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Insights into dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) distribution along an elevational gradient in a tepui table-top mountain in the Brazilian Amazon

Published online by Cambridge University Press:  17 May 2023

Renato Portela Salomão
Affiliation:
Instituto Nacional de Pesquisas da Amazônia, Avenida André Araújo, 2936, CEP 69060-000, Manaus, Amazonas, Brazil Instituto de Ecología, Universidad Nacional Autónoma de México, Mexico City, Mexico
Bert Kohlmann
Affiliation:
BioAlfa Barcoding Project, Santo Domingo, Heredia, Costa Rica
Célio Vandré Raia Mendes
Affiliation:
Universidade Estadual da Paraíba, R. Baraúnas, 351, CEP 58429-500, Campina Grande, Paraíba, Brazil
Fernando Vaz-de-Mello
Affiliation:
Universidade Federal de Mato Grosso, Avenida Fernando Corrêa de Costa, 2367, CEP 78060-900, Cuiabá, Mato Grosso, Brazil
André Felipe Araujo Lira*
Affiliation:
Universidade Federal de Campina Grande, Sítio Olho D'água da Bica, Zona Rural, CEP 58175-000, Cuité, Paraíba, Brazil
*
Corresponding author: André Felipe Araujo Lira; Email: andref.lira@gmail.com

Abstract

Elevational gradients are excellent models to understand species distribution across sites with marked shifts in environmental conditions. In northern South America, tepuis are table-top mountains with elevations above 1000 m and high biodiversity and endemism levels. In this study, we assessed the effect of elevation on dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) assemblage structure (species richness, abundance, and biomass) in Tepequém, a tepui located in northern Brazil. Dung beetles were sampled with pitfall traps within seven elevational bands from 250 to 850 m. A total of 83 individuals from 14 species were collected, Oxysternon festivum (Linnaeus, 1758) and an unidentified Onthophagus species being the most abundant. Elevation did not affect beetle species richness and biomass. However, species composition from 750 to 850 m differed statistically from that recorded at lower elevations. Our results suggest that beetle assemblages possess a bimodal distribution along an altitudinal gradient on the Tepequém. The contrasting vegetation structure of tepuis between highlands (shrubland savannah vegetation) and lowlands (tropical rainforest) explains the different composition of the assemblages. This study should be considered as a starting point in improving our understanding of the dung beetle diversity of tepuis, which present a unique singular relationship between elevation and species diversity.

Type
Research Paper
Copyright
© The Author(s), 2023. Published by Cambridge University Press on behalf of The Entomological Society of Canada

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Footnotes

Subject Editor: Andrew Smith

References

Almeida-Filho, R. and Shimabukuro, Y.E. 2010. Detecting areas disturbed by gold mining activities through JERS-1 SAR images, Roraima State, Brazilian Amazon. International Journal of Remote Sensing, 21: 33573362.CrossRefGoogle Scholar
Alvarado, F., Escobar, F., and Montero-Muñoz, J. 2014. Diversity and biogeographical makeup of the dung beetle communities inhabiting two mountains in the Mexican Transition Zone. Organisms Diversity & Evolution, 14: 105114.CrossRefGoogle Scholar
Alvarado, F., Salomão, R.P., Hernández-Rivera, A., and Lira, A.F.A. 2020. Different responses of dung beetle diversity and feeding guilds from natural and disturbed habitats across a subtropical elevational gradient. Acta Oecologica, 104: 103533.CrossRefGoogle Scholar
Andrade, R.B., Barlow, J., Louzada, J., Vaz-de-Mello, F.Z., Silveira, J., and Cochrane, M.A. 2014. Tropical forest fires and biodiversity: dung beetle community and biomass responses in a northern Brazilian Amazon forest. Journal of Insect Conservation, 18: 10971104.CrossRefGoogle Scholar
