Skip to main content
Log in

The relative and combined effects of herbivore assemblage and soil nitrogen on plant diversity

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Plant diversity can be affected by both herbivore grazing and soil resources. However, it is unclear if the joint effects of herbivores and soil resources might vary with components of plant diversity. Here, we evaluated the relative and combined effects of herbivore assemblage and soil nitrogen (N) quantity and heterogeneity on the α and β components of plant diversity in a grassland that was subjected to four years of grazing under differing herbivore assemblages (no grazing, cattle grazing, sheep grazing, and mixed grazing). We found that herbivore assemblage combined with soil N quantity explained 41% of the variation in plant α-diversity, while herbivore assemblage combined with soil N heterogeneity explained 15% of the variation in plant β-diversity. The independent effects of herbivore assemblage explained more than those of soil N for both α- and β-diversity (α-diversity: 12% vs. 4%; β-diversity: 18% vs. 16%). We concluded that the effects of herbivores are stronger than those of soil N, and that grazing-induced changes in soil resources are important drivers of plant diversity change, especially α-diversity. Therefore, we suggest that managing herbivore species by accounting for the effects that their grazing can have on soil resources may be significant for plant diversity maintenance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adler, P., Raff, D., and Lauenroth, W. (2001). The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128, 465–479.

    Article  CAS  PubMed  Google Scholar 

  • Augustine, D.J., and Frank, D.A. (2001). Effects of migratory grazers on spatial heterogeneity of soil nitrogen properties in a grassland ecosystem. Ecology 82, 3149–3162.

    Article  Google Scholar 

  • Bailey, D.W., Gross, J.E., Laca, E.A., Rittenhouse, L.R., Coughenour, M. B., Swift, D.M., and Sims, P.L. (1996). Mechanisms that result in large herbivore grazing distribution patterns. J Range Manage 49, 386–400.

    Article  Google Scholar 

  • Bakker, E.S., Olff, H., Boekhoff, M., Gleichman, J.M., and Berendse, F. (2004). Impact of herbivores on nitrogen cycling: contrasting effects of small and large species. Oecologia 138, 91–101.

    Article  CAS  PubMed  Google Scholar 

  • Bakker, E.S., Ritchie, M.E., Olff, H., Milchunas, D.G., and Knops, J.M.H. (2006). Herbivore impact on grassland plant diversity depends on habitat productivity and herbivore size. Ecol Lett 9, 780–788.

    Article  PubMed  Google Scholar 

  • Bartels, S.F., and Chen, H.Y.H. (2010). Is understory plant species diversity driven by resource quantity or resource heterogeneity? Ecology 91, 1931–1938.

    Article  PubMed  Google Scholar 

  • Berger, J. (1978). Group size, foraging, and antipredator ploys: an analysis of bighorn sheep decisions. Behav Ecol Sociobiol 4, 91–99.

    Article  Google Scholar 

  • Bloor, J.M.G., and Pottier, J. (2014). Grazing and spatial heterogeneity: Implications for grassland structure and function. In: Mariotte, P., and Kardol, P., eds. Grasslands Biodiversity and Conservation in a Changing World. New York: Nova Science Publishers Inc. 135–162.

    Google Scholar 

  • Cardinale, B.J., Duffy, J.E., Gonzalez, A., Hooper, D.U., Perrings, C., Venail, P., Narwani, A., Mace, G.M., Tilman, D., Wardle, D.A., et al. (2012). Biodiversity loss and its impact on humanity. Nature 486, 59–67.

    Article  CAS  PubMed  Google Scholar 

  • Chase, J.M., and Leibold, M.A. (2003). Ecological Niches: Linking Classical and Contemporary Approaches. Chicago: University of Chicago Press.

    Book  Google Scholar 

  • Clough, Y., Holzschuh, A., Gabriel, D., Purtauf, T., Kleijn, D., Kruess, A., Steffan-dewenter, I., and Tscharntke, T. (2007). Alpha and beta diversity of arthropods and plants in organically and conventionally managed wheat fields. J Appl Ecol 44, 804–812.

