Skip to main content

Advertisement

SpringerLink
Log in

Contributions of the mammal community, habitat structure, and spatial distance to dung beetle community structure

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Dung beetles feed and nest in mammal feces, are influenced by habitat quality and have limited dispersal ability. We hypothesized that dung beetle community structure is affected by mammal composition, habitat structure, and spatial distance, and that these predictors vary among the functional groups in communities. Dung beetles and mammals were sampled using pitfall traps and camera traps, respectively, at 15 Atlantic Forest sites between 2005 and 2013. Habitat structure was described using the point-quadrant method. We utilized descriptive ecological values and used variation partitioning to identify predictors of dung beetle community composition both as a whole, and after organizing the community into functional groups. We recorded 43 dung beetle species and 28 mammal species. Mammal and dung beetle species richness were positively correlated. Mammals and habitat explained the majority of the variation among dung beetle communities, and explanatory values varied substantially when using the functional group approach. Our results indicate that mammals are, indeed, important drivers of dung beetle community structure. Individually, or in combination with habitat structure, mammal composition explained 40 % of the total variation in dung beetle data, i.e., the abundance and species composition of dung beetles and mammals covary. However, herbivorous mammals, medium-sized mammals and omnivorous mammals numerically contributed more than did other groups to the explanation of variation in dung beetle guilds. Habitat structure was an important determinant for dung beetle functional group abundance, and spatial distance influenced covariation between dung beetles and mammals. Thus, the integrity and maintenance of ecological processes in the Atlantic Forest may be dependent on these groups, and further fragmentation, habitat loss and defaunation may increase the sensitivity of this already reduced and threatened biome.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

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(1):32–43. doi:10.1590/S1519-566X2009000100003

    Article  Google Scholar 

  • Barlow J, Gardner TA, Araujo IS et al (2007) Quantifying the biodiversity value of tropical primary, secondary and plantation Forest. Proc Natl Acad Sci 104(47):18555–18560. doi:10.1073/pnas.0703333104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barlow J, Louzada J, Parry L et al (2010) Improving the design and management of forest strips in human-dominated tropical landscapes: a field test on Amazonian dung beetles. J Appl Ecol 47:779–788. doi:10.1111/j.1365-2664.2010.01825.x

    Article  Google Scholar 

  • Barnosky AD, Hadly EA, Bascompte J et al (2012) Approaching a state shift in Earth’s biosphere. Nature 486:52–58. doi:10.1038/nature11018

    Article  CAS  PubMed  Google Scholar 

  • Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632

    Article  PubMed  Google Scholar 

  • Bogoni JA, Hernández MIM (2014) Attractiveness of native mammals feces of different trophic guilds to dung beetles (Coleoptera: Scarabaeinae). J Insect Sci. doi:10.1093/jisesa/ieu161

    PubMed  Google Scholar 

  • Bogoni JA, Cherem JJ, Giehl ELH et al (2016) Landscape features lead to shifts in communities of medium- to large-bodied mammals in subtropical Atlantic Forest. J Mammal. doi:10.1093/jmammal/gyv215

    Google Scholar 

  • Borcard D, Legendre P, Avois-Jacquet C, Tuomisto H (2004) Dissecting the spatial structure of ecological data at multiple scales. Ecology 85(7):1826–1832

    Article  Google Scholar 

  • Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York

    Book  Google Scholar 

  • Brocardo CR, Ziparro VB, de Lima RAF, Guevara R, Galetti M (2013) No changes in seedling recruitment when terrestrial mammals are excluded in a partially defaunated Atlantic rainforest. Biol Conserv 163:107–114. doi:10.1016/j.biocon.2013.04.024

    Article  Google Scholar 

  • Brower JE, Zar J, von Ende CN (1998) Field and laboratory methods for general ecology, 4th edn. McGraw-Hill, Dubuque

    Google Scholar 

  • Cáceres NC, Cherem JJ, Graipel ME (2007) Distribuição geográfica de mamíferos terrestres na região sul do Brasil. Ciência & Ambiente 35:167–180

