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Grazing Regulates the Spatial Heterogeneity of Soil Microbial Communities Within Ecological Networks

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Abstract

Grazing is a major driver of the composition of microbial communities, which play important roles in soil functioning. Mechanisms whereby grazing might regulate the spatial heterogeneity of microbial communities within ecological networks remain largely untested. We used network analysis to identify the impacts of increasing grazing intensity by livestock (cattle, sheep, goats), and native (kangaroos) and wild (rabbits) animals, on the spatial heterogeneity of the relative abundance of eight ecological clusters of co-occurring soil microbial taxa: four from Grasslands and four from Forests. Grazing effects on microbial spatial heterogeneity were strongly nuanced and depended on (1) plant community type, (2) herbivore type and (3) microbial identity. Microbial within-site spatial heterogeneity was greater in Grasslands than in Forests, and most effects of grazing on microbial spatial heterogeneity were in Forests, effecting three of the four Forest clusters, but only one Grassland cluster. The associations between grazing intensity and microbial heterogeneity were driven indirectly by changes in the spatial heterogeneity of litter cover and soil pH. For Grasslands, we also detected a direct effect of grazing intensity on the heterogeneity of particular microbial groups. Our results indicate that increased grazing intensity will advantage some microbial clusters but disadvantage others. Together, our study provides evidence that grazing intensity regulates the abundance and spatial heterogeneity of microbial communities within ecological networks. Knowing the potential effects of herbivores on different microbial clusters can help us predict the likely effects of grazing on soil function. This has important implications for future sustainable management and conservation policies.

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Data Availability

Data are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.94kq1.

References

  • Adler PB, Raff DA, Lauenroth WK. 2001. The effect of grazing on the spatial heterogeneity of vegetation. Oecol 128:465–79.

    CAS  Google Scholar 

  • Andrew MH. 1988. Grazing impact in relation to livestock watering points. Trends Ecol Evol 3:7–11.

    Google Scholar 

  • Barberán A, Bates ST, Casamayor EO, Fierer N. 2012. Using network analysis to explore co-occurrence patterns in soil microbial communities. ISME J 6:343–51.

    PubMed  Google Scholar 

  • Bardgett RD, van der Putten WH. 2014. Belowground biodiversity and ecosystem functioning. Nature 515:505–11.

    CAS  PubMed  Google Scholar 

  • Bastian M, Heymann S, Jacomy M. 2009. Gephi: an open source software for exploring and manipulating networks. International AAAI Conference on Weblogs and Social Media.

  • Bergmann GT, Bates ST, Eilers KG, Lauber CL, Caporaso JG, Walters WG, Knight R, Fierer N. 2011. The under-recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biol Biochem 43:1450–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brandt AJ, Kroon H, Reynolds HL, Burns JH. 2013. Soil heterogeneity generated by plant–soil feedbacks has implications for species recruitment and coexistence. J Ecol 101:277–86.

    Google Scholar 

  • Caldwell MM, Pearcy W. 1994. Exploitation of environmental heterogeneity by plants: ecophysiological processes above- and belowground. San Diego: Academic Press.

    Google Scholar 

  • Daryanto S, Eldridge DJ. 2010. Plant and soil surface responses to a combination of shrub removal and grazing in a shrub-encroached woodland. J Environ Manage 91:2639–48.

    PubMed  Google Scholar 

  • Davies KF, Chesson P, Harrison S, Inouye BD, Melbourne BA, Rice KJ. 2005. Spatial heterogeneity explains the scale dependence of the native–exotic diversity relationship. Ecology 86:1602–10.

    Google Scholar 

  • de Kroon H, Hutchings MJ. 1995. Morphological plasticity in clonal plants: the foraging concept reconsidered. J Ecol 83:143–52.

    Google Scholar 

  • Delgado-Baquerizo M, Maestre FT, Escolar C, Gallardo A, Ochoa V, Gozalo B, Prado-Comesana A. 2014. Direct and indirect impacts of climate change on microbial and biocrust communities alter the resistance of the N cycle in a semiarid grassland. J Ecol 102:1592–605.

