Abstract
Tropical montane cloud forests (TMCF) are ecosystems particularly sensitive to climate change; however, the effects of warmer and drier conditions on TMCF ecohydrology remain poorly understood. To investigate functional responses of TMCF trees to reduced water availability, we conducted a study during the 2014 dry season in the lower altitudinal limit of TMCF in central Veracruz, Mexico. Temporal variations of transpiration, depth of water uptake and tree water sources were examined for three dominant, brevi-deciduous species using micrometeorological, sap flow and soil moisture measurements, in combination with oxygen and hydrogen stable isotope composition of rainfall, tree xylem, soil and stream water. Over the course of the dry season, reductions in crown conductance and transpiration were observed in canopy species (43 and 34%, respectively) and mid-story trees (23 and 8%), as atmospheric demand increased and soil moisture decreased. Canopy species consistently showed more depleted isotope values compared to mid-story trees. However, MixSIAR Bayesian model results showed that the evaporated (enriched) soil water pool was the main source for trees despite reduced soil moisture. Additionally, while increases in tree water uptake from deeper to shallower soil water sources occurred, concomitant decreases in transpiration were observed as the dry season progressed. A larger reduction in deep soil water use was observed for canopy species (from 79 ± 19 to 24 ± 20%) compared to mid-story trees (from 12 ± 17 to 10 ± 12%). The increase in shallower soil water sources may reflect a trade-off between water and nutrient requirements in this forest.
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Ambrose AR, Sillett SC, Koch GW, Van Pelt R, Antoine ME, Dawson TE (2010) Effects of height on treetop transpiration and stomatal conductance in coast redwood (Sequoia sempervirens). Tree Physiol 30:1260–1272. https://doi.org/10.1093/treephys/tpq064
Arreola-Flores DP (2016) Análisis de la dinámica del agua en un suelo de bosque de niebla de montaña baja en el centro de Veracruz. MSc dissertation, Posgrado en Ciencias, INECOL, Xalapa, Veracruz, México
Borchert R, Robertson K, Schwartz MD, Williams-Linera G (2005) Phenology of temperate trees in tropical climates. Int J Biometeorol 50:57–65. https://doi.org/10.1007/s00484-005-0261-7
Bray RH, Kurtz L (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–46
Bréda N, Granier A, Barataud F, Moyne C (1995) Soil water dynamics in an oak stand—i. Soil moisture, water potentials and water uptake by roots. Plant Soil 172:17–27. https://doi.org/10.1007/BF00020856
Brooks JR, Barnard HR, Coulombe R, McDonnell JJ (2010) Ecohydrologic separation of water between trees and streams in a Mediterranean climate. Nat Geosci 3:101–104. https://doi.org/10.1038/ngeo722
Bruijnzeel LA, Mulligan M, Scatena FN (2011) Hydrometeorology of tropical montane cloud forests: emerging patterns. Hydrol Process 25:465–498. https://doi.org/10.1002/hyp.7974
Burgess SSO, Adams MA, Turner NC, Beverly CR, Ong CK, Khan AAH, Bleby TM (2001) An improved heat pulse method to measure low and reverse rates of sap flow in woody plants. Tree Physiol 21:589–598. https://doi.org/10.1093/treephys/21.9.589
Caldwell MM, Dawson TE, Richards JH (1998) Hydraulic lift: consequences of water efflux from the roots of plants. Oecologia 113:151–161. https://doi.org/10.1007/s004420050363
Chadwick R, Good P, Andrews T, Martin M (2014) Surface warming patterns drive tropical rainfall pattern responses to CO2 forcing on all timescales. Geophys Res Lett 41:610–615. https://doi.org/10.1002/2013GL058504
Challenger A (1998) Utilización y conservación de los ecosistemas terrestres de México, pasado, presente y futuro, 1st edn. CONABIO, México
