Abstract
The Brazilian Cerrado harbors great floristic and structural diversity composed of a mosaic of natural vegetation types and anthropogenic environments such as introduced pastures. Here, our goal was to evaluate the patterns of taxonomic and functional diversity of dung beetles in a human-modified landscape in Brazilian Cerrado. For this, we evaluated the species richness, species composition and abundance (non-weighted by abundance) and species diversity (Shannon index—weighted by abundance) and three functional indexes (functional richness, functional evenness and functional dispersion). We collected the insects in fragments of Cerrado (Cerrado stricto sensu), riparian forests under pressure of timber removal and livestock and exotic pastures (Urochloa spp.) in Anastácio and Aquidauana, Mato Grosso do Sul, Brazil. We used pitfall traps baited with human feces and fresh capybara dung, a large native rodent, as a representative of the mammal regional fauna. Dung beetle richness was higher in Cerrado fragments, while the abundance was higher in exotic pastures and riparian forests. Species composition differed among vegetation types. Finally, the species diversity and functional diversity did not differ among vegetation types. Thus, we demonstrated the information generated by conceptually similar indexes (e.g. functional richness, species richness and species diversity) may not provide similar information on dung beetles responses to disturbance due to differences in the weighting on species abundance. Finally, the use of taxonomic and functional metrics generate complementary information that can helps us to reach more efficient conclusions in terms of biodiversity conservation and ecosystem functionality in human-modified variegated landscape.






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Almeida SSP, Louzada JNC (2009) Estrutura da comunidade de Scarabaeinae (Scarabaeidae: Coleoptera) em fitofisionomias do Cerrado e sua importância para a conservação. Neotrop Entomol 38:32–43
Almeida S, Louzada J, Sperber C, Barlow J (2011) Subtle-use change and tropical biodiversity: dung beetle communities in Cerrado grasslands and exotic pastures. Biotropica 43:704–771
Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525
Audino LD, Louzada J, Comita L (2014) Dung beetles as indicators of tropical forest restoration success: is it possible to recover species and functional diversity? Biol Conserv 169:248–257
Barlow J, Gardner TA, Araujo IS et al (2007) Quantifying the biodiversity value of tropical primary, secondary and plantation forests. PNAS 104:18555–18560
Barlow J, Lennox GD, Ferreira J et al (2016) Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 7535:144–147
Barragán F, Moreno CE, Escobar F, Halffter G, Navarrete D (2011) Negative impacts of human land use on dung beetle functional diversity. PLoS ONE 6:e17976
Beiroz W, Sayer E, Slade SM, Audino L, Braga RF, Louzada J, Barlow J (2018) Spatial and temporal shifts in functional and taxonomic diversity of dung beetle in a human-modified tropical forest landscape. Ecol Ind 95:418–526
Bicknell JE, Phelps SP, Davies RG, Mann DJ, Struebig MJ, Davies GD (2014) Dung beetles as indicators for rapid impact assessments: evaluating best practice forestry in the neotropics. Ecol Ind 43:154–161
Braga RF, Korasaki V, Audino LD, Louzada J (2012) Are dung beetles driving dung-fly abundance in traditional agricultural areas in the Amazon? Ecosystems 15:1173–1181
Braga RF, Korasaki V, Andresen E, 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:e5778
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087
Chao A, Shen T-J (2003) Nonparametric estimation of Shannon’s index of diversity when there are unseen species in sample. Environ Ecol Stat 10:429–443
Chapman ASA, Tunnicliffe V, Bates AE (2018) Both rare and common species make unique contributions to functional diversity in an ecosystem unaffected by human activities. Divers Distrib 24:568–578
Clarke KR, Gorley RN (2006) Primer v6 Permanova+. Primer-E Ltd., Plymouth
Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples
Correa CMA, Puker A, Korasaki V, Oliveira NG (2013) Dung beetles (Coleoptera, Scarabaeinae) attracted to sheep dung in exotic pastures. Rev Bras Entomol 57:113–116
Correa CMA, Puker A, Ferreira KR, Cristaldo CM, Ferreira FNF, Abot AR, Korasaki V (2016a) Using dung beetles to evaluate the conversion effects from native to introduced pasture in the Brazilian Pantanal. J Insect Conserv 20:447–456
