, Volume 183, Issue 1, pp 177–190 | Cite as

Linking functional group richness and ecosystem functions of dung beetles: an experimental quantification

  • Tanja Milotić
  • Stijn Quidé
  • Thomas Van Loo
  • Maurice Hoffmann
Community ecology – original research


Dung beetles form an insect group that fulfils important functions in terrestrial ecosystems throughout the world. These include nutrient cycling through dung removal, soil bioturbation, plant growth, secondary seed dispersal and parasite control. We conducted field experiments at two sites in the northern hemisphere temperate region in which dung removal and secondary seed dispersal were assessed. Dung beetles were classified in three functional groups, depending on their size and dung manipulation method: dwellers, large and small tunnelers. Other soil inhabiting fauna were included as a fourth functional group. Dung removal and seed dispersal by each individual functional group and combinations thereof were estimated in exclusion experiments using different dung types. Dwellers were the most diverse and abundant group, but tunnelers were dominant in terms of biomass. All dung beetle functional groups had a clear preference for fresh dung. The ecosystem services in dung removal and secondary seed dispersal provided by dung beetles were significant and differed between functional groups. Although in absolute numbers more dwellers were found, large tunnelers were disproportionally important for dung burial and seed removal. In the absence of dung beetles, other soil inhabiting fauna, such as earthworms, partly took over the dung decomposing role of dung beetles while most dung was processed when all native functional groups were present. Our results, therefore, emphasize the need to conserve functionally complete dung ecosystems to maintain full ecosystem functioning.


Dung beetles Dung removal Secondary seed dispersal Functional groups 



This study is part of a larger pan-European multisite project supported by the ALTER-Net consortium, Europe’s Ecosystem Research Network; it is co-financed within their multisite experiment programme. We thank the Flemish government and the Agency for Nature and Forest (ANB) for access to their nature reserves, the allowance to sample the dung fauna, and their foresters Koen Marechal and Karel Molenberghs for logistical help. We would like to express our gratitude to the taxonomist Geoffrey Miessen for his help in the identification of many of our dung beetle samples, and the laboratory technicians at INBO for soil texture analysis. We also thank two anonymous reviewers for their helpful comments to improve the first version of this manuscript.

Author contribution statement

TM and MH conceived and designed the experiment and developed the methodology. SQ and TVL conducted fieldwork and identified specimens. TM, SQ and TVL analysed the data. TM, SQ, TVL and MH wrote the manuscript. SQ and TVL equally contributed to the manuscript and are listed in an alphabetical order.

Supplementary material

442_2016_3756_MOESM1_ESM.pdf (901 kb)
Supplementary material 1 (PDF 900 kb)


