Interspecific interactions between burrowing dung beetles and earthworms on yak dung removal and herbage growth in an alpine meadow
Mingda Xie, Xinwei Wu, Shucun Sun
Interspecific interactions between burrowing dung beetles and earthworms on yak dung removal and herbage growth in an alpine meadow
• A one-sided negative relationship existed between tunneling beetles and earthworms.
• Beetles and earthworms interactively increased dung removal.
• Beetles and earthworms additively facilitated plant growth.
Interspecific interactions between two spatiotemporally co-occurred species sharing a single resource are considered to be either competitive or facilitative. This study examined the possible interspecific interactions between a dung-tunneling beetle species (Onthophagus yubarinus) and an earthworm species (Aporrectodea nocturna), two major detritivores responsible for dung removal in a Tibetan alpine meadow. We conducted a two-way, factorial field experiment using replicated chambers, and measured the performances of beetles and earthworms, as well as yak dung removal, soil properties and aboveground plant biomass over two months. Earthworm presence significantly decreased the body size of beetle larvae and the weight of tunnel dung that beetle larvae live on. In contrast, beetle presence did not affect the performance of earthworms. Beetles, earthworms and their interaction significantly increased dung removal and soil organic carbon concentration at the end of the experiment. Beetles alone significantly increased soil total N and P, soluble N and P concentrations, but earthworms alone had nonsignificant effects on these nutrient variables. Beetles and earthworms additively enhanced soluble N and P concentrations, and aboveground plant biomass at the end of the experiment. These results indicate 1) there was a one-sided negative relationship between dung-tunneling beetles and earthworms, resulting from the consumption of earthworms on food resource of beetle larvae; and 2) the coexistence of beetles and earthworms facilitated dung removal interactively and plant growth additively by increasing nutrient availability.
Detritivore / Dung / Qinghai-Tibet Plateau / Soil animal / Species interaction
[1] |
Bird, G., Kaczvinsky, C., Wilson, A.E., Hardy, N.B., 2019. When do herbivorous insects compete? A phylogenetic meta-analysis. Ecology Letters 22, 875–883
CrossRef
Google scholar
|
[2] |
Bottinelli, N., Jouquet, P., Capowiez, Y., Podwojewski, P., Grimaldi, M., Peng, X., 2015. Why is the influence of soil macrofauna on soil structure only considered by soil ecologists? Soil & Tillage Research 146, 118–124
CrossRef
Google scholar
|
[3] |
Brown, J., Scholtz, C., Janeau, J.L., Grellier, S., Podwojewski, P., 2010. Dung beetles (Coleoptera: Scarabaeidae) can improve soil hydrological properties. Applied Soil Ecology 46, 9–16
CrossRef
Google scholar
|
[4] |
Chen, Y., Cao, J., He, X., Liu, T., Shao, Y., Zhang, C., Zhou, Q., Li, F., Mao, P., Tao, L., Liu, Z., Lin, Y., Zhou, L., Zhang, W., Fu, S., 2020. Plant leaf litter plays a more important role than roots in maintaining earthworm communities in subtropical plantations. Soil Biology and Biochemistry,
|
[5] |
Chew, R.M., 1974. Consumers as regulators of ecosystems: An alternative to energetics. Ohio Journal of Science 74, 359–370.
|
[6] |
Denno, R.F., McClure, M.S., Ott, G.R., 1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annual Review of Entomology 40, 297–331
CrossRef
Google scholar
|
[7] |
Doube, B.M., 1990. A functional classification for analysis of the structure of dung beetle assemblages. Ecological Entomology 15, 371–383
CrossRef
Google scholar
|
[8] |
Edwards, C.A., Lofty, J.R., 1977. Biology of earthworms. 2nd ed. London: Chapman and Hall Ltd.
|
[9] |
Edwards, P.B., Aschenborn, H.H., 1987. Patterns of nesting and dung burial in Onitis dung beetles: Implications for pasture productivity and fly control. Journal of Applied Ecology 24, 837–851
CrossRef
Google scholar
|
[10] |
Fonte, S.J., Kong, A.Y.Y., Kessel, C.V., Hendrix, P.F., Six, J., 2007. Influence of earthworm activity on aggregate-associated carbon and nitrogen dynamics differs with agroecosystem management. Soil Biology & Biochemistry 39, 1014–1022
CrossRef
Google scholar
|
[11] |
Freymann, B.P., Buitenwerf, R., DeSouza, O., Olff, H., 2008. The importance of termites (Isoptera) for the recycling of herbivore dung in tropical ecosystems: A review. European Journal of Entomology 105, 165–173
CrossRef
Google scholar
|
[12] |
Gause, G.F., 1934. The Struggle for Existence. Williams and Wilkens.
|
[13] |
Gessner, M.O., Swan, C.M., Dang, C.K., McKie, B.G., Bardgett, R.D., Wall, D.H., Hättenschwiler, S., 2010. Diversity meets decomposition. Trends in Ecology & Evolution 25, 372–380
CrossRef
Google scholar
|
[14] |
Halffter, G., Edmonds, W.D., 1982. The nesting behavior of dung beetles (Scarabaeinae): An Ecological and Evolutive Approach. Mexico: Instituto de Ecologica.
