Plant and Soil

, Volume 424, Issue 1–2, pp 221–231 | Cite as

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

  • Gemma RuttenEmail author
  • Lorena Gómez-Aparicio
Regular Article



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.


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.


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.


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.


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



plant soil feedback


leaf mass fraction


root mass fraction


Specific leaf area


Specific root length


Root tissue density


root diameter



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).

Supplementary material

11104_2018_3567_MOESM1_ESM.pdf (762 kb)
ESM 1 (PDF 762 kb)
11104_2018_3567_MOESM2_ESM.pdf (108 kb)
ESM 2 (PDF 107 kb)
11104_2018_3567_MOESM3_ESM.pdf (91 kb)
ESM 3 (PDF 91.1 kb)


  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. CrossRefGoogle 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. CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J statistical Softw. 67:1.
  4. Borenstein M, Hedges LV, Higgins J, Rothstein HR (2009) Introduction to meta-analysis. John Wiley and Sons, ChichesterCrossRefGoogle Scholar
  5. Brasier CM (1996) Review article in Phytophthora cinnamomi and oak decline southern Europe. Environmental constraints including climate change. Ann For Sci 53:347–358CrossRefGoogle Scholar
  6. Brunner I, Herzog C, M a D et al (2015) How tree roots respond to drought. Front Plant Sci 6:547. CrossRefPubMedPubMedCentralGoogle 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 23:1661–1674CrossRefPubMedGoogle Scholar
  8. Callaway RM, Brooker RW, Choler P et al (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848CrossRefPubMedGoogle 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. CrossRefPubMedGoogle 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. CrossRefPubMedPubMedCentralGoogle 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 298–312Google Scholar
  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. CrossRefGoogle 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. CrossRefGoogle Scholar
  14. Friesen ML, Porter SS, Stark SC et al (2011) Microbially mediated plant functional traits. Annu Rev Ecol Evol Syst 42:23–46CrossRefGoogle 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 194:1014–1024CrossRefPubMedGoogle Scholar
  16. Gómez-Aparicio L, Domínguez-Begines J, Kardol P et al (2017) Plant-soil feedbacks in declining forests: implications for species coexistence. Ecology.
  17. Gribko LS, Jones WE (1995) Test of the float method of assessing northern red oak acorn condition. Tree Planters' Notes 46:143–147Google 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. CrossRefPubMedGoogle Scholar
  19. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706CrossRefPubMedGoogle 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. CrossRefGoogle Scholar
  21. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528CrossRefGoogle Scholar
  22. Kardol P, Bezemer MT, van der Putten WH (2006) Temporal variation in plant–soil feedback controls succession. Ecol Lett 9:1080–1088. CrossRefPubMedGoogle Scholar
  23. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70. CrossRefPubMedGoogle 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. CrossRefGoogle 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. CrossRefGoogle 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.
  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. CrossRefPubMedGoogle 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.
  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. CrossRefGoogle 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. CrossRefGoogle 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. CrossRefGoogle 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. CrossRefGoogle 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.
  34. R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
  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. CrossRefGoogle 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. CrossRefPubMedGoogle Scholar
  37. Rousseau JVD, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza to the potential nutrient- absorbing surface of pine. New Phytol 128:639–644CrossRefGoogle 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. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317. CrossRefPubMedGoogle Scholar
  40. Rutten G, Prati D, Hemp A, Fischer M (2016) Plant–soil feedback in east- African savanna trees. Ecology 97:294–301. CrossRefPubMedGoogle Scholar
  41. Sanders IR (2003) Preference, specificity and cheating in the arbuscular mycorrhizal symbiosis. Trends Plant Sci 8:143–145CrossRefPubMedGoogle 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. CrossRefPubMedGoogle 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.
  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 2:1408–1413CrossRefPubMedPubMedCentralGoogle 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.
  46. Van Der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150CrossRefGoogle 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. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), Consejo Superior de Investigaciones Cientificas (CSIC)SevillaSpain

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