Skip to main content

Advertisement

Log in

Greenspace sites conserve taxonomic and functional diversity of dung beetles in an urbanized landscape in the Brazilian Cerrado

  • Published:
Urban Ecosystems Aims and scope Submit manuscript

Abstract

Urbanization transforms natural ecosystems, creating an environmental mosaic, characterized by native vegetation sites mixed with constructed sites. In this study, we compared dung beetle taxonomic and functional diversity between residential and greenspace sites (remnants of native vegetation) in an urban landscape in the Brazilian Cerrado. We sampled dung beetles in February (2013–2014 – 2015) in four sites of remnants of native Cerado (here called “greenspace”) and four residential sites in the city of Aquidauana, Mato Grosso do Sul, Brazil. Greenspace sites are characterized by a mixture of plants of two distinct strata (phytophysiognomy Cerrado sensu stricto), a woody layer of trees and large shrubs, while residential sites are characterized by residential buildings (housing and commercial sites), unpaved roads with tree-lined streets. Dung beetle abundance and species richness were higher in greenspace sites. Species composition differed significantly among habitats but functional composition did not differ. Functional dispersion and functional richness was higher in greenspace sites. On the other hand, functional evenness was similar between greenspace and residential sites. In this study, we found higher taxonomic and functional components of dung beetle diversity in greenspace when compared to residential sites in the Brazilian Cerrado. Thus, we highlight the importance greenspace sites for the conservation of dung beetle biodiversity and consequently their ecological services (i.e. such as soil aeration, secondary seed dispersal, parasite regulation), which indirectly can affect human life quality in the urban matrix.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Additional data are available upon request.

References

  • 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

    Article  Google Scholar 

  • Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728

    Article  Google Scholar 

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525

    Article  Google Scholar 

  • Audino L, 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

    Article  Google Scholar 

  • Audino LD, Murphy SJ, Zambaldi L, Louzada J, Comita LS (2017) Drivers of community assembly in tropical forest restoration sites: role of local environment, landscape and space. Ecol Appl 27:1731–1745

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barros WM, Gomes RL, Marcato Júnior J (2015) Análise dos contingentes populacional e habitacional da cidade de Aquidauana-MS: atualização e perspectiva. Rev GeoPantanal 19:59–69

    Google Scholar 

  • 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 Indic 95:418–526

    Article  Google Scholar 

  • Bogoni JA, da Silva PG, Peres CA (2019) Co‐declining mammal–dung beetle faunas throughout the Atlantic Forest biome of South America. Ecography 42:1803–18018

  • Bolund P, Hunhammar S (1999) Ecosystem services in urban areas. Ecol Econ 29:293–301

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Brannstrom C, Jepson W, Filippi AM, Redo D, Xu Z, Ganesh S (2008) Land change in Brazilian savanna (Cerrado), 1986-2002: comparative analysis and implications for land use policy. Land Use Policy 25:579–575

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Carpaneto GM, Mazziotta A, Piattella E (2005) Changes in food resources and conservation of scarab beetles: from sheep to dog dung in a green area of Rome (Coleoptera: Scarabaeoidea). Biol Conserv 123:547–556

    Article  Google Scholar 

  • Carvalho JMA (2004) Crescimento populacional e estrutura demográfica do Brasil. UFMG/Cedeplar, Belo Horizonte

    Google Scholar 

  • Carvalho FMV, Marco Junior P, Ferreira LG (2009) The Cerrado into-pieces: habitat fragmentation as a function of landscape use in the savannas of Central Brazil. Biol Conserv 142:1392–1403

    Article  Google Scholar 

  • Cave RD (2005) Observations of urban dung beetles utilizing dog feces (Coleoptera: Scarabaeidae). Coleopt Bull 59:400–401

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Clarke KR (1993) Nonparametric analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) Primer v6 Permanova+. Primer-E Ltd., Plymouth

    Google Scholar 

  • Correa CMA, Puker A, Korasaki V, Ferreira KR, Abot AR (2016) Attractiveness of baits to dung beetles in Brazilian savanna and exotic pasturelands. Entomol Sci 19:112–123

    Article  Google Scholar 

  • Correa CMA, Braga RF, Puker A, Korasaki V (2019) Patterns of taxonomic and functional diversity of dung beetles in a human-modified variegated landscape in Brazilian Cerrado. J Insect Conserv 23:89–99

    Article  Google Scholar 

  • Costa C, Oliveira VHF, Maciel R, Beiroz W, Korasaki V, Louzada J (2017) Variegated tropical landscapes conserve diverse dung beetle communities. PeerJ 5:e3125

    Article  PubMed  PubMed Central  Google Scholar 

  • 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:e012611

    Google Scholar 

  • Derhé MA, Murphy H, Monteith G, Menéndez R (2016) Measuring the success of restoration for restoring biodiversity and ecosystem functioning. J Appl Ecol 53:1714–1724

