Abstract
Dung beetles present a high specificity degree to certain habitat types and they are widely used as bioindicators of environmental changes. Pitfall traps usually baited with human feces are the main method for collecting these insects. However, despite dung beetles being good flyers and actively move in the environment, collections with flight intercept traps have been little used in inventories of these insects in the wild. The fact that the intercept trap usually does not use any attractants, randomly capturing individuals can minimize sampling artifacts related with bait, light or other attractive methods. Here, we use flight intercept traps to analyze the dung beetle assemblages in different habitats in the Amazon rainforest. Dung beetles were sampled weekly from March 2017 to February 2018 in an Amazon forest fragment under anthropic pressure, cupuaçu orchard, and exotic pasture in Porto Velho, Rondônia, Brazil. A total of 1041 individuals belonging to 35 species of dung beetles were collected. The species accumulation curve showed no significant difference in the number of species among the three different habitats. The dung beetle species composition found in the forest fragment and cupuaçu orchard was similar, but the community of these two habitats was different from the exotic pasture. Our study provides a list of dung beetle species sampled using a method that is still little used in ecological studies using dung beetles as a study model. Finally, the flight intercept trap is a useful tool for dung beetle inventories in different habitats in the Amazon rainforest.
References
Abot AR, Puker A, Taira TL, Rodrigues SR, Korasaki V, Oliveira HN (2012) Abundance and diversity of coprophagous beetles (Coleoptera: Scarabaeidae) caught with a light trap in a pasture area of the Brazilian Cerrado. Stud Neotropical Fauna Environ 47:53–60. https://doi.org/10.1080/01650521.2012.662846
Almeida LM, Ribeiro-Costa CS, Marinoni L (2012) Coleta, montagem, preservação e métodos para estudo. In: Rafael JA, Melo GAR, Carvalho CJB, Casari AS, Constantino R (eds) Insetos do Brasil: diversidade e taxonomia. Holos, Ribeirão Preto, pp 176–190
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2
Andrade RB, Barlow J, Louzada J, Vaz-de-Mello FZ, Souza M, Silveira JM, Cochrane MA (2011) Quantifying responses of dung beetles to fire disturbance in tropical forests: the importance of trapping method and seasonality. PLoS One 6:e26208. https://doi.org/10.1371/journal.pone.0026208
Audino LD, Silva PG, Nogueira JM, Moraes LP, Vaz-de-Mello FZ (2011) Scarabaeinae (Coleoptera, Scarabaeidae) de um bosque de eucalipto introduzido em uma região originalmente campestre. Iheringia Ser Zool 101:121–126. https://doi.org/10.1590/S0073-47212011000100017
Campos WG, Pereira DBS, Schoereder JH (2000) Comparison of the efficiency of flight interception trap models for sampling Hymenoptera and other insects. An Soc Entomol Bras 29(3):381–389. https://doi.org/10.1590/S0301-80592000000300001
Carvalho de Santana EC, Pacheco TL, Vaz-de-Mello FZ (2019) Taxonomic revision of the Canthidium Erichson, 1847 species of the gigas group (Coleoptera, Scarabaeidae, Scarabaeinae). Eur J Taxon 530:1–24. https://doi.org/10.5852/ejt.2019.530
Castro DC (2017) Comunidade de Scarabaeinae (Coleoptera: Scarabaeidae) em sistemas agroflorestais na zona da mata rondoniense. Dissertation, Universidade Federal de Rondônia
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. https://doi.org/10.1890/13-0133.1
Clarke KR, Gorley RN (2006) Primer v6 Permanova+. Primer-E Ltd., Plymouth
