Abstract
Silviculture can be considered a sustainable alternative to the extraction of wood from natural forests in Brazil. However, the high demand for wood products has decreased the area of natural Cerrado due to land transformation for forestry activities. This transformation could lead to the loss of species, including insects that cannot tolerate the new environment dominated by exotic plant species. This study aims to evaluate whether the presence of an extensive Eucalyptus silviculture in the Brazilian Cerrado decreases the integrity of nearby riparian environments and, consequently, decreases odonate diversity. Thirteen ponds were selected in patches of Cerrado embedded within a matrix of Eucalyptus silviculture in order to assess habitat integrity of ponds and their riparian zones and collect adult odonates. The physical integrity of the study sites was measured using a Habitat Integrity Index (HII) designed to determine the degree of conservation of aquatic environments. The HII of the study sites varied between 0.44 and 0.80, indicating differences in the degree of conservation. Therefore, a positive relationship was found between odonate richness and abundance and HII, and between the abundance of zygopterans and anisopterans and HII. These findings may be due to the fact that these insects are adapted to the natural resources maintained at the most conserved habitats, and which were lost in degraded riparian zones, such as the presence of aquatic vegetation and a diversity of organic debris on pond banks. We conclude that the conversion of natural areas to Eucalyptus silviculture can alter the integrity of nearby riparian zones and, consequently, odonate diversity.
Graphical abstract
Similar content being viewed by others
References
Allan, J. D. (2004). Landscapes and riverscapes: the influence of land use on stream ecosystems. Annual Review of Ecology, Evolution, and Systematics, 35, 257–284. https://doi.org/10.1146/annurev.ecolsys.35.120202.110122.
Allan, D., Erickson, D., & Fay, J. (1997). The influence of catchment land use onstream integrity across multiple spatial scales. Freshwater Biology, 37, 149–161. https://doi.org/10.1046/j.1365-2427.1997.d01-546.x.
Andow, D. A. (1991). Vegetational diversity and arthropod population response. Annual Review of Entomology, 36, 561–586. https://doi.org/10.1146/annurev.en.36.010191.003021.
Banks-Leite, C., Ewers, R. M., & Metsger, J. P. (2012). Unraveling the drivers of community dissimilarity and species extinction in fragmented landscapes. Ecology, 93, 2560–2569. https://doi.org/10.1890/11-2054.1.
Benstead, J. P., & Pringle, C. M. (2004). Deforestation alters the resource base and biomass of endemic stream insects in eastern Madagascar. Freshwater Biology, 49, 490–501. https://doi.org/10.1111/j.1365-2427.2004.01203.x.
Benstead, J. P., Douglas, M. M., & Pringle, C. M. (2003). Relationships of stream invertebrate communities to deforestation in eastern Madagascar. Ecological Applications, 13, 1473–1490. https://doi.org/10.1890/02-5125.
Bragança, M. A. L., Zanuncio, J. C., Picanço, M., & Laranjeiro, A. J. (1998). Effects of environmental heterogeneity on Lepidoptera and Hymenopera populations in Eucalyptus plantations in Brazil. Forest Ecology and Management, 103, 287–292. https://doi.org/10.1016/S0378-1127(97)00226-0.
Brasil (2012). Lei Federal n° 12.651, de 25 de maio de 2012. Novo Código Florestal Brasileiro. http://www.planalto.gov.br/ccivil_03/_ato2011-2014/2012/lei/l12651.htm. Accessed 17 June 2019
Brasil, L. S., Shimano, Y., Batista, J. D., & Cabette, H. S. R. (2013). Effects of environmental factors on community structure of Leptophlebiidae (Insecta, Ephemeroptera) in Cerrado streams, Brazil. Iheringia, 103, 260–265. https://doi.org/10.1590/S0073-47212013000300008.
Brasil, L. S., Lima, E. L., Spigoloni, Z. A., Ribeiro-Brasil, D. R. G., & Juen, L. (2020). The habitat integrity index and the aquatic insects communities in tropical streams: a meta-analysis. Ecological Indicators, 116, 106495. https://doi.org/10.1016/j.ecolind.2020.106495.
