Acta Limnologica Brasiliensia
https://actalb.org/article/doi/10.1590/S2179-975X1019
Acta Limnologica Brasiliensia
Original Article

Pollution tolerance, flight capacity and natural history explain metacommunity structure in high-altitude stream insects

Tolerância à poluição, capacidade de voo e história natural explicam a estrutura da metacomunidade em insetos de riachos de alta altitude

Mireile Reis dos Santos; Victor Satoru Saito; Paulo Augusto Zaitune Pamplin; Allan Arantes Pereira; Alaíde Aparecida Fonseca-Gessner

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Abstract

Abstract:: Aim: To test how different taxonomic and functional groups of aquatic insects from high-altitude streams respond to environmental and spatial gradients at multiple scales in Southeast of Brazil.

Methods: Specimens were collected in 26 high-altitude streams distributed over a gradient of previously defined environmental quality. The taxonomic identification was made at the genus level and the functional classification was based on traits of flight capacity and pollution tolerance compiled from specific literature. We obtained local in situ data (limnological, sediments, and organic matter), as well as calculated land use at the riparian and drainage basin scale. A variation partitioning approach was used to explain species composition based on different response matrices deconstructed by both taxonomic groups and functional traits. The explanatory matrices encompassed environmental variables at three spatial scales and spatial variables extracted from Principal Components of Neighbor Matrices analysis. A linear model was applied to verify the possible correlation between spatial and environmental components.

Results: The contribution of the spatial and environmental components varied strongly between taxonomic and functional groups. For taxonomic groups, the pure environmental component was more important for Odonata and Trichoptera, while spatial variables were more important for Diptera (non-Chironomidae) and Chironomidae, Coleoptera, Ephemeroptera, Plecoptera and Megaloptera. The sensitive groups with good flight capacity showed a greater environmental signature while the tolerant groups with low flight capacity had a greater spatial signature. Moreover, the important variables for explaining community variation were from different spatial scale (local, riparian and watershed) depending either on the analyzed taxonomic or on functional groups. However, a general effect of forests was found in several groups.

Conclusions: It is necessary to consider the joint effect of evolutionary natural history of groups, as well as their functional traits in the structuring of metacommunities, since only taxonomic resolutions may not be sufficient to detect assembly processes at multiple spatial scales.

Keywords

aquatic invertebrates, metacommunity, streams altitude, Poços de Caldas Plateau, environmental filtering

Resumo

Resumo:

Objetivo: Testar como as diferenças taxonômicas e de grupos funcionais de insetos aquáticos de riachos de altitude respondem ao gradiente ambiental e espacial em múltiplas escalas no sudeste do Brasil.

Métodos: As amostras foram coletadas em 26 riachos de altitude distribuídos em um gradiente de qualidade ambiental previamente definido. A identificação taxonômica foi feita no nível de gênero e a classificação funcional foi baseada em características de capacidade de voo e tolerância à poluição compiladas a partir de literatura específica. Obtivemos dados locais in situ (limnológicos, sedimentos e matéria orgânica), bem como calculamos o uso da terra na zona ripária e na escala da bacia hidrográfica. O particionamento de variância foi usado para explicar a composição de espécies com base em matrizes de resposta desconstruídas por grupos taxonômicos e características funcionais. As matrizes explicativas abrangeram as variáveis ​​ambientais em três escalas e as variáveis ​​espaciais extraídas da análise de Componentes Principais das Matrizes Vizinhas. Um modelo linear foi aplicado para verificar a possível correlação entre componentes espaciais e ambientais.

Resultados: A contribuição dos componentes espaciais e ambientais variou fortemente entre os grupos taxonômico e funcional. Para os grupos taxonômicos Odonata e Trichoptera, o componente ambiental puro foi mais importante, enquanto as variáveis ​​espaciais foram mais importantes para Diptera (exceto-Chironomidae) e Chironomidae, Coleoptera, Ephemeroptera, Plecoptera and Megaloptera. Os grupos sensíveis com boa capacidade de voo apresentaram maior assinatura ambiental, enquanto os grupos tolerantes e com baixa capacidade de voo tiveram maior assinatura espacial. Além disso, as variáveis ​​importantes para explicar a variação da comunidade foram de diferentes escalas espaciais (local, riparia e da bacia hidrográfica), dependendo dos grupos taxonômicos ou funcionais analisados, mas um efeito geral das florestas foi encontrado em vários grupos.

Conclusões: É necessário considerar o efeito conjunto da história natural evolutiva dos grupos, bem como seus traços funcionais na estruturação de metacomunidades, uma vez que apenas resoluções taxonômicas podem não ser suficientes para detectar processos de montagem em múltiplas escalas espaciais.
 