Barbosa, R.I. and Miranda, I.S. 2004. Fitofisionomias e diversidade vegetal das savanas de Roraima [Phytophysiology from the vegetal diversity of the savannas of Roraima]. In Savanas de Roraima: etnoecologia, biodiversidade e potencialidades agrossilvipastoris [Savannas of Roraima: ethnoecology, biodiversity from the potentialities of agroforestry]. Edited by Barbosa, R.I., Xand, H.A.M., and Costa e Souza, E.M.. Fundação Estadual do Meio Ambiente e Recursos Hídricos, Boa Vista, Brazil. Pp. 6178.Google Scholar
Barbosa-Silva, R.G., Bueno, M.L., Labiak, P.H., Nadruz, M.A., Martinelli, C.G., and Forzza, R.C. 2020. The Pantepui in the Brazilian Amazon: vascular flora of Serra do Aracá, a cradle of diversity, richness and endemism. The Botanical Review, 86: 359375.CrossRefGoogle Scholar
Barraza, J.M., Montes, J.F., Martínez, N.H., and Deloya, C. 2010. Assemblage of coprophagous beetles (Scarabaeidae: Scarabaeinae) of tropical dry forest in Bahía Concha, Santa Marta (Colombia). Revista Colombiana de Entomología, 36: 285291.CrossRefGoogle Scholar
Barros, L.S., Melo, V.F., Senwo, Z.N., Evald, A., Siqueira, R.H.S., Bardales, R.M., and Nunes, T.K.O. 2018. Effects of management practices and land use on biological and enzymatic attributes of an agricultural area. Journal of Agricultural Science, 10: 110122.CrossRefGoogle Scholar
Berry, P.E. and Riina, R. 2005. Insights into the diversity of the Pantepui flora and the biogeographic complexity of the Guayana Shield. Biologiske Skrifter, 55: 145167.Google Scholar
Braga, R.F., Korasaki, V., Andresen, E., and Louzada, J. 2013. Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: a rapid assessment of ecological functions associated to biodiversity. PLOS One, 8: e57786.CrossRefGoogle ScholarPubMed
Campos, P.V., Schaefer, C.E.G.R., Pontara, V., Xavier, M.V.B., Júnior, J.F.V., Corrêa, G.R., and Villa, P.M. 2022. Local-scale environmental filtering shape plant taxonomic and phylogenetic diversity in an isolated Amazonian tepui (Tepequém table mountain). Evolutionary Ecology, 36: 5573.CrossRefGoogle Scholar
Cassenote, S., Valois, M.C., Maldaner, M.E., and Vaz-de-Mello, F.Z. 2020. Taxonomic revision of Dichotomius (Selenocopris) nisus (Olivier, 1719) and Dichotomius (Selenocopris) superbus (Felsche, 1901). Revista Brasileira de Entomologia, 64: 111.CrossRefGoogle Scholar
Celi, J., Terneus, E., Torres, J., and Ortega, M. 2004. Dung beetle (Coleoptera: Scarabaeinae) diversity in an altitudinal gradient in the Cutucú range, Morona Santiago, Ecuadorian Amazon. Lyonia, 7: 3752.Google Scholar
Chao, A. and Jost, L. 2012. Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology, 93: 25332547.CrossRefGoogle ScholarPubMed
Choo, J., Gill, B.D., Zuur, A.F., Zent, E., and Economo, E.P. 2019. Impacts of an Indigenous settlement on the taxonomic and functional structure of dung beetle communities in the Venezuelan Amazon. Biodiversity and Conservation, 29: 207228.CrossRefGoogle Scholar
Clarke, K.R. and Gorley, R.N. 2006. Primer v6: user manual/tutorial. Primer-e, Plymouth, United Kingdom.Google Scholar
Climate Data. 2023. Dados climáticos para cidades mundiais [Climate dice for world wars; online]. Available from https://pt.climate-data.org/search/?q=Amajari [accessed 7 February 2023].Google Scholar
Crawley, M. 2013. The R book. Second edition. Wiley & Sons, London, United Kingdom.Google Scholar
Cupello, M. and Vaz-de-Mello, F.Z. 2013. New evidence for the validity of Coprophanaeus (C.) terrali Arnaud, 2002 (Coleoptera: Scarabaeidae: Scarabaeinae: Phanaeini), a dung beetle from Brazil. Zootaxa, 3717: 359368.CrossRefGoogle ScholarPubMed
