vieira NK, Finn DS, Simmons MP, Kondratieff BC (2006) Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. J N Am Benthol Soc 25(4):730–755
QGIS Development Team. QGIS Geographic Information System. Open Source Geospatial Foundation Project (2019) Available in: http://qgis.osgeo.org. Accessed May 2018
RapidEye. (2015). Satellite imagery product specific cations. Retrieved February 20, 2016, from http://www.rapideye.de/
Rocha CFD, Bergallo HG (1990) Thermal biology and flight distance of Tropidurus oreadicus (Sauria Iguanidae) in an area of Amazonian Brazil. Ethol Ecol Evol 2(3):263–268
Salino A, Arruda AJ, Almeida TE (2018) Ferns and lycophytes from Serra dos Carajás, an Eastern Amazonian mountain range. Rodriguésia 69(3):1417–1434
Shimano Y, Juen L, Salles FF,, Nogueira DS, Cabette H.S.R (2013). Environmental and spatial processes determining Ephemeroptera (Insecta) structures in tropical streams. In Annales de Limnologie-International Journal of Limnology (Vol. 49, No. 1, pp. 31-41). EDP Sci
Shimano Y, Cardoso M, Juen L (2018) Ecological studies of mayflies (Insecta, Ephemeroptera): can sampling effort be reduced without losing essential taxonomic and ecological information? Acta Amazon 48(2):137–145. https://doi.org/10.1590/1809-4392201700583
Southwood TR (1977) Habitat, the templet for ecological strategies? J Anim Ecol 46(2):337–365
Souza-Filho PWM, Souza EB, Silva Júnior RO, Nascimento-Jr W, Mendonça BRV, Guimarães JTF, Dall’Agnol R, Siqueira JO (2016) Four decades of land-cover, land-use and hydroclimatology changes in the Itacaiúnas River watershed, southeastern Amazon. J Environ Manag 167:175–184. https://doi.org/10.1016/j.jenvman.2015.11.039
Strahler AN (1957) Quantitative analysis of watershed geomorphology. Trans Am Geophys Union 38:913–920. https://doi.org/10.1029/TR038i006p00913
Townsend CR, Hildrew AG (1994) Species traits in relation to a habitat templet for river systems. Freshw Biol 31:265–275
Valle IC, Buss DF, Baptista DF (2013) The influence of connectivity in forest patches, and riparian vegetation width on stream macroinvertebrate fauna. Braz J Biol 73(2):231–238. https://doi.org/10.1590/S1519-69842013000200002
Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37(1):130–137
Viana PL, Mota NF, Gil AD, Salino A, Zappi DC, Harley RM, Ilkiu-Borges AL, Secco RD, Almeida TE, Watanabe MT, Santos JU (2016) Flora das cangas da Serra dos Carajás, Pará, Brasil: história, área de estudos e metodologia. Rodriguésia 67(5SPE):1107–1124. https://doi.org/10.1590/2175-7860201667501
Wantzen KM, Wagner R (2006) Detritus processing by invertebrate shredders: a neotropical temperate comparison. J N Am Benthol Soc 25(1):216–232
Wootton A, Pearson RG, Boyero L (2018) Patterns of flow, leaf litter and shredder abundance in a tropical stream. Hydrobiologia 826:353–365. https://doi.org/10.1007/s10750-018-3748-z
Wright IA, Ryan MM (2016) Impact of mining and industrial pollution on stream macroinvertebrates: importance of taxonomic resolution, water geochemistry and EPT indices for impact detection. Hydrobiologia 772:103–115. https://doi.org/10.1007/s10750-016-2644-7
Acknowledgments
We are very grateful to Fernando G. Carvalho, Thiago P. Mendes, and Gilberto Nicácio for their assistance during the field expeditions. We are indebted to Yulie Shimano and Ana Paula Justino de Faria for identifying the ephemeropterans and trichopterans collected during this study, which would not have been possible without their contribution. We are also grateful to the Brazilian National Council for Scientific and Technological Development (CNPq) for granting a research productivity fellowship to LJ (304710/2019-9) and a PhD scholarship to ALA (1401991/2016-0), and to the Coordination for Higher Education Personnel Training (CAPES) for granting a postdoctoral scholarship to LSB (PNPD/UFPA 086/2013) and a PhD scholarship to NRT (88882.460087/2019-01). We are also grateful to the Brazilian Institute for the Environment and Renewable Resources (IBAMA) and the Chico Mendes Institute for the Conservation of Biodiversity (ICMBio), which are responsible for the licensing of mining operations, environmental monitoring programs, and issuing the permits for the collection of the biological material analyzed in the present study. We thank the Vale Company and Amplo Engenharia e Gestão de Projeto for enabling the field campaigns on their property and for their support in the field.
Author information
Authors and Affiliations
Contributions
All the authors contributed to the conception and design of the study. The material was prepared and the data were collected by ALA, JB, LSB, NRT, and LJ. The data were analyzed and discussed by ALA, LSB, RRS, and LJ. The first draft of the manuscript was written by ALA and all the authors commented on the previous versions of the manuscript. All the authors read and approved the final manuscript.
Corresponding author
Additional information
Macroinvertebrates of a unique Amazon phytophysiognomy
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Edited by Angelo Pallini – UFV
Electronic Supplementary Material
ESM 1
(PDF 766 kb)
Rights and permissions
About this article
Cite this article
Luiza-Andrade, A., Brasil, L.S., Torres, N.R. et al. Effects of Local Environmental and Landscape Variables on the Taxonomic and Trophic Composition of Aquatic Insects in a Rare Forest Formation of the Brazilian Amazon. Neotrop Entomol 49, 821–831 (2020). https://doi.org/10.1007/s13744-020-00814-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-020-00814-6