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Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics

Abstract

Plant–soil feedbacks (PSF) are important interactions that may influence range dynamics in a changing world. What remains largely unknown is the generality of plant–soil biotic interactions across populations and the potential role of specific soil biota, both of which are key for understanding how PSF might change future communities and ecosystems. We combined landscape-level field observations and experimental soil treatments to test whether a dominant tree alters soil environments to impact its own performance and range shifts towards higher elevations. We show: (1) soil conditioning by trees varies with elevation, (2) soil biota relate to PSF, (3) under simulated conditions, biotic PSF constrain range shifts at lower elevations but allow for expansions at higher elevations, and (4) differences in soil conditioning predict feedback outcomes in specific range-shift scenarios. These results suggest that variable plant–soil biotic interactions may influence the migration and fragmentation of tree species, and that models incorporating soil parameters will more accurately predict future species distributions.

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Figure 1: Field sampling and experimental design to test how PSF may contribute to P. angustifolia range shifts.
Figure 2: Indicative of a positive plant–soil biotic feedback, tree growth relates to conditioned soil communities and the relative abundance of Betaproteobacteria.
Figure 3: Range-shift PSF changed from positive to negative as trees were simulated to move upwards in elevation by interacting with soil communities from higher sites.
Figure 4: Range-shift PSF are related to residual variation in conditioned soil differences between elevation sites after accounting for natural soil variation (unconditioned soils) across elevation gradients.

References

  1. 1

    Coudon, C., Gegout, J. C., Piedallu, C. & Rameau, J. C. Soil nutritional factors improve models of plant species distribution: an illustration with Acer campestre (L.) in France. J. Biogeogr. 33, 1750–1763 (2006).

    Article  Google Scholar 

  2. 2

    Beauregard, F. & de Blois, S. Beyond a climate-centric view of plant distribution: edaphic variables add value to distribution models. PLoS ONE 9, e92642 (2014).

    Article  Google Scholar 

  3. 3

    van der Putten, W. H. Climate change, aboveground–belowground interactions, and species’ range shifts. Annu. Rev. Ecol. Evol. S. 43, 365–383 (2012).

    Article  Google Scholar 

  4. 4

    van der Putten, W. H. et al. Plant–soil feedbacks: the past, the present and future challenges. J. Ecol. 101, 265–276 (2013).

    Article  Google Scholar 

  5. 5

    Bailey, J. K. et al. Indirect genetic effects: an evolutionary mechanism linking feedbacks, genotypic diversity and coadaptation in a climate change context. Funct. Ecol. 28, 87–95 (2014).

    Article  Google Scholar 

  6. 6

    Van Nuland, M. E. et al. Plant–soil feedbacks: connecting ecosystem ecology and evolution. Funct. Ecol. 30, 1032–1042 (2016).

    Article  Google Scholar 

  7. 7

    Bever, J. D., Westover, K. M. & Antonovics, J. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J. Ecol. 85, 561–573 (1997).

    Article  Google Scholar 

  8. 8

    Morriën, E. & van der Putten, W. H. Soil microbial community structure of range-expanding plant species differs from co-occurring natives. J. Ecol. 101, 1093–1102 (2013).

    Article  Google Scholar 

  9. 9

    Engelkes, T. et al. Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456, 946–948 (2008).

    Article  Google Scholar 

  10. 10

    Van Grunsven, R. H. A., van der Putten, W. H., Bezemer T. M. & Veenendaal, E. M. Plant–soil feedback of native and range-expanding plant species is insensitive to temperature. Oecologia 162, 1059–1069 (2010).

    Article  Google Scholar 

  11. 11

    McCarthy-Neumann, S. & Ibáñez, I. Tree range expansion may be enhanced by escape from negative plant–soil feedbacks. Ecology 93, 2637–2649 (2012).

    Article  Google Scholar 

  12. 12

    Gundale, M. J. et al. Interactions with soil biota shift from negative to positive when a tree species is moved outside its native range. New Phytol. 202, 415–421 (2014).

    Article  Google Scholar 

  13. 13

    Jump, A. S., Mátyás, C. & Peñuelas, J. The altitude-for-latitude disparity in the range retractions of woody species. Trends Ecol. Evol. 24, 694–701 (2009).