    CAS  Google Scholar 

  • Delgado-Baquerizo M et al. 2016. Microbial diversity drives multifunctionality in terrestrial ecosystems. Nat Commun 7:10541. https://doi.org/10.1038/ncomms10541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado-Baquerizo M et al. 2017. It is elemental: Soil nutrient stoichiometry drives bacterial diversity. Environ Micro 19:1176–88.

    CAS  Google Scholar 

  • Delgado-Baquerizo M et al. 2018a. A global atlas of the dominant bacteria found in soil. Science 359:320–5.

    CAS  PubMed  Google Scholar 

  • Delgado-Baquerizo M, Reith P, Dennis PG, Hamonts K, Powell JF, Young A, Singh BK, Bissett A. 2018b. Ecological drivers of soil microbial diversity and soil biological networks in the Southern Hemisphere. Ecology 99:583–96.

    PubMed  Google Scholar 

  • Delgado-Baquerizo M et al. 2018c. Plant attributes explain the distribution of soil microbial communities in two contrasting regions of the globe. New Phytol 219:574–87.

    PubMed  Google Scholar 

  • Eldridge DJ, Delgado-Baquerizo M. 2018. Functional groups of soil fungi decline under grazing. Plant Soil 426:51–60.

    CAS  Google Scholar 

  • Eldridge DJ, Poore AG, Ruiz-Colmenero M, Letnic M, Soliveres S. 2016. Ecosystem structure, function and composition in rangelands are negatively affected by livestock grazing. Ecol Appl 26:1273–83.

    PubMed  Google Scholar 

  • Eldridge DJ, Delgado-Baquerizo M, Travers SK, Val J, Oliver I. 2017a. Do grazing intensity and herbivore type affect soil health? Insights from a semi-arid productivity gradient. J Appl Ecol 54:976–85.

    Google Scholar 

  • Eldridge DJ, Delgado-Baquerizo M, Travers SK, Val J, Oliver I, Hamonts K, Singh BK. 2017b. Competition drives the response of soil microbial diversity to increased grazing by vertebrate herbivores. Ecology 98:1922–31.

    PubMed  Google Scholar 

  • Eldridge DJ, Travers SK, Val J, Zaja A, Veblen KE. 2019. Horse activity is associated with degraded subalpine grassland structure and reduced habitat for a threatened rodent. Range Ecol Manage 72:467–73.

    Google Scholar 

  • Fierer N, Bradford MA, Jackson RB. 2007. Toward an ecological classification of soil bacteria. Ecology 88:1354–64.

    PubMed  Google Scholar 

  • Finzi AC, Canham CD, Van Breeme N. 1998. Canopy tree–soil interactions within temperate forests: species effects on pH and cations. Ecol Appl 8:447–54.

    Google Scholar 

  • Herlemann DP, Labrenz M, Jürgens K, Bertilsson S, Waniek JJ, Andersson AF. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J 5:1571–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes AJ, Bowyer J, Holley MP, O’Donoghue M, Montgomery M, Gillings MR. 2000. Diverse, yet-to-be-cultured members of the Rubrobacter subdivision of the Actinobacteria are widespread in Australian arid soils. FEMS Micro Ecol 33:111–20.

    CAS  Google Scholar 

  • Ihrmark K et al. 2012. New primers to amplify the fungal ITS2 region-evaluation by 454-sequencing of artificial and natural communities. FEMS Micro Ecol 82:666–77.

    CAS  Google Scholar 

  • Jackson RB, Caldwell MM. 1993. Geostatistical patterns of soil heterogeneity around individual perennial plants. J Ecol 81:683–92.

    Google Scholar 

  • Jackson RB, Caldwell MM. 1996. Integrating resource heterogeneity and plant plasticity: modelling nitrate and phosphate uptake in a patchy soil environment. J Ecol 84:891–903.