Correa CMA, Puker A, Korasaki V, Ferreira KR, Abot AR (2016b) The attractiveness of baits to dung beetles in Brazilian Cerrado and exotic pasturelands. Entomol Sci 19:112–123
Costa C, Oliveira VHF, Maciel R, Beiroz W, Korasaki V, Louzada J (2017) Variegated tropical lndscapes conserve diverse dung betle communities. PeerJ 5:e3125
Crawley MJ (2002) Statistical computing—an introduction to data analysis using s-plus. Wiley, London
DeClerck FAJ, Chazdon R, Holl KD et al (2010) Biodiversity conservation in human-modified landscapes of Mesoamerica: present, past and future. Biol Conserv 143:2301–2313
Derhé MA, Murphy H, Monteith G, Menéndez R (2016) Measuring the sucess of restoration for restoring biodiversity and ecosystem functioning. J Appl Ecol 53:1714–1724
Driscoll DA, Weir T (2005) Beetle responses to habitat fragmentation depend on ecological traits, habitat condition and remnant size. Conserv Biol 19:182–194
Escobar F, Hallfter G, Arellano L (2007) From forest to pasture: an evaluation of the influence of environment and biogeography on the structure of dung beetle (Sscarabaeinae) assemblages along three altitudinal gradients in the Neotropical region. Ecography 30:193–208
Estrada A, Anzures DA, Coates-Estrada R (1999) Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. Am J Primatol 48:253–262
Ferreira J, Aragao LEOC, Barlow J et al (2014) Brazil’s environmental leadership at risk. Science 346:706–707
Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science 309:570–574
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
Gardner TA, Barlow J, Araujo IS et al (2008) The cost-effectiveness of biodiversity surveys in tropical forests. Ecol Lett 11:139–150
Gerisch M, Agostinelli V, Henle K, Dziock F (2012) More species, but all do the same: contrasting effects of flood disturbance on ground beetle functional and species diversity. Oikos 121:508–515
Gómez-Cifuentes A, Munevar A, Gimenez VC, Gatti MG, Zurita GA (2017) Influence of land use on the taxonomic and functional diversity of dung beetles (Coleoptera: Scarabaeinae) in the southern Atlantic forest of Argentina. J Insect Conserv 21:147–156
Gorelick R (2006) Combining richness and abundance into a single diversity index using matrix analogues of Shannon’s and Simpson’s indices. Ecography 29:525–530
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391
Gray CL, Slade EM, Mann DJ, Lewis TO (2014) Do riparian reserves support dung beetle biodiversity and ecosystem services in oil palm-dominated tropical landscape? Ecol Evol 4:1049–1060
Gries R, Louzada J, Almeida S, Macedo R, Barlow J (2012) Evaluating the impacts and conservation value of exotic and native tree afforestation in Cerrado grasslands using dung beetles. Insect Conserv Divers 5:175–185
Halffter G (1991) Historical and ecological factors determining the geographical distribution of beetles (Coleoptera. Scarabaeidae. Scarabaeinae). Folia Entomol Mex 82:195–238
Halffter G, Arellano L (2002) Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34:144–154
Halffter G, Favila ME, Halffter V (1992) A comparative study of the structure of the scarab guild in Mexican tropical rain forest and derived ecosystem. Folia Entomol Mex 84:131–156
Hanski I, Cambefort Y (1991) Dung beetle ecology. Princeton University Press, Princeton
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
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Laliberté E, Wells JA, Declerck F et al (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecol Lett 13:76–86
Larsen TH (2012) Upslope range shifts of Andean dung beetles in response to deforestation: compounding and confounding effects of microclimatic change. Biotropica 44:82–89
Lobo JM, Martín-Piera F (2002) Searching for a predictive model for species richness of Iberian dung beetle based on spatial and environmental variables. Conserv Biol 16:158–173
Louzada JNC, Carvalho e Silva PR (2009) Utilisation of introduced Brazilian pastures ecosystems by native dung beetles: diversity patterns and resource use. Insect Conserv Divers 2:45–52
Magnago LFS, Edwards DP, Edwards FA, Magrach A, Martins SV, Laurence WF (2014) Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J Ecol 102:465–485
Marris E (2005) Conservation in Brazil: the forgotten ecosystem. Nature 437:944–945
Martello F, Andriolli F, Souza TB, Dodonov P, Ribeiro MC (2016) Edge and land use effects on dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) in Brazilian cerrado vegetation. J Insect Conserv 20:967–970
Mlambo MC (2014) Not all traits are ‘functional’: insights from taxonomic and biodiversity-ecosystem functioning research. Biodivers Conserv 23:781–790
