Skip to main content

Advertisement

Log in

Precipitation mediates sap flux sensitivity to evaporative demand in the neotropics

  • Physiological ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Transpiration in humid tropical forests modulates the global water cycle and is a key driver of climate regulation. Yet, our understanding of how tropical trees regulate sap flux in response to climate variability remains elusive. With a progressively warming climate, atmospheric evaporative demand [i.e., vapor pressure deficit (VPD)] will be increasingly important for plant functioning, becoming the major control of plant water use in the twenty-first century. Using measurements in 34 tree species at seven sites across a precipitation gradient in the neotropics, we determined how the maximum sap flux velocity (vmax) and the VPD threshold at which vmax is reached (VPDmax) vary with precipitation regime [mean annual precipitation (MAP); seasonal drought intensity (PDRY)] and two functional traits related to foliar and wood economics spectra [leaf mass per area (LMA); wood specific gravity (WSG)]. We show that, even though vmax is highly variable within sites, it follows a negative trend in response to increasing MAP and PDRY across sites. LMA and WSG exerted little effect on vmax and VPDmax, suggesting that these widely used functional traits provide limited explanatory power of dynamic plant responses to environmental variation within hyper-diverse forests. This study demonstrates that long-term precipitation plays an important role in the sap flux response of humid tropical forests to VPD. Our findings suggest that under higher evaporative demand, trees growing in wetter environments in humid tropical regions may be subjected to reduced water exchange with the atmosphere relative to trees growing in drier climates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aparecido LMT, Miller GR, Cahill AT, Moore GW (2016) Comparison of tree transpiration under wet and dry canopy conditions in a Costa Rican Premontane tropical forest. Hydrol Process 30(26):5000–5011

    Article  Google Scholar 

  • Baraloto C, Timothy Paine CE, Poorter L, Beauchene J, Bonal D, Domenach A-M, Hérault B, Patiño S, Roggy J-C, Chave J (2010) Decoupled leaf and stem economics in rain forest trees. Ecol Lett 13:1338–1347

    Article  PubMed  Google Scholar 

  • Barbour MM, Whitehead D (2003) A demonstration of the theoretical prediction that sap velocity is related to wood density in the conifer Dacrydium cupressinum. New Phytol 158:477–488

    Article  Google Scholar 

  • Bartlett MK, Scoffoni C, Sack L (2012) The determinants of leaf turgor loss point and prediction of drought tolerance of species and biomes: a global meta-analysis. Ecol Lett 15:393–405

    Article  PubMed  Google Scholar 

  • Bonal D, Bosc A, Ponton S, Goret J-Y, Burban B, Gross P, Bonnefond J-M, Elbers J, Longdoz B, Epron D, Guehl J-M, Granier A (2008) Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana. Glob Change Biol 14:1917–1933

    Article  Google Scholar 

  • Brodribb TJ (2017) Progressing from ‘functional’ to mechanistic traits. New Phytol 215:9–11

    Article  PubMed  Google Scholar 

  • Brum M, Vadeboncoeur MA, Ivanov V, Asbjornsen H, Saleska S, Alves LF, Penha D, Dias JD, Aragão LE, Barros F, Bittencourt P (2019) Hydrological niche segregation defines forest structure and drought tolerance strategies in a seasonal Amazon forest. J Ecol. https://doi.org/10.1111/1365-2745.13022

    Article  Google Scholar 

  • Burgess SS, Adams MA, Turner NC, Ong CK (1998) The redistribution of soil water by tree root systems. Oecologia 115:306–311

    Article  PubMed  Google Scholar 

  • Bush SE, Hultine KR, Sperry JS, Ehleringer JR (2010) Calibration of thermal dissipation sap flow probes for ring-and diffuse-porous trees. Tree Physiol 30:1545–1554

    Article  PubMed  Google Scholar 

  • Chave J, Rejou-Mechain M, Burquez A, Chidumay E, Colgan MS, Delitti WBC et al (2014) Improved allometric models to estimate the aboveground biomass of tropical trees. Glob Change Biol 20:3177–3190