Correa CMA, Puker A, Korasaki V, Ferreira KR, Abot AR (2016) The attractiveness of baits to dung beetles in Brazilian Cerrado and exotic pasturelands. Entomol Sci 19:112–123. https://doi.org/10.1111/ens.12169
Correa CMA, Braga RF, Puker A, Abot AR, Korasaki V (2018) Optimising methods for dung beetle (Coleoptera: Scarabaeidae) sampling in Brazilian pastures. Environ Entomol 47:48–54. https://doi.org/10.1093/ee/nvx191
Costa CMD, Silva FAB, Farias AI, Moura RC (2009) Diversidade de Scarabaeinae (Coleoptera, Scarabaeidae) coletados com armadilha de interceptação de vôo no Refúgio Ecológico Charles Darwin, Igarassu-PE, Brasil. Rev Bras Entomol 53:88–94. https://doi.org/10.1590/S0085-56262009000100021
Cupello M (2018) On the types species of the New World dung beetle genus Canthidium Erichson, 1847 (Coleoptera: Scarabaeidae: Scarabaeinae), with an annotated checklist of species. Zootaxa 4388:451–486. https://doi.org/10.11646/zootaxa.4388.4.1
da Silva PG, Hernández MIM (2015) Spatial patterns of movement of dung beetle species in a tropical forest suggest a new trap spacing for dung beetle biodiversity studies. PLoS One 10:e0126112. https://doi.org/10.1371/journal.pone.0126112
da Silva PG, Audino LD, Nogueira JM, Moraes LP, Vaz-de-Mello FZ (2012) Escarabeíneos (Coleoptera: Scarabaeidae: Scarabaeinae) de uma área de campo nativo no bioma Pampa, Rio Grande do Sul, Brasil. Biota Neotrop 12:246–253. https://doi.org/10.1590/S1676-06032012000300024
Davis AJ, Holloway JD, Huijbregts H, Krikken J, Kirk-Spriggs AH, Sutton SL (2001) Dung beetles as indicators of change in the forests of northern Borneo. J Appl Ecol 38:593–616. https://doi.org/10.1046/j.1365-2664.2001.00619.x
Escobar F, Halffter G, Arellano L (2007) From forest to pasture: an evaluation of the influence of environment and biogeography on the structure of dung beetle (Scarabaeinae) assemblages along three altitudinal gradients in the Neotropical region. Ecography 30:193–208. https://doi.org/10.1111/j.0906-7590.2007.04818.x
França F, Louzada J, Korasaki V, Griffiths H, Silveira JM, Barlow J (2016) Do space-for-time assessments underestimate the impacts of logging on tropical biodiversity? An Amazonian case study using dung beetles. J Appl Ecol 53:1098–1105. https://doi.org/10.1111/1365-2664.12657
Gardner TA, Barlow J, Araujo IS, Ávila-Pires TC, Bonaldo AB, Costa JE et al (2008) The cost-effectiveness of biodiversity surveys in tropical forests. Ecol Lett 11:139–150. https://doi.org/10.1111/j.1461-0248.2007.01133.x
Génier F, Arnaud P (2016) Dendropaemon Perty, 1830: taxonomy, systematics and phylogeny of the morphologically most derived phanaeine genus (Coleoptera: Scarabaeidae, Scarabaeinae, Phanaeini). Zootaxa 4099:1–125. https://doi.org/10.11646/zootaxa.4099.1.1
Génier F, Cupello M (2018) Canthidium alvarezi Martínez and Halffter, 1986: a remarkable Ateuchus Weber, 1801 (Coleoptera: Scarabaeidae: Scarabaeinae). Insecta Mundi 646:1–4
Gerlach J, Samways M, Pryke J (2013) Terrestrial invertebrates as bioindicators: an overview of available taxonomic groups. J Insect Conserv 17:831–850. https://doi.org/10.1007/s10841-013-9565-9
Halffter G, Favila ME (1993) The Scarabaeinae (Insecta: Coleoptera) an animal group for analyzing, inventorying and monitoring biodiversity in tropical rain forest and modified landscapes. Biol Int 27:15–23
Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomol Mex 12–14:1–312
Hanski I, Cambefort Y (1991) Dung beetle ecology. Princeton University Press, Princeton
Hsieh TC, Ma KH, Chao A (2013) iNEXT online: interpolation and extrapolation. (version 1.0) [software]. http://chao.stat.nthu.edu.tw/blog/softwaredownload/. Accessed 30 November 2019