Mouillot D, Bellwood DR, Baraloto C et al (2013a) Rare species support vulnerable functions in high-diversity ecosystems. PLoS Biol 11:e1001569
Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013b) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Navarrete D, Halffter G (2008) Dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) diversity in continuous forest, forest fragments and cattle pastures in a landscape of Chiapas, Mexico: the effects of anthropogenic changes. Biodivers Conserv 17:2869–2898
Nichols E, Gómez A (2014) Dung beetles and the epidemiology of parasitic nematodes: patterns, mechanisms and questions. Parasitology 141:614–623
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
Nichols E, Spector S, Louzada JNC, Larsen TS, Favila M, The Scarabaeinae Research Network (2008) Ecological functions and services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474
Nichols E, Uriarte M, Peres CA, Louzada J, Braga RF, Schiffler G et al (2013) Human-induced trophic cascades along the fecal detritus pathway. PLoS ONE 8:e75819
Oliveira-Filho T, Ratter JA (2002) Vegetation physiognomies and woody flora of the Cerrado biome. In: Oliveira PS, Marquis RJ (eds) The Cerrados of Brazil—ecology and natural history of a neotropical Savanna. Columbia University Press, New York, pp 91–120
Puker A, Correa CMA, Korasaki V, Ferreira KR, Oliveira NG (2013) Dung beetles (Coleoptera: Scarabaeidae) attracted to dung of the largest herbivorous rodent on Earth: a comparison with human feces. Environ Entomol 42:1218–1225
Queiroz ACM, Rabello AM, Braga DL et al (2017) Cerrado vegetation types determine how land use impacts ant biodiversity. Biodivers Conserv. https://doi.org/10.1007/s10531-017-1379-8
R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.RProject.org
Rodrigues MM, Uchôa MA, Ide S (2013) Dung beetle (Coleoptera: Scarabaeoidea) in three landscapes in Mato Grosso do Sul, Brazil. Braz J Biol 73:211–220
Rös M, Escobar F, Halffter G (2012) How dung beetles respond to a human-modified variegated landscape in Mexican cloud forest: a study of biodiversity integrating ecological and biogeographical perspectives. Divers Distrib 18:377–384
Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162
Santos-Heredia C, Andresen E, Zárate DA, Escobar F (2018) Dung beetles and their ecological functions in three agroforestry systems in Lacandona rainforest of México. Biodivers Conserv 27:2379–2394
Shannon CE, Wiener W (1949) The mathematical theory of communication. Illinois Press, Urbana
Silva JMC, Bates JM (2002) Biogeographic patterns and conservation in the South American Cerrado: a tropical savanna hotspot. Bioscience 52:225–233
Silva PG, Hernandez 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(5):e012611
Soares-Filho B, Rajão R, Macedo M, Carneiro A, Costa W, Coe M, Rodrigues H, Alencar A (2014) Cracking Brazil’s forest code. Science 344:363–364
Tabarelli M, Aguiar AV, Ribeiro MC, Metzeger JP, Peres AC (2010) Prospects for biodiversity conservation in the Atlantic forest: lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340
Viegas G, Stenert C, Schulz UH, Maltchik L (2014) Dung beetle communities as biological indicators of riparian forest widths in southern Brazil. Ecol Ind 36:703–710
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301
Acknowledgements
We thank the father of the first author, Agenor Martinho Correa, for the encouragement and logistical support, and FAPEMIG (APQ—02696-15) for the financial support. We also thank Fernando Z. Vaz-de-Mello (UFMT) for identification of the dung beetle species; Cezar F. Borges for the map confection, Cleilsom M. Cristaldo, Naiara G. Oliveira and Kleyton R. Ferreira, for the field support; Mrs. Marcos Crestani, Gélio P. Brum and Jorge de Deus Ricardo for access to their properties, Wallace Beiroz and three anonymous reviewers for the fruitful comments on the manuscript. CMAC received a PhD scholarschip from the Conselho Nacional de Desenvolvimento Científico 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 Pessoa de Nível Superior (CAPES, Brazil) (88881.134292/2016-01).
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Correa, C.M.A., Braga, R.F., Puker, A. et al. Patterns of taxonomic and functional diversity of dung beetles in a human-modified variegated landscape in Brazilian Cerrado. J Insect Conserv 23, 89–99 (2019). https://doi.org/10.1007/s10841-018-00118-6
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DOI: https://doi.org/10.1007/s10841-018-00118-6