Palavras-chave

invertebrados aquáticos, metacomunidade, riachos de altitude, Planalto de Poços de Caldas, filtragem ambiental

References

ALBERTI, H.L.C. Caracterização fisiográfica e avaliação hidrológica na bacia do Ribeirão das Antas, Planalto de Poços de Caldas, MG [Dissertação de Mestrado em Geociências]. Campinas: Universidade Estadual de Campinas, 2008.

ALEMU, T., BAHRNDORFF, S., HUNDERA, K., ALEMAYEHU, E. and AMBELU, A. Effect of riparian land use on environmental conditions and riparian vegetation in the east African highland streams. Limnologica, 2017, 66(1), 1-11. http://dx.doi.org/10.1016/j.limno.2017.07.001.

ALLAN, J.D. and CASTILLO, M.M. Stream ecology structure and function of running waters. Michigan: Chapman & Hall, 1995. http://dx.doi.org/10.1007/978-94-011-0729-7.

ALLAN, J.D. Landscape and riverscape: the influence of land use on stream ecosystems. Annual Review of Ecology Evolution and Systematics, 2004, 35(1), 257-284. http://dx.doi.org/10.1146/annurev.ecolsys.35.120202.110122.

BENETTI, C.J., CUETO, J.A.R. and FIORENTIN, G.L. Gêneros de Hydraphaga (Coleoptera: Dytiscidae, Gyrinidae, Haliplidae, Noteridae) citados para o Brasil, com chaves. Biota Neotropica, 2003, 3(1), 1-20. http://dx.doi.org/10.1590/S1676-06032003000100010.

BIE, T., MEESTER, L., BRENDONCK, L., MARTENS, K., GODDEERIS, B., ERCKEN, D., HAMPEL, H., DENYS, L., VANHECKE, L., GUCHT, K., WICHELEN, J., VYVERMAN, W. and DECLERCK, S.A.J. R Body size and dispersal mode as key traits determining metacommunity structure of aquatic organisms. Ecology Letters, 2012, 15(7), 740-747. http://dx.doi.org/10.1111/j.1461-0248.2012.01794.x. PMid:22583795.

BILTON, D.T., FREELAND, J.R. and OKAMURA, B. Dispersal in freshwater invertebrates. Annual Review of Ecology and Systematics, 2001, 32(1), 159-181. http://dx.doi.org/10.1146/annurev.ecolsys.32.081501.114016.

BORCARD, D. and LEGENDRE, P. All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling, 2002, 153(1-2), 51-68. http://dx.doi.org/10.1016/S0304-3800(01)00501-4.

BORCARD, D., GILLET, F. and LEGENDRE, P. Numerical ecology with R.1. New York: Springer, 2011. http://dx.doi.org/10.1007/978-1-4419-7976-6.

BORCARD, D., LEGENDRE, P. and DRAPEAU, P. Partialling out the spatial component of ecological variation. Ecology, 1992, 73(3), 1045-1055. http://dx.doi.org/10.2307/1940179.

BORCARD, D., LEGENDRE, P., AVOIS-JACQUET, C. and TUOMISTO, H. Dissecting the spatial structure of ecological data at multiple scales. Ecology, 2004, 85(7), 1826-1832. http://dx.doi.org/10.1890/03-3111.

BRAUN, B.M., SALVARREY, A.V.B., KOTZIAN, C.B., SPIES, M.R. and PIRES, M.M. Diversity and distribution of riffle beetle assemblages (Coleoptera, Elmidae) in montane rivers of Southern Brazil. Biota Neotropica, 2014, 14(2), 1-11. http://dx.doi.org/10.1590/1676-060320140615183046.

CALLISTO, M., BARBOSA, F.A. and MORENO, P. Aplicação de um protocolo de avaliação rapida da diversidade de habitats em atividades de ensino e pesquisa (MG-RJ). Acta Limnologica Brasiliensia, 2002, 14(1), 91-98.

COSTA, D.S.M., BRANCO, C.C.Z. and BISPO, P.D.C. O Papel dos Fatores Ambientais e Espaciais Sobre a Fauna de Ephemeroptera (Insecta) em Riachos de Mata Atlântica. EntomoBrasilis, 2014, 7(2), 86-92. http://dx.doi.org/10.12741/ebrasilis.v7i2.368.

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. and ROQUE, F.O. Thresholds of freshwater biodiversity in response to riparian vegetation loss in the Neotropical region. Journal of Applied Ecology, 2020, 5, 1-12. http://dx.doi.org/10.1111/1365-2664.13657.

