Hostname: page-component-848d4c4894-nr4z6 Total loading time: 0 Render date: 2024-05-23T19:52:15.828Z Has data issue: false hasContentIssue false

Diversity and body size of dung beetles attracted to different dung types along a tropical land-use gradient in Sulawesi, Indonesia

Published online by Cambridge University Press:  08 December 2009

Faculty of Agriculture, University of Tadulako, Palu, Central Sulawesi, Indonesia
Purnama Hidayat
Department of Plant Protection, Faculty of Agriculture, Bogor Agricultural University (IPB), Indonesia
Sjafrida Manuwoto
Department of Plant Protection, Faculty of Agriculture, Bogor Agricultural University (IPB), Indonesia
Woro A. Noerdjito
Museum Zoologicum Bogoriense, LIPI, Cibinong, Bogor, Indonesia
Teja Tscharntke
Agroecology, Georg-August University, Waldweg 26, D-37073 Göttingen, Germany
Christian H. Schulze*
Department of Population Ecology, Faculty of Life Sciences, University of Vienna, Althanstraße 14, A-1090 Wien, Austria
1Corresponding author. Email:


Dung beetles are a functionally important component of most terrestrial ecosystems, but communities change with habitat disturbance and deforestation. In this study, we tested if dung beetle ensembles on dung of introduced cattle and of the endemic anoa, a small buffalo, are affected differentially by habitat disturbance. Therefore, we exposed 10 pitfall traps, five baited with anoa and five baited with cattle dung, per site in six habitat types ranging from natural and selectively logged rain forest to three types of agroforestry system (characterized by different management intensity) and open areas (n = 4 replicate sites per habitat type) at the margin of Lore Lindu National Park, Central Sulawesi, Indonesia. We found 28 species, 43% of which were endemic to Sulawesi. Species richness, abundance and biomass declined from natural forest towards open area. Large-bodied species appeared to be more sensitive to habitat disturbance and the ratio of large to small-sized dung beetles declined with land-use intensity. Although selectively logged forest and cocoa agroforestry systems had lower species richness compared with natural forest, they appeared to maintain a high portion of species originally inhabiting forest sites. The similarity of dung beetle ensembles recorded at forest and agroforestry sites reflects the high similarity of some habitat variables (e.g. vegetation structure and microclimate) between both habitat types compared with open areas. Species richness and abundances as well as species composition, which was characterized by decreases in mean body size, changed with land-use intensity, indicating that dung type is less important than habitat type for determining ensemble structure of these Indonesian dung beetles.

Research Article
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)



AL-HOUTY, W. & AL-MUSALAM, F. 1997. Dung preference of the dung beetle Scarabeus cristatus Fab (Coleoptera: Scarabaeidae). Journal of Arid Environment 35:511516.CrossRefGoogle Scholar
ANDRESEN, E. 2002. Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecological Entomology 27:257270.CrossRefGoogle Scholar
ANDRESEN, E. 2003. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography 26:8797.Google Scholar
ANDRESEN, E. & LEVEY, D. J. 2004. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:4554.CrossRefGoogle ScholarPubMed
ARELLANO, L., FAVILA, M. E. & HUERTA, C. 2005. Diversity of dung and carrion beetles in a disturbed Mexican tropical montane cloud forest and on shade coffee plantations. Biodiversity and Conservation 14:601615.CrossRefGoogle Scholar
AVENDAÑO-MENDOZA, C., MORÓN-RÍOS, A., CANO, E. B. & LEÓN-CORTÉS, J. 2005. Dung beetle community (Coleoptera: Scarabaeidae: Scarabaeinae) in a tropical landscape at the Lachua Region, Guatemala. Biodiversity and Conservation 14:801822.CrossRefGoogle Scholar
