Abstract
Key message
Increasing water-use efficiency, due to rising atmospheric CO2, did not stimulate radial growth in tropical trees, probably because negative impacts of changing climate on tree growth have overridden the small positive influence of rising atmospheric CO2.
Abstract
Global environmental changes affect tree growth and physiological behavior across the major biomes around the world. However, it is not yet clear how tree growth and physiology of tropical trees responded to global environmental changes in a long term, yet such information is critical to get insight into how tropical trees will respond to future global changes. The main objective of this review article is to explore the long-term trends in tree growth, carbon isotope discrimination (Δ13C), intercellular CO2 concentration (Ci), and intrinsic water-use efficiency (iWUE) across the tropics and subtropics. We distinguished between data generated on plot levels or on species or tree individual levels. Stand-level growth trends were not consistent across the studies and plots, although recent studies indicated a declining growth trend. Ci and iWUE consistently increased during the past decades, while Δ13C remained nearly constant. Increased iWUE either caused by higher photosynthetic capacity or reduced stomatal conductance did not translate into tree- and species-level radial growth, probably because assimilated carbon was allocated more to the root development to facilitate water absorption from moisture-limited soils rather than to basal area growth or xylem cell differentiation and maturation processess were impared by cavitation induced hydraulic limitations. Thus, higher temperature or drought-induced soil moisture deficit might have strongly impaired radial growth which has probably overridden the small positive effect of atmospheric CO2. Yet, disentangling the role of multiple drivers in explaining stem radial growth variation and their interactive effects on tropical trees under natural field conditions are not adequately studied and hence future research should focus on this aspect. Tree hydraulics should be taken into account in future research when predicting radial growth variability in tropical trees.
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References
Abiyu A, Mokria M, Gebrekirstos A, Bräuning A (2018) Tree-ring record in Ethiopian church forests reveals successive generation differences in growth rates and disturbance events. For Ecol Manag 409:835–844. https://doi.org/10.1016/j.foreco.2017.12.015
Acker SA, Mckee WA, Harmon ME, Franklin JF (1998) Long-term research on forest dynamics in the Pacific Northwest: a network of permanent forest plots. In: Dallmeier F, Comiskey JA (eds) Forest biodiversity in North, Central and South America, and the Caribbean. The Parthenon Publishing Group, Carnforth, pp 93–106
Ågren G (1981) Problems involved in modelling tree growth. In: Linder S (ed) Understanding and predicting tree growth. Swedish University of Agricultural Sciences, Uppsala, pp 7–17
Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372. https://doi.org/10.1111/j.1469-8137.2004.01224.x
Amthor JS (1989) Respiration and crop productivity. Springer, New York
Andreu-Hayles L, Planells O, Gutiérrez E et al (2011) Long tree-ring chronologies reveal 20th century increases in water-use efficiency but no enhancement of tree growth at five Iberian pine forests. Glob Change Biol 17:2095–2112. https://doi.org/10.1111/j.1365-2486.2010.02373.x
Aragão LEOC, Poulter B, Barlow JB et al (2014) Environmental change and the carbon balance of Amazonian forests. Biol Rev 89:913–931. https://doi.org/10.1111/brv.12088
Asner GP, Powell GVN, Mascaro J et al (2010) High-resolution forest carbon stocks and emissions in the Amazon. Proc Natl Acad Sci 107:16738–16742. https://doi.org/10.1073/pnas.1004875107
Atkin OK, Bruhn D, Hurry VM, Tjoelker MG (2005) Evans Review No. 2—the hot and the cold: unravelling the variable response of plant respiration to temperature. Funct Plant Biol 32:87–105. https://doi.org/10.1071/FP03176
