Below-ground hydraulic constraints during drought-induced decline in Scots pine
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Below-crown hydraulic resistance, a proxy for below-ground hydraulic resistance, increased during drought in Scots pine, but larger increases were not associated to drought-induced defoliation. Accounting for variable below-ground hydraulic conductance in response to drought may be needed for accurate predictions of forest water fluxes and drought responses in xeric forests.
Hydraulic deterioration is an important trigger of drought-induced tree mortality. However, the role of below-ground hydraulic constraints remains largely unknown.
We investigated the association between drought-induced defoliation and seasonal dynamics of below-crown hydraulic resistance (a proxy for below-ground hydraulic resistance), associated to variations in water supply and demand in a field population of Scots pine (Pinus sylvestris L.)
Below-crown hydraulic resistance (rbc) of defoliated and non-defoliated pines was obtained from the relationship between maximum leaf-specific sap flow rates and maximum stem pressure difference estimated from xylem radius variations. The percent contribution of rbc to whole-tree hydraulic resistance (%rbc) was calculated by comparing stem water potential variations with the water potential difference between the leaves and the soil.
rbc and %rbc increased with drought in both defoliated and non-defoliated pines. However, non-defoliated trees showed larger increases in rbc between spring and summer. The difference between defoliation classes is unexplained by differences in root embolism, and it is possibly related to seasonal changes in other properties of the roots and the soil-root interface.
Our results highlight the importance of increasing below-ground hydraulic constraints during summer drought but do not clearly link drought-induced defoliation with severe below-ground hydraulic impairment in Scots pine.
KeywordsDrought Forest mortality Hydraulic resistance Rhizosphere Roots Xylem pressure
The authors would like to thank J. Barba, P. Meir, M. Mencuccini, H. Romanos, A. Palomares, Y. Salmon and T. Hölttä for their help with the experimental design and fieldwork. We are also very grateful to the staff from the Poblet Forest Natural Reserve for their support to our research at ‘Barranc del Tillar’.
This work was funded by competitive grants CGL2010-16373, CGL2013-46808-R and CGL2014-55883-JIN from the Spanish Ministry of Economy and Competitiveness. D.A. was funded by a FPU predoctoral fellowship (AP2010-4573).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Adams HD, Zeppel MJB, Anderegg WRL, Hartmann H, Landhäusser SM, Tissue DT, Huxman TE, Hudson PJ, Franz TE, Allen CD, Anderegg LDL, Barron-Gafford GA, Beerling DJ, Breshears DD, Brodribb TJ, Bugmann H, Cobb RC, Collins AD, Dickman LT, Duan H, Ewers BE, Galiano L, Galvez DA, Garcia-Forner N, Gaylord ML, Germino MJ, Gessler A, Hacke UG, Hakamada R, Hector A, Jenkins MW, Kane JM, Kolb TE, Law DJ, Lewis JD, Limousin J-M, Love DM, Macalady AK, Martínez-Vilalta J, Mencuccini M, Mitchell PJ, Muss JD, O’Brien MJ, O’Grady AP, Pangle RE, Pinkard EA, Piper FI, Plaut JA, Pockman WT, Quirk J, Reinhardt K, Ripullone F, Ryan MG, Sala A, Sevanto S, Sperry JS, Vargas R, Vennetier M, Way DA, Xu C, Yepez EA, McDowell NG (2017) A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nat Ecol Evol 1:1285–1291. https://doi.org/10.1038/s41559-017-0248-x CrossRefPubMedGoogle Scholar
- Aguadé Vidal D (2016) Understanding the physiological mechanisms of drought-induced decline in Scots pine (Pinus sylvestris L.). PhD Thesis, Universitat Autònoma de Barcelona. http://hdl.handle.net/10803/402253
- Aguadé D, Poyatos R, Gómez M, Oliva J, Martínez-Vilalta J (2015a) The role of defoliation and root rot pathogen infection in driving the mode of drought-related physiological decline in Scots pine (Pinus sylvestris L.). Tree Physiol 35:229–242. https://doi.org/10.1093/treephys/tpv005 CrossRefPubMedGoogle Scholar
- Bartoń K (2017) MuMIn: multi-model inferenceGoogle Scholar
- Brunner I, Pannatier EG, Frey B, Rigling A, Landolt W, Zimmermann S, Dobbertin M (2009) Morphological and physiological responses of Scots pine fine roots to water supply in a dry climatic region in Switzerland. Tree Physiol 29:541–550. https://doi.org/10.1093/treephys/tpn046 CrossRefPubMedGoogle Scholar
- Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C (2015) How tree roots respond to drought. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.00547
- Dietze MC, Sala A, Carbone MS, Czimczik CI, Mantooth JA, Richardson AD, Vargas R (2014) Nonstructural carbon in woody plants. Annu Rev Plant Biol 65:667–687. https://doi.org/10.1146/annurev-arplant-050213-040054 CrossRefPubMedGoogle Scholar
