Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-25T03:24:20.116Z Has data issue: false hasContentIssue false

Dung beetle community assemblages in a southern African landscape: niche overlap between domestic and wild herbivore dung

Published online by Cambridge University Press:  20 August 2021

B. Sands*
Affiliation:
School of Biological Sciences, University of Bristol, Bristol, UK
N. Mgidiswa
Affiliation:
Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana
S. Curson
Affiliation:
School of Biological Sciences, University of Bristol, Bristol, UK
C. Nyamukondiwa
Affiliation:
Department of Biological Sciences and Biotechnology, Botswana International University of Science and Technology, Palapye, Botswana
R. Wall
Affiliation:
School of Biological Sciences, University of Bristol, Bristol, UK
*
Author for correspondence: B. Sands, Email: [email protected]

Abstract

Dung beetles provide important ecosystem functions in semiarid environments, improving the physiochemical characteristics of the soil through tunnelling and burying nutrient-rich dung. In sub-Saharan Africa, diverse indigenous mammal communities support highly abundant dung beetle populations in savannah ecosystems. However, the conversion of landscapes to livestock agriculture may result in changes in the abundance and diversity of wild mammal species. This is likely to have significant impacts on dung beetle communities, particularly because domestic livestock dung may be contaminated with toxic residues of veterinary parasiticides. The environmental impact is likely to be affected by the degree of niche overlap between the beetle communities that colonize cattle dung and those that colonize the dung of wild mammals. We compared dung beetle communities between a pristine national park habitat dominated by large wild herbivores, and a pastoral farming community dominated by domestic livestock. Diurnal dung beetles were attracted to cattle dung in greater abundance and diversity compared to elephant, zebra or giraffe dung. Nocturnal/crepuscular dung beetles were attracted to non-ruminant dung (elephant and zebra) in higher abundance compared to ruminant dung (cattle and giraffe). Although there were no clear trophic specializations, three diurnal species showed an association with cattle dung, whereas eight nocturnal/crepuscular species showed an association with non-ruminant (elephant and zebra) dung. Diurnal species may be at greater risk from the toxic effects of residues of veterinary parasiticides in domestic livestock dung. Although many species showed trophic associations with wild herbivore dung, these beetles can utilize a wide range of dung and will readily colonize cattle dung in the absence of other options. As more land is converted to livestock agriculture, the contamination of dung with toxic residues from veterinary parasiticides could therefore negatively impact the majority of dung beetle species.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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.)