Babst F, Alexander MR, Szejner P et al (2014) A tree-ring perspective on the terrestrial carbon cycle. Oecologia 176:307–322. https://doi.org/10.1007/s00442-014-3031-6
Baccini A, Walker W, Carvalho L et al (2017) Tropical forests are a net carbon source based on aboveground measurements of gain and loss. Science 358:230–234. https://doi.org/10.1126/science.aam5962
Baker TR, Phillips OL, Malhi Y et al (2004) Increasing biomass in Amazonian forest plots. Philos Trans R Soc B Biol Sci 359:353–365. https://doi.org/10.1098/rstb.2003.1422
Baker PJ, Bunyavejchewin S, Oliver CD, Ashton PS (2005) Disturbance history and historical stand dynamics of a seasonal tropical forest in western Thailand. Ecol Monogr 75:317–343. https://doi.org/10.1890/04-0488
Ballantyne AP, Baker PA, Chambers JQ et al (2011) Regional differences in south american monsoon precipitation inferred from the growth and isotopic composition of tropical trees. Earth Interact 15:1–35. https://doi.org/10.1175/2010EI277.1
Ben T, Hart PJ, Helle G (2017) Towards establishing a new environmental archive—annual growth periodicity, stable carbon isotope variability and reconstruction potential of Akoko (Euphorbia olowaluana), a native Hawaiian tree with C4 photosynthetic pathway. Erdkunde 71:77–92. https://doi.org/10.3112/ERDKUNDE.2017.01.05
Bennett AC, Mcdowell NG, Allen CD, Anderson-Teixeira KJ (2015) Larger trees suffer most during drought in forests worldwide. Nat Plants. https://doi.org/10.1038/nplants.2015.139
Berry J, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543. https://doi.org/10.1146/annurev.pp.31.060180.002423
Betts RA, Boucher O, Collins M et al (2007) Projected increase in continental runoff due to plant responses to increasing carbon dioxide. Nature 448:1037–1041. https://doi.org/10.1038/nature06045
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science 320:1444–1449. https://doi.org/10.1126/science.1155121
Bowman DMJS, Brienen RJW, Gloor E et al (2013) Detecting trends in tree growth: not so simple. Trends Plant Sci 18:11–17. https://doi.org/10.1016/j.tplants.2012.08.005
Boyce CK, Lee J-E (2010) An exceptional role for flowering plant physiology in the expansion of tropical rainforests and biodiversity. Proc R Soc B Biol Sci 277:3437–3443. https://doi.org/10.1098/rspb.2010.0485
Brienen RJW, Lebrija-Trejos E, Zuidema PA, Martínez-Ramos M (2010a) Climate-growth analysis for a Mexican dry forest tree shows strong impact of sea surface temperatures and predicts future growth declines. Glob Change Biol 16:2001–2012. https://doi.org/10.1111/j.1365-2486.2009.02059.x
Brienen RJW, Zuidema PA, Martínez-Ramos M (2010b) Attaining the canopy in dry and moist tropical forests: strong differences in tree growth trajectories reflect variation in growing conditions. Oecologia 163:485–496. https://doi.org/10.1007/s00442-009-1540-5
Brienen RJW, Wanek W, Hietz P (2011) Stable carbon isotopes in tree rings indicate improved water use efficiency and drought responses of a tropical dry forest tree species. Trees 25:103–113. https://doi.org/10.1007/s00468-010-0474-1
Brienen RJW, Gloor E, Zuidema PA (2012a) Detecting evidence for CO2 fertilization from tree ring studies: the potential role of sampling biases. Glob Biogeochem Cycles 26:GB1025. https://doi.org/10.1029/2011GB004143
Brienen RJW, Helle G, Pons TL et al (2012b) Oxygen isotopes in tree rings are a good proxy for Amazon precipitation and El Nino-Southern Oscillation variability. Proc Natl Acad Sci 109:16957–16962. https://doi.org/10.1073/pnas.1205977109
Brienen RJW, Phillips OL, Feldpausch TR et al (2015) Long-term decline of the Amazon carbon sink. Nature 519:344–348. https://doi.org/10.1038/nature14283
Brienen RJW, Schöngart J, Zuidema A (2016) Tree rings in the tropics: insights into the ecology and climate sensitivity of tropical trees. In: Goldstein G, Santiago LS (eds) Tropical tree physiology: adaptations and responses in a changing environment. Springer, Basel, pp 439–461