Cohen Y, Fuchs M, Green G (1981) Improvement of the heat pulse method for determining sapflow in trees. Plant Cell Environ 4:391–397. https://doi.org/10.1111/j.1365-3040.1981.tb02117.x
Cramer MD, Hawkins HJ, Verboom GA (2009) The importance of nutritional regulation of plant water flux. Oecologia 161:15–24. https://doi.org/10.1007/s00442-009-1364-3
Dansgaard W (1964) Stable isotopes in precipitation. Tellus 16:436–468. https://doi.org/10.1111/j.2153-3490.1964.tb00181.x
Dawson TE (1993) Hydraulic lift and water use by plants: implications for water balance, performance and plant-plant interactions. Oecologia 95:565–574. https://doi.org/10.1007/BF00317442
Dawson TE (1996) Determining water use by trees and forests from isotopic, energy balance and transpiration analyses: the roles of tree size and hydraulic lift. Tree Physiol 16:263–272. https://doi.org/10.3390/s100807748
Dawson TE, Pate JS (1996) Seasonal water uptake and movement in root systems of Australian phreatophytic plants of dimorphic root morphology: a stable isotope investigation. Oecologia 107:13–20. https://doi.org/10.1007/BF00582230
Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559. https://doi.org/10.1146/annurev.ecolsys.33.020602.095451
Ehleringer JR, Dawson TE (1992) Water uptake by plants: perspectives from stable isotope composition. Plant Cell Environ 15:1073–1082. https://doi.org/10.1111/j.1365-3040.1992.tb01657.x
Eller CB, Burgess SS, Oliveria RS (2015) Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae). Tree Physiol 35:387–399. https://doi.org/10.1093/treephys/tpv001
Evaristo J, McDonnell JJ (2017) Prevalence and magnitude of groundwater use by vegetation: a global stable isotope meta-analysis. Sci Rep 7:44110. https://doi.org/10.1038/srep44110
Evaristo J, McDonnell JJ, Scholl MA, Bruijnzeel A, Chun KP (2016) Insights into plant water uptake from xylem-water isotope measurements in two tropical catchments with contrasting moisture conditions. Hydrol Process 30:3210–3227. https://doi.org/10.1002/hyp.10841
Feeley KJ, Hurtado J, Saatchi S, Silman MR, Clark DB (2013) Compositional shifts in Costa Rican forests due to climate-driven species migrations. Glob Change Biol 19:3472–3480. https://doi.org/10.1111/gcb.12300
Fisher JB, Malhi Y, Bonal D, Da Rocha HR, De Araújo AC, Gamo M, Von Randow C (2009) The land-atmosphere water flux in the tropics. Glob Change Biol 15:2694–2714. https://doi.org/10.1111/j.1365-2486.2008.01813.x
Foster P (2001) The potential negative impacts of global climate change on tropical montane cloud forests. Earth Sci Rev 55:73–106. https://doi.org/10.1016/S0012-8252(01)00056-3
Gaines KP, Stanley JW, Meinzer FC, McCulloh KA, Woodruff DR, Chen W, Adams TS, Lin H, Eissenstat DM (2016) Reliance on shallow soil water in a mixed-hardwood forest in central Pennsylvania. Tree Physiol 36:444–458. https://doi.org/10.1093/treephys/tpv113
García-Santos G, Bruijnzeel LA, Dolman AJ (2009) Modelling canopy conductance under wet and dry conditions in a subtropical cloud forest. Agr Forest Meteorol 149:1565–1572. https://doi.org/10.1016/j.agrformet.2009.03.008
Gelman A, Carlin JB, Stern HS, Dunson DB, Vehtari A, Rubin DB (2014) Bayesian data analysis, 3rd edn. Taylor and Francis Group, UK
Geris J, Tetzlaff D, McDonnell JJ, Anderson J, Paton G, Soulsby C (2015) Ecohydrological separation in wet, low energy northern environments? a preliminary assessment using different soil water extraction techniques. Hydrol Process 29:5139–5152. https://doi.org/10.1002/hyp.10603
Goldsmith GR, Muñoz-Villers LE, Holwerda F, McDonnell JJ, Asbjornsen H, Dawson TE (2012) Stable isotopes reveal linkages among ecohydrological processes in a seasonally dry tropical montane cloud forest. Ecohydrol 5:779–790. https://doi.org/10.1002/eco.268
Goldstein G, Andrade JL, Meinzer FC, Holbrook NM, Cavelier J, Jackson P, Celis A (1998) Stem water storage and diurnal patterns of water use in tropical forest canopy trees. Plant Cell Environ 21:397–406. https://doi.org/10.1046/j.1365-3040.1998.00273.x