References

Alexander, M and Wardhaugh, K (2001) Workshop on the effects of parasiticides on dung beetles report of proceedings. Technical Report No. 89. The Bardon Centre, Brisbane, Queensland, Australia.Google Scholar
Bang, HS, Lee, J-H, Kwon, OA, Na, Y-E, Jang, YS and Kim, WH (2005) Effects of paracoprid dung beetles (Coleoptera: Scarabaeidae) on the growth of pasture herbage and on the underlying soil. Applied Soil Ecology 29, 165171. doi: 10.1016/j.apsoil.2004.11.001CrossRefGoogle Scholar
Bang, HS, Lee, J-H, Na, YE and Wall, R (2007) Reproduction of the dung beetles (Copris tripartitus) in the dung of cattle treated with cis-cypermethrin and chlorpyrifos. Applied Soil Ecology 35, 546552.CrossRefGoogle Scholar
Bertone, MA, Green, JT, Washburn, SP, Poore, MH and Watson, DW (2006) The contribution of tunnelling dung beetles to pasture soil nutrition. Forage and Grazing Lands 4, 112.CrossRefGoogle Scholar
Bianchin, I, Honer, MR, Gomes, A and Koller, WW (1992) Efeito de alguns carrapaticides/insecticidas sobre Onthophagus gazella. EMBRAPA Communicado Tecnico 45, 17.Google Scholar
Bianchin, I, Alves, RGO and Koller, WW (1997) Efeito de alguns carrapaticides/insecticidas de aspersão sobre os adultos de Onthophagus gazella (F.). Ecossistema 22, 116119.Google Scholar
Bianchin, I, Alves, RGO and Koller, WW (1998) Efeito de carrapaticides/insecticidas ‘pour-on’ sobre adultos do besouro coprofago Africano Onthophagus gazella Fabr. (Coleoptera: Scarabaeidae). Anais da Sociedade Entomologica do Brazil 27, 275279.CrossRefGoogle Scholar
Bozdogan, H (1987) Model selection and Akaike's information criterion (AIC): the general theory and its analytical extensions. Psychometrika 52, 345370.CrossRefGoogle Scholar
Byrne, M and Dacke, M (2011) The visual ecology of dung beetles. In Simmons, LW and Ridsill-Smith, TJ (eds), Ecology and Evolution of Dung Beetles. Sussex, UK: Wiley-Blackwell, pp. 177199.CrossRefGoogle Scholar
Carvalho, R, Frazao, F, Ferreira-Châline, RS and França, FM (2018) Dung burial by roller dung beetles (Coleoptera: Scarabaeinae): an individual and specific-level study. International Journal of Tropical Insect Science 38, 373380. doi: 10.1017/S1742758418000206CrossRefGoogle Scholar
Chao, A, Gotelli, NJ, Hsieh, TC, Sander, EL, Ma, KH, Colwell, RK and Ellison, AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs 84, 4576.CrossRefGoogle Scholar
Dacke, M, Nordström, P and Scholtz, CH (2003) Twilight orientation to polarised light in the crepuscular dung beetle Scarabeaus zambezianus. The Journal of Experimental Biology 206, 15351543.CrossRefGoogle Scholar
Dacke, M, Baird, E, Byrne, M, Scholtz, C and Warrant, EJ (2013) Dung beetles use the Milky Way for orientation. Current Biology 23, 298300.CrossRefGoogle ScholarPubMed
da Silva, PG and 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, e0126112.CrossRefGoogle Scholar
Davis, ALV (1996a) Community organization of dung beetles (Coleoptera: Scarabaeidae): differences in body size and functional group structure between habitats. African Journal of Ecology 34, 258275.CrossRefGoogle Scholar
Davis, ALV (1996b) Diel and seasonal community dynamics in an assemblage of coprophagous, Afrotropical, dung beetles (Coleoptera: Scarabaeidae s. str., Aphodiidae, and Staphylinidae: Oxytelinae). Journal of African Zoology 110, 291308.Google Scholar
Davis, AJ (1999) Species packing in tropical forests: diel flight activity of rainforest dung-feeding beetles (Coleoptera: Aphodiidae, Scarabeisae, Hybosoridae) in Borneo. The Raffles Bulletin of Zoology 47, 473486.Google Scholar
Davis, A (2002) Dung beetle diversity in South Africa: influential factors, conservation status, data inadequacies and survey design. African Entomology 10, 5365.Google Scholar
