Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X2323
Acta Limnologica Brasiliensia
Original Article

Agriculture affects functional diversity of aquatic insects in Subtropical Atlantic Forest streams

Agricultura afeta a diversidade funcional de insetos aquáticos em riachos Subtropicais de Mata Atlântica

Luiz Ubiratan Hepp; Silvia Vendruscolo Milesi; Rayana Caroline Picolotto; Vanderlei Secretti Decian; Rozane Maria Restello; Julio Serrano Huiñocana; Edélti Faria Albertoni

Downloads: 0
Views: 292

Abstract

Aim: We evaluated the effects of native vegetation and agricultural activities on functional characteristics of aquatic insects’ assemblages in Atlantic Forest streams southern Brazil.

Methods: We collected information on land uses, riparian zone structural characteristics, and limnological variables of ten streams to characterize their environmental quality. In the same streams, we collected aquatic insects (Ephemeroptera, Plecoptera, and Trichoptera) and determined their functional characteristics (e.g. food habits, mobility, shape, and body size). The information for each trait category was quantified using a fuzzy code technique. To test the environmental conditions on aquatic insect functional attributes, we used an RLQ analysis.

Results: In our study, only five environmental variables showed variation in streams (temperature, pH, DO, native vegetation, and agriculture use). We collected a total of 2591 organisms distributed in 21 EPT genera. We observed that the functional attributes of EPT formed distinct groups in relation to the stream categories defined by the measured environmental variables. We observed that shredders and larger and flattened organisms were associated with natural streams. These attributes were associated with the genera Phylloicus, Anacroneuria, Tupiperla, and Farrodes. On the other hand, we observed greater proportions of scrapers, with spherical bodies and shelter builders in streams impacted by agriculture. The most frequent genera in these streams were Itaura, Wormaldia and Helicopsyche.

Conclusions: The modification of natural landscapes by agricultural areas caused significant functional changes in the aquatic invertebrate communities. Since aquatic insects participate effectively in ecological processes, alterations in the functional characteristics of these communities can cause changes in the streams’ functioning.

Keywords

biological traits, environmental quality, ecological integrity

Resumo

Objetivo: Neste estudo avaliamos os efeitos da vegetação nativa e atividades agrícolas sobre as características funcionais de assembleias de insetos aquáticos em riachos de Mata Atlântica, sul do Brasil.

Métodos: Coletamos informações sobre usos do solo, características estruturais da zona ripária e variáveis limnológicas de dez córregos para caracterizar sua qualidade ambiental. Nos mesmos riachos coletamos insetos aquáticos (Ephemeroptera, Plecoptera e Trichoptera) e determinamos as características funcionais (e.g., hábitos alimentares, mobilidade, forma, tamanho do corpo). A informação para cada categoria de característica foi quantificada usando uma técnica de código fuzzy. Para testar as condições ambientais nos atributos funcionais de insetos aquáticos, utilizamos uma análise RLQ.

Resultados: Em nosso estudo, apenas cinco variáveis ambientais apresentaram variação entre os riachos (temperatura, pH, DO, vegetação nativa, uso agrícola). Coletamos um total de 2591 organismos distribuídos em 21 gêneros das ordens EPT. Observamos que os atributos funcionais do EPT formaram grupos distintos em relação às categorias de riachos definidas pelas medidas das variáveis ambientais. Observamos que fragmentadores e organismos maiores e achatados estiveram associados a riachos naturais. Esses atributos foram associados aos gêneros Phylloicus, Anacroneuria, Tupiperla e Farrodes. Por outro lado, em riachos impactados pela agricultura, observamos maiores proporções de raspadores, com corpos esféricos e construtores de abrigos. Nesses riachos, os gêneros mais frequentes foram Itaura, Wormaldia e Helicopsyche.

Conclusões: A modificação das paisagens naturais por áreas agrícolas causou mudanças funcionais significativas nas comunidades de invertebrados aquáticos. Como os insetos aquáticos participam efetivamente dos processos ecológicos, alterações nas características funcionais dessas comunidades podem causar mudanças no funcionamento dos riachos.

Palavras-chave

características biológicas, qualidade ambiental, integridade ecológica

References

Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M. & Sparovek, G., 2013. Köppen’s climate classification map for Brazil. Meteorol. Z., 22(6), 711-728. http://dx.doi.org/10.1127/0941-2948/2013/0507.