    Article  Google Scholar 

  • Cole, L., Buckland, S.M., and Bardgett, R.D. (2008). Influence of disturbance and nitrogen addition on plant and soil animal diversity in grassland. Soil Biol Biochem 40, 505–514.

    Article  CAS  Google Scholar 

  • Collins, S.L. (1992). Fire frequency and community heterogeneity in tallgrass prairie vegetation. Ecology 73, 2001–2006.

    Article  Google Scholar 

  • Collins, S.L., Knapp, A.K., Briggs, J.M., Blair, J.M., and Steinauer, E.M. (1998). Modulation of diversity by grazing and mowing in native tallgrass prairie. Science 280, 745–747.

    Article  CAS  PubMed  Google Scholar 

  • Connell, J.H. (1978). Diversity in tropical rain forests and coral reefs. Science 199, 1302–1310.

    Article  CAS  PubMed  Google Scholar 

  • Denyer, J.L., Hartley, S.E., and John, E.A. (2010). Both bottom-up and top-down processes contribute to plant diversity maintenance in an edaphically heterogeneous ecosystem. J Ecol 98, 498–508.

    Article  Google Scholar 

  • Esse, P.C., Buerkert, A., Hiernaux, P., and Assa, A. (2001). Decomposition of and nutrient release from ruminant manure on acid sandy soils in the Sahelian zone of Niger, West Africa. Agr Ecosyst Environ 83, 55–63.

    Article  Google Scholar 

  • Frank, D.A., Groffman, P.M., Evans, R.D., and Tracy, B.F. (2000). Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grasslands. Oecologia 123, 116–121.

    Article  CAS  PubMed  Google Scholar 

  • Frank, D.A., Wallen, R.L., Hamilton, E.W., White, P.J., and Fridley, J.D. (2018). Manipulating the system: How large herbivores control bottom-up regulation of grasslands. J Ecol 106, 434–443.

    Article  CAS  Google Scholar 

  • Gianuca, A.T., Declerck, S.A.J., Lemmens, P., and De Meester, L. (2017). Effects of dispersal and environmental heterogeneity on the replacement and nestedness components of β-diversity. Ecology 98, 525–533.

    Article  PubMed  Google Scholar 

  • Golodets, C., Kigel, J., and Sternberg, M. (2011). Plant diversity partitioning in grazed Mediterranean grassland at multiple spatial and temporal scales. J Appl Ecol 48, 1260–1268.

    Article  Google Scholar 

  • Huang, Y., Wang, L., Wang, D., Zeng, D.H., Li, Y., Liu, J., and Wang, Y. (2018). Foraging responses of sheep to plant spatial micro-patterns can cause diverse associational effects of focal plant at individual and population levels. J Anim Ecol 87, 863–873.

    Article  PubMed  Google Scholar 

  • Huston, M.A. (1979). A general hypothesis of species diversity. Am Natist 113, 81–101.

    Article  Google Scholar 

  • Kleynhans, E.J., Jolles, A.E., Bos, M.R.E., and Olff, H. (2011). Resource partitioning along multiple niche dimensions in differently sized African savanna grazers. Oikos 120, 591–600.

    Article  Google Scholar 

  • Koerner, S.E., Smith, M.D., Burkepile, D.E., Hanan, N.P., Avolio, M.L., Collins, S.L., Knapp, A.K., Lemoine, N.P., Forrestel, E.J., Eby, S., et al. (2018). Change in dominance determines herbivore effects on plant biodiversity. Nat Ecol Evol 2, 1925–1932.

    Article  PubMed  Google Scholar 

  • Laca, E.A., Sokolow, S., Galli, J.R., and Cangiano, C.A. (2010). Allometry and spatial scales of foraging in mammalian herbivores. Ecol Lett 13, 311–320.

    Article  PubMed  Google Scholar 

  • Landsberg, J., James, C.D., Maconochie, J., Nicholls, A.O., Stol, J., and Tynan, R. (2002). Scale-related effects of grazing on native plant communities in an arid rangeland region of South Australia. J Appl Ecol 39, 427–444.

