Elsevier

Biological Conservation

Volume 141, Issue 6, June 2008, Pages 1461-1474
Biological Conservation

Review
Ecological functions and ecosystem services provided by Scarabaeinae dung beetles

https://doi.org/10.1016/j.biocon.2008.04.011Get rights and content

Abstract

Clear understanding of the links between ecological functions and biodiversity is needed to assess and predict the true environmental consequences of human activities. Several key ecosystem functions are provided by coprophagous beetles in the subfamily Scarabaeinae (Coleoptera: Scarabaeidae), which feed on animal excreta as both adults and larvae. Through manipulating feces during the feeding process, dung beetles instigate a series of ecosystem functions ranging from secondary seed dispersal to nutrient cycling and parasite suppression. Many of these ecological functions provide valuable ecosystem services such as biological pest control and soil fertilization. Here we summarize the contributions of dung beetles to nutrient cycling, bioturbation, plant growth enhancement, secondary seed dispersal and parasite control, as well as highlight their more limited role in pollination and trophic regulation. We discuss where these ecosystem functions clearly translate into ecosystem services, outline areas in critical need of additional research and describe a research agenda to fill those gaps. Due to the high sensitivity of dung beetles to habitat modification and changing dung resources, many of these ecological processes have already been disrupted or may be affected in the future. Prediction of the functional consequences of dung beetle decline demands functional studies conducted with naturally assembled beetle communities, which broaden the geographic scope of existing work, assess the spatio-temporal distribution of multiple functions, and link these ecosystem processes more clearly to ecosystem services.

Introduction

Human economy, health and wellbeing are intimately linked to functionally intact ecosystems (MEA, 2005), and well characterized relationships between biodiversity and ecosystem function are key to predicting the ecological and economic impacts of human activities (Armsworth et al., 2007). In terrestrial systems, insects play important ecological roles in diverse ecological processes such as nutrient cycling, seed dispersal, bioturbation and pollination. Dung beetles in the coleopteran subfamily Scarabaeinae mediate several of these processes.

Dung beetles are a globally distributed insect group, with their highest diversity in tropical forests and savannas (Hanski and Cambefort, 1991). Largely coprophagous, dung beetle species feed on the microorganism-rich liquid component of mammalian dung (and less commonly that of other vertebrates, as well as rotting fruit, fungus and carrion) and use the more fibrous material to brood their larvae (Halffter and Edmonds, 1982, Halffter and Matthews, 1966).

Most dung beetles use one of three broad nesting strategies, each with implications for ecological function. Paracoprid (tunneler) species bury brood balls in vertical chambers in close proximity to original deposition site. Telocoprid (roller) species transport balls some horizontal distance away, before burial beneath the soil surface. Endocoprid (dweller) species brood their young inside the dung mass itself (Halffter and Edmonds, 1982). Ecological linkages between dung beetles and mammals have played an important role in shaping the evolution of the Scarabaeinae and the structure of extant dung beetle communities for at least the last 40 million years (Cambefort, 1991). Recent fossil evidence of dung-provisioned burrows strongly suggests that dung beetles evolved coprophagy through association with dinosaurs even before the diversification of mammals (Chin and Gill, 1996).

The amount of dung buried by a beetle species is primarily related to mean female body size (Horgan, 2001), though factors such as soil type and moisture (Sowig, 1995), pair cooperation (Sowig, 1996) and dung quality (Dadour and Cook, 1996) also play a role. These varied patterns of consumption and relocation of dung by beetles drive a series of ecological processes that include nutrient cycling, soil aeration, secondary seed burial, and parasite suppression.

Where they are directly relevant to humans, these ecosystem functions often provide important and/or economically beneficial ecosystem services (De Groot et al., 2002). Here we summarize our current knowledge about dung beetle ecosystem functions. We outline the circumstances wherein these functions become ecosystem services and highlight areas in need of further empirical study. We frame the importance of these ecological processes with a discussion of the numerous threats to dung beetle persistence.

Section snippets

Nutrient cycling

A significant proportion of the nutrients consumed by vertebrates are voided in excreta (Steinfeld et al., 2006) and the extent to which these nutrients can be returned to the plant growth cycle has strong implications for plant productivity. The transfer of freshly deposited waste below the soil surface by tunneler and roller dung beetle species physically relocates nutrient rich organic material and instigates micro-organismal and chemical changes in the upper soil layers.