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613
Korasaki V, Vaz-de-Mello FZ, Braga RF, Zanetti R, Louzada J (2012) Taxocenose de Scarabaeinae (Coleoptera: Scarabaeidae) em Benjamin Constant, AM. Acta Amaz 42:423–432. https://doi.org/10.1590/S0044-59672012000300015
Korasaki V, Braga RF, Zanetti R, Moreira FMS, Vaz-de-Mello FZ, Louzada J (2013) Conservation value of alternative land-use systems for dung beetles in Amazon: valuing traditional farming practices. Biodivers Conserv 22:1485–1499. https://doi.org/10.1007/s10531-013-0487-3
Louzada J, Gardner T, Peres C, Barlow J (2010) A multi-taxa assessment of nestedness patterns across a multiple-use Amazonian forest landscape. Biol Conserv 143:1102–1109. https://doi.org/10.1016/j.biocon.2010.02.003
Marsh CJ, Louzada J, Beiroz W, Ewers RM (2013) Optimising bait for pitfall trapping of Amazonian dung beetles (Coleoptera: Scarabaeinae). PLoS One 8:e73147. https://doi.org/10.1371/journal.pone.0073147
McGeoch MA, van Rensburg BJ, Botes A (2002) The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. J Appl Ecol 39:661–672. https://doi.org/10.1046/j.1365-2664.2002.00743.x
Milhomem MS, Vaz-de-Mello FZ, Diniz IR (2003) Técnicas de coleta de besouros copronecrófagos no Cerrado. Pesqu Agropecu Bras 38:1249–1256. https://doi.org/10.1590/S0100-204X2003001100001
Navarrete D, Halffter G (2008) Dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) diversity in continous forest, forest fragments and cattle pastures in a landscape of Chiapas, México: the effects of anthropogenic changes. Biodivers Conserv 17:2869–2898. https://doi.org/10.1007/s10531-008-9402-8
Nichols E, Larsen T, Spector S, Davis AL, Escobar F, Favila M, Vulinec K (2007) Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biol Conserv 137:1–19. https://doi.org/10.1016/j.biocon.2007.01.023
Nichols E, Spector S, Larsen J, Amezquita S, Favila ME (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474. https://doi.org/10.1016/j.biocon.2008.04.011
Philips TK (2011) The evolutionary history and diversification of dung beetles. In: Simmons LW, Ridsdill-Smith TJ (eds) Ecology and evolution of dung beetles. John Wiley & Sons, Chichester, pp 21–45
Quintero I, Halffter G (2009) Temporal changes in a community of dung beetles (Insecta: Coleoptera: Scarabaeinae) resulting from the modification and fragmentation of tropical rain forest. Acta Zool Mex 25:625–649
Ratcliffe BC (2013) The dung and carrion-feeding scarabs (Coleoptera: Scarabaeoidea) of an Amazonian Blackwater rainforest: results of a continuous 56-week, baited-pitfall trap study. Coleopt Bull 67:481–520. https://doi.org/10.1649/0010-065X-67.4.481
Rodrigues SR, Barros ATM, Puker A, Taira TL (2010) Diversidade de besouros coprófagos (Coleoptera, Scarabaeidae) coletados com armadilha de interceptação de voo no Pantanal Sul-Mato-Grossense, Brasil. Biota Neotrop 10:123–127. https://doi.org/10.1590/S1676-06032010000200015
Scheffler PY (2005) Dung beetles (Coleoptera: Scarabaeidae) diversity and community structure across three disturbance regimes in eastern Amazonia. J Trop Ecol 21:9–19. https://doi.org/10.1017/S0266467404001683
Schoolmeesters P (2020) Scarabs: World Scarabaeidae Database (version Jan 2019). In: Roskov Y, Ower G, Orrell T, Nicolson D, Bailly N, Kirk PM, Bourgoin T, DeWalt RE, Decock W, Nieukerken E van, Zarucchi J, Penev L (eds) Species 2000 & ITIS Catalogue of Life, 2019 Annual Checklist. www.catalogueoflife.org/annual-checklist/2019. Species 2000: Naturalis, Leiden, The Netherlands. Accessed 18 February 2020