Gotsch SG, Asbjornsen H, Holwerda F, Goldsmith GR, Weintraub AE, Dawson TE (2014) Foggy days and dry nights determine crown-level water balance in a seasonal tropical montane cloud forest. Plant Cell Environ 37:261–272. https://doi.org/10.1111/pce.12151
Grossiord C, Gessler A, Granier A, Pollastrini M, Bussotti F, Bonal D (2014) Interspecific competition influences the response of oak transpiration to increasing drought stress in Mediterranean forest. For Ecol Manage 318:54–61. https://doi.org/10.1016/j.foreco.2014.01.004
Gupta P, Noone D, Galewsky J, Sweeney C, Vaughn BH (2009) Demonstration of high-precision continuous measurements of water vapor isotopologues in laboratory and remote field deployments using wavelength-scanned cavity ring-downspectroscopy (WS-CRDS) technology. Rapid Commun Mass Sp 23:2534. https://doi.org/10.1002/rcm.4100
Hahm WJ, Dietrich WE, Dawson TE (2018) The ecophysiology of the Mediterranean oak Quercus garryana under severe water-limitation and roles of tolerance and resilience. Ecosphere (in press)
Harris PP, Huntingford C, Cox PM, Gash JHC, Malhi Y (2004) Effect of soil moisture on canopy conductance of amazonian rainforest. Agr Forest Meteorol 122:215–227. https://doi.org/10.1016/j.agrformet.2003.09.006
Holwerda F, Bruijnzeel LA, Muñoz-Villers LE, Equihua M, Asbjornsen H (2010) Rainfall and cloud water interception in mature and secondary lower montane cloud forests of central Veracruz, Mexico. J Hydrol 384:84–96. https://doi.org/10.1016/j.jhydrol.2010.01.012
Holwerda F, Alvarado-Barrientos MA, González-Martínez TM (2016) Surface energy exchange in a tropical montane cloud forest environment: flux partitioning, and seasonal and land cover-related variations. Agr Forest Meteorol 228:13–28. https://doi.org/10.1016/j.agrformet.2016.06.011
Iida S, Shimizu T, Tamai K, Kabeya N, Shimizu A, Ito E, Ohnuki Y, Chann S, Keth N (2016) Interrelationships among dry season leaf fall, leaf flush and transpiration: insights from sap flux measurements in a tropical dry deciduous forest. Ecohydrol 9:472–486. https://doi.org/10.1002/eco.1650
Jackson PC, Cavelier J, Goldstein G, Meinzer FC, Holbrook NM (1995) Partitioning of water resources among plants of a lowland tropical forest. Oecologia 101:197–203. https://doi.org/10.1007/BF00317284
Jarvis PG (1976) The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos T Roy Soc B 273:593–610. https://doi.org/10.1098/rstb.1976.0035
Kluitenberg GJ, Ham JM (2004) Improved theory for calculating sap flow with the heat pulse method. Agr Forest Meteorol 126:169–173. https://doi.org/10.1016/j.agrformet.2004.05.008
Köstner BMM, Shulze ED, Kelliher FM, Hollinger DY, Byers JN, Hunt JE, Weir PL (1992) Transpiration and canopy conductance in a pristine broad-leaved forest of Nothofagus: an analysis of xylem sapflow and eddy correlation measurements. Oecologia 91:350–359. https://doi.org/10.1007/BF00317623
Mayle FE, Beerling DJ, Gosling WD, Bush MB (2004) Responses of amazonian ecosystems to climatic and atmospheric carbon dioxide changes since the last glacial maximum. Philos T Roy Soc B 359:499–514. https://doi.org/10.1098/rstb.2003.1434
McJannet D, Fitch P, Disher M, Wallace J (2007) Measurements of transpiration in four tropical rainforest types of north Queensland Australia. Hydrol Process 21:3549–3564. https://doi.org/10.1002/hyp.6576
Meinzer FC, Andrade JL, Goldstein G, Holbrook NM, Cavelier J, Wright SJ (1999) Partitioning of soil water among canopy trees in a seasonally dry tropical forest. Oecologia 121:293–301. https://doi.org/10.1007/s004420050931
Meinzer FC, Warren JM, Brooks JR (2007) Species-specific partitioning of soil water resources in an old-growth Douglas-fir-western hemlock forest. Tree Physiol 27:871–880. https://doi.org/10.1093/treephys/27.6.871
Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480. https://doi.org/10.1111/j.1461-0248.2008.01163.x
Muñoz-Villers LE, McDonnell JJ (2012) Runoff generation in a steep, tropical montane cloud forest catchment on permeable volcanic substrate. Water Resour Res 48:W09528. https://doi.org/10.1029/2011WR011316
Muñoz-Villers LE, Geissert DR, Holwerda F, McDonnell JJ (2016) Factors influencing stream baseflow transit times in tropical montane watersheds. Hydrol Earth Syst Sc 20:1621–1635. https://doi.org/10.5194/hess-20-1621-2016
Nobel PS (2005) Physiochemical and Environmental Plant Physiology, 3rd edn. WH Freeman and Company, New York
Oliveira RS, Dawson TE, Burgess SSO, Nepstad DC (2005) Hydraulic redistribution in three Amazonian trees. Oecologia 145:354–363. https://doi.org/10.1007/s00442-005-0108-2
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. PCE 22:1515–1526. https://doi.org/10.1046/j.1365-3040.1999.00513.x
Oren R, Sperry JS, Ewers BE, Pataki DE, Phillips N, Megonigal JP (2001) Sensitivity of mean canopy stomatal conductance to vapor pressure deficit in flooded Taxodium distichum L. forest: hydraulic and non-hydraulic effects. Oecologia 126:21–29. https://doi.org/10.1007/s004420000497
Pineda E, Halffter G (2004) Species diversity and habitat fragmentation: frogs in a tropical montane landscape in Mexico. Biol Conserv 117:499–508. https://doi.org/10.1016/j.biocon.2003.08.009
Pounds JA, Fogden MPL, Campbell JH (1999) Biological response to climate change on a tropical mountain. Nature 398:611–615. https://doi.org/10.1038/19297
R Development Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
Reich PB, Borchert R (1988) Changes with leaf age in stomatal function and water status of several tropical tree species. Biotropica 20:60–69
Rodríguez SR, Morales-Barrera W, Layer P, González-Mercado E (2010) A quaternary monogenetic volcanic field in the Xalapa region, eastern trans-mexican volcanic belt: geology, distribution and morphology of the volcanic vents. J Volcanol Geoth Res 197:149–166. https://doi.org/10.1016/j.jvolgeores.2009.08.003
Rojas-Jiménez K, Holbrook NM, Gutiérrez-Soto MV (2007) Dry-season leaf flushing of Enterolobium cyclocarpum (ear-pod tree): above- and belowground phenology and water relations. Tree Physiol 27:1561–1568. https://doi.org/10.1093/treephys/27.11.1561
Romero-Saltos H, Da L, Sternberg SL, Moreira MZ, Nepstad DC (2005) Rainfall exclusion in an eastern Amazonian forest alters soil water movement and depth of water uptake. Am J Bot 92:443–455. https://doi.org/10.3732/ajb.92.3.443
Rzedowski J (1978) Vegetación de México. Limusa, México
Schwendenmann L, Pendall E, Sánchez-Bragado R, Kunnert N, Hölscher D (2015) Tree water uptake in a tropical plantation varying in tree diversity: interspecific differences, seasonal shifts and complementarity. Ecohydrol 8:1–12. https://doi.org/10.1002/eco.1479
SMN: http://smn.cna.gob.mx/ (last access: 31 August 2015), 2015
Stahl C, Hérault B, Rossi V, Burban B, Bréchet C, Bonal D (2013) Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter? Oecologia 173:1191–1201. https://doi.org/10.1007/s00442-013-2724-6
Starr JL, Palineanu IC (2002) Methods for measurement of soil water content: capacitance devices. In: Dane JH, Topp GC (eds) Methods of soil analysis: part 4 physical methods. Soil Science Society of America, Madison, pp 463–474
Stewart JB (1988) Modelling surface conductance of pine forest. Agr Forest Meteorol 43:19–35. https://doi.org/10.1016/0168-1923(88)90003-2
Stock BC, Semmens BX (2016) MixSIAR GUI user manual. Version 3.1 https://github.com/brianstock/MixSIAR/. Accessed 14 May 2016
Tanaka K, Takizawa H, Tanaka N, Kosaka I, Yoshifuji N, Tantasirin C, Tangtham N (2003) Transpiration peak over a hill evergreen forest in northern Thailand in the late dry season: assessing the seasonal changes in evapotranspiration using a multilayer model. J Geophys Res-Atmos 108:4533. https://doi.org/10.1029/2002JD003028