    Article  Google Scholar 

  14. 14

    Schweitzer, J. A. et al. Are there evolutionary consequences of plant–soil feedbacks along soil gradients? Funct. Ecol. 28, 55–64 (2014).

    Article  Google Scholar 

  15. 15

    terHorst, C. P. & Zee, P. C. Eco-evolutionary dynamics in plant–soil feedbacks. Funct. Ecol. 30, 1062–1072 (2016).

    Article  Google Scholar 

  16. 16

    Chen, I. C., Hill, J. K., Ohlemüller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).

    Article  Google Scholar 

  17. 17

    Bridle, J. R. & Vines, T. H. Limits to evolution at range margins: when and why does adaptation fail? Trends Ecol. Evol. 22, 140–147 (2007).

    Article  Google Scholar 

  18. 18

    Angert, A. L. The niche, limits to species’ distributions, and spatiotemporal variation in demography across the elevation ranges of two monkeyflowers. Proc. Natl Acad. Sci. USA 106, 19693–19698 (2009).

    Article  Google Scholar 

  19. 19

    Ettema, C. H. & Wardle, D. A. (2002). Spatial soil ecology. Trends Ecol. Evol. 17, 177–183 (2002).

    Article  Google Scholar 

  20. 20

    Yang, Y. et al. The microbial gene diversity along an elevation gradient of the Tibetan grassland. ISME J. 8, 430–440 (2014).

    Article  Google Scholar 

  21. 21

    Wagg, C., Husband, B. C., Green, D. S., Massicotte, H. B. & Peterson, R. L. Soil microbial communities from an elevational cline differ in their effect on conifer seedling growth. Plant Soil 340, 491–504 (2010).

    Article  Google Scholar 

  22. 22

    Classen, A. T. et al. Direct and indirect effects of climate change on soil microbial and soil microbial–plant interactions: what lies ahead? Ecosphere 6, 1–21 (2015).

    Article  Google Scholar 

  23. 23

    Sedlacek, J. F., Bossdorf, O., Cortés, A. J., Wheeler, J. A. & van Kleunen, M. What role do plant–soil interactions play in the habitat suitability and potential range expansion of the alpine dwarf shrub Salix herbacea? Basic Appl. Ecol. 15, 305–315 (2014).

    Article  Google Scholar 

  24. 24

    Bardgett, R. D. & Wardle, D. A. Aboveground–Belowground Linkages: Biotic Interactions, Ecosystem Processes, and Global Change (Oxford Univ. Press, 2010).

    Google Scholar 

  25. 25

    Fierer, N. & Jackson, R. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. USA 103, 626–631 (2006).

    Article  Google Scholar 

  26. 26

    Woolbright, S. A, Whitham, T. G ., Gehring, C. A ., Allan, G. J & Bailey, J. K. Climate relicts and their associated communities as natural ecology and evolution laboratories. Trends Ecol. Evol. 29, 406–416 (2014).

    Article  Google Scholar 

  27. 27

    Kardol, P., De Deyn, G. B., Laliberte, E., Mariotte, P. & Hawkes. C. V. Biotic plant–soil feedbacks across temporal scales. J. Ecol. 101, 309–315 (2013).

    Article  Google Scholar 

  28. 28

    Sundqvist, M. K., Sanders, N. J. & Wardle, D. A. Community and ecosystem responses to elevational gradients: processes, mechanisms, and insights for global change. Annu. Rev. Ecol. Evol. S. 44, 261–280 (2013).

    Article  Google Scholar 

  29. 29

    Braatne, J. H., Rood, S. B. & Heilman P. E. in Biology of Populus and its Implications for Management and Conservation (eds Stattler, R. F. et al.) 57–85 (NRC Research, 1996).

    Google Scholar 

  30. 30

    Capon, S. J. et al. Riparian ecosystems in the 21st century: hotspots for climate change adaptation? Ecosystems 16, 359–381 (2013).

    Article  Google Scholar 

  31. 31

    Fischer, D. G. et al. Plant genetic effects on soils under climate change. Plant Soil 379, 1–19 (2013).

    Article  Google Scholar 

  32. 32

    Hargreaves, A. L., Samis, K. E. & Eckert, C. G. Are species’ range limits simply niche limits writ large? A review of transplant experiments beyond the range. Am. Nat. 183, 157–173 (2014).