Brienen RJW, Gloor M, Ziv G (2017) Tree demography dominates long-term growth trends inferred from tree rings. Glob Change Biol 23:474–484. https://doi.org/10.1111/gcb.13410
Briffa KR, Melvin TM (2011) A closer look at regional curve standardization of tree-ring records: justification of the need, a warning of some pitfalls, and suggested improvements in its application BT. In: Hughes MK, Swetnam TW, Diaz HF (eds) Dendroclimatology: progress and prospects. Springer Netherlands, Dordrecht, pp 113–145
Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143:1–10. https://doi.org/10.1007/s00442-004-1788-8
Chave J, Condit R, Muller-Landau HC et al (2008) Assessing evidence for a pervasive alteration in tropical tree communities. PLoS Biol 6:0455–0462. https://doi.org/10.1371/journal.pbio.0060045
Cherubini P, Dobbertin M, Innes JL (1998) Potential sampling bias in long-term forest growth trends reconstructed from tree rings: a case study from the Italian Alps. For Ecol Manag 109:103–118. https://doi.org/10.1016/S0378-1127(98)00242-4
Clark DA (2002) Are tropical forests an important carbon sink? Reanalysis of the long-term plot data. Ecol Appl 12:3–7. https://doi.org/10.1890/1051-0761(2002)012%5B0003:ATFAIC%5D2.0.CO;2
Clark DA, Piper SC, Keeling CD, Clark DB (2003) Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984–2000. Proc Natl Acad Sci 100:5852–5857. https://doi.org/10.1073/pnas.0935903100
Clark DB, Clark DA, Oberbauer SF (2010) Annual wood production in a tropical rain forest in NE Costa Rica linked to climatic variation but not to increasing CO2. Glob Change Biol 16:747–759. https://doi.org/10.1111/j.1365-2486.2009.02004.x
Clark DA, Clark DB, Oberbauer SF (2013) Field-quantified responses of tropical rainforest aboveground productivity to increasing CO2 and climatic stress, 1997–2009. J Geophys Res Biogeosci 118:783–794. https://doi.org/10.1002/jgrg.20067
Corlett RT (2011) Impacts of warming on tropical lowland rainforests. Trends Ecol Evol 26:606–613. https://doi.org/10.1016/j.tree.2011.06.015
Corlett RT (2016) The impacts of droughts in tropical forests. Trends Plant Sci 21:584–593. https://doi.org/10.1016/j.tplants.2016.02.003
Cox PM, Pearson D, Booth BB et al (2013) Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494:341–344. https://doi.org/10.1038/nature11882
Cunningham SC, Read J (2003) Do temperate rainforest trees have a greater ability to acclimate to changing temperatures than tropical rainforest trees? New Phytol 157:55–64. https://doi.org/10.1046/j.1469-8137.2003.00652.x
Dewar RC (2000) A model of the coupling between respiration, active processes and passive transport. Ann Bot 86:279–286. https://doi.org/10.1006/anbo.2000.1211
Diffenbaugh NS, Scherer M (2011) Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries. Clim Change 107:615–624. https://doi.org/10.1007/s10584-011-0112-y
Dong SX, Davies SJ, Ashton PS et al (2012) Variability in solar radiation and temperature explains observed patterns and trends in tree growth rates across four tropical forests. Proc R Soc B Biol Sci 279:3923–3931. https://doi.org/10.1098/rspb.2012.1124
Doughty CE (2011) An in situ leaf and branch warming experiment in the Amazon. Biotropica 43:658–665. https://doi.org/10.1111/j.1744-7429.2010.00746.x
Doughty CE, Goulden ML (2009) Are tropical forests near a high temperature threshold? J Geophys Res Biogeosci. https://doi.org/10.1029/2007JG000632
Doughty CE, Malhi Y, Araujo-Murakami A et al (2014) Allocation trade-offs dominate the response of tropical forest growth to seasonal and interannual drought. Ecology 95:2192–2201. https://doi.org/10.1890/13-1507.1
Drake BG, Gonzàlez-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2? Annu Rev Plant Physiol Plant Mol Biol 48:609–639. https://doi.org/10.1146/annurev.arplant.48.1.609
Eller BC, de V. Barros, Bittencourt FRL P, et al (2018) Xylem hydraulic safety and construction costs determine tropical tree growth. Plant Cell Environ 41:548–562. https://doi.org/10.1111/pce.13106