da Silva, P.G., Lobo, J.M., Hensen, M.C., Vaz-de-Mello, F.Z., and Hernández, M.I.M. 2018. Turnover and nestedness in subtropical dung beetle assemblages along an elevational gradient. Diversity and Distribution, 24: 12771290.CrossRefGoogle Scholar
Désamoré, A., Vanderpoorten, A., Laenen, B., Gradstein, S.R., and Kok, P.J.R. 2010. Biogeography of the Lost World (Pantepui region, northeastern South America): insights from bryophytes. Phytotaxa, 9: 254265.CrossRefGoogle Scholar
Edmonds, W.D. and Zidek, J. 2010. A taxonomic review of the Neotropical genus Coprophanaeus Olsoufieff, 1924 (Coleoptera: Scarabaeidae, Scarabaeinae). Insecta Mundi, 129: 1111.Google Scholar
Escobar, F., Halffter, G., and Arellano, L. 2007. From forest to pasture: an evaluation of the influence of environment and biogeography on the structure of beetle (Scarabaeinae) assemblages along three elevational gradients in the Neotropical region. Ecography, 30: 193208.CrossRefGoogle Scholar
Escobar, F., Lobo, J.M., and Halffter, G. 2005. Altitudinal variation of dung beetle (Scarabaeidae: Scarabaeinae) assemblages in the Colombian Andes. Global Ecology and Biogeography, 14: 327337.CrossRefGoogle Scholar
Espinoza, V.R. and Noriega, J.A. 2018. Diversity of the dung beetles (Coleoptera: Scarabaeinae) in an altitudinal gradient in the east slope of Los Andes, Napo Province, Ecuador. Neotropical Biodiversity, 4: 145151.CrossRefGoogle Scholar
Filgueiras, B.K.C., Iannuzzi, L., and Leal, I.R. 2011. Habitat fragmentation alters the structure of dung beetle communities in the Atlantic Forest. Biological Conservation, 144: 362369.CrossRefGoogle Scholar
Fletchmann, C.A.H., Tabet, V.G., and Quintero, I. 2009. Influence of carrion smell and rebaiting time on the efficiency of pitfall traps to dung beetle sampling. Entomologia Experimentalis et Applicata, 132: 211217.CrossRefGoogle Scholar
França, F.M., Korasaki, V., Louzada, J., and Vaz-de-Mello, F.Z. 2016. First report on dung beetles in intra-Amazonian savannahs in Roraima, Brazil. Biota Neotropica, 16: e0034.CrossRefGoogle Scholar
Génier, F. 2009. Le genre Eurysternus Dalman, 1824 (Scarabaeidae: Scarabaeinae: Oniticellini): révision taxonomique et clés de détermination illustrées [The genus Eurysternus Dalman, 1824 (Scarabaeidae: Scarabaeinae: Oniticellini): taxonomic revision and illustrated identification keys]. Pensoft, Sofia, Bulgaria.Google Scholar
Génier, F. and Cupello, M. 2018. Canthidium alvarezi Martínez and Halffter, 1986: a remarkable Ateuchus Weber, 1801 (Coleoptera: Scarabaeidae: Scarabaeinae). Insecta Mundi, 646: 14.Google Scholar
González-Alvarado, A. and Vaz-de-Mello, F.Z. 2014. Taxonomic review of the subgenus Hybomidium Shipp, 1897 (Coleoptera: Scarabaeidae: Scarabaeinae: Deltochilum). Annales de la Société Entomologique de France, 40: 431476.CrossRefGoogle Scholar
González-Alvarado, A. and Vaz-de-Mello, F.Z. 2021. Towards a comprehensive taxonomic revision of the Neotropical dung beetle subgenus, Deltochilum (Deltohyboma) Lane, 1946 (Coleoptera: Scarabaeidae: Scarabaeinae): division into species-groups. PLOS One, 16: e0244657.CrossRefGoogle ScholarPubMed
Graf, M., Reid, M.L., Aukema, B.H., and Lindgren, B.S. 2012. Association of tree diameter with body size and lipid content of mountain pine beetles. The Canadian Entomologist, 1441: 467477. https://doi.org/10.4039/tce.2012.38.CrossRefGoogle Scholar
Halffter, G. and Favila, M.E. 1993. The Scarabaeinae (Insecta: Coleoptera): an animal group for analyzing, inventorying and monitoring biodiversity in tropical rainforest and modified landscapes. Biology International, 27: 1521.Google Scholar
Hanski, I. and Cambefort, Y. 1991. The dung beetle ecology. Princeton University Press, Princeton, New Jersey, United States of America.CrossRefGoogle Scholar