  1. Andresen E (1999) Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica 31:145–158Google Scholar
  2. Andresen E (2002a) Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecol Entomol 27:257–270CrossRefGoogle Scholar
  3. Andresen E (2002b) Primary seed dispersal by red howler monkeys and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 34:261–272CrossRefGoogle Scholar
  4. Andresen E (2003) Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography 26:87–97CrossRefGoogle Scholar
  5. 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) Seed fate. Predation, dispersal and seedling establishment. CABI, Oxon, pp 331–349CrossRefGoogle Scholar
  6. Andresen E, Levey DJ (2004) Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:45–54CrossRefPubMedGoogle Scholar
  7. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D, Schmid B (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156CrossRefPubMedGoogle Scholar
  8. Bang HS, Lee JH, Kwon OS, Na YE, Jang YS, Kim WH (2005) Effects of paracoprid dung beetles (Coleoptera: Scarabaeidae) on the growth of pasture herbage and on the underlying soil. Appl Soil Ecol 29:165–171CrossRefGoogle Scholar
  9. Baraud J (1992) Coléoptères Scarabaeoidea d’Europe. Fédération française des Sociétés de Sciences naturelles et Société linnéenne de LyonGoogle Scholar
  10. Barnosky AD, Matzke N, Tomiya S, Wogan GOU, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC (2011) Has the earth’s sixth mass extinction already arrived? Nature 471:51–57CrossRefPubMedGoogle Scholar
  11. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823
  12. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MH, White JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. TREE 24:127–135PubMedGoogle Scholar
  13. Borghesio L, Luzzatto M, Palestrini C (1999) Interactions between dung, plants and the dung fauna in a heathland in northern Italy. Pedobiologia 43:97–109Google Scholar
  14. 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:e57786CrossRefPubMedPubMedCentralGoogle Scholar
  15. Brown J, Scholtz CH, Janeau JL, Grellier S, Podwojewski P (2010) Dung beetles (Coleoptera: Scarabaeidae) can improve soil hydrological properties. Appl Soil Ecol 46:9–16CrossRefGoogle Scholar
  16. Brussaard L, Visser WJF (1987) Dung exploitation of the dung beetle Typhaeus typhoeus (Coleoptera: Geotrupidae). Oecologia 72:21–27CrossRefGoogle Scholar
  17. Bryan RP (1973) The effects of dung beetles activity on the numbers of parasitic gastrointestinal helmintic larvae recovered from pasture samples. Aust J Agric Res 24:161–168CrossRefGoogle Scholar
  18. Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429CrossRefPubMedGoogle Scholar
  19. Chevan A, Sutherland M (1991) Hierarchical partitioning. Am Stat 45:90–96Google Scholar
  20. Couvreur M, Menschaert J, Sevenant M, Ronse A, Van Landuyt W, De Blust G, Antrop M, Hermy M (2004) Ecodistricten en ecoregio’s als instrument voor natuurstudie en milieubeleid. Natuur Focus 3:51–58Google Scholar
  21. D’hondt B, Bossuyt B, Hoffmann M, Bonte D (2008) Dung beetles as secondary seed dispersers in a temperate grassland. Basic Appl Ecol 9:542–549CrossRefGoogle Scholar
  22. Davis ALV (1996) Seasonal dung beetle activity and dung dispersal in selected South African habitats: implications for pasture improvement in Australia. Agric Ecosyst Environ 58:157–169CrossRefGoogle Scholar
  23. Dormont L, Epinat G, Lumaret JP (2004) Trophic preferences mediated by olfactory cues in dung beetles colonizing cattle and horse dung. Environ Entomol 33:370–377CrossRefGoogle Scholar
  24. Dormont L, Rapior S, McKey DB, Lumaret JP (2007) Influence of dung volatiles on the process of resource selection by coprophagous beetles. Chemoecology 17:23–30CrossRefGoogle Scholar
  25. Doube BM (1990) A functional classification for analysis of the structure of dung beetle assemblages. Ecol Entomol 15:371–383CrossRefGoogle Scholar
  26. Feer F (1999) Effects of dung beetles (Scarabaeidae) on seeds dispersed by Howler monkeys (Alouatta seniculus) in the French Guianan rain forest. J Trop Ecol 15:129–142CrossRefGoogle Scholar
  27. Fincher GT (1973) Dung beetles as biological-control agents for gastrointestinal parasites of livestock. J Parasitol 59:396–399CrossRefPubMedGoogle Scholar
  28. Fincher GT (1975) Effects of dung beetle activity on the number of nematode parasites acquired by grazing cattle. J Parasitol 61:759–762CrossRefPubMedGoogle Scholar
  29. Finn JA (2001) Ephemeral resource patches as model systems for diversity-function experiments. Oikos 92:363–366CrossRefGoogle Scholar