Farquhar GD, Von Caemmerer S (1982) Modelling of photosynthetic response to environmental conditions. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Encyclopedia of plant physiology. Springer, Heidelberg, pp 549–587
Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90. https://doi.org/10.1007/BF00386231
Farquhar GD, Hubick KT, Condon AG, Richards RA (1989) Carbon isotope fractionation and plant water-use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, New York, pp 21–40
Farquhar GD, Cernusak LA, Barnes B (2007) Heavy water fractionation during transpiration. Plant Physiol 143:11–18. https://doi.org/10.1104/pp.106.093278
Feeley KJ, Wright SJ, Supardi MNN et al (2007) Decelerating growth in tropical forest trees. Ecol Lett 10:461–469. https://doi.org/10.1111/j.1461-0248.2007.01033.x
Fichtler E, Helle G, Worbes M (2010) Stable-carbon isotope time series from tropical tree rings indicate a precipitation signal. Tree Ring Res 66:35–49. https://doi.org/10.3959/2008-20.1
Fisher JI, Hurtt GC, Thomas RQ, Chambers JQ (2008) Clustered disturbances lead to bias in large-scale estimates based on forest sample plots. Ecol Lett 11:554–563. https://doi.org/10.1111/j.1461-0248.2008.01169.x
Fritts HC (1976) Tree rings and climate. Academic Press, London
Fu P-L, Grießinger J, Gebrekirstos A et al (2017) Earlywood and latewood stable carbon and oxygen isotope variations in two pine species in southwestern China during the recent decades. Front Plant Sci. https://doi.org/10.3389/fpls.2016.02050
Gagen M, Finsinger W, Wagner-Cremer F et al (2011) Evidence of changing intrinsic water-use efficiency under rising atmospheric CO2 concentrations in boreal Fennoscandia from subfossil leaves and tree ring δ13C ratios. Glob Change Biol 17:1064–1072. https://doi.org/10.1111/j.1365-2486.2010.02273.x
Galbraith D, Levy PE, Sitch S et al (2010) Multiple mechanisms of Amazonian forest biomass losses in three dynamic global vegetation models under climate change. New Phytol 187:647–665. https://doi.org/10.1111/j.1469-8137.2010.03350.x
Gebrekirstos A, Mitlöhner R, Teketay D, Worbes M (2008) Climate-growth relationships of the dominant tree species from semi-arid savanna woodland in Ethiopia. Trees Struct Funct 22:631–641. https://doi.org/10.1007/s00468-008-0221-z
Gebrekirstos A, Worbes M, Teketay D et al (2009) Stable carbon isotope ratios in tree rings of co-occurring species from semi-arid tropics in Africa: patterns and climatic signals. Glob Planet Change 66:253–260. https://doi.org/10.1016/j.gloplacha.2009.01.002
Gebrekirstos A, van Noordwijk M, Neufeldt H, Mitlöhner R (2011) Relationships of stable carbon isotopes, plant water potential and growth: an approach to asses water use efficiency and growth strategies of dry land agroforestry species. Trees Struct Funct 25:95–102. https://doi.org/10.1007/s00468-010-0467-0
Gerant D, Podor M, Grieu P et al (1996) Carbon metabolism enzyme activities and carbon partitioning in Pinus halepensis Mill, exposed to mild drought and ozone. J Plant Physiol 148:142–147. https://doi.org/10.1016/S0176-1617(96)80306-3
Gessler A, Brandes E, Buchmann N et al (2009) Tracing carbon and oxygen isotope signals from newly assimilated sugars in the leaves to the tree-ring archive. Plant Cell Environ 32:780–795. https://doi.org/10.1111/j.1365-3040.2009.01957.x
Ghannoum O, Phillips NG, Sears MA et al (2010) Photosynthetic responses of two eucalypts to industrial-age changes in atmospheric [CO2] and temperature. Plant Cell Environ 33:1671–1681. https://doi.org/10.1111/j.1365-3040.2010.02172.x
Gloor M, Gatti L, Brienen R et al (2012) The carbon balance of South America: a review of the status, decadal trends and main determinants. Biogeosciences 9:5407–5430. https://doi.org/10.5194/bg-9-5407-2012
Gonzalez P, Neilson RP, Lenihan JM, Drapek RJ (2010) Global patterns in the vulnerability of ecosystems to vegetation shifts due to climate change. Glob Ecol Biogeogr 19:755–768. https://doi.org/10.1111/j.1466-8238.2010.00558.x