- Domec J-C, Noormets A, King JS, Sun GE, McNulty SG, Gavazzi MJ, Boggs JL, Treasure EA (2009) Decoupling the influence of leaf and root hydraulic conductances on stomatal conductance and its sensitivity to vapour pressure deficit as soil dries in a drained loblolly pine plantation. Plant Cell Environ 32:980–991. https://doi.org/10.1111/j.1365-3040.2009.01981.x CrossRefPubMedGoogle Scholar
- Duursma R, Kolari P, Perämäki M, Nikinmaa E, Hari P, Delzon S, Loustau D, Ilvesniemi H, Pumpanen J, Mäkelä A (2008) Predicting the decline in daily maximum transpiration rate of two pine stands during drought based on constant minimum leaf water potential and plant hydraulic conductance. Tree Physiol 28:265–276. https://doi.org/10.1093/treephys/28.2.265 CrossRefPubMedGoogle Scholar
- Johnson DM, Domec J-C, Berry ZC, Schwantes AM, KA MC, Woodruff DR, Polley HW, Wortemann R, Swenson JJ, Mackay DS, McDowell NG, Jackson RB (2018) Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought. Plant Cell Environ 41:576–588. https://doi.org/10.1111/pce.13121 CrossRefPubMedGoogle Scholar
- Matías L, González-Díaz P, Jump AS (2014) Larger investment in roots in southern range-edge populations of Scots pine is associated with increased growth and seedling resistance to extreme drought in response to simulated climate change. Environ Exp Bot 105:32–38. https://doi.org/10.1016/j.envexpbot.2014.04.003 CrossRefGoogle Scholar
- Maurel C, Verdoucq L, Luu D-T, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624. https://doi.org/10.1146/annurev.arplant.59.032607.092734 CrossRefPubMedGoogle Scholar
- McDowell N, Pockman WT, Allen CD, Breshears DD, Cobb N, Kolb T, Plaut J, Sperry J, West A, Williams DG, Yepez EA (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. https://doi.org/10.1111/j.1469-8137.2008.02436.x CrossRefPubMedGoogle Scholar
- Nardini A, Casolo V, Dal Borgo A, Savi T, Stenni B, Bertoncin P, Zini L, McDowell NG (2016) Rooting depth, water relations and non-structural carbohydrate dynamics in three woody angiosperms differentially affected by an extreme summer drought. Plant Cell Environ 39:618–627. https://doi.org/10.1111/pce.12646 CrossRefPubMedGoogle Scholar
- Pangle RE, Limousin J-M, Plaut JA, Yepez EA, Hudson PJ, Boutz AL, Gehres N, Pockman WT, McDowell NG (2015) Prolonged experimental drought reduces plant hydraulic conductance and transpiration and increases mortality in a piñon–juniper woodland. Ecol Evol 5:1618–1638. https://doi.org/10.1002/ece3.1422 CrossRefPubMedPubMedCentralGoogle Scholar
- Pinheiro J, Bates D, DebRoy S, et al (2018) nlme: linear and nonlinear mixed effects modelsGoogle Scholar
- Poyatos R, Aguadé D, Martínez-Vilalta J. (2018) Below-ground hydraulic constraints during drought-induced decline in Scots pine. V1.0.0. Zenodo. [Dataset]. https://doi.org/10.5281/zenodo.1415468
- R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
- Rodríguez-Calcerrada J, Li M, López R, Cano FJ, Oleksyn J, Atkin OK, Pita P, Aranda I, Gil L (2016) Drought-induced shoot dieback starts with massive root xylem embolism and variable depletion of nonstructural carbohydrates in seedlings of two tree species. New Phytol 213:597–610. https://doi.org/10.1111/nph.14150 CrossRefPubMedGoogle Scholar
- Salmon Y, Torres-Ruiz JM, Poyatos R, Martinez-Vilalta J, Meir P, Cochard H, Mencuccini M (2015) Balancing the risks of hydraulic failure and carbon starvation: a twig scale analysis in declining Scots pine. Plant Cell Environ 38:2575–2588. https://doi.org/10.1111/pce.12572 CrossRefPubMedPubMedCentralGoogle Scholar
- Sevanto S, Holtta T, Hirsikko A, Vesala T, Nikinmaa E (2005a) Determination of thermal expansion of green wood and the accuracy of tree stem diameter variation measurements. Boreal Environ Res 10:437Google Scholar
- Sevanto S, Holtta T, Markkanen T, Peramaki M, Nikinmaa E, Vesala T (2005b) Relationships between diurnal xylem diameter variation and environmental factors in Scots pine. Boreal Environ Res 10:447Google Scholar
- Sus O, Poyatos R, Barba J, Carvalhais N, Llorens P, Williams M, Vilalta JM (2014) Time variable hydraulic parameters improve the performance of a mechanistic stand transpiration model. A case study of Mediterranean Scots pine sap flow data assimilation. Agric For Meteorol 198–199:168–180. https://doi.org/10.1016/j.agrformet.2014.08.009 CrossRefGoogle Scholar
- Vandeleur RK, Mayo G, Shelden MC, Gilliham M, Kaiser BN, Tyerman SD (2009) The role of plasma membrane intrinsic protein aquaporins in water transport through roots: diurnal and drought stress responses reveal different strategies between isohydric and anisohydric cultivars of grapevine. Plant Physiol 149:445–460. https://doi.org/10.1104/pp.108.128645 CrossRefPubMedPubMedCentralGoogle Scholar