Relationship between land uses and diversity of dung beetles (Coleoptera: Scarabaeinae) in the southern Atlantic forest of Argentina: which are the key factors?

Abstract

The loss of natural habitats is one of the main drivers of biodiversity decline. Anthropogenic land uses preserving biotic and abiotic conditions of the native ecosystem are more suitable to preserve the native biodiversity. In this study, we explored changes in species richness and composition in different land uses of the southern Atlantic forest, considering three independent factors: (1) canopy (presence–absence), (2) type of vegetation (native–exotic) and (3) livestock (presence–absence). We expected a gradient of response in the richness and composition of the native forest dung beetle community, from land uses preserving canopy and native vegetation to open land uses with exotic vegetation. Dung beetles were sampled in protected native forests and four land uses, using two potential food resources: human dung and carrion. The species richness and composition of each habitat, as well as differences in composition and the influence of factors over diversity, were then analyzed. As expected, our results showed that land uses preserving canopy and native vegetation maintain the dung beetle diversity of the native forest. Moreover, while the three factors analyzed influenced dung beetle diversity, canopy cover was the main driver of dung beetle diversity loss. The main conclusion of this study is that the conservation of canopy (either native or exotic) is determinant to preserve highly diverse dung beetle communities and subsequently, the ecological functions performed by this taxon. However, the ecophysiological mechanism behind the response of dung beetles to habitat disturbance is poorly understood.

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References

  1. Alvarado F, Escobar F, Williams DR, Arroyo-Rodriguez V, Escobar-Hernández F (2018) The role of livestock intensification and landscape structure in maintaining tropical biodiversity. J Appl Ecol 55:185–194

    Article  Google Scholar 

  2. Andresen E, Feer F (2005) The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. In: Forget PM, Lambert JE, Hulme PE, Vander Wall SB (eds) Predation, dispersal and seedling establishment. CABI International, Wallingford, pp 331–349

    Google Scholar 

  3. Arellano L, León-Cortés J, Halffter G (2008) Response of dung beetle assemblages to landscape structure in remnant natural and modified habitats in southern Mexico. Insect Conserv Diver 1:253–262

    Article  Google Scholar 

  4. Audino I, 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 

  5. Bogoni JA, Graipel ME, Volkmer de Castilho P, Moreli Fantacini F, Villanova Kuhnen V, Ribeiro Luiz M, Bernardes Maccarini T, Marcon CB, Pimentel Teixeira CS, Tortato MA, Vaz-de-Mello FZ, Hernández MIM (2016) Contributions of the mammal community, habitat structure, and spatial distance to dung beetle community structure. Biodivers Conserv 25:1661–1675

    Article  Google Scholar 

  6. Campanello PI, Montti L, Goldstein G, Mac Donagh P (2009) Reduced impact logging and post-harvesting forest management in the Atlantic Forest: alternative approaches to enhance canopy tree growth and regeneration and to reduce the impact of invasive species. In: Grossberg SP (ed) forest management. Nova Science, New York, pp 39–59

    Google Scholar 

  7. Chao A, Ma KH, Hsieh TC (2016) iNEXT (iNterpolation and EXTrapolation) Online: software for interpolation and extrapolation of species diversity. Program and user’s guide. http://chao.stat.nthu.edu.tw/wordpress/software_download/

  8. Chown SL (2001) Physiological variation in insects: hierarchical levels and implications. J Insect Physiol 47:649–660

    Article  PubMed  CAS  Google Scholar 

  9. Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  10. Clarke KR, Gorley RN (2006) PRIMER v6. User manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  11. Culot L, Bovy 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

    Article  Google Scholar 

  12. Da Silva PG, Hernández MIM (2016) Spatial variation of dung beetle assemblages associated with forest structure in remnants of southern Brazilian Atlantic Forest. Rev Bras Entomol 60:73–81

    Article  Google Scholar 

  13. Davies KF, Margules CR (1998) Effects of habitat fragmentation on carabid beetles: experimental evidence. J Anim Ecol 67:460–471

    Article  Google Scholar 

  14. Davis ALV, Chown SL, McGeoch MA, Scholtz CH (2000) A comparative analysis of metabolic rate in six Scarabaeus species (Coleoptera: Scarabaeidae) from southern Africa: further caveats when inferring adaptation. J Insect Physiol 46:553–562