Buss, D. F., Baptista, D. F., Nessimian, J. L., & Egler, M. (2004). Substrate specificity, environmental degradation and disturbance structuring macroinvertebrate assemblages in neotropical streams. Hydrobiologia, 518, 179–188. https://doi.org/10.1023/B:HYDR.0000025067.66126.1c.
Byers, J. E., Cuddington, K., Jones, C. G., Talley, T. S., Hastings, A., Lambrinos, J. G., Crooks, J. A., & Wilson, W. G. (2006). Using ecosystem engineers to restore ecological systems. Trends in Ecology & Evolution, 21, 493–500. https://doi.org/10.1016/j.tree.2006.06.002.
Carvalho, F. G., Pinto, N. S., Oliveira-Junior, J. M. B., & Juen, L. (2013). Effects of marginal vegetation removal on Odonata communities. Acta Limnologica Brasiliensia, 25, 10–18. https://doi.org/10.1590/S2179-975X2013005000013.
Carvalho, F. G., Roque, F. O., Barbosa, L., Montag, L. F. A., & Juen, L. (2018). Oil palm plantation is not a suitable environment for most forest specialist species of Odonata in Amazonia. Animal Conservation, 21, 526–533. https://doi.org/10.1111/acv.12427.
Conrad, K. F., & Pritchard, G. (1992). An ecological classification of odonate mating systems: the relative influence of natural, inter- and intra-sexual selection on males. Biological Journal of the Linnean Society London, 45, 255–269. https://doi.org/10.1111/j.1095-8312.1992.tb00643.x.
Costa, J. M., Lourenço, A. N., Vieira, L. P. (2002) Micrathyria pseudhypodidyma sp.n. (Odonata: Libellulidae), com chave das espécies do gênero que ocorrem no estado do Rio de Janeiro.
Couceiro, S. R. M., Hamada, N., Luz, S. L. B., Fosberg, B. R., & Pimentel, T. P. (2007). Deforestation and sewage effects on aquatic macroinvertebrates in urban streams in Manaus, Amazonas, Brazil. Hydrobiologia, 575, 271–284. https://doi.org/10.1007/s10750-006-0373-z.
Davidson, E. A., Neill, C., Krusche, A. V., Ballester, V. V. R., Markewitz, D., & Figueiredo, R. O. (2004). Loss of nutrients from terrestrial ecosystems to streams and the atmosphere following land use change in Amazonia. In R. S. Defries, G. P. Asner, & R. A. Houghton (Eds.), Ecosystems and land use change (pp. 147–158). Washington: American Geophysical Union. https://doi.org/10.1029/153GM12.
De Marco Jr, P., Batista, J. D., & Cabette, H. S. R. (2015). Community assembly of adult odonates in tropical streams: an ecophysiological hypothesis. PLoS One, 10, 1–17. https://doi.org/10.1371/journal.pone.0123023.
Delong, M. D., & Brusven, M. A. (1994). Allochthonous input of organic matter from different riparian habitats of an agriculturally impacted stream. Environmental Management, 18, 59–71. https://doi.org/10.1007/BF02393750.
Dias-Silva, K., Cabette, H. S. R., Juen, L., & De Marco Jr, P. (2010). The influence of habitat integrity and physical-chemical water variables on the structure of aquatic and semi-aquatic Heteroptera. Zoologia, 27, 918–930. https://doi.org/10.1590/S1984-46702010000600013.
Estavillo, C., Pardini, R., & Rocha, P. L. B. (2013). Forest loss and the biodiversity threshold: an evaluation considering species habitat requirements and the use of matrix habitats. PLoS One, 8, 1–10. https://doi.org/10.1371/journal.pone.0082369.
Ferraz, S. F. B., Rodrigues, C. B., Garcia, L. G., Alvares, C. A., & Lima, W. P. (2019). Effects of Eucalyptus plantations on streamflow in Brazil: moving beyond the water use debate. Forest Ecology and Management, 453, 117571. https://doi.org/10.1016/j.foreco.2019.117571.
