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Does Drought Influence the Relationship Between Biodiversity and Ecosystem Functioning in Boreal Forests?


In mixed forests, interactions among species influence ecosystem functioning but environmental conditions also play an important role in shaping relationships between biodiversity and ecosystem functioning. In the context of climate change, the carbon and water balance in pure versus mixed forest stands may be differentially influenced by changing soil water availability. To test this hypothesis, we compared the influence of biodiversity on stand water use efficiency (WUES) in boreal forests between wet and dry years. We assessed the carbon isotope composition (δ 13C) of tree rings in Betula pendula, Pinus sylvestris, and Picea abies growing in pure versus mixed stands. In addition, we tested whether differences in WUES affected patterns of stand basal area increment (BAIS). No biodiversity effect was found for stand δ 13C (δ 13CS) during the wet year. However, there was a significant increase in δ 13CS between the wet and the dry year and a significant effect of biodiversity on δ 13CS in the dry year. The increase in δ 13CS in mixed stands was associated with both selection and complementarity effects. Although BAIS decreased significantly in the dry year, changes in δ 13CS did not translate into variations in BAIS along the biodiversity gradient. Our results confirmed that the physiological response of boreal forest ecosystems to changing soil water conditions is influenced by species interactions and that during dry growing seasons, species interactions in mixed stands can lead to lower soil moisture availability. This illustrates that biodiversity effects can also be negative in mixed stands in the sense that soil resources can be more intensively exhausted. Overall, our results confirm that in boreal forests, the biodiversity–ecosystem functioning relationship depends on local environmental conditions.

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  1. Andreu L, Planells O, Gutiérrez E, Helle G, Schleser GH. 2008. Climatic significance of tree-ring width and δ 13C in a Spanish pine forest network. Tellus B 60:771–81.

  2. Axelsson E, Axelsson B. 1986. Changes in carbon allocation patterns in spruce and pine trees following irrigation and fertilization. Tree Physiol 2:189–204.

  3. Belote RT, Prisley S, Jones RH, Fitzpatrick M, de Beurs K. 2011. Forest productivity and tree diversity relationships depend on ecological context within mid-Atlantic and Appalachian forests (USA). For Ecol Manag 261:1315–24.

  4. Bertness M, Callaway RM. 1994. Positive interactions in communities. Trends Ecol Evol 9:191–3.

  5. Boisvenue C, Running SW. 2006. Impacts of climate change on natural forest productivity—evidence since the middle of the 20th century. Glob Change Biol 12:862–82.

  6. Bonal D, Sabatier D, Montpied P, Tremeaux D, Guehl JM. 2000. Interspecific variability of δ 13C among trees in rainforests of French Guiana: functional groups and canopy integration. Oecologia 124:454–68.

  7. Bradford JB. 2011. Divergence in forest-type response to climate and weather: evidence for regional links between forest-type evenness and net primary productivity. Ecosystems 14:975–86.

  8. Dulamsuren C, Hauck M, Khishigjargal M, Leuschner H, Leuschner C. 2010. Diverging climate trends in Mongolian taiga forests influence growth and regeneration of Larix sibirica. Oecologia 163:1091–102.

  9. Fargione J, Tilman D, Dybzinski R, Lambers JHR, Clark C, Harpole WS, Knops JMH, Reich PB, Loreau M. 2007. From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proc R Soc B Biol Sci 274:871–6.

  10. Farquhar GD, O’Leary MH, Berry JA. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9:121–37.

  11. Flanagan LB, Johnsen KH. 1995. Genetic variation in carbon isotope discrimination and its relationship to growth under field conditions in full-sib families of Picea mariana. Can J For Res 25:39–47.

  12. Forrester DI, Theiveyanathan S, Collopy JJ, Marcar NE. 2010. Enhanced water use efficiency in a mixed Eucalyptus globules and Acacia mearnsii plantation. For Ecol Manag 259:1761–70.