    Article  PubMed  CAS  Google Scholar 

  15. Davis ALV, Van Aarde RJ, Scholtz CH, Delport JH (2002) Increasing representation of localized dung beetles across a chronosequence of regenerating vegetation and natural dune forest in South Africa. Glob Ecol Biogeogr 11:191–209

    Article  Google Scholar 

  16. Davis ALV, Frolov AV, Scholtz CH (2008) The African dung beetle genera. Protea Book Publishers, Pretoria

    Google Scholar 

  17. Dinghi PA, Sánchez MV, Cantil LF, Sarzetti LC, Genise JF (2013) Leaf-litter brood chambers in dichotomius (luederwaldtinia) carbonarius (mannerheim, 1829) (coleoptera: scarabaeidae): a novel behavior for dung beetles. Coleopt Bull 67:388–396

    Article  Google Scholar 

  18. Dinno A (2017) Conover.test: conover-iman test of multiple comparisons using rank sums. R package version 1.1.4. https://CRAN.R-project.org/package=conover.test. Accessed 2nd Dec 2017

  19. Dirzo R, Raven PH (2003) Global state of biodiversity and loss. Annu Rev Environ Resour 28:137–167

    Article  Google Scholar 

  20. Duncan FD, Byrne MJ (2000) Discontinuous gas exchange in dung beetles: patterns and ecological implications. Oecologia 122:452–458

    Article  PubMed  CAS  Google Scholar 

  21. Filgueiras B, Tabarelli M, Leal I, Vaz-De-Mello FZ, Iannuzzi L (2015) Dung beetle persistence in human-modified landscapes: combining indicator species with anthropogenic land uses and fragmentation- related effects. Ecol Indic 55:65–73

    Article  Google Scholar 

  22. Filloy J, Zurita GA, Corbelli J, Bellocq MI (2010) On the similarity among bird communities: testing the influence of distance and land use. Acta Oecol 36:333–338

    Article  Google Scholar 

  23. Gardner TA, Hernández MIM, Barlow J, Peres CA (2008) 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 

  24. Giménez Gómez VC, Verdú JR, Gómez-Cifuentes A, Vaz-de-Mello FZ, Zurita GA (2018) Influence of land use on the trophic niche overlap of dung beetles in the semideciduous Atlantic forest of Argentina. Insect Conserv Divers. https://doi.org/10.1111/icad.12299

    Article  Google Scholar 

  25. 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

    Article  Google Scholar 

  26. 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 

  27. Halffter G, Halffter V (2009) Why and where coprophagous beetles (Coleoptera: Scarabaeinae) eat seed, fruits or vegetable detritus. Bol SEA 45:1–22

    Google Scholar 

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

    Google Scholar 

  29. Halffter G, Favila ME, Halffter V (1992) A comparative study of the structure of the scarab guild in Mexican tropical rain forests and derived ecosystems. Folia Entomol Mex 84:131–156

    Google Scholar 

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

    Google Scholar 

  31. Hernández MIM, Vaz-de-Mello FZ (2009) Seasonal and spatial species richness variation of dung beetle (Coleoptera, Scarabaeidae s. str.) in the Atlantic Forest of southeastern Brazil. Rev Bras Entomol 153:607–613

    Article  Google Scholar 

  32. Hernández MIM, Barreto PSCS, Costa VH, Creao-Duarte J, Favila ME (2014) Response of a dung beetle assemblage along a reforestation gradient in Restinga forest. J Insect Conserv 18:539–546

    Article  Google Scholar 

  33. Hewavithana DK, Wijesinghe MR, Dangalle CD, Dharmarathna HAS (2016) Habitat and dung preferences of scarab beetles of the subfamily Scarabaeinae: a case study in a tropical monsoon forest in Sri Lanka. Int J Trop Insect Sci 36:97–105

    Article  Google Scholar 

  34. Holter P, Scholtz CH, Stenseng L (2009) Desert detritivory: nutritional ecology of a dung beetle (Pachysoma glentoni) subsisting on plant litter in arid South African sand dunes. J Arid Environ 73:1090–1094

    Article  Google Scholar 

  35. Izquierdo AE, De Angelo CD, Aide TM (2008) Thirty years of human demography and land use change in the Atlantic Forest of Misiones, Argentina: an evaluation of the forest transition model. Ecol Soc 13:3. http://www.ecologyandsociety.org/vol13/iss2/art3/