Ferreira, V., Koricheva, J., Pozo, J., & Graça, M. A. S. (2016). A meta-analysis on the effects of changes in the composition of native forests on litter decomposition in streams. Forest Ecology and Management, 364, 27–38. https://doi.org/10.1016/j.foreco.2016.01.002.
Fincke, O. M. (1992). Consequences of larval ecology for territoriality and reproductive success of a Neotropical damselfly. Ecology, 73, 449–462. https://doi.org/10.2307/1940752.
Garrison, R. W., von Ellenrieder, N., & Louton, J. A. (2006). Dragonfly genera of the new world: an illustrated and annotated key to the Anisoptera. Baltimore: The Johns Hopkins University Press.
Garrison, R. W., von Ellenrieder, N., & Louton, J. A. (2010). Damselfly genera of the new world: an illustrated and annotated key to the Zygoptera. Baltimore: The Johns Hopkins University Press.
Gonçalves, J. L. M., Stape, J. L., Laclau, J. P., Bouillet, J. P., & Ranger, J. (2008). Assessing the effects of early silvicultural management on long-term site productivity of fast growing eucalypt plantations: the Brazilian experience. Southern Forests: a Journal of Forest Science, 70, 105–118. https://doi.org/10.2989/SOUTH.FOR.2008.70.2.6.534.
Guillermo-Ferreira, R., & Del-Claro, K. (2011). Oviposition site selection in Oxyagrion microstigma Selys, 1876 (Odonata: Coenagrionidae) is related to aquatic vegetation structure. International Journal of Odonatology, 14, 275–279. https://doi.org/10.1080/13887890.2011.621109.
Hanski, I. (2011). Habitat loss, the dynamics of biodiversity, and a perspective on conservation. Ambio, 40, 248–255. https://doi.org/10.1007/s13280-011-0147-3.
Heino, J., & Grönroos, M. (2013). Does environmental heterogeneity affect species cooccurrence in ecological guilds across stream macroinvertebrate metacommunities? Ecography, 36, 926–936. https://doi.org/10.1111/j.1600-0587.2012.00057.x.
Hilbe, J. M. (2011). Negative Binomial Regression (2nd ed.). Cambridge: Cambridge University Press.
Holzman, R., Collar, D. C., Mehta, R. S., & Wainwright, P. C. (2011). Functional complexity can mitigate performance trade–offs. The American Naturalist, 177, 69–83. https://doi.org/10.1086/658366.
Hood, W. G., & Naiman, R. J. (2000). Vulnerability of riparian zones to invasion by exotic vascular plants. Plant Ecology, 148, 105–114. https://doi.org/10.1023/A:1009800327334.
IBA (2019). Indústria Brasileira de Árvores/Brazilian Tree Industry. Report 2019. https://www.iba.org/datafiles/publicacoes/relatorios/iba-relatorioanual2019.pdf Accessed 10 April 2020.
Johansson, F. (1991). Foraging modes in an assemblage of odonate larvae: effects of prey and interference. Hydrobiologia, 209, 79–87. https://doi.org/10.1007/BF00006721.
Kasangki, A., Chapman, L. J., & Balirwa, J. (2008). Land use and the ecology of benthic macroinvertebrate assemblages of high-altitude rainforest streams in Uganda. Freshwater Biology, 53, 681–697. https://doi.org/10.1111/j.1365-2427.2007.01925.x.
Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi
King, R. S., Baker, M. E., Kazyak, P. F., & Weller, D. E. (2011). How novel is too novel? Stream community thresholds at exceptionally low levels of catchment urbanization. Ecological Applications, 21, 1659–1678. https://doi.org/10.1890/10-1357.1.
Klecka, J., & Boukal, D. S. (2014). The effect of habitat structure on prey mortality depends on predator and prey microhabitat use. Oecologia, 176, 183–119. https://doi.org/10.1007/s00442-014-3007-6.
Legendre, P., & Legendre, L. (1998). Numerical Ecology (2nd ed.). Elsevier.
Lencioni, F. A. A. (2005). Damselflies of Brazil, an illustrated indentification guide: I - Noncoenagrionidae families. São Paulo: All Print.