Davis, ALV and Scholtz, CH (2001) Historical vs. ecological factors influencing global patterns of Scarabaeine dung beetle diversity. Diversity and Distributions 7, 161174.CrossRefGoogle Scholar
Davis, A, Frolov, V and Scholtz, C (2008) The African Dung Beetle Genera. Pretoria, South Africa: Protea Book House.Google Scholar
D. E. A. (2016) National Biodiversity Strategy and Action Plan. Gaborone, Botswana: Department of Environmental Affairs.Google Scholar
De Caceres, M and Legendre, P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90, 35663574. doi: 10.1890/08-1823.1CrossRefGoogle ScholarPubMed
De Wit, P and Nachtergaele, F (1990) Soil Map of the Republic of Botswana. Soil Mapping and Advisory Services Project FAO/BOT/85/011. Map 1 of 2. FAO.Google Scholar
Dufrêne, M and Legendre, P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67, 345366.Google Scholar
DWNP (2012) Aerial Census of Animals in Botswana 2012 dry Season. Gaborone, Republic of Botswana: Department of Wildlife and National Parks.Google Scholar
Edwards, PB (1991) Seasonal variation in the dung of African grazing mammals, and its consequences for coprophagous insects. Functional Ecology 5, 617628.CrossRefGoogle Scholar
Feer, F and Pincebourde (2005) Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles. Journal of Tropical Ecology 21, 2130.CrossRefGoogle Scholar
FEWS (2016) Illustrating he extent and severity of the 2015-16 drought. Southern Africa Special Report. Famine Early Warning Network, USAID.Google Scholar
Fincher, G (1981) The potential value of dung beetles in pasture ecosystems [Texas]. The Journal of the Georgia Entomological Society 16, 316333.Google Scholar
Floate, KD, Wardhaugh, KG, Boxall, ABA and Sherratt, TN (2005) Faecal residues of veterinary parasiticides: nontarget effects in the pasture environment. Annual Review of Entomology 50, 153179.CrossRefGoogle ScholarPubMed
Frank, K, Brückner, A, Hilpert, A, Heethoff, M and Blüthgen, N (2017) Nutrient quality of vertebrate dung as a diet for dung beetles. Scientific Reports 7, 12141.CrossRefGoogle ScholarPubMed
Gaynor, KM, Branco, PS, Long, RA, Gonçalves, DD, Granli, PK and Poole, JH (2018) Effects of human settlement and roads on diel activity patterns of elephants (Loxodonta africana). African Journal of Ecology 56, 872881.CrossRefGoogle Scholar
Gotcha, N, Machekano, H, Cuthbert, RN and Nyamukondiwa, C (2020) Heat tolerance may determine activity time in coprophagic beetle species (Coleoptera: Scarabaeidae). Insect Science 28, 10761086. doi: 10.1111/1744-7917.12844CrossRefGoogle Scholar
Hamer, KC, Humphreys, EM, Magalhaes, MC, Garthe, S, Hennicke, J, Peters, G, Grémillet, D, Skov, H and Wanless, S (2009) Fine-scale foraging behaviour of a medium-ranging marine predator. Journal of Animal Ecology 78, 880889.CrossRefGoogle ScholarPubMed
Hanski, I and Cambefort, Y (1991) Dung Beetle Ecology. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
Holter, P (1979) Effect of dung-beetles (Aphodius spp.) and earthworms on the disappearance of cattle dung. OIKOS 32, 393402.CrossRefGoogle Scholar
Holter, P, Scholtz, CH and Wardhaugh, KG (2002) Dung feeding in adult Scarabaeines (tunnellers and endocoprids): even large dung beetles eat small particles. Ecological Entomology 27, 169176.CrossRefGoogle Scholar
Hothorn, T, Bretz, F and Westfall, P (2008) Simultaneous inference in general parametric models. Biometric Journal 50, 346363.CrossRefGoogle ScholarPubMed
Hsieh, TC, Ma, KH and Chao, A (2020) iNEXT: iNterpolation and EXTrapolation for species diversity. R package version 2.0.20 URL. Available at http://chao.stat.nthu.edu.tw/wordpress/software-download/.Google Scholar
Krell-Westerwalbesloh, S, Krell, FT and Linsenmair, KE (2004) Diel separation of Afrotropical dung beetle guilds – avoiding competition and neglecting resources (Coleoptera: Scarabaeoidea). Journal of Natural History 38, 22252249.CrossRefGoogle Scholar