    Article  Google Scholar 

  • Christianson DS, Varadharajan C, Christofferson B, Detto M, Faybishenko BA, Jardine KJ, Negron-Juarez R, Gimenez BO, Pastorello GZ, Powell T, Warren J, Wolfe B, Chambers JC, Kueppers LM, McDowell NG, Agarwal D (2017) A metadata reporting framework for standardization and synthesis of ecohydrological field observations for ecosystem model parameterization and benchmarking. Ecol Inform 42:148–158

    Article  Google Scholar 

  • Christoffersen BO et al (2016) Linking hydraulic traits to tropical forest function in a size-structured and trait-driven model (TFS v. 1-Hydro). Geosci Model Dev 9:4227

    Article  Google Scholar 

  • Compo GP et al (2011) The Twentieth Century Reanalysis Project. Q J R Meteorol Soc 137:1–28

    Article  Google Scholar 

  • Cosme LHM, Schietti J, Costa FRC, Oliveira RS (2017) The importance of hydraulic architecture to the distribution patterns of trees in a central Amazonian forest. New Phytol 215:113–125

    Article  PubMed  Google Scholar 

  • Dawson TE, Goldsmith GR (2018) The value of wet leaves. New Phytol 219:1156–1169

    Article  PubMed  Google Scholar 

  • Detto M, Wright SJ, Calderón O, Muller-Landau HC (2018) Resource acquisition and reproductive strategies of tropical forest in response to the El Niño-Southern Oscillation. Nat Commun 9:913

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dias AS, Oliveira RS, Martins FR, Bongers F, Anten NPR, Sterck F (2019) How do lianas and trees change their vascular strategy in seasonal versus rain forest? Perspect Plant Ecol Evol Syst 40:125465

    Article  Google Scholar 

  • Edwards WRN, Becker P, Èermák J (1997) A unified nomenclature for sap flow measurements. Tree Physiol 17:65–67

    Article  CAS  PubMed  Google Scholar 

  • Eltahir EAB, Bras RL (1994) Precipitation recycling in the Amazon basin. Q J R Meteorol Soc 120:861–880

    Article  Google Scholar 

  • Fisher RA et al (2015) Taking off the training wheels: the properties of a dynamic vegetation model without climate envelopes, CLM4. 5 (ED). Geosci Model Dev 8(11):3593–3619

    Article  Google Scholar 

  • Fisher RA et al (2018) Vegetation demographics in earth system models: a review of progress and priorities. Glob Change Biol 24:35–54

    Article  Google Scholar 

  • Foley JA et al (2007) Amazonia revealed: forest degradation and loss of ecosystem goods and services in the Amazon Basin. Front Ecol Environ 5:25–32

    Article  Google Scholar 

  • Fonti P, Jansen S (2012) Xylem plasticity in response to climate. New Phytol 195:734–736

    Article  PubMed  Google Scholar 

  • Fortunel C, Fine PVA, Baraloto C, Dalling J (2012) Leaf, stem and root tissue strategies across 758 Neotropical tree species. Funct Ecol 26:1153–1161

    Article  Google Scholar 

  • Fortunel C, Ruelle J, Beauchene J, Fine PV, Baraloto C (2014) Wood specific gravity and anatomy of branches and roots in 113 Amazonian rainforest tree species across environmental gradients. New Phytol 202:79–94

    Article  PubMed  Google Scholar 

  • Franks PJ, Cowan IR, Farquhar GD (1997) The apparent feedforward response of stomata to air vapour pressure deficit: information revealed by different experimental procedures with two rainforest trees. Plant Cell Environ 20:142–145

    Article  Google Scholar 

  • Granier A (1987) Evaluation of transpiration in a Douglas-fir stand by means of sap flow measurements. Tree Physiol 3:309–320

    Article  CAS  PubMed  Google Scholar 

  • Griffin-Nolan RJ, Bushey JA, Carroll CJW, Challis A, Chieppa J, Garbowski M, Hoffmann AM, Post AK, Slette IJ, Spitzer D, Zambonini D (2018) Trait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes. Funct Ecol 32:1746–1756

    Article  Google Scholar 

  • Grossiord C, Sevanto S, Borrego I, Chan AM, Collins AD, Dickman LT, Hudson P, McBranch N, Michaletz ST, Pockman WT, Vilagrosa A, McDowell NG (2017) Tree water dynamics in a drying and warming world. Plant Cell Environ 40:1861–1873