Grießinger J, Bräuning A, Helle G et al (2017) Late Holocene relative humidity history on the southeastern Tibetan plateau inferred from a tree-ring δ18O record: recent decrease and conditions during the last 1500 years. Quat Int 430:52–59. https://doi.org/10.1016/j.quaint.2016.02.011
Groenendijk P, van der Sleen P, Vlam M et al (2015) No evidence for consistent long-term growth stimulation of 13 tropical tree species: results from tree-ring analysis. Glob Change Biol 21:3762–3776. https://doi.org/10.1111/gcb.12955
Grossman D (2016) Amazon rainforest to get a growth check. Science 352:635–636. https://doi.org/10.1126/science.352.6286.635
Gunderson CA, O’hara KH, Campion CM et al (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Glob Change Biol 16:2272–2286. https://doi.org/10.1111/j.1365-2486.2009.02090.x
Hietz P, Wanek W, Dünisch O (2005) Long-term trends in cellulose δ13C and water-use efficiency of tropical Cedrela and Swietenia from Brazil. Tree Physiol 25:745–752
Hochreuther P, Wernicke J, Grießinger J et al (2016) Influence of the Indian Ocean Dipole on tree-ring δ18O of monsoonal Southeast Tibet. Clim Change 137:217–230. https://doi.org/10.1007/s10584-016-1663-8
Hogan KP, Whitehead D, Kallarackal J et al (1996) Photosynthetic activity of leaves of Pinus radiata and Nothofagus fusca after 1 year of growth at elevated CO2. Aust J Plant Physiol 23:623–630
Hu J, Riveros-Iregui DA (2016) Life in the clouds: are tropical montane cloud forests responding to changes in climate? Oecologia 180:1061–1073. https://doi.org/10.1007/s00442-015-3533-x
Huang JG, Bergeron Y, Denneler B et al (2007) Response of forest trees to increased atmospheric CO2. CRC Crit Rev Plant Sci 26:265–283. https://doi.org/10.1080/07352680701626978
Huang R, Zhu H, Liu X et al (2017) Does increasing intrinsic water use efficiency (iWUE) stimulate tree growth at natural alpine timberline on the southeastern Tibetan Plateau? Glob Planet Change 148:217–226. https://doi.org/10.1016/j.gloplacha.2016.11.017
Huntingford C, Zelazowski P, Galbraith D et al (2013) Simulated resilience of tropical rainforests to CO2-induced climate change. Nat Geosci 6:268–273. https://doi.org/10.1038/ngeo1741
Ibrahim L, Proe MF, Cameron AD (1997) Main effects of nitrogen supply and drought stress upon whole-plant carbon allocation in poplar. Can J For Res 27:1413–1419. https://doi.org/10.1139/x97-080
IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner GK et al (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, p 1535
IPCC (2014) Part A: global and sectoral aspects (Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change). In: Field CV et al (ed) Climate change 2014: impacts, adaptation, and vulnerability. Cambridge University Press, Cambridge, p 1132
Islam M, Rahman M, Bräuning A (2018a) Growth-ring boundary anatomy and dendrochronological potential in a moist tropical forest in Northeastern Bangladesh. Tree Ring Res 74:76–93
Islam M, Rahman M, Bräuning A (2018b) Xylem anatomical responses of diffuse porous Chukrasia tabularis to climate in a South Asian moist tropical forest. For Ecol Manag 412:9–20. https://doi.org/10.1016/j.foreco.2018.01.035
Islam M, Rahman M, Bräuning A (2018c) Long-term hydraulic adjustment of three tropical moist forest tree species to changing climate. Front Plant Sci 9:1761. https://doi.org/10.3389/fpls.2018.01761
Islam M, Rahman M, Bräuning A (2019a) Impact of extreme drought on tree-ring width and vessel anatomical features of Chukrasia tabularis. Dendrochronologia 53:63–72. https://doi.org/10.1016/j.dendro.2018.11.007
Islam M, Rahman M, Bräuning A (2019b) Long-term wood anatomical time series of two ecologically contrasting tropical tree species reveal differential hydraulic adjustment to climatic stress. Agric For Meteorol 265:412–423. https://doi.org/10.1016/j.agrformet.2018.11.037
Jones JA, Wei X, van Noordwijk M et al (2018) Forest landscape hydrology in a “new normal” era of climate and land use change. In: Creed IF, van Noordwijk M (eds) Forest and water on a changing planet: vulnerability, adaptation and governance opportunities. International Union of Forest Research Organizations (IUFRO), Vienna, pp 81–99