BALTHASAR, V. 1963. Monographie der Scarabaeidae und Aphodiidae der palaearktischen und orientalischen Region. Band 1. Verlag der Tschechoslowakischen Akademie der Wissenschaften, Prague. 391 pp.Google Scholar
BARBERO, E., PALESTRINI, C. & ROLANDO, A. 1999. Dung beetle conservation: effects of habitat and resource selection (Coleoptera: Scarabaeoidea). Journal of Insect Conservation 3:7584.CrossRefGoogle Scholar
BOS, M. 2006. Insect diversity and trophic interactions in shaded cacao agroforestry and natural forests in Indonesia. PhD thesis. Georg-August-Universität Göttingen, Göttingen. 104 pp.Google Scholar
BOS, M., HÖHN, P., SHAHABUDDIN, S., BUCHORI, D., STEFFAN-DEWENTER, I. & TSCHARNTKE, T. 2007. Insect responses to forest conversion and agroforestry management. Pp. 279296 in Tscharntke, T., Leuschner, C., Guhardja, E. & Zeller, M. (eds.). The stability of tropical rainforest margins: linking ecological, economic and social constraints of land-use and conservation. Springer, Berlin.Google Scholar
BROSE, U., MARTINEZ, N. D. & WILLIAMS, R. J. 2003. Estimating species richness: sensitivity to sample coverage and insensitivity to spatial patterns. Ecology 84:23642377.CrossRefGoogle Scholar
CLARKE, K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal Ecology 18:117143.Google Scholar
CLARKE, K. R. & WARWICK, R. M. 2001. Change in marine communities: an approach to statistical analysis and interpretation. Primer-E, Plymouth. 163 pp.Google Scholar
COLWELL, R. K. & CODDINGTON, J. A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London Series B 345:101118.Google Scholar
DAVIS, A. J. & SUTTON, S. L. 1998. The effects of rainforest canopy loss on arboreal dung beetles in Borneo: implications for the measurement of biodiversity in derived tropical ecosystems. Diversity and Distributions 4:167173.CrossRefGoogle Scholar
DAVIS, A. J., HUIJBREGTS, H. & KRIKKEN, J. 2000. The role of local and regional processes in shaping dung beetle communities in tropical forest plantations in Borneo. Global Ecology and Biogeography 9:281292.CrossRefGoogle Scholar
DAVIS, A. J., HOLLOWAY, J. D., HUIJBREGTS, H., KRIKKEN, J. & SUTTON, S. L. 2001. Dung beetles as indicators of change in the forests of Northern Borneo. Journal of Applied Ecology 38:593616.Google Scholar
DORMONT, L., GUILLAUME, E. & LUMARET, J. P. 2004. Trophic preferences mediated by olfactory cues in dung beetles colonizing cattle and horse dung. Environmental Entomology 33:370377.CrossRefGoogle Scholar
DOUBE, B. M. 1991. Dung beetles of Southern Africa. Pp. 133155 in Hanski, I. & Cambefort, Y. (eds.). Dung beetle ecology. Princeton University Press, Princeton.CrossRefGoogle Scholar
ERROUISSI, F., HALOTI, S., ROBERT, P. J., IDRISSI, A. J. & LUMARET, J. P. 2004. Effect of the attractiveness for dung beetles of dung pat origin and size along climatic gradient. Environmental Entomology 33:4553.CrossRefGoogle Scholar
ESTRADA, A., HALFFTER, G., COATES-ESTRADA, R. & MERRIT, D. A. 1993. Dung beetles attracted to mammalian herbivore (Alouatta palliata) and omnivore (Nasua narica) dung in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology 9:4554.CrossRefGoogle Scholar
FINCHER, G. T. 1973. Nidification and reproduction of Phanaeus spp. in three textural classes of soil (Coleoptera: Scarabaeidae). Coleopterists’ Bulletin 27:3337.Google Scholar
FINN, J. & GILLER, P. S. 2002. Experimental investigations of colonisation by north temperate dung beetles of different types of domestic herbivore dung. Applied Soil Ecology 20:113.CrossRefGoogle Scholar
GALANTE, E. & CARTAGENA, C. 1999. Comparison of Mediterranean dung beetles (Coleoptera: Scarabaeoidea) in cattle and rabbit dung. Environmental Entomology 28:420424.CrossRefGoogle Scholar
GARDNER, T. A., HERNÁNDEZ, M. I. M., BARLOW, J. & PERES, C. A. 2008. Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of Applied Ecology 45:883893.Google Scholar