    Google Scholar 

  • Jeanbille M, Buée M, Bach C, Cébron A, Frey-Klett P, Turpault MP, Uroz S. 2015. Soil parameters drive the structure, diversity and metabolic potentials of the bacterial communities across temperate beech forest soil sequences. Microb Ecol 71:482–93.

    PubMed  Google Scholar 

  • Johnson CN, Jarman PJ. 1987. Macropod studies at Wallaby Creek. VI: A validation of the use of dung-pellet counts for measuring absolute densities of populations of macropodids. Aust Wildl Res 14:139–46.

    Google Scholar 

  • Lamoot I, Callebaut J, Degezelle T, Demeulenaere E, Laquière J, Vandenberg C, Hoffmann M. 2003. Eliminative behaviour of free-ranging horses: do they show latrine behaviour or do they defecate where they graze? Appl Anim Behav Sci 86:105–21.

    Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N. 2009. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microb 75:5111–20.

    CAS  Google Scholar 

  • Li J, Okin GS, Epstein HE. 2009. Effects of enhanced wind erosion on surface soil texture and characteristics of windblown sediments. J Geophys Res 114:G02003. https://doi.org/10.1029/2008JG000903.

    Article  CAS  Google Scholar 

  • Lin Y, Hong M, Han G, Zhao M, Bai Y, Chang SX. 2010. Grazing intensity affected spatial patterns of vegetation and soil fertility in a desert steppe. Agric Ecosyst Environ 138:282–92.

    Google Scholar 

  • Lundholm JT, Larson DW. 2003. Relationships between spatial environmental heterogeneity and plant species diversity on a limestone pavement. Ecography 26:715–22.

    Google Scholar 

  • Maestre FT et al. 2015. Increasing aridity reduces soil microbial diversity and abundance in global drylands. Proc Nat Acad Sci USA 112:15684–9.

    CAS  PubMed  Google Scholar 

  • Marques FF, Buckland ST, Goffin D, Dixon CE, Borchers DL, Mayle BL, Peace AJ. 2001. Estimating deer abundance from line transect surveys of dung: sika deer in southern Scotland. J Appl Ecol 38:349–63.

    Google Scholar 

  • Noble JC, Tongway DJ. 1986. Pastoral settlement in arid and semi-arid rangelands. In: Russell JS, Isbell RF, Eds. Australian Soils: The Human Impact. Brisbane: University of Queensland Press. p 217–42.

    Google Scholar 

  • Nunes PADA, Bredemeier C, Bremm C, Caetano LAM, Menezes de Almeida G, de Souza Filho W, Anghinoni I, de Faccio César, Carvalho P. 2018. Grazing intensity determines pasture spatial heterogeneity and productivity in an integrated crop-livestock system. Grassl Sci 65:49–55.

    Google Scholar 

  • Rampelotto PH, de Siqueira Ferreira A, Barboza ADM, Roesch LFW. 2013. Changes in diversity, abundance, and structure of soil bacterial communities in Brazilian savanna under different land use systems. Microb Ecol 66:593–607.

    PubMed  Google Scholar 

  • Reisner MD, Grace JB, Pyke DA, Doescher PS. 2013. Conditions favouring Bromus tectorum dominance of endangered sagebrush steppe ecosystems. J Appl Ecol 50:1039–49.

    Google Scholar 

  • Ren H, Han G, Ohm M, Schonbach P, Gierus M, Taube F. 2015. Do sheep grazing patterns affect ecosystem functioning in steppe grassland ecosystems in Inner Mongolia? Agric Ecosyst Environ 213:1–10.

    Google Scholar 

  • Reynolds HL, Haubensak KA. 2009. Soil fertility, heterogeneity, and microbes: towards an integrated understanding of grassland structure and dynamics. Appl Veget Sci 12:33–44.

    Google Scholar 

  • Rojas-Downing MM, Nejadhashemi AP, Harrigan T, Woznicki SA. 2017. Climate change and livestock: Impacts, adaptation, and mitigation. Clim Risk Manage 16:145–63.

    Google Scholar 

  • Schlesinger WH, Pilmanis AM. 1998. Plant-soil interactions in deserts. Biogeochemistry 42:169–87.