|
[15] |
Holter, P., 1977. An experiment on dung removal by Aphodius larvae (Scarabaeidae) and earthworms. Oikos 28, 130–136
CrossRef
Google scholar
|
[16] |
Holter, P., 1979. Effect of dung-beetles (Aphodius spp.) and earthworms on the disappearance of cattle dung. Oikos 32, 393–402
CrossRef
Google scholar
|
[17] |
Holter, P., 2016. Herbivore dung as food for dung beetles: elementary coprology for entomologists. Ecological Entomology 41, 367–377
CrossRef
Google scholar
|
[18] |
Huhta, V., 2007. The role of soil fauna in ecosystems: a historical review. Pedobiologia 50, 489–495
CrossRef
Google scholar
|
[19] |
Jones, C.G., Lawton, J.H., Shachak, M., 1994. Organisms as ecosystem engineers. Oikos 69, 373–386
CrossRef
Google scholar
|
[20] |
Lavelle, P., Decaëns, T., Aubert, M., Barot, S., Blouin, M., Bureau, F., Margerie, P., Mora, P., Rossi, J.P., 2006. Soil invertebrates and ecosystem services. European Journal of Soil Biology 42, 3–15
CrossRef
Google scholar
|
[21] |
Lumaret, J.P., Kadiri, N., Bertrand, M., 1992. Changes in resources: Consequences for the dynamics of dung beetle communities. Journal of Applied Ecology 29, 349–356
CrossRef
Google scholar
|
[22] |
Mohr, C.O., 1943. Cattle droppings as ecological units. Ecological Monographs 13, 275–298
CrossRef
Google scholar
|
[23] |
Moore, J.C., Berlow, E.L., Coleman, D.C., Ruiter, P.C.D., Dong, Q., Hastings, A., Johnson, N.C., McCann, K.S., Melville, K., Morin, P.J., Nadelhoffer, K., Rosemond, A.D., Post, D.M., Sabo, J.L., Scow, K.M., Vanni, M.J., Wall, D.H., 2004. Detritus, trophic dynamics and biodiversity. Ecology Letters 7, 584–600
CrossRef
Google scholar
|
[24] |
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, 1461–1474
CrossRef
Google scholar
|
[25] |
R Core Team, 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
|
[26] |
Reitz, S.R., Trumble, J.T., 2002. Competitive displacement among insects and arachnids. Annual Review of Entomology 47, 435–465
CrossRef
Google scholar
|
[27] |
Scown, J., Baker, G., 2006. The influence of livestock dung on the abundance of exotic and native earthworms in a grassland in south-eastern Australia. European Journal of Soil Biology 42, 310–315
CrossRef
Google scholar
|
[28] |
Slade, E.M., Roslin, T., 2016. Dung beetle species interactions and multifunctionality are affected by an experimentally warmed climate. Oikos 125, 1607–1616
CrossRef
Google scholar
|
[29] |
Slade, E.M., Roslin, T., Santalahti, M., Bell, T., 2016. Disentangling the ‘brown world’ faecal–detritus interaction web: dung beetle effects on soil microbial properties. Oikos 125, 629–635
CrossRef
Google scholar
|
[30] |
Sowig, P., 1995. Habitat selection and offspring survival rate in three paracoprid dung beetles: the influence of soil type and soil moisture. Ecography 18, 147–154
CrossRef
Google scholar
|
[31] |
Sowig, P., 1996. Brood care in the dung beetle Onthophagzis uacca (Coleoptera:Scarabaeidae): the effect of soil moisture on time budget, nest structure, and reproductive success. Ecography 19, 254–258.
|
[32] |
White, E., 1960. The distribution and subsequent disappearance of sheep dung in the Pennine moorland. Journal of Animal Ecology 29, 243–250
CrossRef
Google scholar
|
[33] |
Wu, X., Duffy,, J.E., Reich,P.B., Sun,S., 2011. A brown-world cascade in the dung decomposer food web of alpine meadow: Effects of predator interactions and warming. Ecological Monographs 81, 313–328
|
[34] |
Wu, X., Griffin, J.N., Sun, S., 2014. Cascading effects of predator detritivore interactions depend on environmental context in a Tibetan alpine meadow. Journal of Animal Ecology 83, 546–556
CrossRef
Google scholar
|
[35] |
Wu, X., Griffin, J.N., Xi, X., Sun,S., 2015. The sign of cascading predator effects varies with prey traits in a detrital system. Journal of Animal Ecology 84, 1610–1617.
|
[36] |
Wu, X., Sun, S., 2010. The roles of beetles and flies in yak dung removal in an alpine meadow of eastern Qinghai-Tibetan Plateau. Ecoscience 17, 146–155
CrossRef
Google scholar
|
[37] |
Wu, X., Wang, Y ., Sun, S., 2019. Long-term fencing decreases plant diversity and soil organic carbon concentration of the Zoige alpine meadows on the eastern Tibetan plateau. Plant and Soil, https://doi.org/10.1007/s11104-019-04373-7.
|
[38] |
Xiang, S., Guo, R., Wu, N., Sun, S., 2009. Current status and future prospects of Zoige marsh in eastern Qinghai-Tibet plateau. Ecological Engineering 35, 553–562
CrossRef
Google scholar
|
[39] |
Yamada, D., Imura, O., Shi, K., Shibuya, T., 2007. Effect of tunneler dung beetles on cattle dung decomposition, soil nutrients and herbage growth. Grassland Science 53, 121–129
CrossRef
Google scholar
|
[40] |
Zhao, C., Griffin, J.N., Wu, X., Sun, S., 2013. Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. Journal of Animal Ecology 82, 749–758
CrossRef
Google scholar
|
/
〈 | 〉 |