  36. Larsen TH, Forsyth A (2005) Trap spacing and transect design for dung beetles biodiversity studies. Biotropica 37:322–325

    Article  Google Scholar 

  37. Lobo JM, Lumaret JP, Jay-Robert P (1998) Sampling dung beetles in the French Mediterranean area: effects of abiotic factors and farm practices. Pedobiologia 42:252–266

    Google Scholar 

  38. Mittermeier RA, Myers N, Thomsen JB, Da Fonseca GAB, Olivieri S (1998) Biodiversity hotspots and major tropical wilderness areas: approaches to setting conservation priorities. Conserv Biol 12:516–520

    Article  Google Scholar 

  39. Monteith GB, Storey RI (1981) The biology of Cephalodesmius, a genus of dung beetles which synthesizes “dung” from plant material (Coleoptera: Scarabaeidae: Scarabaeinae). Mem Queensl Mus 20:253–277

    Google Scholar 

  40. Myers N, Knoll AH (2001) The biotic crisis and the future of evolution. Proc Natl Acad Sci USA 98:5389–5392

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  42. Neita JC, Escobar F (2012) The potential value of agroforestry to dung beetle diversity in the wet tropical forests of the Pacific lowlands of Colombia. Agrofor Syst 85:121–131

    Article  Google Scholar 

  43. 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 

  44. Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474

    Article  Google Scholar 

  45. Nichols E, Uriarte M, Bunker DE, Favila ME, Slade EM, Vulinec K (2013) Trait-dependent response of dung beetle populations to tropical forest conversion at local and regional scales. Ecology 94:180–189

    Article  PubMed  Google Scholar 

  46. Novacek MJ, Cleland EE (2001) The current biodiversity extinction event: scenarios for mitigation and recovery. Proc Natl Acad Sci USA 98:5466–5470

    Article  PubMed  CAS  Google Scholar 

  47. Ocampo FC, Hawks DC (2006) Molecular phylogenetics and evolution of the food relocation behaviour of the dung beetle tribe Euraniini (Coleoptera: Scarabaeidae: Scarabaeinae). Invertebr Syst 20:557–570

    Article  CAS  Google Scholar 

  48. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHM, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R package version 2.4-3. https://CRAN.R-project.org/package=vegan2012. Accessed 6 Nov 2017

  49. Oliveira-Filho AT, Fontes IAM (2000) Patterns of floristic differentiation among Atlantic forests in Southeastern Brazil and the influence of climate. Biotropica 32:793–810

    Article  Google Scholar 

  50. Osberg DC, Doube BM, Hanrahan SA (1993) Habitat specificity in African dung beetles: the effect of soil type on dung burial by two species of ball-rolling dung beetles (Coleoptera: Scarabaeidae). Trop Zool 6:243–251

    Article  Google Scholar 

  51. Peyras M, Vespa N, Bellocq M, Zurita G (2012) Quantifying edge effects: the role of habitat contrast and species specialization. J Insect Conserv 17:807–820

    Article  Google Scholar 

  52. Philips K, Pretorius E, Scholtz C (2004) A phylogenetic analysis of dung beetles (Scarabaeinae: Scarabaeidae): unrolling an evolutionary history. Invertebr Taxon 18:53–88

    Article  Google Scholar 

  53. Pineda E, Moreno C, Escobar F, Halffter G (2005) Frog, bat and dung beetle diversity in the cloud forest and coffee agroecosystems of Veracruz, Mexico. Conserv Biol 19:400–410

    Article  Google Scholar 

  54. Quintero I, Roslin T (2005) Rapid recovery of dung beetle communities following habitat fragmentation in central Amazonia. Ecology 12:3303–3311

    Article  Google Scholar 

  55. R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org

  56. Sánchez-de-Jesús H, Arroyo-Rodríguez V, Andresen E, Escobar F (2016) Forest loss and matrix composition are the major drivers shaping dung beetle assemblages in a fragmented rainforest. Landsc Ecol 31:843–854

    Article  Google Scholar 

  57. Scheffler PY (2005) Dung beetle (Coleoptera: Scarabaeidae) diversity and community structure across three disturbance regimes in eastern Amazonia. J Trop Ecol 21:9–19