DOLNÝ, A., HARABIŠ, F. and MIŽIČOVÁ, H. Home Range, movement, and distribution patterns of the threatened dragonfly Sympetrum depressiusculum (Odonata: Libellulidae): a thousand times greater territory to protect? PLoS One, 2014, 9(7), e100408. http://dx.doi.org/10.1371/journal.pone.0100408. PMid:25006671.

DOMINGUEZ, E.F. and FERNÁNDEZ, R. H. Macroinvertebrados bentónicos sudamericanos: sistemática y biologica. Tucuman: Fund. Miguel Lillo, 2009.

DRAY, S., LEGENDRE, P. and PERES-NETO, P. Spatial modelling: a comprehensive framework for principal coordinate analysis of neighbour matrices (PCNM). Ecological Modelling, 2006, 196(3-4), 483-493. http://dx.doi.org/10.1016/j.ecolmodel.2006.02.015.

EPLER, J.H. Identification manual for the Larval Chironomidae (Diptera) of North and South Carolina. Raleigh, North Carolina: North Carolina Department of Environment and Natural Resources, 2001.

FINN, D.S. and POFF, N.L. Variability and convergence in benthic communities along the longitudinal gradients of four physically similar Rocky Mountain streams. Freshwater Biology, 2005, 50(2), 243-261. http://dx.doi.org/10.1111/j.1365-2427.2004.01320.x.

FINN, D.S., BONADA, N., MÚRRIA, C. and HUGHES, J.M. Small but mighty: headwaters are vital to stream network biodiversity at two levels of organization. Freshwater Science, 2011, 30(4), 963-980.

FRISSELL, C.A., LISS, W.J., WARREN, C.E. and HURLEY, M.D. A hierarchical framework for stream habitat classification: viewing streams in a watershed context. Environmental Management, 1986, 10(2), 199-214. http://dx.doi.org/10.1007/BF01867358.

FROEHLICH, C.G. Checklist dos Plecoptera (Insecta) do Estado de São Paulo, Brasil. Biota Neotropica, 2011, 11(1), 601-606, Supplement 1. http://dx.doi.org/10.1590/S1676-06032011000500026.

HAMADA, N., NESSIMIAN, J.L. and BARBOSA, R. Insetos aquáticos na Amazônia brasileira: taxonomia, biologia e ecologia. Manaus: INPA, 2014.

HECKMAN, C.W. Encyclopedia of South American Aquatic Insects: Odonata Anisopera. Netherlands: Springer, 2006.

HECKMAN, C.W. Encyclopedia of South American Aquatic Insects: Odonata Zygoptera. Netherlands: Springer, 2008. http://dx.doi.org/10.1007/978-1-4020-8176-7.

HEINO, J. Does dispersal ability affect the relative importance of environmental control and spatial structuring of littoral macroinvertebrate communities? Oecologia, 2013, 171(4), 971-980. http://dx.doi.org/10.1007/s00442-012-2451-4. PMid:22961400.

HEINO, J., MELO, A.S., SIQUEIRA, T., SOININEN, J., VALANKO, S. and BINI, L.M. Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshwater Biology, 2015a, 60(5), 845-886. http://dx.doi.org/10.1111/fwb.12533.

HEINO, J., NOKELA, T., SOININEN, J., TOLKKINEN, M., VIRTANEN, L. and VIRTANEN, R. Elements of metacommunity structure and community environment relationships in stream organisms environment. Freshwater Biology, 2015b, 60(5), 973-988. http://dx.doi.org/10.1111/fwb.12556.

HEINO, J., SOININEN, J., ALAHUHTA, J., LAPPALAINEN, J. and VIRTANEN, R. Metacommunity ecology meets biogeography: effects of geographical region, spatial dynamics and environmentalfiltering on community structure in aquatic organisms. Oecologia, 2016, 183(1), 121-137. http://dx.doi.org/10.1007/s00442-016-3750-y. PMid:27714463.

HEINO, J., ALAHUHTA, J., ALA-HULKKO, T., ANTIKAINEN, H., BINI, L.M., BONADA, N., DATRY, T., ERŐS, T., HJORT, J., KOTAVAARA, O., MELO, A.S. and SOININEN, J. Integrating dispersal proxies in ecological and environmental research in the freshwater realm. Environmental Reviews, 2017, 25(3), 334-349. http://dx.doi.org/10.1139/er-2016-0110.

JUNQUEIRA, V.M. and CAMPOS, S.C.M. Adaptation of the “BMWP” method for water quality evaluation to Rio das Velhas Watershed (Minas Gerais, Brazil). Acta Limnologica Brasiliensia, 1998, 10, 125-135.