    Google Scholar 

  • Campos RC, Hernández MIM (2013) Dung beetles assemblages (Coleoptera, Scarabaeinae) in Atlantic Forest fragments in southern Brazil. Rev Bras Entomol 57(1):47–54. doi:10.1590/S0085-56262013000100008

    Article  Google Scholar 

  • Canale GR, Peres CA, Guidorizzi CE et al (2012) Pervasive defaunation of forest remnants in a tropical biodiversity hotspot. PLos One. doi:10.1371/journal.pone.0041671

    Google Scholar 

  • Cardinale BJ, Duffy E, Gonzalez A et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67. doi:10.1038/nature11148

    Article  CAS  PubMed  Google Scholar 

  • Cassano CR, Barlow J, Pardini R (2012) Large mammals in an agroforestry mosaic in the Brazilian Atlantic Forest. Biotropica 44(6):818–825. doi:10.1111/j.1744-7429.2012.00870.x

    Article  Google Scholar 

  • Colwell RK, Chao A, Gotelli NJ et al (2012) Models and estimators linking individual-based and sample-based rarefaction, extrapolation and comparison of assemblages. J Plant Ecol. 5(1):3–21. doi:10.1093/jpe/rtr044

    Article  Google Scholar 

  • Culot L, Bovi E, Vaz-de-Mello FZ, Guevara R, Galetti M (2013) Selective defaunation affects dung beetle communities in continuous Atlantic rainforest. Biol Conserv 163:79–89. doi:10.1016/j.biocon.2013.04.004

    Article  Google Scholar 

  • da Silva PG, Hernández MIM (2014) Local and regional effects on community structure of dung beetles in a mainland-island scenario. PLos One 9(10):e111883

    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(5):e0126112

    Article  PubMed  PubMed Central  Google Scholar 

  • Davis ALV (1996) Community organization of dung beetles (Coleoptera: Scarabaeidae): differences in body size and functional group structure between habitats. Afr J Ecol 34:258–275

    Article  Google Scholar 

  • Dirzo R, Young HS, Galetti M et al (2014) Defaunation in the anthropocene. Science 345:401–406

    Article  CAS  PubMed  Google Scholar 

  • Dray S, Legendre P, Blanchet G (2013) Packfor: forward selection with permutation (Canoco p.46). R package version 0.0-8/r109. http://R-Forge.R-project.org/projects/sedar/

  • Eduardo AA (2011) Spatial patterns of mammalian diversity in a fragmented landscape in southern Brazil. Rev Bras Biociênc 9(2):252–255

    Google Scholar 

  • Espartosa KD, Pinotti BT, Pardini R (2011) Performance of camera trapping and track counts for surveying large mammals in rainforest remnants. Biodivers Conserv 20:2815–2829

    Article  Google Scholar 

  • Estrada A, Halffter G, Coates-Estrada R, Meritt DA Jr (1993) Dung beetles attracted to mammalian herbivore (Alouatta palliata) and omnivore (Nasua narica) dung in the tropical rainforest of Los Tuxtlas Mexico. J Trop Ecol 9:45–54

    Article  Google Scholar 

  • Favila ME, Halffter G (1997) The use of indicator groups for measuring biodiversity as related to community structure and function. Acta Zool Mex 72:1–25

    Google Scholar 

  • Filgueiras BKC, Liberal CN, Aguiar CDM et al (2009) Attractivity of omnivore carnivore and herbivore mammalian dung to Scarabaeinae (Coleoptera Scarabaeidae) in a tropical Atlantic Forest remnant. Rev Bras Entomol 53:422–427

    Article  Google Scholar 

  • Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science 309:570–574

    Article  CAS  PubMed  Google Scholar 

  • Galetti M, Dirzo R (2013) Ecological and evolutionary consequences of living in a defaunated world. Biol Conserv 163:1–6

    Article  Google Scholar 

  • Gardner TA, Barlow J, Araujo IS et al (2008a) The cost-effectiveness of biodiversity surveys in tropical Forests. Ecol Lett 11:139–150

    Article  PubMed  Google Scholar 

  • Gardner TA, Hernández MIM, Barlow J, Peres CA (2008b) Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for Neotropical dung beetles. J Appl Ecol 45:883–893