Arimoro, F.O. & Muller, W.J., 2010. Mayfly (Insecta: Ephemeroptera) community structure as an indicator of the ecological status of a stream in the Niger Delta area of Nigeria. Environ. Monit. Assess., 166(1-4), 581-594. PMid:19543701. http://dx.doi.org/10.1007/s10661-009-1025-3.

Breda, M., Restello, R.M., Giovenardi, R., Vizzotto, A.P., Soares, B. & Hepp, L.U., 2020. Alpha and beta diversities of Trichoptera (Insecta) assemblages in natural and rural subtropical streams. Acta Limnol. Bras., 32, e14. http://dx.doi.org/10.1590/s2179-975x3219.

Castro, E.R., Veras, D.S., Lustosa, G.S., Azevêdo, C.A.S. & Juen, L., 2021. Effects of environmental variables and habitat integrity on the structure of the aquatic insect communities of streams in the Cerrado-Caatinga ecotone in Northeastern Brazil. Neotrop. Entomol., 50(1), 21-31. PMid:33104980. http://dx.doi.org/10.1007/s13744-020-00816-4.

Chevene, F., Doléadec, S. & Chessel, D., 1994. A fuzzy coding approach for the analysis of long-term ecological data. Freshw. Biol., 31(3), 295-309. http://dx.doi.org/10.1111/j.1365-2427.1994.tb01742.x.

Collyer, G., Perkins, D.M., Petsch, D.K., Siqueira, T. & Saito, V., 2023. Land-use intensification systematically alters the size structure of aquatic communities in the Neotropics. Glob. Change Biol., 29(14), 4094-4106. PMid:37059700. http://dx.doi.org/10.1111/gcb.16720.

Conceição, A.A., Albertoni, E.F., Milesi, S.V. & Hepp, L.U., 2020. Influence of anthropic impacts on the functional structure of aquatic invertebrates in subtropical wetlands. Wetlands, 40(6), 2287-2296. http://dx.doi.org/10.1007/s13157-020-01317-1.

Cornejo, A., Tonin, A.M., Checa, B., Tunon, A.R., Perez, D., Coronado, E., Gonzalez, S., Rios, T., Macchi, P., Correa-Araneda, F. & Boyero, L., 2019. Effects of multiple stressors associated with agriculture on stream macroinvertebrate communities in a tropical catchment. PLoS One, 14(8), e0220528. PMid:31393898. http://dx.doi.org/10.1371/journal.pone.0220528.

Dala‐Corte, R.B., Melo, A.S., Siqueira, T., Bini, L.M., Martins, R.T., Cunico, A.M., Pes, A.M., Magalhães, A.L.B., Godoy, B.S., Leal, C.G., Monteiro‐Júnior, C.S., Stenert, C., Castro, D.M.P., Macedo, D.R., Lima‐Junior, D.P., Gubiani, É.A., Massariol, F.C., Teresa, F.B., Becker, F.G., Souza, F.N., Valente‐Neto, F., Souza, F.L., Salles, F.F., Brejão, G.L., Brito, J.G., Vitule, J.R.S., Simião‐Ferreira, J., Dias‐Silva, K., Albuquerque, L., Juen, L., Maltchik, L., Casatti, L., Montag, L., Rodrigues, M.E., Callisto, M., Nogueira, M.A.M., Santos, M.R., Hamada, N., Pamplin, P.A.Z., Pompeu, P.S., Leitão, R.P., Ruaro, R., Mariano, R., Couceiro, S.R.M., Abilhoa, V., Oliveira, V.C., Shimano, Y., Moretto, Y., Súarez, Y.R. & Roque, F.O., 2020. Thresholds of freshwater biodiversity in response to riparian vegetation loss in the Neotropical region. J. Appl. Ecol., 57(7), 1391-1402. http://dx.doi.org/10.1111/1365-2664.13657.

Díaz, A.M., Alonso, M.L.S. & Gutiérrez, M.R.V.A., 2008. Biological traits of stream macroinvertebrates from a semi-arid catchment: patterns along complex environmental gradients. Freshw. Biol., 53(1), 1-21. http://dx.doi.org/10.1111/j.1365-2427.2007.01854.x.