LECCI, L.S. and FROEHLICH, C.G. Guia on-line: identificação de larvas de insetos aquáticos do Estado de São Paulo: Plecoptera [online]. Ribeirão Preto: Laboratório de Entomologia Aquática, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo Campus de São Carlos, 2007 [viewed 15 June 2017]. Available from: http://sites.ffclrp.usp.br/aguadoce/Guia_online/Guia_identifica%C3%A7%C3%A3o_larvas_Plecoptera.pdf

LEGENDRE, P. and GALLAGHER, E.D. Ecologically meaningful transformations for ordination of species data. Oecologia, 2001, 129(2), 271-280. http://dx.doi.org/10.1007/s004420100716. PMid:28547606.

LEIBOLD, M.A., HOLYOAK, M., MOUQUET, N., AMARASEKARE, P., CHASE, J.M., HOOPES, M.F., HOLT, R.D., SHURIN, J.B., LAW, R., TILMAN, D., LOREAU, M. and GONZALEZ, A. The metacommunity concept: a framework for multi-scale community ecology. Ecology Letters, 2004, 7(7), 601-613. http://dx.doi.org/10.1111/j.1461-0248.2004.00608.x.

MALMQVIST, B. How does wing length relate to distribution patterns of stoneflies (Plecoptera) and mayflies (Ephemeroptera)? Biological Conservation, 2000, 93(2), 271-276. http://dx.doi.org/10.1016/S0006-3207(99)00139-1.

MARIANO, R. and FROEHLICH, C.G. Ephemeroptera. In: Universidade de São Paulo. Guia on-line: identificação de larvas de insetos aquáticos do Estado de São Paulo [online]. Ribeirão Preto: Laboratório de Entomologia Aquática, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, 2007. [viewed 18 June 2017]. Available from: http://sites.ffclrp.usp.br/aguadoce/guiaonline

MERRITT, R.W. and CUMMINS, K.W. An introduction to the aquatic insects of North America. Dubuque: Kendall, Hunt, 1996.

MICHAT, M.C., ARCHANGELSKY, M. and BACHMANN, A.O. Generic keys for the identifi cation of larval Dytiscidae from Argentina (Coleoptera: Adephaga). Revista de la Sociedad Entomológica Argentina, 2008, 67, 3-4.

MORAES, F.T. and JIMÉNEZ-RUEDA, J.R. Fisiografia da região do planalto de Poços de Caldas, MG/SP. Revista Brasileira de Geociencias, 2008, 38(1), 196-208. http://dx.doi.org/10.25249/0375-7536.2008381196208.

MORAES, F.T. Zoneamento geoambiental do planalto de Poços de Caldas, MG/SP a partir de análise fisiográfica e pedoestratigráfica [Tese de Doutorado em em Geociências e Meio Ambiente]. Rio Claro: Universidade Estadual Paulista, 2007.

MUGNAI, R., NESSIMIAN, J.L. and BAPTISTA, D.F. Manual de identificação de macroinvertebrados aquáticos do Estado do Rio de Janeiro. Rio de Janeiro: Technical Books, 2010.

OKSANEN, J., BLANCHET, F.G., FRIENDLY, M., KINDT, R., LEGENDRE, P., MCGLINN, D., MINCHIN, P.R., O’HARA, R.B., SIMPSON, G.L., SOLYMOS, P., HENRY, M., STEVENS, H., SZOECS, E. and WAGNER, H. Vegan: Community Ecology Package. R package version 2.4-3 [online]. Vienna: R Foundation for Statistical Computing, 2017 [viewed 15 June 2017]. Available from: https: //CRAN.R-project.org/package=vegan

PADIAL, A., CESCHIN, F., DECLERCK, S.A.J., MEESTER, L., BONECKER, C.C., LANSAC-TÔHA, F.A., RODRIGUES, L., RODRIGUES, L.C., TRAIN, S., VELHO, L.F. and BINI, L.M. Dispersal ability determines the role of environmental, spatial and temporal drivers of metacommunity structure. PLoS One, 2014, 9(10), e111227. http://dx.doi.org/10.1371/journal.pone.0111227. PMid:25340577.

POFF, L.N., OLDEN, J.D., VIEIRA, N.K.M., FINN, D.S., SIMMONS, M.P. and KONDRATIEFF, B.C. Functional trait niches of North American lotic insects: traits-based ecological applications in light of phylogenetic relationships. Journal of the North American Benthological Society, 2006, 25(4), 730-755. http://dx.doi.org/10.1899/0887-3593(2006)025[0730:FTNONA]2.0.CO;2.