  13. Gamfeldt L, Snäll T, Bagchi R, Jonsson M, Gustafsson L, Kjellander P, Ruiz-Jaen MC, Fröberg M, Stendahl J, Philipson CD, Mikusinski G, Andersson A, Westerlund B, Andren H, Moberg F, Moen J, Bengtsson J. 2013. Higher levels of multiple ecosystem services are found in forests with more tree species. Nat Commun 4:1340.

  14. Gebauer T, Horna V, Leuschner C. 2012. Canopy transpiration of pure and mixed forest stands with variable abundance of European beech. J Hydrol 442–443:2–14.

  15. Granier A, Bréda N, Biron P, Villette S. 1999. A lumped water balance model to evaluate duration and intensity of drought constraints in forest stands. Ecol Model 116:269–83.

  16. Grossiord C, Granier A, Gessler A, Pollastrini M, Bonal D. 2013a. The influence of tree species mixture on ecosystem-level carbon accumulation and water use in a mixed boreal plantation. For Ecol Manag 298:82–92.

  17. Grossiord C, Granier A, Gessler A, Scherer-Lorenzen M, Pollastrini M, Bonal D. 2013b. Application of Loreau & Hector’s (2001) partitioning method to complex functional traits. Methods Ecol Evol 4:954–960.

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

  19. Herbert DA, Rastetter EB, Gough L, Shaver GR. 2004. Species diversity across nutrient gradients: an analysis of resource competition in model ecosystems. Ecosystems 7:296–310.

  20. Hooper DU, Dukes JS. 2004. Overyielding among plant functional groups in a long-term experiment. Ecol Lett 7:95–105.

  21. Hughes AR, Stachowicz JJ. 2004. Genetic diversity enhances the resistance of a seagrass ecosystem to disturbance. Proc Natl Acad Sci USA 101:8998–9002.

  22. IPCC. 2007. Climate change 2007: synthesis report. In: Pachauri RK, Reisinger A, Eds. Contribution of working groups I, II and III to the fourth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press. p 104.

  23. Isbell FI, Polley HW, Wilsey BJ. 2009. Biodiversity, productivity and the temporal stability of productivity: patterns and processes. Ecol Lett 12:443–51.

  24. Jucker T, Coomes DA. 2012. Comment on “Plant Species Richness and Ecosystem Multifunctionality in Global Drylands”. Science 337:155.

  25. Jylhä K, Tuomenvirta H, Ruosteenoja K, Niemi-Hugaerts H, Keisu K, Karhu JA. 2010. Observed and projected future shifts of climatic zones in Europe and their use to visualize climate change information. Weather Clim Soc 2:148–67.

  26. Kalliokoski T, Nygren P, Sievänen R. 2008. Coarse root architecture of three boreal tree species growing in mixed stands. Silva Fennica 42:189–210.

  27. Kelty MJ. 2006. The role of species mixtures in plantation forestry. For Ecol Manag 233:195–204.

  28. Kljun N, Black TA, Griffis TJ, Barr AG, Gaumont-Guay D, Morgenstern K, McCaughey JH, Nesic Z. 2007. Response of net ecosystem productivity of three boreal forest stands to drought. Ecosystems 10:1039–55.

  29. Kozlowski TT, Pallardy SG. 2002. Acclimation and adaptive responses of woody plants to environmental stresses. Bot Rev 68:270–334.

  30. Kunert N, Schwendenmann L, Potvin C, Hölscher D. 2012. Tree diversity enhances tree transpiration in a Panamanian forest plantation. J Appl Ecol 49:135–44.

  31. Lloyd J, Farquhar GD. 1994. 13C discrimination during CO2 assimilation by the terrestrial biosphere. Oecologia 99:201–15.

  32. Loreau M, Hector A. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–6.

  33. Maestre FT, Callaway RM, Valladares F, Lortie CJ. 2009. Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205.

  34. Meinen C, Hertel D, Leuschner C. 2009. Root growth and recovery in temperate broad-leaved forest stands differing in tree species diversity. Ecosystems 12:1103–16.

  35. Mölder I, Leuschner C, Leuschner HH. 2011. δ 13C signature of tree rings and radial increment of Fagus sylvatica as dependent on tree neighbourhood and climate. Trees 25:215–29.