Harada, L.M., Araújo, I.S., Overal, W.L., and Silva, F.A.B. 2020. Comparison of dung beetle communities (Coleoptera: Scarabaeidae: Scarabaeinae) in oil palm plantations and native forest in the eastern Amazon, Brazil. Revista Brasileira de Entomologia, 64: e2019102.CrossRefGoogle Scholar
Hsieh, T.C., Ma, K.H., and Chao, A. 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods in Ecology and Evolution, 7: 14511456.CrossRefGoogle Scholar
Hunt, J. and Simmons, L.W. 2000. Maternal and paternal effects on offspring phenotype in the dung beetle Onthophagus taurus . Evolution, 54: 936941.Google ScholarPubMed
Iannuzzi, L., Salomão, R.P., Costa, F.C., and Liberal, C.N. 2016. Environmental patterns and daily activity of dung beetles (Coleoptera: Scarabaeidae) in the Atlantic Rainforest of Brazil. Entomotropica, 31: 196207.Google Scholar
Kohlmann, B., Arriaga-Jiménez, A., and Salomão, R.P. 2021. Rapoport’s Rule and the effect of the last glaciation upon elevational range size: an analysis using a dung beetle model (Coleoptera: Scarabaeidae: Onthophagus) in Mexican tropical mountains. The Holocene, 32: 208219.CrossRefGoogle Scholar
Körner, C. 2007. The use of ‘altitude’ in ecological research. Trends in Ecology and Evolution, 22: 569574.CrossRefGoogle ScholarPubMed
Lara, A.C.F., Fernandes, G.W., and Gonçalves-Alvim, S.J. 2002. Tests of hypotheses on patterns of gall distribution along an altitudinal gradient. Tropical Zoology, 15: 219232.CrossRefGoogle Scholar
Larsen, T.H., Lopera, A., and Forsyth, A. 2006. Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin, 60: 315324.CrossRefGoogle Scholar
Liberal, C.N., Farias, A.M.I., Meiado, M.V., Filgueiras, B.K.C., and Iannuzzi, L. 2011. How habitat change and rainfall affect dung beetle diversity in Caatinga, a Brazilian semi-arid ecosystem. Journal of Insect Science, 11: 111.CrossRefGoogle ScholarPubMed
Lobo, J.M., Hortal, J., and Cabrero-Sañudo, F.J. 2006. Regional and local influence of grazing activity on the diversity of a semi-arid dung beetle community. Diversity and Distribution, 12: 111123.CrossRefGoogle Scholar
Lobo, J.M., Lumarett, J., and Jay-Robert, P. 2001. Diversity, distinctiveness and conservation status of the Mediterranean coastal dung beetle assemblage in the Regional Natural Park of the Camargue (France). Diversity and Distribution, 7: 257270.CrossRefGoogle Scholar
Lomolino, M.V. 2001. Elevation gradients of species-density: historical and prospective views. Global Ecology and Biogeography, 10: 313.CrossRefGoogle Scholar
MacCain, C.M. and Grythes, J. 2010. Elevational gradients in species richness. Encyclopedia of Life Sciences. John Wiley & Sons, Chichester, United Kingdom.Google Scholar
Macedo, R., Audino, L.D., Korasaki, V., and Louzada, J. 2020. Conversion of Cerrado savannas into exotic pastures: the relative importance of vegetation and food resources for dung beetle assemblages. Agriculture, Ecosystems & Environment, 288: 106709.CrossRefGoogle Scholar
Mark, A.F., Dickinson, K.J.M., and Hofstede, R.G.M. 2000. Alpine vegetation, plant distribution, life forms, and environments in a perhumid New Zealand region: oceanic and tropical high mountain affinities. Arctic, Antarctic, and Alpine Research, 32: 240254.CrossRefGoogle Scholar
McDiarmid, R.W. and Donnelly, M.A. 2005. The herpetofauna of the Guayana Highlands: amphibians and reptiles of the Lost World. In Ecology and evolution in the tropics: a herpetological perspective. Edited by Donnelly, M., Crother, B.I., Guyer, C., Wake, M.H., and White, M.E.. University of Chicago Press, Chicago, Illinois, United States of America. Pp. 461560.Google Scholar