Dolédec, S., Chessel, D., ter Braak, C.J.F. & Champely, S., 1996. Matching species traits to environmental variables: a new three-table ordination method. Environ. Ecol. Stat., 3(2), 143-166. http://dx.doi.org/10.1007/BF02427859.

Dray, S. & Dufour, A.B., 2007. The ade4 Package: implementing the duality diagram for ecologists. J. Stat. Softw., 22(4), 1-20. http://dx.doi.org/10.18637/jss.v022.i04.

Dray, S., Choler, P., Dolédec, S., Peres-Neto, P.R., Thuiller, W., Pavoine, S. & Ter Braak, C.J.F., 2014. Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology, 95(1), 14-21. PMid:24649641. http://dx.doi.org/10.1890/13-0196.1.

Fernandez, H.R. & Dominguez, E., 2001. Guia para determinación de los artropodos bentônicos sudamericanos. Tucumán: Universidad Nacional de Tucumán.

Ferreira, W.R., Hepp, L.U., Ligeiro, R., Macedo, D.R., Hughes, R.M., Kaufmann, P.R. & Callisto, M., 2017. Partitioning taxonomic diversity of aquatic insect assemblages and functional feeding groups in neotropical savanna headwater streams. Ecol. Indic., 72, 365-373. http://dx.doi.org/10.1016/j.ecolind.2016.08.042.

Gomes, W.I.A., Jovem-Azevêdo, D.S., Paiva, F.F., Milesi, S.V. & Molozzi, J., 2018. Functional attributes of Chironomidae for detecting anthropogenic impacts on reservoirs: a biomonitoring approach. Ecol. Indic., 93, 404-410. http://dx.doi.org/10.1016/j.ecolind.2018.05.006.

Graeber, D., Boechat, I.G., Encina-Montoya, F., Esse, C., Gelbrecht, J., Goyenola, G., Gucker, B., Heinz, M., Kronvang, B., Meerhoff, M., Nimptsch, J., Pusch, M.T., Silva, R.C., von Schiller, D. & Zwirnmann, E., 2015. Global effects of agriculture on fluvial dissolved organic matter. Sci. Rep., 5(1), 16328. PMid:26541809. http://dx.doi.org/10.1038/srep16328.

Hepp, L.U., Milesi, S.V., Biasi, C. & Restello, R.M., 2010. Effects of agriculture and urban impacts on macroinvertebrates assemblages in streams (Rio Grande do Sul, Brazil). Zoologia, 27(1), 106-113. http://dx.doi.org/10.1590/S1984-46702010000100016.

Hepp, L.U., Milesi, S.V., Nava, D. & Restello, R.M., 2021. Nestedness of stream insects in Subtropical region: importance of inter-annual temporal scale. Iheringia Ser. Zool., 111, e2021005. http://dx.doi.org/10.1590/1678-4766e2021005.

Hershkovitz, Y. & Gasith, A., 2013. Resistance, resilience, and community dynamics in mediterranean-climate streams. Hydrobiologia, 719(1), 59-75. http://dx.doi.org/10.1007/s10750-012-1387-3.

Huiñocana, J.C.S., Albertoni, E.F., Picolotto, R.C., Milesi, S.V. & Hepp, L.U., 2020. Nestedness of insect assemblages in agriculture-impacted Atlantic forest streams. Ann. Limnol. Int. J. Lim., 56, 3. http://dx.doi.org/10.1051/limn/2020002.

Ippolito, A., Todeschini, R. & Vighi, M., 2012. Sensitivity assessment of freshwater macroinvertebrates to pesticides using biological traits. Ecotoxicology, 21(2), 336-352. PMid:21983753. http://dx.doi.org/10.1007/s10646-011-0795-x.

Lamouroux, N., Doledec, S. & Gayraud, S., 2004. Biological traits of stream macroinvertebrate communities: effects of microhabitat, reach, and basin filters. J. N. Am. Benthol. Soc., 23(3), 449-466. http://dx.doi.org/10.1899/0887-3593(2004)023<0449:BTOSMC>2.0.CO;2.