    Article  Google Scholar 

  • Goulart FVB, Cáceres NC, Graipel ME et al (2009) Habitat selection by large mammals in a southern Brazilian Atlantic Forest. Mamm Biol 74:182–190

    Google Scholar 

  • Halffter G, Arellano L (2002) Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica 34(1):144–154

    Article  Google Scholar 

  • Halffter G, Edmonds WD (1982) The nesting behavior of dung beetles (Scarabaeinae): an ecologic and evolutive approach. Man and Biosphere Program Unesco, Mexico City

    Google Scholar 

  • Halffter G, Favila ME (1993) The Scarabaeinae (Insecta: Coleoptera) an animal group for analyzing, inventorying, and monitoring biodiversity in tropical Rainforest and modified landscapes. Biol Int 27:15–21

    Google Scholar 

  • Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomol Mex 12(14):1–312

    Google Scholar 

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

    Google Scholar 

  • Hernández MIM (2002) The night and day of dung beetles (Coleoptera: Scarabaeinae) in the Serra do Japi, Brazil: elytra color related to daily activity. Rev Bras Entomol 46(4):597–600

    Article  Google Scholar 

  • Hernández MIM (2007) Besouros escarabeíneos (Coleoptera: Scarabaeidae) da caatinga paraibana, Brasil. Oecol Bras 11(3):356–364

    Article  Google Scholar 

  • Hernández MIM, Vaz-de-Mello FZ (2009) Seasonal and spatial species richness variation of dung beetles (Coleoptera: Scarabaeidae s. str.) in the Atlantic Forest of southern Brazil. Rev Bras Entomol 53(4):607–613

    Article  Google Scholar 

  • Hernández MIM, Monteiro LR, Favila ME (2011) The role of body size and shape in understanding competitive interactions within a community of Neotropical dung beetles. J Insect Sci 11:13

    PubMed  PubMed Central  Google Scholar 

  • Hernández MIM, Barreto PSCS, Costa VH et al (2014) Response of a dung beetle assemblage along a reforestation gradient in Restinga forest. J Insect Conserv 18:539–546

    Article  Google Scholar 

  • Holyoak M, Leibold MA, Holt RD (eds) (2005) Metacommunities: spatial dynamics and ecological communities. University of Chicago Press, Chicago

    Google Scholar 

  • Instituto Brasileiro de Geografia e Estatística (IBGE) (1992) Manual técnico da vegetação brasileira. Departamento de Recursos Naturais e Estudos Ambientais, Rio de Janeiro

    Google Scholar 

  • Kurten EL (2013) Cascading effects of contemporaneous defaunation on tropical forests communities. Biol Conserv 163:22–32

    Article  Google Scholar 

  • Larsen T, Forsyth A (2005) Trap spacing and transect design for dung beetle biodiversity studies. Biotropica 37:322–325

    Article  Google Scholar 

  • Larsen T, Lopera A, Forsyth A (2006) Extreme trophic and habitat specialization by peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Coleopt Bull 60:315–324

    Article  Google Scholar 

  • Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  • Legendre P, Borcard D, Roberts DW (2012) Variation partitioning involving orthogonal spatial eigen function submodels. Ecology 93(5):1234–1240

    Article  PubMed  Google Scholar 

  • Lyra-Jorge MC, Ciochetti G, Pivello VR, Meirelles ST (2008) Comparing methods for sampling large- and medium-sized mammals: camera traps and track plots. Eur J Wildl Res 54:739–744

    Article  Google Scholar 

  • Magioli M, Ribeiro MC, Ferraz KMPMB, Rodrigues MG (2015) Thresholds in the relationship between functional diversity and patch size for mammals in the Brazilian Atlantic Forest. Anim Conserv 18(6):499–511

    Article  Google Scholar 

  • Marsh CJ, Louzada J, Beiroz W, Ewers RM (2013) Optimising bait for pitfall trapping of Amazonian dung beetles (Coleoptera: Scarabaeinae). PLoS One 8(8):e73147. doi:10.1371/journal.pone.0073147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Nichols E, Uriarte M, Bunker DE et al (2013a) Trait-dependent response of dung beetles populations to tropical forest conversion at local and regional scales. Ecology 94(1):180–189