Lencioni, F. A. A. (2006). Damselflies of Brazil, an illustrated indentification guide: II - Coenagrionidae families. São Paulo: All Print.
Lencioni, F. A. A. (2017). Damselflies of Brazil - an illustrated identification guide - Southeast region. Jacareí: Author e-book.
Lima, M. M., & Mariano-Neto, E. (2014). Extinction thresholds for Sapotaceae due to forest cover in Atlantic forest landscapes. Forest Ecology and Management, 312, 260–270. https://doi.org/10.1016/j.foreco.2013.09.003.
Marsden, S. J., Whiffin, M., & Galetti, M. (2001). Bird diversity and abundance in forest fragments and Eucalyptus plantations around an Atlantic forest reserve, Brazil. Biodiversity and Conservation, 10, 737–751. https://doi.org/10.1023/A:1016669118956.
McClain, M. E., & Elsenbeer, H. (2001). Terrestrial inputs to Amazon streams and internal biogeochemical processing. In M. E. McClain, E. Victoria, & J. Rishey (Eds.), The biogeochemistry of the Amazon Basin (pp. 185–207). Oxford: Oxford University Press.
Mendes L (2016) Brazilian Forestry and Timber Yearbook. Ed. Gazeta, Santa Cruz do Sul.
Merilaita, S. (2003). Visual background complexity facilitates the evolution of camouflage. Evolution, 57, 1248–1254. https://doi.org/10.1111/j.0014-3820.2003.tb00333.x.
Monteiro-Junior, C. S., Couceiro, S. R. M., Hamada, N., & Juen, L. (2013). Effect of vegetation removal for road building on richness and composition of Odonata communities in Amazonia, Brazil. International Journal of Odonatology, 16, 135–144. https://doi.org/10.1080/13887890.2013.764798.
Monteiro-Junior, C. S., Juen, L., & Hamada, N. (2014). Effects of urbanization on stream habitats and associated adult dragonfly and damselfly communities in central Brazilian Amazonia. Landscape and Urban Planning, 127, 28–40. https://doi.org/10.1016/j.landurbplan.2014.03.006.
Monteiro-Junior, C. S., Juen, L., & Hamada, N. (2015). Analysis of urban impacts on aquatic habitats in the central Amazon Basin: adult odonates as bioindicators of environmental quality. Ecological Indicators, 48, 303–311. https://doi.org/10.1016/j.ecolind.2014.08.021.
Moretti, M. S., Becker, B., Kiffer Jr., W. P., Penha, L. O., & Callisto, M. (2020). Eucalyptus leaves are preferred to cerrado native species but do not constitute a better food resource to stream shredders. Journal of Arid Environments, 181, 104221. https://doi.org/10.1016/j.jaridenv.2020.104221.
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858. https://doi.org/10.1038/35002501.
Nessimian, J. L., Venticinque, E. M., Zuanon, J., De Marco Jr, P., Gordo, M., Fidelis, L., Batista, J. D., & Juen, L. (2008). Land use, habitat integrity, and aquatic insect assemblages in Central Amazonian streams. Hydrobiologia, 614, 117–131. https://doi.org/10.1007/s10750-008-9441-x.
Ochoa-Quintero, J. M., Gardner, T. A., Rosa, I., Ferraz, S. F. B., & Sutherland, J. W. (2015). Thresholds of species loss in Amazonian deforestation frontier landscapes. Conservation Biology, 29, 440–451. https://doi.org/10.1111/cobi.12446.
Oliveira-Junior, J. M. B., De Marco Jr, P., Dias-Silva, K., Leitão, R. P., Leal, C. G., Pompeu, P. S., Gardner, T. A., Hughes, R. M., & Juen, L. (2017). Effects of human disturbance and riparian conditions on Odonata (Insecta) assemblages in eastern Amazon basin streams. Limnologica, 66, 31–39. https://doi.org/10.1016/j.limno.2017.04.007.
