Plant-soil feedbacks and root responses of two Mediterranean oaks along a precipitation gradient

Abstract

Aims

Plant-soil feedbacks (PSFs) have been shown to be relevant drivers of forest community dynamics. However, few studies have explored variation of PSFs along environmental gradients. In a framework of climate change, there is a great need to understand how interactions between plants and soil microbes respond along climatic gradients. Therefore, we compared PSFs along a precipitation gradient in Mediterranean oak forests and included trait responses. Following the Stress Gradient Hypothesis (SGH), we expected less negative or even positive PSFs in the physically harsh dry end of our gradient and more negative PSFs in the wettest end.

Methods

We grew Quercus ilex and Quercus suber acorns on soil inoculated with microbes sampled under adults of both species in six sites ranging in annual precipitation. After 4 months, we measured shoot biomass and allocation and morphological traits above and belowground.

Results

We found negative PSFs for Q. ilex independent of precipitation, whereas for Q. suber PSFs ranged from positive in dry sites to negative in wet sites, in agreement with the SGH. The leaf allocation showed patterns similar to shoot biomass, but belowground allocation and morphological traits revealed responses which could not be detected aboveground.

Conclusions

We provide first evidence for context-dependent PSFs along a precipitation gradient. Moreover, we show that measuring root traits can help improve our understanding of climate-dependent PSFs. Such understanding helps to predict plant soil microbe interactions, and their role as drivers of plant community dynamics under ongoing climate change.

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Abbreviations

PSF:

plant soil feedback

LMF:

leaf mass fraction

RMF:

root mass fraction

SLA:

Specific leaf area

SRL:

Specific root length

RTD:

Root tissue density

D:

root diameter

References

  1. Aponte C, García LV, Pérez-Ramos IM et al (2011) Oak trees and soil interactions in Mediterranean forests: a positive feedback model. J Veg Sci 22:856–867. https://doi.org/10.1111/j.1654-1103.2011.01298.x

    Article  Google Scholar 

  2. Armas C, Rodríguez-Echeverría S, Pugnaire FI (2011) A field test of the stress-gradient hypothesis along an aridity gradient. J Veg Sci 22:818–827. https://doi.org/10.1111/j.1654-1103.2011.01301.x

    Article  Google Scholar 

  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J statistical Softw. 67:1. https://doi.org/10.18637/jss.v.067.i01

  4. Borenstein M, Hedges LV, Higgins J, Rothstein HR (2009) Introduction to meta-analysis. John Wiley and Sons, Chichester

    Google Scholar 

  5. Brasier CM (1996) Review article in Phytophthora cinnamomi and oak decline southern Europe. Environmental constraints including climate change. Ann For Sci 53:347–358

    Article  Google Scholar 

  6. Brunner I, Herzog C, M a D et al (2015) How tree roots respond to drought. Front Plant Sci 6:547. https://doi.org/10.3389/fpls.2015.00547

    Article  PubMed  PubMed Central  Google Scholar 

  7. Burgess TI, Scott JK, Mcdougall KL et al (2017) Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Glob Chang Biol 23:1661–1674

    Article  PubMed  Google Scholar 

  8. Callaway RM, Brooker RW, Choler P et al (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848

    CAS  Article  PubMed  Google Scholar 

  9. Cantarel AAM, Pommier T, Desclos-Theveniau M et al (2015) Using plant traits to explain plant-microbe relationships involved in nitrogen acquisition. Ecology 96:788–799. https://doi.org/10.1890/13-2107.1.sm

    Article  PubMed  Google Scholar 

  10. Comas LH, Becker SR, Von Mark VC et al (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442. https://doi.org/10.3389/fpls.2013.00442

    Article  PubMed  PubMed Central  Google Scholar 

  11. Connell HJ (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rainforest trees. In: Dynamics of populations: proceedings of the advanced study institute on 'Dynamics and numbers in Populations' eds. Den Boer PJ and Gradwell GR Pudoc Oosterbeek, the, Netherlands, pp 298–312

  12. Cortois R, Schroeder-Georgi T, Weigelt A et al (2016) Plant-soil feedbacks: role of plant functional group and plant traits. J Ecol 104:1608–1617. https://doi.org/10.1111/1365-2745.12643