    Article  Google Scholar 

  • Dufrene M, Legendre P (1997) Species assemblages and indicators species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Filgueiras BKC, Tabarelli M, Leal IR, Vaz-de-Mello FZ, Iannuzzi I (2015) Dung beetle persistence in human-modified landscapes: combining indicators species with anthropogenic land use and fragmentation-related effects. Ecol Indic 55:65–73

    Article  Google Scholar 

  • Fina BG, Monteiro R (2013) Análise da estrutura arbustivo-arbórea de uma área de Cerrado sensu stricto, município de Aquidauana-Mato Grosso do Sul. Rev Arvore 37:577–585

    Article  Google Scholar 

  • Frizzas MR, Batista JLFL, Rocha MVC, Oliveira CM (2020) Diversity of Scarabaeinae (Coleoptera: Scarabaeidae) in an urban fragment of Cerrado in Central Brazil. Eur J Entomol 117:273–281

    Article  Google Scholar 

  • Gardner TA, Barlow J, Araujo IS, Ávila-Pires TC, Bonaldo AB, Costa JE, Esposito MC, Ferreira LV, Hawes J, Hernandez MIM, Hoogmoed MS, Leite RN, Lo-Man-Hung NF, Malcolm JR, Martins MB, Mestre LAM, Miranda-Santos R, Overal WL, Parry L, Peters SL, Ribeiro-Junior MA, da Silva MNF, da Silva Motta C, Peres CA (2008) The cost-effectiveness of biodiversity surveys in tropical forests. Ecol Lett 11:139–150

    Article  PubMed  Google Scholar 

  • Gerten C, Fina S, Rusche K (2019) The sprawling planet: simplifying the measurement of global urbanization trends. Front Environ Sci 7:140

    Article  Google Scholar 

  • Gómez-Cifuentez 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Halffter G (1991) Historical and ecological factors determining the geographical distribution of beetles (Coleoptera. Scarabaeidae. Scarabaeinae). Folia Entomol Mex 82:195–238

    Google Scholar 

  • Halffter G, Arellano L (2002) Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34:144–154

    Article  Google Scholar 

  • Halffter G, Edmonds WD (1982) The nesting behavior of dung beetles (Scarabaeinae) – an ecological and evolutive approach. Instituto de Ecología, Xalapa

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9

    Google Scholar 

  • Hanski I, Cambefort Y (1991) Dung beetle ecology. Princeton University Press, Princeton

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • IBGE (Instituto Brasileiro de Geografia e Estatística) (2019) Cidades. Rio de Janeiro, Brazil. http://www.ibge.gov.br. Accessed 08 Sept 2020

  • Klink CA, Moreira A (2002) Past and current human occupation, and land use. In: Oliveira P, Marquis R (eds) The Cerrados of Brazil ecology and natural history of a Neotropical savanna. Columbia University Press, New York, pp 51–69

    Google Scholar 

  • Korasaki V, Lopes J, Brown GG, Louzada J (2013) Using dung beetles to evaluate the effects of urbanization on Atlantic Forest biodiversity. Insect Sci 20:393–406

    Article  PubMed  Google Scholar 

  • Kuebbing SE, Maynard DS, Bradford MA (2018) Linking functional diversity and ecosystem processes: a framework for using functional diversity metrics to predict the ecosystem impact of functionally unique species. J Ecol 106:687–698

    Article  Google Scholar 

  • Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lobo JM (1993) Estimation of dung beetle biomass (Coleoptera: Scarabaeoidea). Eur J Entomol 90:235–238

    Google Scholar 

  • Macedo R, Audino LD, Korasaki V, Louzada J (2020) Conversion of Cerrado savannas into exotic pastures: the relative importance of vegetation and food resources for dung beetle assemblages. Agric Ecosyst Environ 288:106709

    Article  Google Scholar 

  • MacGregor-Fors I, Escobar-Ibáñez JF (2017) Avian ecology in Latin American cityscapes. Springer, New York

    Book  Google Scholar 

  • Marris E (2005) Conservation in Brazil: the forgotten ecosystem. Nature 437:944–945

    Article  CAS  PubMed  Google Scholar 

  • Martinson HM, Raupp MJ (2013) A meta-analysis of the effects of urbanization on ground beetle communities. Ecosphere 4:1–24

    Article  Google Scholar 

  • McDonald RI, Kareiva P, Forman RTT (2008) The implications of current and future urbanization for global protected areas and biodiversity conservation. Biol Conserv 141:1695–1703

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • McKinney ML (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–890

    Article  Google Scholar 

  • McKinney ML (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecosyst 11:161–176

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nagy DD, Magura T, Horváth R, Debnár Z, Tóthmérész B (2018) Arthropod assemblages and functional responses along an urbanization gradient: a trait-based multi-taxa approach. Urban For Urban Green 30:157–168