Ometto, J. P. H. B., Martinelli, L. A., Ballester, M. V., Gessner, A., Krusche, A. V., Victoria, R. L., & Williams, M. (2000). Effects of land use and water chemistry and macroinvertebrates in two streams of the Piracicaba river basin, south-east Brazil. Freshwater Biology, 44, 327–337. https://doi.org/10.1046/j.1365-2427.2000.00557.x.
Pereira, L. R., Cabette, H. S. R., & Juen, L. (2012). Trichoptera as bioindicators of habitat integrity in the Pindaíba River basin, Mato Grosso (Central Brazil). Annales de Limnologie - International Journal of Limnology, 48, 295–302. https://doi.org/10.1051/limn/2012018.
Petersen Jr., R. C. (1992). The RCE: A riparian, channel, and environmental inventory for small streams in agricultural landscape. Freshwater Biology, 27, 295–306. https://doi.org/10.1111/j.1365-2427.1992.tb00541.x.
Petersen, I., Masters, Z., Hildrew, A. G., & Ormerod, S. J. (2004). Dispersal of adult aquatic insects in catchments of differing land use. Journal of Applied Ecology, 41, 934–950. https://doi.org/10.1111/j.0021-8901.2004.00942.x.
Popielarz, P. A., & Neal, Z. P. (2007). The niche as a theoretical tool. Annual Review of Sociology, 33, 65–84. https://doi.org/10.1146/annurev.soc.32.061604.123118.
Pozo, J., González, E., Díez, J. R., Molinero, J., & Elósegui, A. (1997). Inputs of particulate organic matter to streams with different riparian vegetation. Journal of the North American Benthological Society, 16, 602–611. https://doi.org/10.2307/1468147.
Quinn, G. P., & Keought, M. J. (2002). Experimental design and data analysis for biologists. Cambridge: Cambridge University Press. https://doi.org/10.1017/CBO9780511806384.
R Core Team. (2017). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing https://www.R-project.org.
Raebel, E. M., Merckx, T., Feber, R. E., Riordan, P., Thompson, D. J., & Macdonald, D. W. (2012). Multi-scale effects of farmland management on dragonfly and damselfly assemblages of farmland ponds. Agriculture, Ecosystems and Environment, 161, 80–87. https://doi.org/10.1016/j.agee.2012.07.015.
Rodrigues, M. E., Roque, F. O., Quintero, J. M. O., Pena, J. C. C., Souza, D. C., & De Marco Jr, P. (2016). Nonlinear responses in damselfly community along a gradient of habitat loss in a savanna landscape. Biological Conservation, 194, 113–120. https://doi.org/10.1016/j.biocon.2015.12.001.
Rodrigues, L. C., Correa, F. S., Juen, L., & Santos-Costa, M. C. (2018). Effects of pond structural complexity on the reproduction of Physalaemus ephippifer (Anura, Leptodactylidae). Animal Biology, 68, 405–415. https://doi.org/10.1163/15707563-17000152.
Sanderson, R. A., Eyre, M. D., & Rushton, S. P. (2005). The influence of stream invertebrate composition at neighbouring sites on local assemblage composition. Freshwater Biology, 50, 221–231. https://doi.org/10.1111/j.1365-2427.2004.01313.x.
Silva, D. P., De Marco Jr, P., & Resende, D. C. (2010). Adult odonate abundance and community assemblage measures as indicators of stream ecological integrity: a case study. Ecological Indicators, 10, 744–752. https://doi.org/10.1016/j.ecolind.2009.12.004.
Simaika, J. P., & Samways, M. J. (2009). Reserve selection using red listed taxa in three global biodiversity hotspots: dragonflies in South Africa. Biological Conservation, 142, 638–651. https://doi.org/10.1016/j.biocon.2008.11.012.
Smethurst, P. J., Almeida, A. C., & Loos, R. A. (2015). Stream flow unaffected by Eucalyptus plantation harvesting implicates water use by the native forest streamside reserve. Journal of Hydrology, 3, 187–198. https://doi.org/10.1016/j.ejrh.2014.11.002.
