DUNG TYPE OR INTRASPECIFIC VARIATION IN BIOMASS: WHAT IS MORE IMPORTANT IN DETERMINING DUNG BEETLE ECOLOGICAL FUNCTION?

Authors

  • Paula Braga Universidade Federal de Lavras
  • Raquel Luiza de Carvalho Universidade Federal de Lavras
  • Julio Louzada Universidade Federal de Lavras
  • Lívia Dorneles Audino Universidade Federal de Lavras

DOI:

https://doi.org/10.4257/oeco.2019.2303.12

Keywords:

Chalcocopris hesperus, Dichotomius bos, dung removal, Scarabaeinae, soil excavated

Abstract

We evaluated the relative importance of dung type and intraspecific variation in biomass on dung beetle function by quantifying the ecological functions (dung removal and soil excavation) of two dung beetle species under laboratory conditions: Dichotomius bos, which preferentially feeds on herbivorous dung, and Chalcocopris hesperus, which is a generalist coprophagous species. Two treatments were used, cattle dung and swine dung, which consisted of a container with soil, dung, and two individuals of the two species that had been weighed prior to the experiment. Dichotomius bos was better at dung removal and soil excavation in the treatment containing the dung of its preference, where as for C. hesperus, there was no difference between the treatments. Only the quantity of ecological functions performed by D. bos was positively related to biomass. For D. bos, dung type was more important than biomass in dung removal, and biomass was more important than dung type in the amount of soil excavated. Neither biomass nor dung type explained C. hesperus functions. In conclusion, variables that affect ecological functions are dependent upon the species in question and the type of function evaluated, so dung beetle ecological functions are species-specific.

References

Alves, S. B., & Nakano, O. 1977. Influência do Dichotomius anaglypticus (Mannerheim, 1829) (Coleoptera, Scarabaeidae) no crescimento de plantas de Napier. Ecossistema, 2, 31–33.

Amézquita, S., & Favila, M. E. 2010. Removal rates of native and exotic dung by dung beetles (Scarabaeidae: Scarabaeinae) in a fragmented tropical rain forest. Environmental entomology, 39 (2), 328–336. DOI: 10.1603/EN09182.

Andresen, E. 2003. Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography, 26 (1), 87–97. DOI: 10.1034/j.1600-0587.2003.03362.x.

Andresen, E. 2005. Effects of season and vegetation type on community organization of dung beetles in a tropical dry forest. Biotropica, 37(2), 291–300. DOI: 10.1111/j.1744-7429.2005.00039.x.

Anduaga, S. 2004. Impact of the activity of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) inhabiting pasture land in Durango, Mexico. Environmental Entomology, 33 (5), 1306–1312. DOI: 10.1603/0046-225X-33.5.1306.

Bates, D., Mächler, M., Bolker, B., & Walker, S. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67.

Braga, R. F., 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. PLoSOne, 8, e57786. DOI: 10.1371/journal.pone.0057786.

Carvalho, R., Ferreira, R. S., Audino, L. D., Châline, N., Braga, P., &Louzada, J. 2018. Factors influencing the production of pygidial secretions in the dung roller beetle Canthon smaragdulus (Coleoptera: Scarabaeinae). Austral Entomology, 57 (4), 403–409. DOI:10.1111/aen.12291.

Carvalho, R., Frazão, F., Ferreira–Châline, R., Louzada, J., Cordeiro, L., & França, F. 2018. Dung burial by roller dung beetles (Coleoptera: Scarabaeinae): An individual and specific-level study. International Journal of Tropical Insect Science, 38(4), 373–380. DOI:10.1017/S1742758418000206.

Clarke, K. R., & Gorley R. N. 2006. PRIMER V6: user manual-tutorial. UK: Plymouth Marine Laboratory: p. 192.

Crawley, M. J. 2002. Statistical computing: an introduction to data analysis using S-Plus. 2nd ed.UK: Wiley–Blackwell: p: 772.

Dalanesi, P. E., Oliveira-Filho, A., & Fontes, M. A. 2004. Flora and structure of the arboreal component of the forest of the Parque Ecológico Quedas do Rio Bonito, Lavras, Minas Gerais State, and correlations between species distribution and environmental variables. Acta Botanica Brasilica, 18(4), 737–757. DOI: 10.1590/S0102-33062004000400005.

Dangles, O., Carpio, C., & Woodward, G. 2012. Size‐dependent species removal impairs ecosystem functioning in a large‐scale tropical field experiment. Ecology, 93(12), 2615–2625. DOI: 10.1890/12-0510.1.

Dormont, L., Epinat, G., & Lumaret, J. P. 2004. Trophic preferences mediated by olfactory cues in dung beetles colonizing cattle and horse dung. Environmental Entomology, 33(2), 370–377. DOI: 10.1603/0046-225X-33.2.370.