Nitrogen is an often

Ecosystem services

Ecosystem services are the subset of ecological functions that are directly relevant or beneficial to the human condition (De Groot et al., 2002). The few studies evaluating dung beetle ecosystem services have predominantly outlined their value to the livestock industry, particularly in the context of the Australian Dung Beetle Project.

Following European colonization, Australian livestock production in the absence of a native ruminant-adapted dung beetle fauna resulted in an estimated

Dung beetle response to anthropogenic threats

Multiple lines of evidence from temperate and tropical systems indicate that local and regional-scale changes in land-use and mammal faunas can severely alter patterns of dung beetle species diversity and abundance. The decline or local extinction of dung beetles will likely have significant short and long-term implications for the maintenance of the ecosystem processes outlined above.

Globally, tropical forest loss, modification and fragmentation are driving high rates of local extinction

Conclusion

In natural systems, dung beetles appear to play an important role in maintaining ecosystem integrity, especially through secondary seed dispersal and nutrient cycling. With the high sensitivity of dung beetles to many kinds of human activities and habitat disturbance, it is imperative to understand and protect these processes. In agricultural systems, dung beetles play an important role in increasing primary productivity and suppressing parasites of livestock. Improved understanding of the

Acknowledgments

We thank Andrés Gómez, Fernando Vaz-de-Mello and several anonymous reviewers whose contributions significantly improved this review. This review was fostered by the Scarabaeinae Research Network (Scarabnet.org), of which the authors are members. ScarabNet and this material are based upon work supported by the National Science Foundation under Grant No. DEB-0043443 to S. Spector (PI), at the Center for Biodiversity and Conservation at the American Museum of Natural History. Any opinions,

References (176)

  • E. Andresen

    Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest

    Biotropica

    (1999)
  • E. Andresen

    Effects of dung presence, dung amount and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae) seeds in Central Amazonia

    Journal of Tropical Ecology

    (2001)
  • E. Andresen

    Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers

    Ecological Entomology

    (2002)
  • E. Andresen et al.

    The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests

  • E. Andresen et al.

    Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees

    Oecologia

    (2004)
  • S. Anduaga et al.

    Importance of dung incorporation activity by three species of coprophagous beetle (Coleoptera: Scarabaeidae: Scarabaeinae) macrofauna in pastureland on “La Michilía” Biosphere Reserve in Durango

    Mexico Environmental Entomology

    (2007)
  • P.R. Armsworth et al.

    Ecosystem-service science and the way forward for conservation

    Conservation Biology

    (2007)
  • G.J. Arrow

    The fauna of the British India, including Ceylon and Burma

  • N.M. Asquith et al.

    Does mammal community composition control recruitment in neotropical forests? Evidence from Panama

    Ecology

    (1997)
  • R.C. Axtell

    Effect of Macrochelidae (Acarina: Megostigmata) on house fly production from dairy cattle manure

    Journal of Economic Entomology

    (1963)
  • G.H. Baker

    Managing earthworms as a resource in Australian pastures

  • R.C. Bergstrom

    Aphodius beetles as biological control agents of elk lungworm, Dictyocaulus hadweni

    Proceedings of the Helminthological Society of Washington

    (1983)
  • Bertone, M., 2004. Dung beetles (Coleoptera: Scarabaeidae and Geotrupidae) in North Carolina Pasture Ecosystem, In...
  • A.L. Bishop et al.

    Interactions between dung beetles (Coleoptera: Scarabaeidae) and the arbovirus vector Culicoides brevitarsis Kieffer (Diptera: Ceratopogonidae)

    Australian Journal of Entomology

    (2005)
  • R.R. Blume et al.