  30. Finn JA, Giller PS (2002) Experimental investigations of colonisation by north temperate dung beetles of different types of domestic herbivore dung. Appl Soil Ecol 20:1–13CrossRefGoogle Scholar
  31. Finn JA, Gittings T (2003) A review of competition in north temperate dung beetle communities. Ecol Entomol 28:1–13CrossRefGoogle Scholar
  32. Finn JA, Gittings T, Giller PS (1999) Spatial and temporal variation in species composition of dung beetle assemblages in southern Ireland. Ecol Entomol 24:24–36CrossRefGoogle Scholar
  33. Gittings T, Giller PS (1997) Life history traits and resource utilisation in an assemblage of north temperate Aphodius dung beetles (Coleoptera: Scarabaeidae). Ecography 20:55–66CrossRefGoogle Scholar
  34. Gittings T, Giller P (1999) Larval dynamics in an assemblage of Aphodius dung beetles. Pedobiologia 43:439–452Google Scholar
  35. Gittings T, Giller PS, Stakelum G (1994) Dung decomposition in contrasting temperate pastures in relation to dung beetle and earthworm activity. Pedobiologia 38:455–474Google Scholar
  36. Gregory N, Gómez A, Oliveira TMFDS, Nichols E (2015) Big dung beetles dig deeper: trait-based consequences for faecal parasite transmission. Int J Parasitol 45:101–105CrossRefPubMedGoogle Scholar
  37. Hanski I (1980) Spatial variation in the timing of the seasonal occurrence in coprophagous beetles. Oikos 34:311–321CrossRefGoogle Scholar
  38. Hanski I (1987) Nutritional ecology of dung and carrion feeding insects. In: Slanky JF, Rodriguez JG (eds) Nutritional ecology of insects, mites and spiders. Wiley, New York, pp 837–884Google Scholar
  39. Hanski I, Cambefort Y (1991) Dung beetle ecology. Princeton University Press, PrincetonCrossRefGoogle Scholar
  40. Hanski I, Koskela H (1979) Resource partitioning in six guilds of dung-inhabiting beetles (Coleoptera). Ann Entomol Fenn 45:1–12Google Scholar
  41. Holter P (1982) Resource utilization and local coexistence in a guild of Scarabaeid dung beetles (Aphodius Spp). Oikos 39:213–227CrossRefGoogle Scholar
  42. Holter P (1983) Effect of earthworms on the disappearance rate of cattle droppings. In: Satchell JE (ed) Earthworm ecology. Springer, New York, pp 49–57CrossRefGoogle Scholar
  43. Holter P (2000) Particle feeding in Aphodius dung beetles (Scarabaeidae): old hypotheses and new experimental evidence. Funct Ecol 14:631–637CrossRefGoogle Scholar
  44. Holter P (2004) Dung feeding in hydrophilid, geotrupid and scarabaeid beetles: examples of parallel evolution. Eur J Entomol 101:365–372CrossRefGoogle Scholar
  45. Holter P, Scholtz CH (2007) What do dung beetles eat? Ecol Entomol 32:690–697CrossRefGoogle Scholar
  46. Holter P, Sommer C, Grønvold J, Madsen M (1993) Effects of ivermectin treatment on the attraction of dung beetles (Coleoptera: Scarabaeidae and Hydrophilidae) to cow pats. Bull Entomol Res 83:53–58CrossRefGoogle Scholar
  47. Horgan FG (2001) Burial of bovine dung by coprophagous dung beetle (Coleoptera: Scarabaeidae) from horse and cow grazing sites in El Salvador. Eur J Soil Biol 37:103–111CrossRefGoogle Scholar
  48. Horgan FG (2005) Effects of deforestation on diversity, biomass and function of dung beetles on the eastern slope of the Peruvian Andes. For Ecol Manag 216:117–133CrossRefGoogle Scholar
  49. Hortal J, Diniz-Filho JAF, Bini LM, Rodríguez MÁ, Baselga A, Nogués-Bravo D, Rangel TF, Hawkins BA, Lobo JM (2011) Ice age climate, evolutionary constraints and diversity patterns of European dung beetles. Ecol Lett 14:741–748CrossRefPubMedGoogle Scholar
  50. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  51. Hutton SA, Giller PS (2003) The effects of the intensification of agriculture on northern temperate dung beetle communities. J Appl Ecol 40:994–1007CrossRefGoogle Scholar
  52. Janssens A (1960) Insectes Coléoptères Lamellicornes. Institut Royal des Sciences Naturelles de Belgique, BrusselsGoogle Scholar
  53. Jessop L (1986) Dung beetles and chafers. Royal Entomological Society of London, LondonGoogle Scholar
  54. Jost L (2006) Entropy and diversity. Oikos 113:363–375CrossRefGoogle Scholar
  55. Larsen TH, Forsyth A (2005) Trap spacing and transect design for dung beetle biodiversity studies. Biotropica 37:322–325CrossRefGoogle Scholar
  56. Larsen TH, Williams NM, Kremen C (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol Lett 8:538–547CrossRefPubMedGoogle Scholar
  57. Losey JE, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323CrossRefGoogle Scholar