  36. Morin X, Fahse L, Scherer-Lorenzen M, Bugmann H. 2011. Tree species richness promotes productivity in temperate forests through strong complementary between species. Ecol Lett 14:1211–19.

  37. Naeem S. 2008. Species redundancy and ecosystem reliability. Conserv Biol 12:39–45.

  38. Peñuelas J, Hunt JM, Ogaya R, Jump AS. 2008. Twentieth century changes of tree-ring δ 13C at the southern range-edge of Fagus sylvatica: increasing water-use efficiency does not avoid the growth decline induced by warming at low altitudes. Glob Change Biol 14:1076–88.

  39. R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

  40. Saurer M, Siegwolf RT, Schweingruber FH. 2004. Carbon isotope discrimination indicates improving water-use efficiency of trees in northern Eurasia over the last 100 years. Glob Change Biol 10:2109–20.

  41. Steudel B, Hector A, Friedl T, Lofke C, Lorenz M, Wesche M, Kessler M. 2012. Biodiversity effects on ecosystem functioning change along environmental stress gradients. Ecol Lett 15:1397–405.

  42. Symstad AJ, Chapin FS, Wall DH, Gross KL, Huenneke LF, Mittelbach GG, Peters DPC, Tilman D. 2003. Long-term and large-scale perspectives on the relationship between biodiversity and ecosystem functioning. BioScience 53:89–98.

  43. Vaganov EA, Schulze ED, Skomarkova MV, Knohl A, Brand WA, Roscher C. 2009. Intra-annual variability of anatomical structure and δ 13C values within tree rings of spruce and pine in alpine, temperate and boreal Europe. Oecologia 161:729–45.

  44. Vilà M, Sardans J. 1999. Plant competition in mediterranean-type vegetation. J Veg Sci 10:281–94.

  45. Vilà M, Carrillo-Gavilán A, Vayreda J, Bugmann H, Fridman J, Grodzki W, Haase J, Kunstler G, Schelhaas M, Trasobares A. 2013. Disentangling biodiversity and climatic determinants of wood production. PLoS ONE 8:e53530.

  46. Wang J, Zhang CB, Chen T, Li WH. 2013. From selection to complementarity: the shift along the abiotic stress gradient in a controlled biodiversity experiment. Oecologia 171:227–35.

  47. Zhang J, Marshall JD. 1994. Population differences in water-use efficiency of well-watered and water-stressed western larch seedlings. Can J For Res 24:92–9.

  48. Zhang Y, Chen HYH, Reich PB. 2012. Forest productivity increases with evenness, species richness and trait variation: a global meta-analysis. J Ecol 100:742–9.

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We thank Leena Finér and Timo Domisch for the selection of the stands and for their help when preparing this study, and Timo Vesala for sharing the climatic data. We also thank Olivier Bouriaud, Daniel Avacaritei, Iulian Danila and Gabriel Duduman for collecting and preparing the productivity wood cores. We would like to acknowledge the two anonymous reviewers who greatly contributed to the improvement of a previous version of this manuscript. The research leading to these results received funding from the European Union Seventh Framework Programme (FP7/2007–2013) under Grant Agreement No. 265171. CG was supported by a Grant from the INRA Nancy in the framework of the FunDivEUROPE project. This work was conducted in the framework of the Laboratory of Excellence ARBRE (ANR-12-LABXARBRE-01) supported the French National Research Agency.

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Correspondence to Damien Bonal.

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Author contributions

DB, AG1, and AG2 designed the experimental study. DB and CG conducted the field work. TJ provided the productivity data. CG, DB, TJ, AG1, and AG2 analyzed the results. CG and DB wrote the first draft of this manuscript and all authors substantially contributed to revisions.

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Grossiord, C., Granier, A., Gessler, A. et al. Does Drought Influence the Relationship Between Biodiversity and Ecosystem Functioning in Boreal Forests?. Ecosystems 17, 394–404 (2014). https://doi.org/10.1007/s10021-013-9729-1

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  • biodiversity
  • boreal forest
  • drought
  • δ 13C
  • mixed forest
  • water use efficiency