    Article  PubMed  Google Scholar 

  • Nichols E, Uriarte M, Peres CA et al (2013b) Human-induced trophic cascades along the fecal detritus pathway. PLos One 8(10):e75819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Connell AF, Nichols JD, Karanth U (eds) (2011) Camera traps in animal ecology. Springer, New York

    Google Scholar 

  • Oksanen J, Blanchet G, Kindt R et al. (2013) Vegan: community ecology package. R package version 2.0-7. http://CRAN.R-project.org/package=vegan

  • Paglia AP, da Fonseca GAB, Rylands AB et al (2012) Annotated checklist of Brazilian mammals, 2nd edn. Occas Pap Conserv Biol 6:1–76

    Google Scholar 

  • Pardini R, Bueno AA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLos One 5(10):e13666

    Article  PubMed  PubMed Central  Google Scholar 

  • Parera A (2002) Los mamíferos de la argentina y la región Austral de Sudamérica. El Ateneo, Buenos Aires

    Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Peres-Neto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87(10):2614–2625

    Article  PubMed  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, New York

    Book  Google Scholar 

  • Pimm SL (1982) Food webs. Chapman and Hall, Chicago

    Book  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing. http://www.r-project.org/

  • Reis NR, Peracchi AL, Pedro WA, Lima IP (eds) (2006) Mamíferos do Brasil. Editora da Universidade Estadual de Londrina, Londrina

    Google Scholar 

  • Schmidt BR (2005) Monitoring the distribution of pond-breeding amphibians when species are detected imperfectly. Aquat Conserv 15:681–692

    Article  Google Scholar 

  • Schmitz OJ, Hawlena D, Trussell GC (2010) Predator control of ecosystem nutrient dynamics. Eco Lett 13:1199–1209

    Article  Google Scholar 

  • Slade EM, Villanueva MDJ, 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, Mann DJ, Lewis OT (2011) Biodiversity and ecosystem function of tropical forest dung beetles under contrasting logging regimes. Biol Conserv 144:166–174

    Article  Google Scholar 

  • Wiederholt R, Fernandez-Duque E, Diefenbach DR, Rudran R (2010) Modeling the impacts of hunting on the population dynamics of red howler monkeys (Alouatta seniculus). Ecol Model 221:2482–2490

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Education Ministry of Brazil (CAPES) for the scholarship to JAB, CNPq (Science and Technology Ministry of Brazil) for funding the project (Process 553880/2010), the Research Productivity Grant for MIMH (Proc. 303800/2010-0) and for FZVM (302997/2013-0). We are grateful to Pedro G. da Silva, Renata C. Campos, and Fernando V.B. Goulart for support during fieldwork and to Pedro G. da Silva, Luis M. Bini, Luciana Iannuzzi, Paulo C. A. Simões-Lopes, and Thiago C. Gomes for opinions and contributions. We thank the anonymous reviewers, and Eckehard Brockerhoff (the Associate Editor) for their important contributions.

Author information

Authors and Affiliations

  1. Departamento de Ecologia e Zoologia, Universidade Federal de Santa Catarina, Florianópolis, SC, 88040-900, Brazil

    Juliano André Bogoni, Maurício Eduardo Graipel, Felipe Moreli Fantacini, Vanessa Villanova Kuhnen, Cássio Batista Marcon & Malva Isabel Medina Hernández

  2. Curso de Pós-Graduação em Engenharia Florestal, Universidade do Estado de Santa Catarina, Laguna, SC, 88790-000, Brazil

    Pedro Volkmer de Castilho

  3. Programa de Pós-Graduação em Gestão de Recursos Naturais, Universidade do Extremo Sul Catarinense, Criciúma, SC, 88806-000, Brazil

    Micheli Ribeiro Luiz

  4. Programa de Pós-Graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal do Mato Grosso Do Sul, Campo Grande, MS, 79070-000, Brazil