Jung M, Reichstein M, Ciais P et al (2010) Recent decline in the global land evapotranspiration trend due to limited moisture supply. Nature 467:951–954. https://doi.org/10.1038/nature09396
Köhl M, Neupane PR, Lotfiomran N (2017) The impact of tree age on biomass growth and carbon accumulation capacity: a retrospective analysis using tree ring data of three tropical tree species grown in natural forests of Suriname. PLoS One 12:e0181187. https://doi.org/10.1371/journal.pone.0181187
Körner C (1998) Tropical forests in a CO2-rich world. Clim Change 39:297–315. https://doi.org/10.1023/A:1005325204713
Körner C (2006) Plant CO2 responses: an issue of definition, time and resource supply. New Phytol 172:393–411. https://doi.org/10.1111/j.1469-8137.2006.01886.x
Kosugi Y, Takanashi S, Matsuo N, Nik AR (2009) Midday depression of leaf CO2 exchange within the crown of Dipterocarpus sublamellatus in a lowland dipterocarp forest in Peninsular Malaysia. Tree Physiol 29:505–515. https://doi.org/10.1093/treephys/tpn041
Krause GH, Winter K, Krause B et al (2010) High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations. Funct Plant Biol 37:890–900. https://doi.org/10.1071/FP10034
Laurance SGW, Laurance WF, Henrique EMN et al (2009) Long-term variation in Amazon forest dynamics. J Veg Sci 20:323–333. https://doi.org/10.1111/j.1654-1103.2009.01044.x
Leakey ADB, Ainsworth EA, Bernacchi CJ et al (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876. https://doi.org/10.1093/jxb/erp096
Leavitt SW, Lone A (1991) Seasonal stable-carbon isotope variability in tree rings: possible paleoenvironmental signals. Chem Geol 87:59–70. https://doi.org/10.1016/0168-9622(91)90033-S
Lewis SL (2006) Tropical forests and the changing earth system. Philos Trans R Soc B Biol Sci 361:195–210. https://doi.org/10.1098/rstb.2005.1711
Lewis SL, Phillips OL, Baker TR et al (2004) Concerted changes in tropical forest structure and dynamics: evidence from 50 South American long-term plots. Philos Trans R Soc Lond B Biol Sci 359:421–436. https://doi.org/10.1098/rstb.2003.1431
Lewis SL, Lopez-Gonzalez G, Sonké B et al (2009) Increasing carbon storage in intact African tropical forests. Nature 457:1003–1006. https://doi.org/10.1038/nature07771
Li D, Fang K, Li Y et al (2017) Climate, intrinsic water-use efficiency and tree growth over the past 150 years in humid subtropical China. PLoS One. https://doi.org/10.1371/journal.pone.0172045
Lloyd J, Farquhar GD (2008) Effects of rising temperatures and [CO2] on the physiology of tropical forest trees. Philos Trans R Soc Lond B Biol Sci 363:1811–1817. https://doi.org/10.1098/rstb.2007.0032
Loader NJ, Walsh RPD, Robertson I et al (2011) Recent trends in the intrinsic water-use efficiency of ringless rainforest trees in Borneo. Philos Trans R Soc B Biol Sci 366:3330–3339. https://doi.org/10.1098/rstb.2011.0037
Locosselli GM, Buckeridge MS, Moreira MZ, Ceccantini G (2013) A multi-proxy dendroecological analysis of two tropical species (Hymenaea spp., Leguminosae) growing in a vegetation mosaic. Trees Struct Funct 27:25–36. https://doi.org/10.1007/s00468-012-0764-x
Locosselli GM, Krottenthaler S, Pitsch P et al (2017) Age and growth rate of congeneric tree species (Hymenaea spp.—Leguminosae) inhabiting different tropical biomes. Erdkunde 71:45–57. https://doi.org/10.3112/erdkunde.2017.01.03
Malhi Y, Phillips OL (2004) Tropical forests and global atmospheric change: a synthesis. Philos Trans R Soc Lond B Biol Sci 359:549–555. https://doi.org/10.1098/rstb.2003.1449
Marcott SA, Shakun JD, Clark PU, Mix AC (2013) A reconstruction of regional and global temperature for the past 11,300 years. Science 339:1198–1201. https://doi.org/10.1126/science.1228026
Markesteijn L, Poorter L, Bongers F et al (2011) Hydraulics and life history of tropical dry forest tree species: coordination of species’ drought and shade tolerance. New Phytol 191:480–495. https://doi.org/10.1111/j.1469-8137.2011.03708.x
McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801. https://doi.org/10.1016/j.quascirev.2003.06.017
Mendivelso HA, Camarero JJ, Obregon OR et al (2013) Differential growth responses to water balance of coexisting deciduous tree species are linked to wood density in a Bolivian tropical dry forest. PLoS One 8:11. https://doi.org/10.1371/journal.pone.0073855
Mokria M, Gebrekirstos A, Aynekulu E, Bräuning A (2015) Tree dieback affects climate change mitigation potential of a dry Afromontane forest in northern Ethiopia. For Ecol Manag 344:73–83. https://doi.org/10.1016/j.foreco.2015.02.008
Mokria M, Gebrekirstos A, Abiyu A et al (2017) Multi-century tree-ring precipitation record reveals increasing frequency of extreme dry events in the upper Blue Nile River catchment. Glob Change Biol 23:5436–5454. https://doi.org/10.1111/gcb.13809
Murphy HT, Bradford MG, Dalongeville A et al (2013) No evidence for long-term increases in biomass and stem density in the tropical rain forests of Australia. J Ecol 101:1589–1597. https://doi.org/10.1111/1365-2745.12163
Nagy RC, Rastetter EB, Neill C, Porder S (2017) Nutrient limitation in tropical secondary forests following different management practices. Ecol Appl 27:734–755. https://doi.org/10.1002/eap.1478
Nock CA, Baker PJ, Wanek W et al (2011) Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand. Glob Change Biol 17:1049–1063. https://doi.org/10.1111/j.1365-2486.2010.02222.x
Norby RJ, Zak DR (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annu Rev Ecol Evol Syst 42:181–203. https://doi.org/10.1146/annurev-ecolsys-102209-144647
Ohashi S, Okada N, Nobuchi T et al (2009) Detecting invisible growth rings of trees in seasonally dry forests in Thailand: isotopic and wood anatomical approaches. Trees 23:813–822. https://doi.org/10.1007/s00468-009-0322-3
Paivinen R, Yli-Kojola H (1989) Permanent sample plots in large-area forest inventory. Silva Fenn 23:243–252
Peñuelas J, Canadell JG, Ogaya R (2011) Increased water-use efficiency during the 20th century did not translate into enhanced tree growth. Glob Ecol Biogeogr 20:597–608. https://doi.org/10.1111/j.1466-8238.2010.00608.x
Peters RL, Groenendijk P, Vlam M, Zuidema PA (2015) Detecting long-term growth trends using tree rings: a critical evaluation of methods. Glob Change Biol 21:2040–2054. https://doi.org/10.1111/gcb.12826
Phillips OL, Malhi Y, Higuchi N et al (1998) Changes in the carbon balance of tropical forests: evidence from long-term plots. Science 282:439–442. https://doi.org/10.1126/science.282.5388.439
Poorter L, McDonald I, Alarcón A et al (2010) The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytol 185:481–492. https://doi.org/10.1111/j.1469-8137.2009.03092.x
Poorter L, van der Sande MT, Thompson J et al (2015) Diversity enhances carbon storage in tropical forests. Glob Ecol Biogeogr 24:1314–1328. https://doi.org/10.1111/geb.12364
Prentice IC, Harrison SP, Bartlein PJ (2011) Global vegetation and terrestrial carbon cycle changes after the last ice age. New Phytol 189:988–998. https://doi.org/10.1111/j.1469-8137.2010.03620.x
Pucha-Cofrep D, Peters T, Bräuning A (2015) Wet season precipitation during the past century reconstructed from tree-rings of a tropical dry forest in Southern Ecuador. Glob Planet Change 133:65–78. https://doi.org/10.1016/j.gloplacha.2015.08.003
Pumijumnong N (2013) Dendrochronology in Southeast Asia. Trees Struct Funct 27:343–358. https://doi.org/10.1007/s00468-012-0775-7
Rahman M, Islam M, Bräuning A (2017a) Local and regional climatic signals recorded in tree-rings of Chukrasia tabularis in Bangladesh. Dendrochronologia 45:1–11. https://doi.org/10.1016/j.dendro.2017.06.006
Rahman M, Islam R, Islam M (2017b) Long-term growth decline in Toona ciliata in a moist tropical forest in Bangladesh: impact of global warming. Acta Oecol Int J Ecol 80:8–17. https://doi.org/10.1016/j.actao.2017.02.004