    Article  Google Scholar 

  58. Scholtz CH, Harrison JG, Grebennikov VV (2004) Dung beetle (Scarabaeus (Pachysoma)) biology and immature stages: reversal to ancestral states under desert conditions (Coleoptera: Scarabaeidae). Biol J Linnean Soc 83:453–460

    Article  Google Scholar 

  59. Sowig P (1995) Habitat selection and offspring survival rate in three paracoprid dung beetles: the influence of soil type and soil moisture. Ecography 18:147–154

    Article  Google Scholar 

  60. Spector S (2006) Scarabaeine dung beetles (Coleopteran: Scarabaeidae: Scarabaeinae): an invertebrate focal taxon for biodiversity research and conservation. Coleopt Bull 60:71–83

    Article  Google Scholar 

  61. Tonelli M, Verdú JR, Zunino M (2017) Effects of grazing intensity and the use of veterinary medical products on dung beetle biodiversity in the sub-mountainous landscape of Central Italy. PeerJ Preprints 4:e2358v1. https://doi.org/10.7287/peerj.preprints.2358v1

    Article  Google Scholar 

  62. Tshikae BP, Davis ALV, Scholtz CH (2013) Species richness e energy relationships and dung beetle diversity across an aridity and trophic resource gradient. Acta Oecol 49:71–82

    Article  Google Scholar 

  63. Tuff KT, Tuff T, Davies KF (2016) A framework for integrating thermal biology into fragmentation research. Ecol Lett 19:361–374

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Verdú JR, Moreno CE, Sánchez-Rojas G, Numa C, Galante E, Halffter G (2007) Grazing promotes dung beetle diversity in the xeric landscape of a Mexican biosphere reserve. Biol Conserv 140:308–317

    Article  Google Scholar 

  65. Verdú JR, Lobo MJ, Sánchez-Piñero F, Gallego B, Numa C, Lumaret JP, Cortez V, Ortiz A, Tonelli M, García-Teba Rey A, Rodriguez A, Durán J (2017) Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: an interdisciplinary field study. Sci Total Environ 618:219–228

    Article  PubMed  CAS  Google Scholar 

  66. Vulinec K (2002) Dung beetle communities and seed dispersal in primary forest and disturbed land in Amazonia. Biotropica 34:297–309

    Article  Google Scholar 

  67. Zaninovich SC, Fontana JL, Gatti MG (2016) Atlantic forest replacement by non-native tree plantations: comparing aboveground necromass between native forest and pine plantation ecosystems. For Ecol Manag 363:39–46

    Article  Google Scholar 

  68. Zurita GA, Bellocq MI (2012) Bird assemblages in anthropogenic habitats: identifying a suitability gradient for native species in the Atlantic forest. Biotropica 44:412–419

    Article  Google Scholar 

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Acknowledgements

We wish to thank Fernando Foletto, Andrés Gómez-Cifuentes, Gisele Jaime, Natalia Vespa and Soledad Soto for their help in the fieldwork. Also, we wish to thank farmers for their hospitality, Fernando Vaz-de-Mello for helping us to examine the taxonomic component in the identification of dung beetles, Santiago José Velazco for the assistance in statistical analysis and Juan Ariel Insaurralde for helping us with the map. Finally, we wish to thank anonymous reviewers who have helped to improve the manuscript. The Centro de Investigaciones del Bosque Atlántico (CeIBA) Misiones, Argentina, provided logistical support. Financial support was provided by CONICET (Project UE IBS # 22920160100130CO to M. Di Bitteti), UCAR-MAGyP (BIO 23, PIA 10105-14057 to G. Zurita) and ANPCyT (PICT-PRH 2702 to G. Zurita). National Park Administration, the Misiones Ministry of Ecology and Arauco Argentina S.A. provided the necessary permissions to collect dung beetles.

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Correspondence to V. C. Giménez Gómez.

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Communicated by David Hawksworth.

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Giménez Gómez, V.C., Verdú, J.R., Guerra Alonso, C.B. et al. Relationship between land uses and diversity of dung beetles (Coleoptera: Scarabaeinae) in the southern Atlantic forest of Argentina: which are the key factors?. Biodivers Conserv 27, 3201–3213 (2018). https://doi.org/10.1007/s10531-018-1597-8

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Keywords

  • Cover vegetation
  • Forest habitat
  • Global change
  • Livestock
  • Microclimatic conditions
  • Scarabaeoidea