    Article  CAS  PubMed  Google Scholar 

  • Grossiord C, Sevanto S, Limousin JM, Meir P, Mencuccini M, Pangle RE, Pockman WT, Salmon Y, Zweifel R, McDowell NG (2018) Manipulative experiments demonstrate how long-term soil moisture changes alter controls of plant water use. Environ Exp Bot 152:19–27

    Article  Google Scholar 

  • Hacke UG, Sperry JS, Pittermann J (2004) Analysis of circular bordered pit function II. Gymnosperm tracheids with torus-margo pit membranes. Am J Bot 91:386–400

    Article  PubMed  Google Scholar 

  • Kennedy D, Swenson S, Oleson KW, Lawrence DM, Fisher R, Lola da Costa AC, Gentine P (2019) Implementing plant hydraulics in the community land model, version 5. J Adv Model Earth Syst 11:485–513

    Article  Google Scholar 

  • Kimball BA, Alonso-Rodríguez AM, Cavaleri MA, Reed SC, González G, Wood TE (2018) Infrared heater system for warming tropical forest understory plants and soils. Ecol Evol 8:1932–1944

    Article  PubMed  PubMed Central  Google Scholar 

  • Kooperman GJ et al (2018) Forest response to rising CO2 drives zonally asymmetric rainfall change over tropical land. Nat Clim Change 8:434

    Article  Google Scholar 

  • Kumagai T, Kanamori H, Chappell NA (2016) Tropical forest hydrology. For Hydrol Process Manag Assess 88–102

  • Larjavaara M, Muller-Landau HC (2010) Rethinking the value of high wood density. Funct Ecol 24:701–705

    Article  Google Scholar 

  • Litvak E, McCarthy HR, Pataki DE (2012) Transpiration sensitivity of urban trees in a semi-arid climate is constrained by xylem vulnerability to cavitation. Tree Physiol 32:373–388

    Article  PubMed  Google Scholar 

  • Luizão RC, Luizão FJ, Paiva RQ, Monteiro TF, Sousa LS, Kruijt B (2004) Variation of carbon and nitrogen cycling processes along a topographic gradient in a central Amazonian forest. Glob Change Biol 10:592–600

    Article  Google Scholar 

  • Luomala E, Laitinen K, Sutinen S, Kellomäki S, Vapaavuori E (2005) Stomatal density, anatomy and nutrient concentrations of Scots pine needles are affected by elevated CO2 and temperature. Plant Cell Environ 28:733–749

    Article  CAS  Google Scholar 

  • Maréchaux I, Bonal D, Bartlett MK, Burban B, Coste S, Courtois EA, Dulormne M, Goret J-Y, Mira E, Mirabel A, Sack L, Stahl C, Chave J (2018) Dry-season decline in tree sapflux is correlated with leaf turgor loss point in a tropical rainforest. Funct Ecol. https://doi.org/10.1111/1365-2435.13188

    Article  Google Scholar 

  • Mayaux P, Holmgren P, Achard F, Eva H, Stibig HJ, Branthomme A (2005) Tropical forest cover change in the 1990s and options for future monitoring. Philos Trans R Soc B Biol Sci 360:373–384

    Article  Google Scholar 

  • Meinzer FC, Goldstein G, Andrade JL (2001) Regulation of water flux through tropical forest canopy trees: do universal rules apply? Tree Physiol 21:19–26

    Article  CAS  PubMed  Google Scholar 

  • Meinzer FC, James SA, Goldstein G, Woodruff D (2003) Whole-tree water transport scales with sapwood capacitance in tropical forest canopy trees. Plant Cell Environ 26:1147–1155

    Article  Google Scholar 

  • Meinzer FC, Woodruff DR, Dome J-C, Goldstein G, Campanello PI, Gatti MG, Villalobos-Vega R (2008) Coordination of leaf and stem water transport properties in tropical forest trees. Oecologia 156:31–41

    Article  PubMed  Google Scholar 

  • Mencuccini M (2003) The ecological significance of long-distance water transport: short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant Cell Environ 26:163–182

    Article  Google Scholar 

  • Moles AT (2018) Being John Harper: using evolutionary ideas to improve understanding of global patterns in plant traits. J Ecol 106:1–18