Loregian, A.C., Silva, B.B., Zanin, E.M., Decian, V.S., Henke-Oliveira, C. & Budke, J.C., 2012. Padrões espaciais e ecológicos de espécies arbóreas refletem a estrutura em mosaicos de uma floresta subtropical. Acta Bot. Bras., 26(3), 593-606. http://dx.doi.org/10.1590/S0102-33062012000300009.

Loureiro, R.C. & Hepp, L.U., 2020. Stream contamination by trace elements: biota incorporation and phytoremediation. Acta Limnol. Bras., 32, e201. http://dx.doi.org/10.1590/s2179-975x2219.

Loureiro, R.C., Calisto, J.F.F., Magro, J.D., Restello, R.M. & Hepp, L.U., 2021. The influence of the environment in the incorporation of copper and cadmium in scraper insects. Environ. Monit. Assess., 193(4), 215. PMid:33759031. http://dx.doi.org/10.1007/s10661-021-08997-0.

Loureiro, R.C., Menegat, M.N., Restello, R.M. & Hepp, L.U., 2018. Incorporation of zinc and copper by insects of different functional feeding groups in agricultural streams. Environ. Sci. Pollut. Res. Int., 25(18), 17402-17408. PMid:29654465. http://dx.doi.org/10.1007/s11356-018-1971-9.

Luiza-Andrade, A., Brasil, L.S., Benone, N.L., Shimano, Y., Farias, A.P.J., Montag, L.F., Dolédec, S. & Juen, L., 2017. Influence of oil palm monoculture on the taxonomic and functional composition of aquatic insect communities in eastern Brazilian Amazonia. Ecol. Indic., 82, 478-483. http://dx.doi.org/10.1016/j.ecolind.2017.07.006.

Luke, S.H., Slade, E.M., Gray, C.L., Annammala, K.V., Drewer, J., Williamson, J., Agama, A.L., Ationg, M., Mitchell, S.L., Vairappan, C.S. & Struebig, M.J., 2019. Riparian buffers in tropical agriculture: scientific support, effectiveness and directions for policy. J. Appl. Ecol., 56(1), 85-92. http://dx.doi.org/10.1111/1365-2664.13280.

Lundquist, M.J. & Zhu, W., 2018. Aquatic insect functional diversity and nutrient content in urban streams in a medium-sized city. Ecosphere, 9(5), e02284. http://dx.doi.org/10.1002/ecs2.2284.

Malacarne, T.J., Machado, N.R. & Moretto, Y., 2023. Influence of land use on the structure and functional diversity of aquatic insects in neotropical streams. Hydrobiologia (Online). http://dx.doi.org/10.1007/s10750-023-05207-5.

Medan, D., Torretta, J.P., Hodara, K., de la Fuente, E.B. & Montaldo, N.H., 2011. Effects of agriculture expansion and intensification on the vertebrate and invertebrate diversity in the Pampas of Argentina. Biodivers. Conserv., 20(13), 3077-3100. http://dx.doi.org/10.1007/s10531-011-0118-9.

Meza-Salazar, A.M., Guevara, G., Gomes-Dias, L. & Cultid-Medina, C.A., 2020. Density and diversity of macroinvertebrates in Colombian Andean streams impacted by mining, agriculture and cattle production. PeerJ, 8, e9619. PMid:32995074. http://dx.doi.org/10.7717/peerj.9619.

Milesi, S.V., Dolédec, S. & Melo, A.S., 2016. Substrate heterogeneity influences the trait composition of stream insect communities: an experimental in situ study. Freshw. Sci., 35(4), 1321-1329. http://dx.doi.org/10.1086/688706.

Milesi, S.V., Melo, A.S. & Dolédec, S., 2019. Assessing community functional attributes during substrate colonization: a field experiment using stream insects. Hydrobiologia, 838(1), 183-192. http://dx.doi.org/10.1007/s10750-019-03988-2.

Mugnai, R., Nessimian, J.L. & Baptista, D.F., 2010. Manual de identificação de macroinvertebrados aquáticos do estado do Rio de Janeiro. Rio de Janeiro: Technical Books, 174 p.

Nicacio, G., Cunha, E.J., Hamada, N. & Juen, L., 2020. How habitat filtering can affect taxonomic and functional composition of aquatic insect communities in small Amazonian streams. Neotrop. Entomol., 49(5), 652-661. PMid:32440832. http://dx.doi.org/10.1007/s13744-020-00780-z.