    Google Scholar 

  • Schlesinger WH, Reynolds JF, Cunningham GL, Huenneke LF, Jarrell WM, Virginia RA, Whitford WA. 1990. Biological feedbacks in global desertification. Science 247:1043–8.

    CAS  PubMed  Google Scholar 

  • Schloss PD et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microb 75:7537–41.

    CAS  Google Scholar 

  • Shorrocks B, Swingland IR. 1990. Living in a patchy environment. Oxford/New York: Oxford University Press.

    Google Scholar 

  • Snedden I. 1991. Latrine use by the European rabbit (Oryctolagus cuniculus). J Mammal 72:769–75.

    Google Scholar 

  • Tongway DJ, Smith EL. 1989. Soil surface features as indicators of rangeland site productivity. Rangel J 11:15–20.

    Google Scholar 

  • van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF. 2012. Microbial diversity determines the invasion of soil by a bacterial pathogen. Proc Nat Acad Sci USA 109:1159–64.

    PubMed  Google Scholar 

  • Wirsenius S, Azar C, Berndes G. 2010. How much land is needed for global food production under scenarios of dietary changes and livestock productivity increases in 2030? Agric Syst 103:621–38.

    Google Scholar 

  • Zhao Y, Peth S, Hallett P, Wang X, Giese M, Gao Y, Horn R. 2011. Factors controlling the spatial patterns of soil moisture in a grazed semi-arid steppe investigated by multivariate geostatistics. Ecohydrology 4:36–48.

    Google Scholar 

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Acknowledgements

We thank Mark Peacock, Ross McDonnell and Sarah Carr (NSW National Parks and Wildlife Service), the Office of Environment and Heritage (OEH), Greg Summerell, and the River Red Gum Scientific Advisory Committee for project management, and Forest Corporation NSW and landholders for allowing access to field sites. Marta Ruiz-Colmenero, James Glasier, Adriana Zaja, Kari Veblen and staff from OEH, Umwelt and Ecology Australia collected and entered field data. The Australian Research Council (DP170104634) funded biodiversity and ecosystem function work in the BKS laboratory.

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Authors and Affiliations

  1. Office of Environment and Heritage, c/- Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, 2052, Australia

    David J. Eldridge

  2. Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, 2052, Australia

    Samantha K. Travers

  3. Office of Environment and Heritage, P.O. Box 363, Buronga, New South Wales, 2739, Australia

    James Val

  4. State Key Laboratory of Urban and Regional Ecology, Research Centre for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, 100085, China

    Jun-Tao Wang

  5. Hawksbury Institute for the Environment, Western Sydney University, Penrith South DC, Sydney, New South Wales, 2751, Australia

    Jun-Tao Wang, Hongwei Liu & Brajesh K. Singh

  6. Global Centre for Land-Based Innovation, Western Sydney University, Penrith South DC, Sydney, New South Wales, 2751, Australia

    Brajesh K. Singh

  7. Departamento de Biología y Geología, Física y Química Inorgánica, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Calle Tulipán Sin Número, 28933, Móstoles, Spain

    Manuel Delgado-Baquerizo

  8. Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, 80309, USA

    Manuel Delgado-Baquerizo

Authors
  1. David J. Eldridge
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  2. Samantha K. Travers
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  3. James Val
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  4. Jun-Tao Wang
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  5. Hongwei Liu
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  6. Brajesh K. Singh
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  7. Manuel Delgado-Baquerizo
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Corresponding author

Correspondence to David J. Eldridge.

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Author Contributions

MD-B and DJE conceived the study; DJE, SKT, and JV collected the field data, and J-TW, HL and BKS undertook the genomics. DJE and MD-B analysed the data and led the writing, and all authors contributed critically to the drafts and approved the final version.

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Eldridge, D.J., Travers, S.K., Val, J. et al. Grazing Regulates the Spatial Heterogeneity of Soil Microbial Communities Within Ecological Networks. Ecosystems 23, 932–942 (2020). https://doi.org/10.1007/s10021-019-00448-9

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