    Article  Google Scholar 

  33. 33

    Ordonez, A. & Williams, J. W. Climatic and biotic velocities for woody taxa distributions over the last 16 000 years in eastern North America. Ecol. Lett. 16, 773–781 (2013).

    Article  Google Scholar 

  34. 34

    Evans, L. M. et al. Geographical barriers and climate influence demographic history in narrowleaf cottonwoods. Heredity 114, 387–396 (2015).

    Article  Google Scholar 

  35. 35

    Holeski, L. M., Zinkgraf, M. S., Couture, J. J., Whitham, T. G. & Lindroth, R. L. Transgenerational effects of herbivory in a group of long-lived tree species: maternal damage reduces offspring allocation to resistance traits, but not growth. J. Ecol. 101, 1062–1073 (2013).

    Article  Google Scholar 

  36. 36

    Madritch, M. D., Greene, S. L. & Lindroth, R. L. Genetic mosaics of ecosystem functioning across aspen-dominated landscapes. Oecologia 160, 119–127 (2009).

    Article  Google Scholar 

  37. 37

    Gehring, C. A., Mueller, R. C. & Whitham, T. G. Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149, 158–164 (2006).

    Article  Google Scholar 

  38. 38

    Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    Article  Google Scholar 

  39. 39

    Krohn, A. et al. Optimization of 16S amplicon analysis using mock communities: implications for estimating community diversity. Preprint at http://doi.org/10.7287/peerj.preprints.2196v2 (2016).

  40. 40

    Bever, J. D. et al. Rooting theories of plant community ecology in microbial interactions. Trends Ecol. Evol. 25, 468–478 (2010).

    Article  Google Scholar 

  41. 41

    Brinkman, P. E., van der Putten, W. H., Bakker, E. J. & Verhoeven, K. Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J. Ecol. 98, 1063–1073 (2010).

    Article  Google Scholar 

  42. 42

    Sykorova, Z., Ineichen, K., Wiemken, A. & Redecker, D. The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18, 1–14 (2007).

    Article  Google Scholar 

  43. 43

    Zinke, P. J. The pattern of influence of individual forest trees on soil properties. Ecology 43, 130–133 (1962).

    Article  Google Scholar 

  44. 44

    McCarthy-Neumann, S. & Kobe, R. K. Conspecific and heterospecific plant–soil feedbacks influence survivorship and growth of temperate tree seedlings. J. Ecol. 98, 408–418 (2010).

    Article  Google Scholar 

  45. 45

    Blanquart, F., Kaltz, O., Nuismer, S. L. & Gandon, S. A practical guide to measuring local adaptation. Ecol. Lett. 16, 1195–1205 (2013).

    Article  Google Scholar 

  46. 46

    Ke, P. J., Miki, T. & Ding, T. S. The soil microbial community predicts the importance of plant traits in plant–soil feedback. New Phytol. 206, 329–341 (2015).

    Article  Google Scholar 

  47. 47

    R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2013); http://www.r-project.org

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Acknowledgements

This material is based on work supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-0929298. Funding for the project was also provided from the University of Tennessee. We thank A. Krohn at the Environmental Genetics and Genomics Laboratory for sequencing and bioinformatics assistance, as well as A. Classen and N. Sanders for providing helpful comments on the manuscript. Special thanks to P. Patterson at Northern Arizona University as well as I. Ware, K. McFarland, P. Meidl, C. Daws, E. Johnson, R. Wooliver, L. Mueller, A. Pfennigwerth and R. Zenni for field, greenhouse and lab support.

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M.E.V.N., J.K.B. and J.A.S. participated in the study design. M.E.V.N. performed the field work, data collection and statistical analyses. All authors discussed the results. M.E.V.N. wrote the initial manuscript draft, with significant edits from J.K.B. and J.A.S.

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Correspondence to Michael E. Van Nuland or Joseph K. Bailey or Jennifer A. Schweitzer.

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The authors declare no competing financial interests.

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Supplementary Discussion; Supplementary Methods; Supplementary Tables 1–10; Supplementary Figures 1–7 (PDF 1728 kb)

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Van Nuland, M., Bailey, J. & Schweitzer, J. Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics. Nat Ecol Evol 1, 0150 (2017). https://doi.org/10.1038/s41559-017-0150

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