    Onthophagus gazella: effect on survival of horn flies in the laboratory

    Environmental Entomology

    (1973)
  • T. Borgmeier

    Canthon dives Harold (Col. Copridae), predator das femeas de Atta laevigata Smith (Hym. Formicidae)

    Revista de Entomologia

    (1937)
  • G.F. Bornemissza

    Could dung eating insects improve our pastures

    Journal of Australian Institute of Agricultural Science

    (1960)
  • G.F. Bornemissza

    Insectary studies on the control of the dung breeding flies by the activity of the dung beetle, Onthophagus gazella F. (Coleoptera, Scarabaeidae)

    Journal of the Australian Entomological Society

    (1970)
  • G.F. Bornemissza

    The Australian dung beetle project 1965–1975

    Australian Meat Research Committee Review

    (1976)
  • G.F. Bornemissza et al.

    An effect of dung beetle activity on plant yield

    Pedobiologia

    (1970)
  • R.P. Bryan

    The effects of dung beetles activity on the numbers of parasitic gastrointestinal helmintic larvae recovered from pasture samples

    Australian Journal of Agricultural Research

    (1973)
  • R.P. Bryan

    The effects of dung beetle, Onthophagus gazella, on the ecology of the infective larvae of gastrointestinal nematodes of cattle

    Australian Journal of Agricultural Research

    (1976)
  • R.L. Byford et al.

    A review of ectoparasites and their effect on cattle production

    Journal of Animal Science

    (1992)
  • Y. Cambefort

    Biogeography and evolution

  • J.E. Campbell et al.

    The effect of seeds of exotic species transported via horse dung on vegetation along trail corridors

    Plant Ecology

    (2001)
  • G.M. Carpaneto et al.

    Inferring species decline from collection records: roller dung beetles in Italy (Coleoptera, Scarabaeidae)

    Diversity and Distributions

    (2007)
  • J.C. Chambers et al.

    A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems

    Annual Review of Ecology and Systematics

    (1994)
  • K. Chin et al.

    Dinosaurs, dung beetles, and conifers: participants in a Cretaceous food web

    Palaios

    (1996)
  • M. Coe

    The role of termites in the removal of elephant dung in the Tsavo (East) National Park Kenya

    Journal of East African Wildlife

    (1977)
  • J.M. Constible et al.

    Dispersal of non-native plants by introduced bison in an island ecosystem

    Biological Invasions

    (2005)
  • V. Cortez-Gallardo et al.

    Actividad antifúngica del ácido 4-metoxi fenilácetico producido en las glándulas esternales de machos del escarabajo rodador Canthon cyanellus cyanellus (Coleoptera: Scarabaeidae)

    Entomología Mexicana

    (2007)
  • Costa, A.N., Vasconcelos, H.L., Vieira-Neto, E.H.M., Bruna, E.M., in press. Do herbivores exert top-down effects in...
  • Dadour, I., 2006. Control of bush flies by dung beetles, In Farmnote 58/91. Department of Agriculture and Food,...
  • I.R. Dadour et al.

    Survival and reproduction in the scarabaeine dung beetle Onthophagus binodis Thunberg (Coleoptera: Scarabaeidae) on dung produced by cattle on grain diets in feedlots

    Environmental Entomology

    (1996)
  • J.W. Dalling

    The fate of seed banks: factors influencing seed survival for light-demanding species in moist tropical forests

  • J.W. Dalling et al.

    Effect of soil depth on seedling emergence in tropical soil seed-bank investigations

    Functional Ecology

    (1995)
  • A.L. Davis et al.

    Scarabaeine dung beetles as indicators of biodiversity, habitat transformation and pest control chemicals in agro-ecosystems

    South African Journal of Science

    (2004)
  • B.M. Doube

    Biological control of the buffalo fly in Australia: the potential of the southern African dung fauna

  • P.B. Edwards et al.

    Patterns of nesting and dung burial in Onitis dung beetles: implications for pasture productivity and fly control

    Journal of Applied Ecology

    (1987)
  • Elphinstone, G., 2006. Queensland dung beetle project in review. Queensland Government Department of Primary Industries...
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    This review was fostered by the Scarabaeinae Research Network (ScarabNet), of which the authors are members. ScarabNet is a collaborative group of dung beetle taxonomists, biogeographers, ecologists and conservation biologists dedicated to developing the use of the Scarabaeinae as an invertebrate biodiversity focal taxon. The following additional ScarabNet members contributed to this effort: Jorge Noriega. ScarabNet is supported by the National Science Foundation’s Research Coordination Network program under Grant DEB-0043443 to S. Spector (P.I.).

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