Strassburg, B., Brooks, T., Feltran-Barbieri, R., Iribarrem, A., Crouzeilles, R., Loyola, R., Latawiec, A. E., Oliveira Filho, F. J. B., Scaramuzza, C. A. M., Scarano, F. R., Soares-Filho, B., & Balmford, A. (2017). Moment of truth for the Cerrado hotspot. Nature Ecology and Evolution, 1, 1–3. https://doi.org/10.1038/s41559-017-0099.
Thomas, C. D. (1991). Habitat use and geographic ranges of butterflies from the lowlands of Costa Rica. Biological Conservation, 55, 269–281. https://doi.org/10.1016/0006-3207(91)90032-5.
Turner, I. M. (1996). Species loss in fragments of tropical rain forest: a review of evidence. Journal of Applied Ecology, 33, 200–209. https://doi.org/10.2307/2404743.
Valente-Neto, F., Koroiva, R., Fonseca-Gessner, A. A., & Roque, F. O. (2015). The effect of riparian deforestation on macroinvertebrates associated with submerged woody debris. Aquatic Ecology, 49, 115–125. https://doi.org/10.1007/s10452-015-9510-y.
Vilela, D. S., Guillermo-Ferreira, R., & Del-Claro, K. (2016). The odonata community of a Brazilian vereda: seasonal patterns, species diversity and rarity in a palm swamp environment. Bioscience Journal, 32, 486–495. https://doi.org/10.14393/BJ-v32n2a2016-30491.
Vilela, D. S., Tosta, T. A., Rodrigues, R. R., Del-Claro, K., & Guillermo-Ferreira, R. (2017). Colours of war: visual signals may influence the outcome of territorial contests in the tiger damselfly, Tigriagrion aurantinigrum. Biological Journal of the Linnean Society London, 121, 786–795. https://doi.org/10.1093/biolinnean/blx024.
von Ellenrieder, N. (2009). Five new species of Orthemis from South America (Odonata: Libellulidae). International Journal of Odonatology, 12, 347–381. https://doi.org/10.1080/13887890.2009.9748351.
Wildermuth, H. (2010). Monitoring the effects of conservation actions in agricultural and urbanized landscapes - also useful for assessing climate change? BioRisk, 5, 175–192. https://doi.org/10.3897/biorisk.5.848.
Willson, M. F., DeSanto, T. L., Sabag, C., & Armesto, J. J. (1994). Avian communities of fragmented southtemperate rainforests in Chile. Conservation Biology, 8, 508–520. https://doi.org/10.1046/j.1523-1739.1994.08020508.x.
Woodkock, T. S., & Huryn, A. (2007). The response of macroinvertebrate production to a pollution gradient in a headwater stream. Freshwater Biology, 52, 77–196. https://doi.org/10.1111/j.1365-2427.2006.01676.x.
Acknowledgments
We express our gratitude to company personal who permitted access to the farm and provided maps and protection equipment, thereby making our fieldwork possible. The work was also supported by: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) through a Master’s fellowship to the first author and to J.C. Santos (CNPq 312752/2018-0); PRONEX (Centers of Excellence Program) through financial support; Programa de Pós-graduação em Ecologia e Conservação de Recursos Naturais (PPGECRN) and Universidade Federal de Uberlândia (UFU), through additional funding and logistic support. We are grateful to DSV and FAAL for help with identifying specimens and providing information about them; personal from the Laboratório de Ecologia-Evolução & Biodiversidade at UFU for field and laboratorial support; and ICMBio for issuing the collection permit (Nr. 28398-1).
Funding
This work was funded partially by the DURATEX Company. The work was also supported by: Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) through a Master’s fellowship to the first author and to J.C. Santos (CNPq 312752/2018-0); PRONEX (Centers of Excellence Program) through financial support; and Universidade Federal de Uberlândia (UFU), through additional funding and logistic support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Borges, L.R., Barbosa, M.S., Carneiro, M.A.A. et al. Habitat integrity drives Odonata diversity in Eucalyptus-dominated landscape. Environ Monit Assess 193, 12 (2021). https://doi.org/10.1007/s10661-020-08740-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10661-020-08740-1