  58. Mac Nally R (2000) Regression and model-building in conservation biology, biogeography and ecology: the distinction between––and reconciliation of––‘predictive’ and ‘explanatory’ models. Biodiv Conserv 9:655–671CrossRefGoogle Scholar
  59. Millennium Ecosystem Assessment (2005) Ecosystems and Human Well-being: Opportunities and Challenges for Business and Industry. World Resources Institute, Washington, DCGoogle Scholar
  60. Miranda CHB, Santos JC, Bianchin I (2000) The role of Digionthophagus gazella on pasture cleaning and production as a result of burial of cattle dung. Pasturas Tropicales 22:14–19Google Scholar
  61. Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579CrossRefGoogle Scholar
  62. Naeem S, Loreau M, Inchausti P (2002) Biodiversity and ecosystem functioning: the emergence of a synthetic ecological framework. In: Loreau M, Naeem S, Inchausti P (eds) Biodiversity and ecosystem functioning: synthesis and perspectives. Oxford University Press, Oxford, pp 3–11Google Scholar
  63. Nathan R, Schurr FM, Spiegel O, Steinitz O, Trakhtenbrot A, Tsoar A (2008) Mechanisms of long-distance seed dispersal. TREE 23:638–647PubMedGoogle Scholar
  64. 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 141:1461–1474CrossRefGoogle Scholar
  65. O’Hea NM, Kirwan L, Finn JA (2010) Experimental mixtures of dung fauna affect dung decomposition through complex effects of species interactions. Oikos 119:1081–1088CrossRefGoogle Scholar
  66. Ojha RB, Devkota D (2014) Earthworms:’Soil and Ecosystem Engineers’––a Review. World J Agric Res 2:257–260CrossRefGoogle Scholar
  67. Penttilä A, Slade EM, Simojoki A, Riutta T, Minkkinen K, Roslin T (2013) Quantifying beetle-mediated effects on gas fluxes from dung pats. PLoS One 8:e71454CrossRefPubMedPubMedCentralGoogle Scholar
  68. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–122Google Scholar
  69. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  70. Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. TREE 24:505–514PubMedGoogle Scholar
  71. Ridsdill-Smith TJ (1993) Effects of avermectin residues in cattle dung on dung beetle (Coleoptera: Scarabaeidae) reproduction and survival. Vet Parasitol 48:127–137CrossRefPubMedGoogle Scholar
  72. Rosenlew H, Roslin T (2008) Habitat fragmentation and the functional efficiency of temperate dung beetles. Oikos 117:1659–1666CrossRefGoogle Scholar
  73. Schmid B, Hector A, Saha P, Loreau M (2008) Biodiversity effects and transgressive overyielding. J Plant Ecol 1:95–102CrossRefGoogle Scholar
  74. Schwartz MW, Brigham CA, Hoeksema JD, Lyons KG, Mills MH, Van Mantgem PJ (2000) Linking biodiversity to ecosystem function: implications for conservation ecology. Oecologia 122:297–305CrossRefGoogle Scholar
  75. Shepherd VE, Chapman CA (1998) Dung beetles as secondary seed dispersers: impact on seed predation and germination. J Trop Ecol 14:199–215CrossRefGoogle Scholar
  76. 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 76:1094–1104CrossRefPubMedGoogle Scholar
  77. Sowig P (1997) Predation among Sphaeridium larvae: the role of starvation and size differences (Coleoptera Hydrophilidae). Ethol Ecol Evol 9:241–251CrossRefGoogle Scholar
  78. Srivastava DS, Vellend M (2005) Biodiversity-ecosystem function research: is it relevant to conservation? Annu Rev Ecol Evol Syst 36:267–294CrossRefGoogle Scholar
  79. Steuer P, Südekum KH, Müller DWH, Kaandorp J, Clauss M, Hummel J (2013) Fibre digestibility in large herbivores as related to digestion type and body mass—an in vitro approach. Comp Biochem Physiol 164:319–326CrossRefGoogle Scholar
  80. Venables W, Ripley B (2002) Modern applied statistics with S. Springer, New YorkCrossRefGoogle Scholar
  81. Verdú JR, Lobo JM (2008) Ecophysiology of thermoregulation in endothermic dung beetles: ecological and geographical implications. In: Fattorini S (eds) Insect Ecology and Conservation. Research Signpost. pp. 1–28Google Scholar
  82. Walsh C, Mac Nally R (2013) hier.part: Hierarchical Partitioning. R package version 1.0–4Google Scholar
  83. Wardhaugh KG, Mahon RJ (1991) Avermectin residues in sheep and cattle dung and their effects on dung-beetle (Coleoptera: Scarabaeidae) colonization and dung burial. Bull Entomol Res 81:333–339CrossRefGoogle Scholar
  84. Yamada D, Imura O, Shi K, Shibuya T (2007) Effect of tunneler dung beetles on cattle dung decomposition, soil nutrients and herbage growth. Grassl Sci 53:121–129CrossRefGoogle Scholar
  85. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Terrestrial Ecology Unit, Department of BiologyGhent UniversityGhentBelgium
  2. 2.Research Institute for Nature and ForestBrusselsBelgium

Personalised recommendations