    Article  Google Scholar 

  • Moorcroft PR, Hurtt GC, Pacala SW (2001) A method for scaling vegetation dynamics: the ecosystem demography model (ED). Ecol Monogr 71:557–586

    Article  Google Scholar 

  • Moore GW, Orozco G, Aparecido LM, Miller GR (2018) Upscaling transpiration in diverse forests: insights from a tropical premontane site. Ecohydrology 11:e1920

    Article  Google Scholar 

  • Moreira M et al (1997) Contribution of transpiration to forest ambient vapor based on isotopic measurements. Glob Change Biol 3:439–450

    Article  Google Scholar 

  • Morris H, Plavcová L, Cvecko P, Fichtler E, Gillingham MA, Martínez-Cabrera HI, McGlinn HI, Wheeler DJ, Zheng E, Ziemińska K, Jansen S (2016) A global analysis of parenchyma tissue fractions in secondary xylem of seed plants. New Phytol 209:1553–1565

    Article  CAS  PubMed  Google Scholar 

  • Murphy PG, Lugo AE (1986) Ecology of tropical dry forest. Annu Rev Ecol Syst 17:67–88

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853

    Article  CAS  PubMed  Google Scholar 

  • Nejad AR, Van Meeteren U (2007) The role of abscisic acid in disturbed stomatal response characteristics of Tradescantia virginiana during growth at high relative air humidity. J Exp Bot 58:627–636

    Article  CAS  PubMed  Google Scholar 

  • Novick KA et al (2016) The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nat Clim Change 6:1023

    Article  CAS  Google Scholar 

  • Oishi AC, Hawthorne DA, Oren R (2016) Baseliner: an open-source, interactive tool for processing sap flux data from thermal dissipation probes. SoftwareX 5:139–143

    Article  Google Scholar 

  • Okamoto M, Tanaka Y, Abrams SR, Kamiya Y, Seki M, Nambara E (2009) High humidity induces abscisic acid 8 ‘-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in arabidopsis. Plant Physiol 149L:825–834

    Article  CAS  Google Scholar 

  • Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schäfer KVR (1999) Survey and synthesis of intra-and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Environ 22:1515–1526

    Article  Google Scholar 

  • Poyatos R, Martínez-Vilalta J, Čermák J, Ceulemans R, Granier A, Irvine J, Köstner B, Lagergren F, Meiresonne L, Nadezhdina N, Zimmermann R, Llorens P, Mencuccini M (2007) Plasticity in hydraulic architecture of Scots pine across Eurasia. Oecologia 153:245–259

    Article  CAS  PubMed  Google Scholar 

  • Poyatos R, Granda V, Molowny-Horas R, Mencuccini M, Steppe K, Martínez-Vilalta J (2016) SAPFLUXNET: towards a global database of sap flow measurements. Tree Physiol 36:1449–1455

    Article  PubMed  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Reich PB (2014) The world-wide ‘fast–slow’plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Article  Google Scholar 

  • Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richards PW (1952) The tropical rain forest; an ecological study. At The University Press, Cambridge

    Google Scholar 

  • Schachtman DP, Goodger JQ (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13:281–287

    Article  CAS  PubMed  Google Scholar 

  • Schlesinger WH, Jasechko S (2014) Transpiration in the global water cycle. Agric For Meteorol 189:115–117

    Article  Google Scholar 

  • Schulze E-D, Lange OL, Buschbom U, Kappen L, Evenari M (1972) Stomatal responses to changes in humidity in plants growing in the desert. Planta 108:259–270

    Article  CAS  PubMed  Google Scholar 

  • Slot M, Winter K (2017) In situ temperature response of photosynthesis of 42 tree and liana species in the canopy of two Panamanian lowland tropical forests with contrasting rainfall regimes. New Phytol 214:1103–1117

    Article  CAS  PubMed  Google Scholar 

  • Sperry JS, Venturas MD, Anderegg WR, Mencuccini M, Mackay DS, Wang Y, Love DM (2017) Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant Cell Environ 40:816–830

    Article  CAS  PubMed  Google Scholar 

  • Stahl C, Burban B, Wagner F, Goret JY, Bompy F, Bonal D (2013a) Influence of seasonal variations in soil water availability on gas exchange of tropical canopy trees. Biotropica 45:155–164