Silva RJ, Coletti F, Costa DA, Vaz-de-Mello FZ (2014) Rola-bostas (Coleoptera: Scarabaeidae: Scarabaeinae) de florestas e pastagens no sudoeste da Amazônia brasileira: levantamento de espécies e guildas alimentares. Acta Amaz 44:345–352. https://doi.org/10.1590/1809-4392201304472
Tarasov S, Dimitrov D (2016) Multigene phylogenetic analysis redefines dung beetles relationships and classification (Coleoptera: Scarabaeidae: Scarabaeinae). BMC Evol Biol 16:257–219. https://doi.org/10.1186/s12862-016-0822-x
Tarasov S, Génier F (2015) Innovative bayesian and parsimony phylogeny of dung beetles (Coleoptera, Scarabaeidae, Scarabaeinae) enhanced by ontology-based partitioning of morphological characters. PLoS One 10(3):e0116671. https://doi.org/10.1371/journal.pone.0116671
Tejas G, Souza RMS, Franca RR, Nunes DD (2012) Estudo da variabilidade climática em Porto Velho/RO-Brasil no período de 1982 a 2011. Rev Geogr (UFPE) 29:63–82
Touroult J, Dalens P-H, Giuglaris J-L, Lapèze J, Boilly O (2017) Structure des communautés de Phanaeini (Coleoptera: Scarabaeidae) de Guyane: étude par échantillonnage massif au piège d’interception. Ann Soc Entomol Fr (NS) 53:143–161. https://doi.org/10.1080/00379271.2017.1319294
Vaz-de-Mello FZ (2007) Revision and phylogeny of the dung beetle genus Zonocopris arrow 1932 (Coleoptera: Scarabaeidae: Scarabaeinae), a phoretic of land snails. Ann Soc Entomol Fr (NS) 43:231–239. https://doi.org/10.1080/00379271.2007.10697516
Vaz-de-Mello FZ (2019) Scarabaeinae in Catálogo Taxonômico da Fauna do Brasil. PNUD. http://fauna.jbrj.gov.br/fauna/faunadobrasil/127498. Accessed 30 November 2019
Vaz-de-Mello FZ, Génier F (2009) Notes on the behavior of Dendropaemon Perty and Tetramereia Klages (Scarabaeidae: Scarabaeinae: Phanaeini). Coleopt Bull 63:364–366. https://doi.org/10.1649/1191.1
Vaz-de-Mello FZ, Edmonds WD, Ocampo FC, Schoolmeesters P (2011) A multilingual key to the genera and subgenera of the subfamily Scarabaeinae of the New World (Coleoptera: Scarabaeidae). Zootaxa 2854:1–73. https://doi.org/10.11646/zootaxa.2854.1.1
Acknowledgements
This paper is part of the monograph of KKGS and DCS presented in the Agronomy Course of the Faculdades Integradas Aparício Carvalho (FIMCA), Porto Velho, Rondônia, Brazil. CMAC received a PhD scholarschip from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) (140741/2015-1) from the Entomology Graduate Program, Universidade Federal de Lavras, and PhD sandwich scholarship from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) (88881.134292/2016-01). FZVM was supported by CNPq (248299/2012-3, 302997/2013-0, 484035/2013-4, 440604/2015-0, 306745/2016-0). We thank three anonymous reviewers for the fruitful comments on the manuscript.
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The experimentation was no invasive and complied with Brazilian law. At the end of the experiment, the specimens were deposited in the “Entomological Collection at the IFMT and in the “Entomological Section of the Zoological Collection at the UFMT (CEMT)” following standard procedures. There are no conflicts of interest (financial and non-financial) among authors.
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Puker, A., da Silva, K.K.G., dos Santos, D.C. et al. Dung beetles collected using flight intercept traps in an Amazon rainforest fragment and adjacent agroecosystems. Int J Trop Insect Sci 40, 1085–1092 (2020). https://doi.org/10.1007/s42690-020-00132-9
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DOI: https://doi.org/10.1007/s42690-020-00132-9