Krüger, K and Scholtz, CH (1998) Changes in the structure of dung insect communities after ivermectin usage in a grassland ecosystem. I. Impact of ivermectin under drought conditions. Acta Oecologica 19, 425438.CrossRefGoogle Scholar
Larsen, TH, Lopera, A and Forsyth, A (2006) Extreme trophic and habitat specialisation by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin 60, 315324.CrossRefGoogle Scholar
Lepš, J and Šmilauer, P (2003) Multivariate Analysis of Ecological Data Using CANOCO. Cambridge, UK: Cambridge Press. Supplementary materials.CrossRefGoogle Scholar
Lovemore, DF (1992) A regional approach to trypanosomiasis control: Activities and progress of the RTTCP (Regional Tsetse Trypanosomiasis Control Programme). Regional Tsetse and Trypanosomiasis Control Programme, Harare, Zimbabwe. Available at http://www.fao.org/docrep/004/T0599E/T0599E12.htm.Google Scholar
Martin-Piera, F and Lobo, JM (1996) A comparative discussion of trophic preferences in dung beetle communities. Miscellania Zoologica 19, 1331.Google Scholar
Mittal, I (1993) Natural manuring and soil conditioning by dung beetles. Tropical Ecology 34, 150159.Google Scholar
Moleele, NM and Mainah, J (2003) Resource use conflicts: the future of the Kalahari ecosystem. Journal of Arid Environments 54, 405423.CrossRefGoogle Scholar
Nieto, M, Hortal, J, Martínez-Maza, C, Morales, J, Ortiz-Jaureguizar, E, Pelaex-Campomanes, P, Pickford, M, Prado, JL, Rodríguez, J, Senut, B, Soria, D and Varela, S (2005) Historical determinants of mammal diversity in Africa: evolution of mammalian body mass distribution in Africa and South America during neogene and quarternary times. In Huber, BA, Sinclair, BJ and Lampe, K-H (eds), African Biodiversity. Boston, MA: Springer, pp. 287295. doi: 10.1007/0-387-24320-8_28.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) Vegan: Community Ecology Package. R package version 2.5-6. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Olson, DM, Dinerstein, E, Wikramanayake, ED, Burgess, ND, Powell, GVN, Underwood, EC, D'amico, JA, Itoua, I, Strand, HE, Morrison, JC, Loucks, CJ, Allnutt, TF, Ricketts, TH, Kura, Y, Lamoreux, JF, Wettengel, WW, Hedao, P and Kassem, KR (2001) Terrestrial ecoregions of the world: a new map of life on earth: a new global map of terrestrial ecoregions provides an innovative tool for conserving biodiversity. BioScience 51, 933938.CrossRefGoogle Scholar
Parmesan, C and Yohe, G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 3742.CrossRefGoogle ScholarPubMed
Philips, TK (2011) The evolutionary history and diversification of dung beetles. In Simmons, LW and Ridsill-Smith, TJ (eds), Ecology and Evolution of Dung Beetles. Sussex, UK: Wiley-Blackwell, pp. 2146.CrossRefGoogle Scholar
Raine, EH and Slade, EM (2019) Dung beetle-mammal associations: methods, research trends and future directions. Proceedings of the Royal Society B 286, 20182002. doi: 10.1098/rspb.2018.2002CrossRefGoogle ScholarPubMed
RStudio Team (2019) RStudio: Integrated Development for R. Boston, MA: RStudio, Inc. URL Available at http://www.rstudio.com/.Google Scholar
Sands, B, Mgidiswa, N, Nyamukondiwa, C and Wall, R (2018) Environmental consequences of deltamethrin residues in cattle feces in an African agricultural landscape. Ecology and Evolution 14, 29382946.CrossRefGoogle Scholar
Simmons, LW and Ridsill-Smith, TJ (2011) Ecology and Evolution of Dung Beetles. Sussex, UK: Wiley-Blackwell.CrossRefGoogle Scholar
Sitters, J, Maechler, M-J, Edwards, PJ, Suter, W and Venterink, HO (2013) Interactions between C:N:P stoichiometry and soil macrofauna control dung decomposition of savanna herbivores. Functional Ecology 28, 776786.CrossRefGoogle Scholar