R CORE TEAM. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing, 2017.

RAMÍREZ, A. Capitulo 5: Odonata. Revista de Biología Tropical, 2010, 58(4), 97-136.

REYNOLDS, C.S., HUSZAR, R.V., KRUK, C., NASELLI-FLORES, L. and MELO, S. Towards a functional classification of the freshwater phytoplankton. Journal of Plankton Research, 2002, 200224(5), 417-428. http://dx.doi.org/10.1093/plankt/24.5.417.

SAITO, V.S., SIQUEIRA, T. and FONSECA-GESSNER, A.A. Should phylogenetic and functional diversity metrics compose macroinvertebrate multimetric indices for stream biomonitoring? Hydrobiologia, 2015a, 745(1), 167-179. http://dx.doi.org/10.1007/s10750-014-2102-3.

SAITO, V.S., SOININEN, J., FONSECA-GESSNER, A.A. and SIQUEIRA, T. Dispersal traits drive the phylogenetic distance decay of similarity in neotropical stream metacommunities. Journal of Biogeography, 2015b, 42(11), 2101-2111. http://dx.doi.org/10.1111/jbi.12577.

SENSOLO, D., HEPP, L.U., DECIAN, V. and RESTELLO, R.M. Influence of landscape on assemblages of Chironomidae in Neotropical streams. International Journal of Limnology, 2012, 48(4), 391-400. http://dx.doi.org/10.1051/limn/2012031.

SHIMANO, Y., JUEN, L., SALLES, F.F., NOGUEIRA, D.S. and CABETTE, H.S.R. Environmental and spatial processes determining Ephemeroptera (Insecta) structures in tropical streams. Annales de Limnologie - International. Journal of Limnology, 2013, 49(1), 31-41. http://dx.doi.org/10.1051/limn/2013036.

SHURIN, J.B., COTTENIE, K. and HILLEBRAND, H. Spatial autocorrelation and dispersal limitation in freshwater organisms. Oecologia, 2009, 159(1), 151-159. http://dx.doi.org/10.1007/s00442-008-1174-z. PMid:18941791.

SIQUEIRA, T., BINI, L.M., ROQUE, F.O. and COTTENIE, K. A metacommunity framework for enhancing the effectiveness of biological monitoring strategies. PLoS One, 2012, 7(8), e43626. http://dx.doi.org/10.1371/journal.pone.0043626. PMid:22937068.

SPRINGER, M. Capítulo 7 Trichoptera. Revista de Biología Tropical, 2010, 58(4), 151-198.

STRAHLER, A.N. Quantitative analysis of watershed geomorphology. Transactions - American Geophysical Union, 1957, 38(6), 913-920. http://dx.doi.org/10.1029/TR038i006p00913.

TER BRAAK, C.A.J.O.J.F. and PRENTICE, C.I. A theory of gradient analysis. Advances in Ecological Research, 1988, 18, 271-317. http://dx.doi.org/10.1016/S0065-2504(08)60183-X.

TOBLER, W. A computer movie simulating urban growth in the Detroit region. Economic Geography, 1970, 46, 234-240. http://dx.doi.org/10.2307/143141.

TONKIN, J.D., ALTERMATT, F., FINN, D.S., HEINO, J., OLDEN, J.D., PAULS, S.U. and LYTLE, D.A. The role of dispersal in river network metacommunities: patterns, processes, and pathways. Freshwater Biology, 2017a, 63(1), 141-163. http://dx.doi.org/10.1111/fwb.13037.

TONKIN, J.D., HEINO, J. and ALTERMATT, F. Metacommunities in river networks: the importance of network structure and connectivity on patterns and processes. Freshwater Biology, 2017b, 63(1), 1-5. http://dx.doi.org/10.1111/fwb.13045.

TRIVINHO-STRIXINO, S. Larvas de Chironomidae: guia de identificação [online]. São Carlos UFSCar, 2011 [viewed 18 June 2017]. Available from: https://sites.google.com/site/brazilianchironomids/keys2/trivinhostrixino2011

VANNOTE, R.L., MINSHALL, G.W., CUMMINS, K.W., SEDELL, J.R. and CUSHING, C.E. The River Continuum Concept. Canadian Journal of Fisheries and Aquatic Sciences, 1980, 37(1), 130-137. http://dx.doi.org/10.1139/f80-017.

WETZEL, R.G. and LIKENS, G.E. Limnological analyses. New York: Springer, 2000. http://dx.doi.org/10.1007/978-1-4757-3250-4.
 


Submitted date:
02/01/2019

Accepted date:
06/16/2020

Publication date:
08/03/2020

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