    Thiago Bernardes Maccarini

  5. Curso de Graduação em Gestão Ambiental, Centro Universitário Estácio de Sá, São José, SC, 88117-001, Brazil

    Christiane de Souza Pimentel Teixeira

  6. Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal do Paraná, Curitiba, PR, 88060-000, Brazil

    Marcos Adriano Tortato

  7. Departamento de Biologia e Zoologia, Instituto de Biociencias, Universidade Federal do Mato Grosso, Cuiabá, MT, 78060-900, Brazil

    Fernando Z. Vaz-de-Mello

Authors
  1. Juliano André Bogoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maurício Eduardo Graipel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pedro Volkmer de Castilho
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Felipe Moreli Fantacini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Vanessa Villanova Kuhnen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Micheli Ribeiro Luiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Thiago Bernardes Maccarini
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Cássio Batista Marcon
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christiane de Souza Pimentel Teixeira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marcos Adriano Tortato
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fernando Z. Vaz-de-Mello
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Malva Isabel Medina Hernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juliano André Bogoni.

Additional information

Communicated by Eckehard G. Brockerhoff.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10531_2016_1147_MOESM1_ESM.doc

Supplementary material 1 (DOC 45 kb) Supplementary Material 1. Geographic locations of sites distributed among protected areas in subtropical Atlantic Forest, Santa Catarina, Brazil

10531_2016_1147_MOESM2_ESM.jpg

Supplementary material 2 (JPEG 155 kb) Supplementary Material 2. Experimental design for sampling medium to large-bodied mammals and dung beetles in 15 subtropical Atlantic Forest sites, Santa Catarina, Brazil

10531_2016_1147_MOESM3_ESM.xls

Supplementary material 3 (XLS 48 kb) Supplementary Material 3. Number and species of dung beetles (collected via pitfall-trap) per site in subtropical Atlantic Forest areas, Santa Catarina, Brazil. S1, S2 and S3: Reserva Particular do Patrimônio Natural (RPPN) Chácara Edith (RCE); sites S4 and S5: RPPN Caraguatá (RCA); S6: RPPN Rio das Lontras (RRL); S7, S8 and S9: Parque Estadual da Serra do Tabuleiro (PEST; Area A) in the municipality of Santo Amaro da Imperatriz (PTA); S10 and S11: PEST (Area B) in the municipality of São Bonifácio (PTB); S12 and S13: RPPN Leão da Montanha (RLM); and S14 and S15: Reserva Biológica Estadual do Aguaí (REA)

10531_2016_1147_MOESM4_ESM.jpg

Supplementary material 4 (JPEG 1306 kb) Supplementary Material 4. Rarefaction curves (with 95 % C.I.) of dung beetle species from 15 Brazilian subtropical Atlantic Forest sites. Site abbreviations are listed in Supplementary Materials 3

10531_2016_1147_MOESM5_ESM.xls

Supplementary material 5 (XLS 43 kb) Supplementary Material 5. Mammal species recorded via camera-trap in 15 subtropical Atlantic Forest sites in Santa Catarina, Brazil. Site and area abbreviations are listed in Supplementary Materials 3

10531_2016_1147_MOESM6_ESM.doc

Supplementary material 6 (DOC 52 kb) Supplementary Material 6. Forward selection results and variation partitioning for communities as a whole (predictors: mammals, habitat and distance; responses: dung beetles) in 15 Brazilian subtropical Atlantic Forest sites

10531_2016_1147_MOESM7_ESM.doc

Supplementary material 7 (DOC 100 kb) Supplementary Material 7. Variation partitioning values for functional groups (statistically significant data only are shown in Fig. 4). Dung beetle trophic guilds are denoted as follows: C = coprophagous; N = necrophagous; and G = generalist. Dung beetle body size is denoted as: L = large; M = medium; and S = small. Dung beetle relocation resource behavior is denoted as: P = paracoprid; T = telecoprid; and E = endocoprid

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bogoni, J.A., Graipel, M.E., de Castilho, P.V. et al. Contributions of the mammal community, habitat structure, and spatial distance to dung beetle community structure. Biodivers Conserv 25, 1661–1675 (2016). https://doi.org/10.1007/s10531-016-1147-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-016-1147-1

Keywords

Search

Navigation