Dormont, L., Jay-Robert, P., Bessiere, J.M., Rapior, S., & Lumaret, J.P. 2010. Innate olfactory preferences in dung beetles. The Journal of Experimental Biology, 213, 3177–3186. DOI:10.1242/jeb.040964

Estrada, A., Anzures, A., & Coates-Estrada, R. 1999. Tropical rain forest fragmentation, Howler Monkeys (Alouatta palliata) and dung beetles at Los Tuxtlas, Mexico. American Journal of Primatology, 48 (4), 253–262. DOI: 10.1002/(SICI)1098-2345(1999)48:4<253::AID-AJP1>3.0.CO;2-D

Favila, M. E. 1993. Some ecological factors affecting the life-style of Canthon cyanellus cyanellus (Coleoptera: Scarabaeidae): an experimental approach. Ethology Ecology and Evolution, 5(3), 319–328. DOI: 10.1080/08927014.1993.9523019.

Filgueiras, B., Liberal, C., Aguiar, C., Hernandéz, M., & Iannuzzi. L. 2009. Attractivity of omnivore, carnivore and herbivore mammalian dung to Scarabaeinae (Coleoptera, Scarabaeidae) in a tropical Atlantic rainforest remnant. Revista Brasileirade Entomologia, 53(3), 422–427. DOI: 10.1590/S0085-56262009000300017.

Fincher, G., Stewart,T., & Davis, R. 1970. Attraction of coprophagous beetles to feces of various animals. Journal of Parasitology, 56(2), 378–383. DOI: 10.2307/3277680.

Frank, K., Krell, F.T., Slade, E. M., Raine, E. H., Chiew, L. Y., Schmitt, T., Vairappan, C., Walter, P., & Blüthgen, N. 2018. Global dung webs: high trophic generalism of dung beetles along the latitudinal diversity gradient. Ecology Letters, 21(8),1229–1236. DOI:10.1111/ele.13095.

Gardner, T., Hernandéz, M., Barlow, J., & Peres, C. 2008. Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. Journal of Applied Ecology, 45(3), 883–893. DOI: 10.1111/j.1365-2664.2008.01454.x.

Gregory, N., Gómez, A., Oliveira, T. M., & Nichols, E. 2015. Big dung beetles dig deeper: trait-based consequences for faecal parasite transmission. International Journal for Parasitology, 45(2-3), 101–105. DOI: 10.1016/j.ijpara.2014.10.006.

Griffiths, H. M., Bardgett, R. D., Louzada, J., & Barlow, J. 2016. The value of trophic interactions for ecosystem function: dung beetle communities influence seed burial and seedling recruitment in tropical forests. Proceedings of the Royal Society B, 283,20161634. DOI: 10.1098/rspb.2016.1634.

Griffiths, H. M., Louzada, J., Bardgett, R. D., Beiroz, W., França, F., Tregidgo, D., & Barlow, J. 2015. Biodiversity and environmental context predict dung beetle‐mediated seed dispersal in a tropical forest field experiment. Ecology, 96(6), 1607–1619. DOI: 10.1890/14-1211.1.

Halffter, G., & Edmonds,W. D. 1983. The nesting behavior of dung beetles (Scarabaeinae). An ecological and evolutive approach. Journal of the New York Entomological Society, 91, 512– 515.

Halffter, G., & Matthews, E. G. 1966. The natural history of dung beetles of subfamily Scarabaeinae (Coleoptera:Scarabaeidae). Folia Entomológica Mexicana, 12, 1–132.

Hanski, I., & Cambefort,Y. 1991. Dung beetle ecology. United States: Princeton University Press, 481.

Hanski, I., & Krikken, J.1991. Dung beetles in tropical forests in South-East Asia. In:I. Hanski & Y. Cambefort (Eds.), Dung beetle ecology. pp. 179–197. USA: Princeton University Press.

Honěk, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship.Oikos, 66(3), 483–492. DOI: 10.2307/3544943.

Kerley, G. I. H., Landman, M., Ficetola, G. F., Boyer, F., Bonin, A., Rioux, D.,Taberlet, P., & Coissac, E. (2018). Diet shifts by adult flightless dung beetles Circellium bacchus, revealed using DNA metabarcoding, reflect complex life histories. Oecologia, 188(1), 107–115. DOI:10.1007/s00442-018-4203-6.

Köppen, W. 1931. Climatologia. México: Fundo de Cultura Econômica.

Landin, B. O. 1961. Ecological studies on dung-beetles: (Col. Scarabaeidae). Oposcula Entomologica, 19, 1–228.