Spickett, AM and Fivaz, BH (1992) A survey of tick control practices in the Eastern Cape province of South Africa. Onderstepoort Journal of Veterinary Research 59, 203210.Google Scholar
Stanbrook, R, Norrey, J, Kisingo, AW and Jones, M (2021) Dung beetle diversity and community composition along a land use gradient in a savannah ecosystem of north western Tanzania. Tropical Conservation Science, 115. doi: 10.1177/19400829211008756Google Scholar
Strong, WL (2002) Assessing species abundance unevenness within and between plant communities. Community Ecology 3, 237246.CrossRefGoogle Scholar
Thomas, CD, Cameron, A, Green, RE, Bakkenes, M, Beaumont, LJ, Collingham, Y,C, Erasmus, BFN, Ferreira de Siqueira, M, Grainger, A, Hannah, L, Hughes, L, Huntley, B, van Jaarsveld, AS, Midgley, GF, Miles, L, Ortega-Huerta, MA, Peterson, AT, Phillips, OL and Williams, SE (2004) Extinction risk from climate change. Nature 427, 145148.CrossRefGoogle ScholarPubMed
Tocco, C, Balmer, JP and Villet, MH (2018) Trophic preference of southern African dung beetles (Scarabaeoidae: Scarabaeinae and Aphodiinae) and its influence on bioindicator surveys. African Journal of Ecology 56, 938948.CrossRefGoogle Scholar
Tshikae, BP, Davis, ALV and Scholtz, CH (2008) Trophic associations of a dung beetle assemblage (Scarabaeidae: Scarabaeinae) in a woodland savanna of Botswana. Environmental Entomology 37, 431441.CrossRefGoogle Scholar
Tshikae, BP, Davis, ALV and Scholtz, CH (2013a) Does an aridity and trophic resource gradient drive patterns of dung beetle food selection across the Botswana Kalahari? Ecological Entomology 38, 8395.CrossRefGoogle Scholar
Tshikae, BP, Davis, ALV and Scholtz, CH (2013b) Dung beetle assemblage structure across the aridity and trophic resource gradient of the Botswana Kalahari: patterns and drivers at regional and local scales. Journal of Insect Conservation 17, 623636.CrossRefGoogle Scholar
Vale, GA, Grant, IF, Dewhurst, CF and Aigreau, D (2004) Biological and chemical assays of pyrethroids in cattle dung. Bulletin of Entomological Research 94, 273282.CrossRefGoogle ScholarPubMed
Venant, A, Belli, P, Borrel, S and Mallet, J (1990) Excretion of deltamethrin in lactating dairy cows. Food Additives and Contaminants 7, 535543.CrossRefGoogle ScholarPubMed
Venema, JH and Kgaswanyane, M (1996) Agricultural land use plan for Letlhakane agricultural district central region. United Nations Development Programme. Food and Agriculture Organization of the United Nations.Google Scholar
Verdú, JR, Cortez, V, Ortiz, AJ, González-Rodríguez, E, Martinez-Pinna, J, Lumaret, J-P, Lobo, JM, Numa, C and Sánchez-Piñero, F (2015) Low doses of ivermectin cause sensory and locomotor disorders in dung beetles. Scientific Reports 5, 13912.CrossRefGoogle ScholarPubMed
Wardhaugh, KG (2005) Insecticidal activity of synthetic pyrethroids, organophosphates, insect growth regulators, and other livestock parasiticides: an Australian perspective. Environmental Toxicology and Chemistry 24, 789796.CrossRefGoogle Scholar
Wardhaugh, KG, Longstaff, BC and Lacey, MJ (1998) Effects of residues of deltamethrin in cattle faeces on the development and survival of three species of dung-breeding insect. Australian Veterinary Journal 76, 273280.CrossRefGoogle ScholarPubMed
Wurmitzer, C, Blüthgen, N, Krell, F-T, Maldonado, B, Ocampo, F, Müller, J and Schmitt, T (2017) Attraction of dung beetles to herbivore dung and synthetic compounds in a comparative field study. Chemoecology 27, 7584.CrossRefGoogle Scholar
Supplementary material: File

Sands et al. supplementary material

Sands et al. supplementary material 1

Download Sands et al. supplementary material(File)
File 21.4 KB
Supplementary material: File

Sands et al. supplementary material

Sands et al. supplementary material 2

Download Sands et al. supplementary material(File)
File 26.5 KB