    Article  Google Scholar 

  13. Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R (2010) Evidence of the “plant economics spectrum” in a subarctic flora. J Ecol 98:362–373. https://doi.org/10.1111/j.1365-2745.2009.01615.x

    Article  Google Scholar 

  14. Friesen ML, Porter SS, Stark SC et al (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46

    Article  Google Scholar 

  15. Gómez-Aparicio L, Ibáñez B, Serrano MS et al (2012) Spatial patterns of soil pathogens in declining Mediterranean forests: implications for tree species regeneration. New Phytol 194:1014–1024

    Article  PubMed  Google Scholar 

  16. Gómez-Aparicio L, Domínguez-Begines J, Kardol P et al (2017) Plant-soil feedbacks in declining forests: implications for species coexistence. Ecology. https://doi.org/10.1002/ecy.1864

  17. Gribko LS, Jones WE (1995) Test of the float method of assessing northern red oak acorn condition. Tree Planters' Notes 46:143–147

    Google Scholar 

  18. Gu J, Xu Y, Dong X et al (2014) Root diameter variations explained by anatomy and phylogeny of 50 tropical and temperate tree species. Tree Physiol 34:415–425. https://doi.org/10.1093/treephys/tpu019

    Article  PubMed  Google Scholar 

  19. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706

    Article  PubMed  Google Scholar 

  20. Jacobs DF, Salifu KF, Davis AS (2009) Drought susceptibility and recovery of transplanted Quercus rubra seedlings in relation to root system morphology. Ann For Sci 66:504–504. https://doi.org/10.1051/forest/2009029

    Article  Google Scholar 

  21. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528

    Article  Google Scholar 

  22. Kardol P, Bezemer MT, van der Putten WH (2006) Temporal variation in plant–soil feedback controls succession. Ecol Lett 9:1080–1088. https://doi.org/10.1111/j.1461-0248.2006.00953.x

    Article  PubMed  Google Scholar 

  23. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. https://doi.org/10.1038/417067a

    CAS  Article  PubMed  Google Scholar 

  24. Kramer-Walter KR, Bellingham PJ, Millar TR et al (2016) Root traits are multidimensional: specific root length is independent from root tissue density and the plant economic spectrum. J Ecol 104:1299–1310. https://doi.org/10.1111/1365-2745.12562

    Article  Google Scholar 

  25. Lionello P, Abrantes F, Gacic M et al (2014) The climate of the Mediterranean region: research progress and climate change impacts. Reg Environ Chang 14:1679–1684. https://doi.org/10.1007/s10113-014-0666-0

    Article  Google Scholar 

  26. Lozano YM, Armas C, Hortal S, et al (2017) Disentangling above- and below- ground facilitation drivers in arid environments: the role of soil microorganisms, soil properties and microhabitat. New Phytol 216:1236–1246. https://doi.org/10.1111/nph.14499

  27. Mangan SA, Schnitzer SA, Herre EA et al (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755. https://doi.org/10.1038/nature09273

    CAS  Article  PubMed  Google Scholar 

  28. Mariotte P, Canarini A, Dijkstra FA (2017) Stoichiometric N: P flexibility and mycorrhizal symbiosis favor plant resistance against drought. J Ecol 105:958–967. https://doi.org/10.1111/1365-2745.12731

  29. McCarthy-Neumann S, Kobe RK (2010a) Conspecific and heterospecific plant–soil feedbacks influence survivorship and growth of temperate tree seedlings. J Ecol 98:408–418. https://doi.org/10.1111/j.1365-2745.2009.01620.x

    Article  Google Scholar 

  30. McCarthy-Neumann S, Kobe RK (2010b) Conspecific plant-soil feedbacks reduce survivorship and growth of tropical tree seedlings. J Ecol 98:396–407. https://doi.org/10.1111/j.1365-2745.2009.01619.x

    Article  Google Scholar 

  31. Nardini A, Salleo S, Tyree MT, Vertovec M (2000) Influence of the ectomycorrhizas formed by tuber melanosporum Vitt . On hydraulic conductance and water relations of Quercus Ilex L . Seedlings. Ann For Sci 57:305–312. https://doi.org/10.1051/forest:2000121