Medina, A.M. and Lopes, P.P. 2014. Resource utilization and temporal segregation of Scarabaeinae (Coleoptera, Scarabaeidae) community in a Caatinga fragment. Neotropical Entomology, 43: 127133.CrossRefGoogle Scholar
Nichols, E., Larsen, T., Spector, S., Davis, A.L., Escobar, F., Favila, M., and Vulinec, K. 2007. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biological Conservation, 137: 119.CrossRefGoogle Scholar
Nogué, S., Rull, V., and Vegas-Vilarrúbia, T. 2013. Elevational gradients in the Neotropical table mountains: patterns of endemism and implications for conservation. Diversity and Distributions, 19: 676687.CrossRefGoogle Scholar
Noriega, J.A., March-Salas, M., Castillo, S., García-Q, H., Hortal, J., and Santos, A.M.C. 2021a. Human perturbations reduce dung beetle diversity and dung removal ecosystem function. Biotropica, 53: 753766.CrossRefGoogle Scholar
Noriega, J.A. and Realpe, E. 2018. Altitudinal turnover of species in a Neotropical peripheral mountain system: a case study with dung beetles (Coleoptera: Aphodiinae and Scarabaeinae). Environmental Entomology, 47: 13761387.Google Scholar
Noriega, J.A., Santos, A.M.C., Calatayud, J., Chozas, S., and Hortal, J. 2021b. Short- and long-term temporal changes in the assemblage structure of Amazonian dung beetles. Oecologia, 195: 719736.CrossRefGoogle Scholar
Noriega, J.A., Solis, C., Escobar, F., and Realpe, E. 2007. Escarabajos coprófagos (Coleoptera: Scarabaeidae) de la província de la Sierra Nevada de Santa Marta [Coprophagous beetles (Coleoptera: Scarabaeidae) from the province of the Sierra Nevada de Santa Marta]. Biota Colombiana, 8: 7786.Google Scholar
Oliveira-Filho, A.T., Dexter, K.G., Pennington, R.T., Simon, M.F., Bueno, M.L., and Neves, D.M. 2021. On the floristic identity of Amazonian vegetation types. Biotropica, 53: 767777.CrossRefGoogle Scholar
Olson, D.M., Dinerstein, E., Wikramanayake, E.D., Burgess, N.D., Powell, G.V.N., Underwood, E.C., et al. 2001. Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience, 51: 933938.CrossRefGoogle Scholar
Otavo, S.E., Parrado-Rosselli, A., and Noriega, J.A. 2013. Scarabaeoidea superfamily (Insecta: Coleoptera) as a bioindicator element of anthropogenic disturbance in an Amazon national park. Revista de Biología Tropical, 61: 735752.CrossRefGoogle Scholar
Pacheco, T.L. and Vaz-de-Mello, F.Z. 2015. Dung beetles of the tribe Phanaeini (Coleoptera: Scarabaeidae: Scarabaeinae) from Roraima state, northern Brazil: checklist and key to species. Biota Neotropica, 15: e20140145.CrossRefGoogle Scholar
Pôrto, K.C., Cabral, J.J.P., and Tabarelli, M. 2004. Brejos de altitude em Pernambuco e Paraíba: história natural, ecologia e conservação [Altitude swamps in Pernambuco and Paraíba: natural history, ecology and conservation]. Ministério do Meio Ambiente, Brasília, Brazil.Google Scholar
Prance, G.T. 1996. Islands in Amazonia. Philosophical Transactions of the Royal Society B, 351: 823833.Google Scholar
Quintero, I. and 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 Zoológica Mexicana, 25: 625649.CrossRefGoogle Scholar
R Development Core Team. 2022. R: a language and environment for statistical computing. R foundation for statistical computing. R Development Core Team, Vienna, Austria.Google Scholar
Rahbek, C., Borregaard, M.K., Colwell, R.K., Dalsgaard, B., Holt, B.G., Morueta-Holme, N., et al. 2019. Humboldt’s enigma: what causes global patterns of mountain biodiversity? Science, 365: 11081113.CrossRefGoogle ScholarPubMed
Ratcliffe, B.C. 2013. The dung- and carrion-feeding scarabs (Coleoptera: Scarabaeoidea) of an Amazonian blackwater rainforest: results of a continuous, 56-week, baited-pitfall trap study. The Coleopterists Bulletin, 67: 481520.CrossRefGoogle Scholar