GEROLD, G., FREMERY, M. & GUHARDJA, E. 2004. Land-use, nature conservation and the stability of rainforest margins in Southeast Asia. Springer, Berlin. 534 pp.CrossRefGoogle Scholar
GITTINGS, T. & GILLER, P. S. 1998. Resource quality and the colonisation and succession of coprophagous beetles. Ecography 21:581592.CrossRefGoogle Scholar
HALFFTER, G. & FAVILA, M. E. 1993. The Scarabaeinae (Coleoptera): an animal group for analysing, inventorying and monitoring biodiversity in tropical rainforest and modified landscapes. Biology International 27:1521.Google Scholar
HANSKI, I. & CAMBEFORT, Y. (eds.). 1991. Dung beetle ecology. Princeton University Press, Princeton.CrossRefGoogle Scholar
HANSKI, I. & KRIKKEN, J. 1991. Dung beetles in tropical forests in South-East Asia. Pp. 179197 in Hanski, I. & Cambefort, Y. (eds.). Dung beetle ecology. Princeton University Press, Princeton.CrossRefGoogle Scholar
HARVEY, C. A., GONZALEZ, J. & SOMARRIBA, E. 2006. Dung beetle and terrestrial mammal diversity in forests, indigenous agroforestry systems and plantain monocultures in Talamanca, Costa Rica. Biodiversity and Conservation 15:555585.CrossRefGoogle Scholar
HILL, C. J. 1996. Habitat specificity and food preferences of an assemblage of tropical Australian dung beetles. Journal of Tropical Ecology 12:449460.CrossRefGoogle Scholar
HOLTER, P., SCHOLTZ, C. H. & WARDHAUGH, K. G. 2002. Dung feeding in adult scarabaeines (tunnellers and endocoprids): even large dung beetles eat small particles. Ecological Entomology 27:169176.Google Scholar
HORGAN, F. G. 2005. Effects of deforestation on diversity, biomass and function of dung beetles on the eastern slopes of the Peruvian Andes. Forest Ecology and Management 216:117133.Google Scholar
JANKIELSOHN, A., SCHOLTZ, C. H. & LOUW, S. V. D. M. 2001. Effect of habitat transformation on dung beetle assemblages: a comparison between a South African nature reserve and neighboring farms. Ecological Entomology 30:474483.Google Scholar
KLEIN, B. C. 1989. Effects of forest fragmentation on dung and carrion beetle communities in Central Amazonia. Ecology 70:17151725.Google Scholar
KLEIN, A. M., STEFFAN-DEWENTER, I. & TSCHARNTKE, T. 2002. Predator-prey ratios on cocoa along a land-use gradient in Indonesia. Biodiversity and Conservation 11:683693.CrossRefGoogle Scholar
KLEIN, A.-M., STEFFAN-DEWENTER, I. & TSCHARNTKE, T. 2003. Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedings of the Royal Society of London Series B 270:955961.CrossRefGoogle ScholarPubMed
LARSEN, T. H., WILLIAMS, N. M. & KREMEN, C. 2005. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters 8:538547.Google Scholar
LAWTON, J. H., BIGNELL, D. E., BOLTON, B., BLOEMERS, G. F., EGGLETON, P., HAMMOND, P. M., HODDA, M., HOLT, R. D., LARSEN, T. B., MAWDSLEY, N. A., STORK, N. E., SRIVASTAVA, D. S. & WATT, A. D. 1998. Biodiversity inventories, indicator taxa and effects of habitat modification in tropical rain forest. Nature 391:7276.CrossRefGoogle Scholar
MARTIN-PIERA, F. & LOBO, J. M. 1996. A comparative discussion of the trophic preferences in dung beetles communities. Miscellània Zoològica 19:1331.Google Scholar
MCGEOCH, M. A., VAN RENSBURG, B. J. & BOTES, A. 2002. The verification and application of bioindicators: a case study of dung beetles in a savanna ecosystem. Journal of Applied Ecology 39:661672.Google Scholar
MENENDEZ, R. & GUTIERREZ, D. 1996. Altitudinal effects on habitat selection of dung beetles (Scarabaeoidea: Aphodiidae) in the northern Iberian Peninsula. Ecography 19:313317.Google Scholar
MIRANDA, C. H. B., DOS SANTOS, J. C. C. & BIANCHIN, I. 1998. Contribution of Onthophagus gazella to soil fertility improvement by bovine fecal mass incorporation into the soil. 1. Greenhouse studies. Revista Brasileira de Zootecnia 27:681685.Google Scholar
MIRANDA, C. H. B, DOS SANTOS, J. C. C. & BIANCHIN, I. 2001. The role of Digitonthophagus gazella in pasture cleaning and production as a result of burial of cattle dung. Pasturas Tropicales 22:1418.Google Scholar