Oliveira-Filho, A.T., Budke, J.C., Jarenkow, J.A., Eisenlohr, P.V. & Neves, D.R.M., 2015. Delving into the variations in tree species composition and richness across South American subtropical Atlantic and Pampean forests. J. Plant Ecol., 8(3), 242-260. http://dx.doi.org/10.1093/jpe/rtt058.

Paz, D.B., Henderson, K. & Loreau, M., 2020. Agricultural land use and the sustainability of social-ecological systems. Ecol. Modell., 437, 109312. PMid:33343058. http://dx.doi.org/10.1016/j.ecolmodel.2020.109312.

R Core Team, 2017. R: a language and environment for statistical computing [online]. Vienna: R Foundation for Statistical Computing. Retrieved in 2018, July 5, from http://www.R-project.org/

Restello, R.M. & Hepp, L.U., 2020. Monitoramento biológico de riachos com o uso de invertebrados aquáticos. In: Hepp, L.U. & Restello, R.M., eds. Ecologia de riachos no Alto Uruguai Gaúcho. Erechim: EdiFapes, 33-51.

Ribeiro, J.C.T., Nunes-Freitas, A.F., Fidalgo, E.C.C. & Uzeda, M.C., 2019. Forest fragmentation and impacts of intensive agriculture: responses from different tree functional groups. PLoS One, 14(8), e0212725. PMid:31369550. http://dx.doi.org/10.1371/journal.pone.0212725.

Rovani, I.L., Decian, V.S., Zanin, E.M., Brandalise, M., Quadros, F.R. & Hepp, L.U., 2020. Socioeconomic changes and land use and land cover of the northern region of Rio Grande do Sul, Brazil. Floresta Ambient., 27(3), e20180258. http://dx.doi.org/10.1590/2179-8087.025818.

Saito, V.S., Siqueira, T., Bini, L.M., Costa-Pereira, R., Santos, E.P. & Pavoine, S., 2020. Comparing taxon- and trait-environment relationships in stream communities. Ecol. Indic., 117, 106625. http://dx.doi.org/10.1016/j.ecolind.2020.106625.

Sensolo, D., Hepp, L.U., Decian, V. & Restello, R.M., 2012. Influence of landscape on assemblages of Chironomidae in Neotropical streams. Ann. Limnol. Int. J. Limnol., 48(4), 391-400. http://dx.doi.org/10.1051/limn/2012031.

Sitati, A., Raburu, P.O., Yegon, M.J. & Masese, F.O., 2021. Land-use influence on the functional organization of Afrotropical macroinvertebrate assemblages. Limnologica, 88, 125875. http://dx.doi.org/10.1016/j.limno.2021.125875.

Tachet, H., Richoux, P., Bournaud, M. & Usseglio-Polatera, P., 2002. Invertébrés d’eau douce. Paris: CNRS Éditions.

Tanentzap, A.J., Lamb, A., Walker, S. & Farmer, A., 2015. Resolving conflicts between agriculture and the natural environment. PLoS Biol., 13(9), e1002242. PMid:26351851. http://dx.doi.org/10.1371/journal.pbio.1002242.

Tomanova, S., Moya, N. & Oberdorff, T., 2008. Using macroinvertebrate biological traits for assessing biotic integrity of neotropical streams. River Res. Appl., 24(9), 1230-1239. http://dx.doi.org/10.1002/rra.1148.

Tonello, G., Decian, V.S., Restello, R.M. & Hepp, L.U., 2021. The conversion of natural riparian forests into agricultural land affects ecological processes in Atlantic forest streams. Limnologica, 91, 125927. http://dx.doi.org/10.1016/j.limno.2021.125927.

Tonin, A.M., Hepp, L.U. & Gonçalves Junior, J.F., 2018. Spatial variability of plant litter decomposition in stream networks: from litter bags to watersheds. Ecosystems, 21(3), 567-581. http://dx.doi.org/10.1007/s10021-017-0169-1.
 


Submitted date:
03/27/2023

Accepted date:
10/17/2023

Publication date:
11/17/2023

6557b2b8a953956b39165943 alb Articles
Links & Downloads

Acta Limnol. Bras. (Online)

Share this page
Page Sections