Vázquez-García JA (1995) Cloud forest archipelagos: preservation of fragmented montane ecosystems in tropical America. In: Hamilton LS, Juvik JO, Scatena FN (eds) Tropical montane cloud forests. Ecological studies (analysis and synthesis), vol 110. Springer, New York, pp 203–216
Wallace J, McJannet D (2010) Processes controlling transpiration in the rainforests of North Queensland, Australia. J Hydrol 384:107–117. https://doi.org/10.1016/j.jhydrol.2010.01.015
West AG, Jackson SJ, Ehleringer JR (2006) Water extraction times for plant and soil materials used in stable isotope analysis. Rapid Commun Mass Sp 20:1317–1321. https://doi.org/10.1002/rcm.2456
Williams JW, Jackson ST, Kutzbach JE (2007) Projected distributions of novel and disappearing climates by 2100 AD. PNAS 104:5738–5742. https://doi.org/10.1073/pnas.0606292104
Williams-Linera G (1997) Phenology of deciduous and broadleaved-evergreen tree species in a Mexican tropical lower montane forest. Glob Ecol Biogeogr Lett 6:115–127. https://doi.org/10.1371/journal.pone.0056283
Williams-Linera G, Toledo-Garibaldi M, Gallardo Hernández C (2013) How heterogeneous are the cloud forest communities in the mountains of central Veracruz, Mexico? Plant Ecol 214:685–701. https://doi.org/10.1007/s11258-013-0199-5
WRB (2007) World reference base for soil resources 2006, first update 2007. FAO, Rome
Yang B, Wena X, Suna X (2015) Seasonal variations in depth of water uptake for a subtropical coniferous plantation subjected to drought in an East Asian monsoon region. Agr Forest Meteorol 201:218–228. https://doi.org/10.1016/j.agrformet.2014.11.020
Acknowledgements
We gratefully thank the Instituto de Ecología, A.C. (INECOL), Xalapa, Veracruz for the permission to conduct this research in the Santuario de Bosque de Niebla. We thank Wenbo Yang and Stefania Mambelli for analyzing the isotope samples and for providing the information about the spectrometers used. Chris Wong is thanked for his guidance with the cryogenic water extractions, Teresa González for constructing the sap flow sensors and help with data collection, Erika Mendoza for her assistance in the field and help in the root sampling and separation, Daniela Arreola for her work in developing the soil moisture calibration curves, and Greg Goldsmith for input and discussions about the study itself. Finally, we appreciate the comments of two anonymous reviewers and the Handling Editor Louis S. Santiago that helped to improve earlier versions of the manuscript. This research was supported by the PAPIIT-UNAM (IB100313 and IB100113) grants, respectively to LE Muñoz-Villers and F Holwerda, and by the INFRA-CONACyT-México (No. 187646) grant to F Holwerda. MS Alvarado-Barrientos was supported by a postdoctoral fellowship from DGAPA-UNAM.
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LEMV developed the idea of this research and designed the study. LEMV, FH and DRG collected the field data. LEMV and MSAB performed the samplings and the cryogenic extractions for isotope analysis. MASB performed the Bayesian mixing model analysis. LEMV and FH analyzed and interpreted the results and wrote the first draft of the manuscript. DRG, MSAB and TED edited and commented on the manuscript. LEMV, FH and TED worked on the revisions and final version.
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Muñoz-Villers, L.E., Holwerda, F., Alvarado-Barrientos, M.S. et al. Reduced dry season transpiration is coupled with shallow soil water use in tropical montane forest trees. Oecologia 188, 303–317 (2018). https://doi.org/10.1007/s00442-018-4209-0
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DOI: https://doi.org/10.1007/s00442-018-4209-0