Rivera, J.D. and Favila, M.E. 2022. Good news! Sampling intensity needed for accurate assessments of dung beetle diversity may be lower in the Neotropics. Frontiers in Ecology and Evolution, 10: 999488.CrossRefGoogle Scholar
Rodríguez-Zorro, P.A., Costa, M.L., and Behling, H. 2017. Mid-Holocene vegetation dynamics with an early expansion of Mauritia flexuosa palm trees inferred from the Serra do Tepequém in the savannas of Roraima State in Amazonia, northwestern Brazil. Vegetation History and Archaeobotany, 26: 455468.CrossRefGoogle Scholar
Rull, V. 2004. Biogeography of the ‘Lost World’: a palaeoecological perspective. Earth-Science Reviews, 67: 125137.CrossRefGoogle Scholar
Rull, V., Huber, O., Vegas-Vilarrúbia, T., and Señaris, C. 2019. Definition and characterization of the Pantepui biogeographical province. In Biodiveristy of Pantepui: the pristine “Lost World” of the Neotropical Guiana Highlands. Edited by Rull, V., Huber, O., Vegas-Vilarrúbia, T., and Señaris, C.. Academic Press, London, United Kingdom. Pp. 332.CrossRefGoogle Scholar
Salomão, R.P., Arriaga-Jiménez, A., and Kohlmann, B. 2021a. The relationship between altitudinal gradients, diversity, and body size in a dung beetle (Coleoptera: Scarabaeinae: Onthophagus) model system. Canadian Journal of Zoology, 99: 3343.CrossRefGoogle Scholar
Salomão, R.P., Cerqueira, L.V.M.P., Gomes, A.A.C., González-Tokman, D., Maia, A.C.D., and Iannuzzi, L. 2021b. Dung or carrion? Sex and age determine resource attraction in dung beetles. Ecological Entomology, 47: 5262.CrossRefGoogle Scholar
Salomão, R.P., González-Tokman, D., Dáttilo, W., López-Acosta, J.C., and Favila, M.E. 2018. Landscape structure and composition define the body condition of dung beetles (Coleoptera: Scarabaeinae) in a fragmented tropical rainforest. Ecological Indicators, 88: 144151.CrossRefGoogle Scholar
Salomão, R.P., Lira, A.F.A., Foerster, S.Í.A., and Vaz-de-Mello, F. 2022. Dung beetle assemblage (Coleoptera: Scarabaeinae) from an altitudinal enclave of rainforest surrounded by a seasonally tropical dry forest in the Neotropics. International Journal of Tropical Insect Science, 42: 5562.CrossRefGoogle Scholar
Scholtz, C.H., Davis, A.L.V., and Kryger, U. 2009. Evolutionary biology and conservation of dung beetles. Pensoft Publishers, Sofia, Bulgaria.Google Scholar
Schoolmeesters, P. 2023. World Scarabaeidae database. In Catalogue of life checklist (version 2023-01-03). Edited by O. Bánki, Y. Roskov, M. Döring, G. Ower, L. Vandepitte, D. Hobern, et al. Available from https://www.catalogueoflife.org/data/dataset/1027 [accessed 12 February 2023].Google Scholar
Servín-Pastor, M., Salomão, R.P., Caselín-Cuevas, F., Córdoba-Aguilar, A., Favila, M.E., Jacome-Hernández, A., et al. 2020. Malnutrition and parasitism shape ecosystem services provided by dung beetles. Ecological Indicators, 121: 107205.CrossRefGoogle Scholar
Silva, F.A.B. 2011. First record of Coprophanaeus bellicosus (Olivier) (Coleoptera, Scarabaeidae) in a ‘brejo de altitude’ forest in northeastern Brazil: a historical biogeographical approach. Revista Brasileira de Entomologia, 55: 615–607.CrossRefGoogle Scholar
Spector, S. 2006. Scarabaeinae dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae): an invertebrate focal taxon for biodiversity research and conservation. The Coleopterists Society Monograph, 5: 7183.Google Scholar
Vaz-de-Mello, F., Edmonds, W.D., Ocampo, F.C., and Schoolmeesters, P. 2011. A multilingual key to the genera and subgenera of the subfamily Scarabaeinae of the New World (Coleoptera: Scarabaeidae). Zootaxa, 2854: 173.CrossRefGoogle Scholar
Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., and Smith, G.M. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, New York, United States of America.CrossRefGoogle Scholar