    Article  Google Scholar 

  32. Olmo M, Lopez-Iglesias B, Villar R (2014) Drought changes the structure and elemental composition of very fine roots in seedlings of ten woody tree species. Implications for a drier climate. Plant Soil 384:113–129. https://doi.org/10.1007/s11104-014-2178-6

    CAS  Article  Google Scholar 

  33. Pérez-Ramos IM, Roumet C, Cruz P et al (2012) Evidence for a “plant community economics spectrum” driven by nutrient and water limitations in a Mediterranean rangeland of southern France. J Ecol 100:1315–1327. https://doi.org/10.1111/1365-2745.12000

  34. R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  35. Rodríguez-Echeverría S, Armas C, Pistón N et al (2013) A role for below-ground biota in plant-plant facilitation. J Ecol 101:1420–1428. https://doi.org/10.1111/1365-2745.12159

    Article  Google Scholar 

  36. Roumet C, Birouste M, Picon-Cochard C et al (2016) Root structure-function relationships in 74 species: evidence of a root economics spectrum related to carbon economy. New Phytol 210:815–826. https://doi.org/10.1111/nph.13828

    Article  PubMed  Google Scholar 

  37. Rousseau JVD, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient- absorbing surface of pine. New Phytol 128:639–644

    Article  Google Scholar 

  38. Ruiz-Benito P, Lines ER, Gomez-Aparicio L, Zavala MA, Coomes DA (2013) Patterns and drivers of tree mortality in Iberian forests: climatic effects are modified by competition. PLoS One 8(2):e56843. https://doi.org/10.1371/journal.pone.0056843

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317. https://doi.org/10.1007/s00572-003-0237-6

    Article  PubMed  Google Scholar 

  40. Rutten G, Prati D, Hemp A, Fischer M (2016) Plant–soil feedback in east- African savanna trees. Ecology 97:294–301. https://doi.org/10.1890/15-1316.1

    Article  PubMed  Google Scholar 

  41. Sanders IR (2003) Preference, specificity and cheating in the arbuscular mycorrhizal symbiosis. Trends Plant Sci 8:143–145

    CAS  Article  PubMed  Google Scholar 

  42. Smith LM, Reynolds HL (2015) Plant–soil feedbacks shift from negative to positive with decreasing light in forest understory species. Ecology 96:2523–2532. https://doi.org/10.1890/14-2150.1

    Article  PubMed  Google Scholar 

  43. Smith-Ramesh LM, Reynolds HL (2017) The next frontier of plant-soil feedback research: unraveling context dependence across biotic and abiotic gradients. J Veg Sci 28:484–494. https://doi.org/10.1111/jvs.12519

  44. Swinfield T, Lewis OT, Bagchi R, Freckleton RP (2012) Consequences of changing rainfall for fungal pathogen- induced mortality in tropical tree seedlings. Ecol Evol 2:1408–1413

    Article  PubMed  PubMed Central  Google Scholar 

  45. Teste FP, Kardol P, Turner BL, et al (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 176:173–176. https://doi.org/10.1126/science.aai8291

  46. Van Der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150

    Article  Google Scholar 

  47. van der Putten WH, Bardgett RD, Bever JD et al (2013) Plant-soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276. https://doi.org/10.1111/1365-2745.12054

    Article  Google Scholar 

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Acknowledgements

We thank P. Ruiz-Benito and L. Matías for help with the NFI3 and field site selection. L. Matías and S. Soliveres for discussions, and three anonymous reviewers for useful comments on earlier versions of the manuscript. This study was supported by the Swiss National Science Foundation (SNSF) in the context of a mobility fellowship granted to G.R. (P2BEP3_162092). L.G.A. acknowledges support from the MICINN project INTERCAPA (CGL-2014-56739-R).

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Correspondence to Gemma Rutten.

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Rutten, G., Gómez-Aparicio, L. Plant-soil feedbacks and root responses of two Mediterranean oaks along a precipitation gradient. Plant Soil 424, 221–231 (2018). https://doi.org/10.1007/s11104-018-3567-z

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Keywords

  • Plant-soil interactions
  • Root morphological traits
  • Mediterranean oaks
  • Drought
  • Recruitment limitation
  • Intraspecific trait variability
  • Soil microbes