    Article  Google Scholar 

  • Nichols E, Goméz A (2014) Dung beetle and fecal helminth transmission: patterns, mechanisms and questions. Parasitology 141:614–623

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Nichols E, Gardner TA, Peres CA, Spector S, The Scarabaeinae Research Network (2009) Co-declining mammals and dung beetles: an impeding ecological cascade. Oikos 118:481–487

    Article  Google Scholar 

  • Nunes RV, Frizzas MR (2007) Microbiota da flora intestinal de besouros (Coleoptera: Scarabaeidae) do Parque Olhos D’Água. Univ Ci Saúde 5:1–11

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Puker A, Correa CMA, Korasaki V (2014) Deltochilini and Phanaeini dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) in introduced and native ecosystems of Brazil. J Nat Hist 48:2105–2116

    Article  Google Scholar 

  • R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, available from: www.RProject.org

  • Raine EH, Slade EM (2019) Dung beetle—mammal associations: methods, research trends and future directions. P Roy Soc B-Biol Sci 286:20182002

    Google Scholar 

  • Ramírez-Restrepo L, Halffter G (2016) Copro-necrophagous beetles (Coleoptera: Scarabaeinae) in urban areas: a global review. Urban Ecosyst 19:1179–1195

    Article  Google Scholar 

  • Salomão RP, Alvarado F, Baena-Díaz F, Favila ME, Iannuzzi L, Liberal CN, Santos BA, Vaz-de-Mello FZ, González-Tokman D (2019) Urbanization effects on dung beetle assemblages in a tropical city. Ecol Indic 103:665–675

    Article  Google Scholar 

  • Sano EE, Rosa R, Brito JLS, Ferreira LG (2010) Land cover mapping of the tropical savanna region in Brazil. Environ Monit Assess 166:133–144

    Article  Google Scholar 

  • Scholes RJ, Archer SR (1997) Tree grass interactions in savannas. Annu Rev Ecol Evol S 28:517–544

  • Slade EM, Mann DJ, Villanueva JF, Lewis OT (2007) Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. J Anim Ecol 76:1094–1104

    Article  PubMed  Google Scholar 

  • Slade EM, Riutta T, Roslin T, Tuomisto HL (2016) The role of dung beetles in reducing greenhouse gas emissions from cattle farming. Sci Rep 6:18140

  • Souza EP, Martins SRO (2010) Conflitos territoriais em torno do Parque da Lagoa Comprida, Aquidauana, MS. Percurso 11:273–289

    Google Scholar 

  • Taylor L, Hochuli DF (2017) Defining greenspaces: multiple uses across multiple disciplines. Landsc Urban Plan 158:25–38

    Article  Google Scholar 

  • Teodoro PE, Correa CCG, Torres EF, Oliveira-Júnior JF, Silva Junior AC, Gois C, Delgado RC (2015) Analysis of the occurrence of wet and drought periods using standardized precipitation index in Mato Grosso do Sul state, Brazil. J Agron 14:80–86

    Article  Google Scholar 

  • United Nations (2018) World Urbanization Prospects: The 2018 Revision [key facts]

  • 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

    Article  Google Scholar 

  • Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

    Article  PubMed  Google Scholar 

  • Ziter C (2016) The biodiversity-ecosystem service relationship in urban areas: a quantitative review. Oikos 125:761–768

    Article  Google Scholar 

Download references

Acknowledgements

We thank Fernando Z. Vaz-de-Mello (UFMT) for identification of the dung beetle species; Alfredo Raúl Abot (Universidade Estadual de Mato Grosso do Sul, Aquidauana, Mato Grosso do Sul, Brazil) for his lab equipment for insect screening, Mateus Alves and Paulo André Silva for the field support, the Editor and four 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 Pessoal de Nível Superior (CAPES, Brazil) (88881.134292/2016-01). VK thanks FAPEMIG for financial support.

Funding

Conselho Nacional de Desenvolvimento Científico, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior.

Author information

Authors and Affiliations

Authors

Contributions

CMAC and KRF conceived the study, they selected the study sites and performed the dung beetle surveys; CMAC analyzed data with substantial input from LDA; CMAC wrote the paper with substantial input from all authors.

Corresponding author

Correspondence to César M. A. Correa.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

CMAC, KRF, AP, LDA and VK declare that they have no conflict of interest.

Supplementary Information

ESM 1

(DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Correa, C.M.A., Ferreira, K.R., Puker, A. et al. Greenspace sites conserve taxonomic and functional diversity of dung beetles in an urbanized landscape in the Brazilian Cerrado. Urban Ecosyst 24, 1023–1034 (2021). https://doi.org/10.1007/s11252-021-01093-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11252-021-01093-8

Keywords

Navigation