    Article  Google Scholar 

  • Lanuza, J.B., Bartomeus, I., and Godoy, O. (2018). Opposing effects of floral visitors and soil conditions on the determinants of competitive outcomes maintain species diversity in heterogeneous landscapes. Ecol Lett 21, 865–874.

    Article  PubMed  Google Scholar 

  • Liu, C., Song, X., Wang, L., Wang, D., Zhou, X., Liu, J., Zhao, X., Li, J., and Lin, H. (2016). Effects of grazing on soil nitrogen spatial heterogeneity depend on herbivore assemblages and pre-grazing plant diversity. J Appl Ecol 53, 242–250.

    Article  Google Scholar 

  • Liu, C., Wang, L., Song, X., Chang, Q., Frank, D.A., Wang, D., Li, D., Lin, H., and Du, F.Y. (2018). Towards a mechanistic understanding of the effect that different species of large grazers have on grassland soil N availability. J Ecol 106, 357–366.

    Article  Google Scholar 

  • Liu, J., Feng, C., Wang, D., Wang, L., Wilsey, B.J., and Zhong, Z. (2015). Impacts of grazing by different large herbivores in grassland depend on plant species diversity. J Appl Ecol 52, 1053–1062.

    Article  Google Scholar 

  • Lundholm, J.T. (2009). Plant species diversity and environmental heterogeneity: spatial scale and competing hypotheses. J Veg Sci 20, 377–391.

    Article  Google Scholar 

  • MacArthur, R.H. (1968). The theory of niche. In: Lewontin, R.C., ed. Population Biology and Evolution. Syracuse: Syracuse University Press. 159–176.

    Google Scholar 

  • McNaughton, S.J. (1985). Ecology of a grazing ecosystem: The Serengeti. Ecol Monographs 55, 259–294.

    Article  Google Scholar 

  • Milchunas, D.G., and Lauenroth, W.K. (1993). Quantitative effects of grazing on vegetation and soils over a global range of environments. Ecol Monogr 63, 327–366.

    Article  Google Scholar 

  • Milchunas, D.G., Sala, O.E., and Lauenroth, W.K. (1988). A generalized model of the effects of grazing by large herbivores on grassland community structure. Am Natist 132, 87–106.

    Article  Google Scholar 

  • Morin, P.J. (2000). Biodiversity’s ups and downs. Nature 406, 463–464.

    Article  CAS  PubMed  Google Scholar 

  • Näsholm, T., Ekblad, A., Nordin, A., Giesler, R., Högberg, M., and Högberg, P. (1998). Boreal forest plants take up organic nitrogen. Nature 392, 914–916.

    Article  Google Scholar 

  • Oksanen, J., Blanchet, G., Kindt, R., Legendre, P., O’Hara, R.G., Simpson, G.L., Solymos, P., Stevens, M.H.H., and Wagne, H. (2010). Vegan: community ecology package. R package Version 1.17-1.

  • Olff, H., and Ritchie, M.E. (1998). Effects of herbivores on grassland plant diversity. Trends Ecol Evol 13, 261–265.

    Article  CAS  PubMed  Google Scholar 

  • Olofsson, J., Hulme, P.E., Oksanen, L., and Suominen, O. (2010). Importance of large and small mammalian herbivores for the plant community structure in the forest tundra ecotone. Oikos 106, 324–334.

    Article  Google Scholar 

  • Peres-Neto, P.R., Legendre, P., Dray, S., and Borcard, D. (2006). Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology 87, 2614–2625.

    Article  PubMed  Google Scholar 

  • Price, J.N., Gazol, A., Tamme, R., Hiiesalu, I., and Pärtel, M. (2014). The functional assembly of experimental grasslands in relation to fertility and resource heterogeneity. Funct Ecol 28, 509–519.

    Article  Google Scholar 

  • Ramankutty, N., Evan, A.T., Monfreda, C., and Foley, J.A. (2008). Farming the planet: 1. Geographic distribution of global agricultural lands in the year 2000. Glob Biogeochem Cycle 22, GB1003.