    Article  Google Scholar 

  • Stahl C, Hérault B, Rossi V, Burban B, Bréchet C, Bonal D (2013b) Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter? Oecologia 173:1191–1201

    Article  PubMed  Google Scholar 

  • Steppe K, De Pauw DJ, Doody TM, Teskey RO (2010) A comparison of sap flux density using thermal dissipation, heat pulse velocity and heat field deformation methods. Agric For Meteorol 150:1046–1056

    Article  Google Scholar 

  • Torre S, Fjeld T (2001) Water loss and postharvest characteristics of cut roses grown at high or moderate relative air humidity. Sci Hortic 89:217–226

    Article  Google Scholar 

  • Torre S, Fjeld T, Gislerød HR, Moe R (2003) Leaf anatomy and stomatal morphology of greenhouse roses grown at moderate or high air humidity. J Am Soc Hortic Sci 128:598–602

    Article  Google Scholar 

  • Wolf A, Anderegg WR, Pacala SW (2016) Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proc Natl Acad Sci 113:E7222–E7230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright IJ et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ et al (2005) Modulation of leaf economic traits and trait relationships byclimate. Glob Ecol Biogeogr 14:411–421

    Article  Google Scholar 

  • Wright IJ et al (2007) Relationships among ecologically important dimensions of plant trait variation in seven neotropical forests. Ann Bot 99:1003–1015

    Article  PubMed  Google Scholar 

  • Xu X, Medvigy D, Powers JS, Becknell JM, Guan K (2016) Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests. New Phytol 212:80–95

    Article  PubMed  Google Scholar 

  • Zemp DC, Schleussner CF, Barbosa HMJ, Van der Ent RJ, Donges JF, Heinke J, Sampaio G, Rammig A (2014) On the importance of cascading moisture recycling in South America. Atmos Chem Phys 14:13337–13359

    Article  CAS  Google Scholar 

  • Zhang K, Kimball JS, Nemani RR, Running SW, Hong Y, Gourley JJ, Yu Z (2015) Vegetation greening and climate change promote multidecadal rises of global land evapotranspiration. Sci Rep 5:15956. https://doi.org/10.1038/srep15956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu SD, Song JJ, Li RH, Ye Q (2013) Plant hydraulics and photosynthesis of 34 woody species from different successional stages of subtropical forests. Plant Cell Environ 36:879–891

    Article  CAS  PubMed  Google Scholar 

  • Ziemińska K, Westoby M, Wright IJ (2015) Broad anatomical variation within a narrow wood density range—a study of twig wood across 69 Australian angiosperms. PLoS One 10:e0124892

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This project was supported in part by the Next Generation Ecosystem Experiments Tropics, funded by the US Department of Energy, Office of Science, Office of Biological and Environmental Research, Terrestrial Ecosystem Sciences Program, under Award Number DE-SC-0011806. CG was supported by the Swiss National Science Foundation SNF (5231.00639.001.01). BC was supported in part by the Laboratory Directed Research and Development Program Project 8872 of Oak Ridge National Laboratory, managed by UT-Battelle, LLC, for the U. S. Department of Energy. This work has benefited from an “Investissements d’Avenir” grant managed by Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01). Data recorded in French Guiana (FRG) were collected at the Guyaflux sites which belong to the SOERE F-ORE-T and is supported annually by Ecofor, Allenvi and the French national research infrastructure, ANAEE-F. We thank Valentine Herrmann for building the probes for the Panamanian and Brazilian sites. We thank all technicians, students and post-docs who helped collect data at all sites.

Author information

Authors and Affiliations

Authors

Contributions

CG, BC, JW and NGM planned the research. AA, HA, BB, BG, BW, CB, CB, CS, CF, DB, DC, MD, BF, CF, KJ, GRM, GWM, CV, JW, BW, NS, LA, TEW and LW contributed data. CG and BC analyzed the data and wrote a first draft of the manuscript, and all authors contributed to revisions.

Corresponding author

Correspondence to Charlotte Grossiord.

Additional information

Communicated by Frederick C. Meinzer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 11169 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grossiord, C., Christoffersen, B., Alonso-Rodríguez, A.M. et al. Precipitation mediates sap flux sensitivity to evaporative demand in the neotropics. Oecologia 191, 519–530 (2019). https://doi.org/10.1007/s00442-019-04513-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04513-x

Keywords

Navigation