Larsen, T. H., Lopera, A., & Forsyth. A. 2006. Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin, 60(4), 315–324. DOI: 10.1649/0010-065X(2006)60[315:ETAHSB]2.0.CO;2

Larsen, T. H.,Williams, N. M., & Kremen, C. 2005. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters, 8(5), 538–547.DOI: 10.1111/j.1461-0248.2005.00749.x.

Louzada, J.,& Carvalho e Silva,P. R. 2009. Utilization of introduced Brazilian pastures ecosystems by native dung beetles: diversity patterns and resource use. Insect Conservation and Diversity, 2(1), 45–52. DOI: 10.1111/j.1752-4598.2008.00038.x.

Lumaret, J. P., Galante, E., Lumbreras, C., Mena, J., Bertrand, M., Bernal, J. L., Cooper, J. F., Kadiri, N., & Crowe, D. 1993. Field effects of Ivermectin residues on dung beetles. Journal of Applied Ecology, 30(3), 428–436. DOI: 10.2307/2404183.

Martín-Piera, F., & Lobo, J. M. 1996. A comparative discussion of trophic preferences in dung beetle communities. Miscellania Zoologica, 19, 13–31.

Moczek, A. P.,& Emlen, D. 2000. Male horn dimorphism in the scarab beetle, Onthophagus taurus: do alternative reproductive tactics favour alternative phenotypes? Animal Behaviour, 59(2), 459– 466. DOI:10.1006/anbe.1999.1342.

Nichols, E., & Gomez, A. 2014. Dung beetles and fecal helminth transmission: patterns, mechanisms and questions. Parasitology, 141(5), 614– 623. DOI: 10.1017/S0031182013002011.

Nichols, E., Larsen, T., Spector, S., Davis, A. L., Escobar, F., Favila, M. E., & Vulinec, K. 2007. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biological Conservation, 137(1), 1– 19. DOI: 10.1016/j.biocon.2007.01.023.

Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S., & Favila, M. E. 2008. Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation, 141(6), 1461– 1474. DOI: 10.1016/j.biocon.2008.04.011.

Pinto,D. G., & Perobelli, F. S. 2016. Determinantes do Crescimento da Pecuária de Leite em Minas Gerais: uma análise para o período de 2005 a 2014. Reflexões Econômicas, 2, 44– 67.

R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

Rainio, M. 1966. Abundance and phenology of some coprophagous beetles in different kinds of dung. Annales Zoologici Fennici, 3, 88– 98.

Ridsdill‐Smith, T. J., & Edwards, P. B. 2011. Biological control: ecosystem functions provided by dung beetles. Ecology and Evolution of Dung Beetles. In: Simmons, L. W., & Ridsdill-Smith, T. J. (Eds.), Ecology and evolution of dung beetles. pp: 245–266. Wiley-Blackwel. DOI: 10.1002/9781444342000.ch12.

Rossini, M., & Vaz-de-Mello, F. 2015. A review of the genus Chalcocopris Burmeister, 1846 (Coleoptera: Scarabaeidae: Scarabaeinae), with description of a new species. Zootaxa 3920(2), 291– 300. DOI: 10.11646/zootaxa.3920.2.5.

Scholtz, C. H., Davis, A. L., & Kryger, U. 2009. Evolutionary biology and conservation of dung beetles. Bulgaria: Pensoft Publishers. p. 567.

Tshikae, B. P., Davis, A. L., & Scholtz, C. H. 2008. Trophic associations of a dung beetle assemblage (Scarabaeidae: Scarabaeinae) in a woodland savanna of Botswana. Environmental of entomology, 37(2), 431– 441. DOI: 10.1093/ee/37.2.431.

Tshikae, B.P., Davis, A., & Scholtz, C.H. 2013. Does an aridity and trophic resource gradient drive patterns of dung beetle food selection across the Botswana Kalahari? Ecological Entomology, 38(1), 83–95. DOI: 10.1111/j.1365-2311.2012.01409.x.

Vernes, K., Pope, L. C., Hill, C. J., & Bärlocher, F. 2005. Seasonality, dung specificity and competition in dung beetle assemblages in the Australian Wet Tropics, north-eastern Australia. Journal of Tropical Ecology, 21(1), 1–8. DOI: 10.1017/S026646740400224X.

Walsh, C. G., Cordo, H. A., Briano, J. A., Gandolfo, D. E., & Logarzo, G. A. 1997. Laboratory culture of beneficial dung scarabs. Journal of economic entomology, 90(1), 124–129. DOI: 10.1093/jee/90.1.124.

Whipple, S. D., & Hoback, W. W. 2012. A comparison of dung beetle (Coleoptera: Scarabaeidae) attraction to native and exotic mammal dung. Environmental Entomology, 41(2), 238– 244. DOI: 10.1603/EN11285

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Published

2019-09-06