    Article  CAS  Google Scholar 

  • Rickert, C., Fichtner, A., van Klink, R., and Bakker, J.P. (2012). α- and β-diversity in moth communities in salt marshes is driven by grazing management. Biol Conservation 146, 24–31.

    Article  Google Scholar 

  • Schrama, M., Veen, G.F.C., Bakker, E.S.L., Ruifrok, J.L., Bakker, J.P., and Olff, H. (2013). An integrated perspective to explain nitrogen mineralization in grazed ecosystems. Perspect Plant Ecol Evol Syst 15, 32–44.

    Article  Google Scholar 

  • Senft, R.L., Coughenour, M.B., Bailey, D.W., Rittenhouse, L.R., Sala, O.E., and Swift, D.M. (1987). Large herbivore foraging and ecological hierarchies. Bioscience 37, 789–799.

    Article  Google Scholar 

  • Segre, H., Ron, R., De Malach, N., Henkin, Z., Mandel, M., and Kadmon, R. (2014). Competitive exclusion, beta diversity, and deterministic vs. stochastic drivers of community assembly. Ecol Lett 17, 1400–1408.

    Article  PubMed  Google Scholar 

  • Shirima, D.D., Totland, Ø., and Moe, S.R. (2016). The relative importance of vertical soil nutrient heterogeneity, and mean and depth-specific soil nutrient availabilities for tree species richness in tropical forests and woodlands. Oecologia 182, 877–888.

    Article  PubMed  Google Scholar 

  • Song, X., Wang, L., Zhao, X., Liu, C., Chang, Q., Wang, Y., Xu, T., and Wang, D. (2017). Sheep grazing and local community diversity interact to control litter decomposition of dominant species in grassland ecosystem. Soil Biol Biochem 115, 364–370.

    Article  CAS  Google Scholar 

  • Souza, L., Zelikova, T.J., and Sanders, N.J. (2016). Bottom-up and top-down effects on plant communities: nutrients limit productivity, but insects determine diversity and composition. Oikos 125, 566–575.

    Article  Google Scholar 

  • Stein, A., Gerstner, K., and Kreft, H. (2014). Environmental heterogeneity as a universal driver of species richness across taxa, biomes and spatial scales. Ecol Lett 17, 866–880.

    Article  PubMed  Google Scholar 

  • Stevens, M.H.H., and Carson, W.P. (2002). Resource quantity, not resource heterogeneity, maintains plant diversity. Ecol Lett 5, 420–426.

    Article  Google Scholar 

  • Sun, J., Liu, M., Fu, B., Kemp, D., Zhao, W., Liu, G., Han, G., Wilkes, A., Lu, X., Chen, Y., et al. (2020). Reconsidering the efficiency of grazing exclusion using fences on the Tibetan Plateau. Sci Bull 65, 1405–1414.

    Article  Google Scholar 

  • Tedersoo, L., Bahram, M., Põlme, S., Kõljalg, U., Yorou, N.S., Wijesundera, R., Villarreal Ruiz, L., Vasco-Palacios, A.M., Thu, P.Q., Suija, A., et al. (2014). Global diversity and geography of soil fungi. Science 346, 1256688.

    Article  PubMed  CAS  Google Scholar 

  • Tilman, D. (1987). Secondary succession and the pattern of plant dominance along experimental nitrogen gradients. Ecol Monogr 57, 189–214.

    Article  Google Scholar 

  • Tilman, D. (2000). Causes, consequences and ethics of biodiversity. Nature 405, 208–211.

    Article  CAS  PubMed  Google Scholar 

  • Turner, W.R., Brandon, K., Brooks, T.M., Costanza, R., da Fonseca, G.A. B., and Portela, R. (2007). Global conservation of biodiversity and ecosystem services. Bioscience 57, 868–873.

    Article  Google Scholar 

  • van der Plas, F., Howison, R.A., Mpanza, N., Cromsigt, J.P.G.M., and Olff, H. (2016). Different-sized grazers have distinctive effects on plant functional composition of an African savannah. J Ecol 104, 864–875.