MITTAL, I. C. 1993. Natural manuring and soil conditioning by dung beetles. Tropical Ecology 34:150159.Google Scholar
MUSSER, G. G. 1987. The mammals of Sulawesi. Pp. 7393 in Whitmore, T. C. (ed.). Biogeographical evolution of the Malay Archipelago. Oxford University Press, Oxford.Google Scholar
MYERS, N., MITTELMEIER, R. A., MITTELMEIER, C. G., DA FONSECA, G. A. B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 493:853858.CrossRefGoogle Scholar
NICHOLS, E., LARSEN, T., SPECTOR, S., DAVIS, A. L., ESCOBAR, F., FAVILA, M. & VULINEC, K. 2007. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biological Conservation 137:119.CrossRefGoogle Scholar
PETERSEN, F. T., MEIER, R. & LARSEN, M. N. 2003. Testing species richness estimation methods using museum label data on the Danish Asilidae. Biodiversity and Conservation 12:687701.Google Scholar
RAMADHANIL, 2006. Structure and composition of vegetation in six land-use types in the Lore Lindu National Park, Central Sulawesi, Indonesia. PhD thesis. Bogor Agricultural University, Bogor.Google Scholar
SCHEFFLER, P. Y. 2005. Dung beetle (Coleoptera: Scarabaeidae) diversity and community structure across three disturbance regimes in eastern Amazonia. Journal of Tropical Ecology 21;919.Google Scholar
SCHULZE, C. H., WALTERT, M., KESSLER, P. J. A, PITOPANG, R., SHAHABUDDIN, , VEDDELER, D., STEFFAN-DEWENTER, I., MÜHLENBERG, M., GRADSTEIN, S. R. & TSCHARNTKE, T. 2004. Biodiversity indicator groups of tropical land-use systems: comparing plants, birds, and insects. Ecological Application 14:13211333.CrossRefGoogle Scholar
SHAHABUDDIN, 2007. Effect of land use on dung beetles (Coleoptera:Scarabaeidae) diversity and dung decomposition in Central Sulawesi, Indonesia. PhD thesis. Bogor Agricultural University, Bogor, Indonesia.Google Scholar
SHAHABUDDIN, , SCHULZE, C. H. & TSCHARNTKE, T. 2005. Changes of dung beetle communities from rainforests towards agroforestry systems and annual cultures. Biodiversity and Conservation 14:863877.Google Scholar
SOKAL, R. R. & ROHLF, F. J. 1994. Biometry: the principles and practice of statistics in biological research. Freeman and Company, New York. 888 pp.Google Scholar
STEFFAN-DEWENTER, I., KESSLER, M., BARKMANN, J., BOS, M. M., BUCHORI, D., ERASMI, S., FAUST, H., GEROLD, G., GLENK, K., GRADSTEIN, R. S., GUHARDJA, E., HARTEVELD, M., HERTEL, D., HOHN, P., KAPPAS, M., KOHLER, S., LEUSCHNER, C., MAERTENS, M., MARGGRAF, R., KLEIAN, S. M., MOGEA, J., PITOPANG, R., SCHAEFER, M., SCHWARTZE, S., SPORN, S. G., STEINGREBE, A., TJITROSOEDIRDJO, S. S., TJITROSOEMITO, S., TWELE, A., WEBER, R., WOLTMANN, L., ZELLER, M. & TSCHARNTKE, T. 2007. Tradeoffs between income, biodiversity, and ecosystem functioning during tropical rainforest conversion and agroforestry intensification. Proceedings of the National Academy of Sciences USA 104:49734978.Google Scholar
STRONG, D. R., LAWTON, J. H. & SOUTHWOOD, R. 1984. Insects on plants. Community patterns and mechanisms. Blackwell Scientific Publications, Oxford. 313 pp.Google Scholar
TSCHARNTKE, T., KLEIN, A.-M., KRUESS, A., STEFFAN-DEWENTER, I. & THIES, C. 2005. Landscape perspectives on agricultural intensification and biodiversity–ecosystem service management. Ecology Letters 8:857874.CrossRefGoogle Scholar
VERDU, J. R., ARELLANO, L. & NUMA, C. 2006. Thermoregulation in endothermic dung beetles (Coleoptera: Scarabaeidae): effect of body size and ecophysiological constraints in flight. Journal of Insect Physiology 52:854860.Google Scholar
WALTHER, B. A. & MOORE, J. L. 2005. The concepts of bias, precision and accuracy, and their use in testing the performance of species richness estimators, with a literature review of estimator performance. Ecography 28:815829.Google Scholar
WHITTEN, A. J., MUSTAFA, M. & HENDERSON, G. S. 2002. The ecology of Sulawesi. Periplus, Hong Kong. 754 pp.Google Scholar