    Article  Google Scholar 

  • Veen, G.F., Blair, J.M., Smith, M.D., and Collins, S.L. (2008). Influence of grazing and fire frequency on small-scale plant community structure and resource variability in native tallgrass prairie. Oikos 117, 859–866.

    Article  Google Scholar 

  • Wang, L., Liu, C., Alves, D.G., Frank, D.A., and Wang, D. (2015). Plant diversity is associated with the amount and spatial structure of soil heterogeneity in meadow steppe of China. Landsc Ecol 30, 1713–1721.

    Article  Google Scholar 

  • Wang, J., Wang, D., Li, C., Seastedt, T.R., Liang, C., Wang, L., Sun, W., Liang, M., and Li, Y. (2018). Feces nitrogen release induced by different large herbivores in a dry grassland. Ecol Appl 28, 201–211.

    Article  PubMed  Google Scholar 

  • Wang, L., Delgado-Baquerizo, M., Wang, D., Isbell, F., Liu, J., Feng, C., Liu, J., Zhong, Z., Zhu, H., Yuan, X., et al. (2019). Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proc Natl Acad Sci USA 116, 6187–6192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, L., Wang, D., He, Z., Liu, G., and Hodgkinson, K.C. (2010a). Mechanisms linking plant species richness to foraging of a large herbivore. J Appl Ecol 47, 868–875.

    Article  Google Scholar 

  • Wang, L., Wang, D., Bai, Y., Jiang, G., Liu, J., Huang, Y., and Li, Y. (2010b). Spatial distributions of multiple plant species affect herbivore foraging selectivity. Oikos 119, 401–408.

    Article  Google Scholar 

  • Wang, L., Wang, D., Bai, Y., Huang, Y., Fan, M., Liu, J., and Li, Y. (2010c). Spatially complex neighboring relationships among grassland plant species as an effective mechanism of defense against herbivory. Oecologia 164, 193–200.

    Article  PubMed  Google Scholar 

  • Worm, B., Lotze, H.K., Hillebrand, H., and Sommer, U. (2002). Consumer versus resource control of species diversity and ecosystem functioning. Nature 417, 848–851.

    Article  CAS  PubMed  Google Scholar 

  • Wu, J.G. (2007). Landscape Ecology—Pattern, Process, Scale and Hierarchy (in Chinese). 2nd ed. Beijing: High Education Press.

    Google Scholar 

  • Yang, Y., Tilman, D., Furey, G., and Lehman, C. (2019). Soil carbon sequestration accelerated by restoration of grassland biodiversity. Nat Commun 10, 718.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Young, H.S., McCauley, D.J., Helgen, K.M., Goheen, J.R., Otárola-Castillo, E., Palmer, T.M., Pringle, R.M., Young, T.P., and Dirzo, R. (2013). Effects of mammalian herbivore declines on plant communities: observations and experiments in an African savanna. J Ecol 101, 1030–1041.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang, M., Li, G., Liu, B., Liu, J., Wang, L., and Wang, D. (2020). Effects of herbivore assemblage on the spatial heterogeneity of soil nitrogen in eastern Eurasian steppe. J Appl Ecol 57, 1551–1560.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31772652, U1603235), the National Key Research and Development Program of China (2016YFC0500602), the Program for Introducing Talents to Universities (B16011) and the Ministry of Education Innovation Team Development Plan (2013-373). We would like to thank Elizabeth Tokarz at Yale University for her assistance with English language and grammatical editing.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jushan Liu or Ling Wang.

Additional information

Compliance and ethics

The author(s) declare that they have no conflict of interest. All of the animal experiments complied with the current laws of China.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, M., Liu, B., Li, G. et al. The relative and combined effects of herbivore assemblage and soil nitrogen on plant diversity. Sci. China Life Sci. 65, 830–837 (2022). https://doi.org/10.1007/s11427-021-1963-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-021-1963-2

Keywords

Navigation