Rahman M, Islam M, Bräuning A (2018a) Tree radial growth is projected to decline in South Asian moist forest trees under climate change. Glob Planet Change 170:106–119. https://doi.org/10.1016/J.GLOPLACHA.2018.08.008
Rahman M, Islam M, Wernicke J et al (2018b) Changes in sensitivity of tree-ring widths to climate in a tropical moist forest tree in Bangladesh. Forests 9:761. https://doi.org/10.3390/f9120761
Rahman M, Islam M, Bräuning A (2019) Species-specific growth resilience to drought in a mixed semi-deciduous tropical moist forest in South Asia. For Ecol Manag 433:487–496. https://doi.org/10.1016/j.foreco.2018.11.034
Reich PB, Hobbie SE, Lee T et al (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925. https://doi.org/10.1038/nature04486
Reich PB, Hobbie SE, Lee TD, Pastore MA (2018) Unexpected reversal of C3 versus C4 grass response to elevated CO2 during a 20-year field experiment. Science 360:317–320. https://doi.org/10.1126/science.aas9313
Rozanski K, Araguas-Araguas L, Gonfiantini R (1992) Relation between long-term trends of oxygen-18 isotope composition of precipitation and climate. Science 258:981–985. https://doi.org/10.1126/science.258.5084.981
Rozendaal DMA, Zuidema PA (2011) Dendroecology in the tropics: a review. Trees Struct Funct 25:3–16. https://doi.org/10.1007/s00468-010-0480-3
Rozendaal DMA, Brienen RJW, Soliz-Gamboa CC, Zuidema PA (2010) Tropical tree rings reveal preferential survival of fast-growing juveniles and increased juvenile growth rates over time. New Phytol 185:759–769. https://doi.org/10.1111/j.1469-8137.2009.03109.x
Rozendaal DMA, Soliz-Gamboa CC, Zuidema PA (2011) Assessing long-term changes in tropical forest dynamics: a first test using tree-ring analysis. Trees - Struct Funct 25:115–124. https://doi.org/10.1007/s00468-010-0478-x
Ryan MG (1991) Effects of climate change on plant respiration. Ecol Appl 1:157–167. https://doi.org/10.2307/1941808
Ryan MG, Yoder BJ (1997) Hydraulic limits to tree height and tree growth. Bioscience 47:235–242. https://doi.org/10.2307/1313077
Saurer M, Spahni R, Frank DC et al (2014) Spatial variability and temporal trends in water-use efficiency of European forests. Glob Change Biol 20:3700–3712. https://doi.org/10.1111/gcb.12717
Saxe H, Cannell MGR, Johnsen O et al (2001) Tree and forest functioning in response to global warming. New Phytol 149:369–400. https://doi.org/10.1046/j.1469-8137.2001.00057.x
Scholz FG, Phillips NG, Bucci SJ et al (2011) Hydraulic capacitande:biophysics and functional significance of internal water sources in relation to tree size. In: Meinzer FC (ed) Size- and age-related changes in tree structure and function. Springer, Berlin, pp 91–119
Schubert BA, Timmermann A (2015) Reconstruction of seasonal precipitation in Hawai’i using high-resolution carbon isotope measurements across tree rings. Chem Geol 417:273–278. https://doi.org/10.1016/j.chemgeo.2015.10.013
Shaver GR, Canadell J, Chapin FS et al (2000) Global warming and terrestrial ecosystems: a conceptual framework for analysis. Bioscience 50:871–882. https://doi.org/10.1641/0006-3568(2000)050%5B0871:gwatea%5D2.0.co;2
Sholtis JD, Gunderson CA, Norby RJ, Tissue DT (2004) Persistent stimulation of photosynthesis by elevated CO2 in a sweetgum (Liquidambar styraciflua) forest stand. New Phytol 162:343–354. https://doi.org/10.1111/j.1469-8137.2004.01028.x
Silva LCR, Anand M (2013) Probing for the influence of atmospheric CO2 and climate change on forest ecosystems across biomes. Glob Ecol Biogeogr 22:83–92. https://doi.org/10.1111/j.1466-8238.2012.00783.x
Silva LCR, Anand M, Oliveira JM, Pillar VD (2009) Past century changes in Araucaria angustifolia (Bertol.) Kuntze water use efficiency and growth in forest and grassland ecosystems of southern Brazil: implications for forest expansion. Glob Change Biol 15:2387–2396. https://doi.org/10.1111/j.1365-2486.2009.01859.x
Silva LCR, Anand M, Leithead MD (2010) Recent widespread tree growth decline despite increasing atmospheric CO2. PLoS One 5:e11543. https://doi.org/10.1371/journal.pone.0011543
Sitch S, Huntingford C, Gedney N et al (2008) Evaluation of the terrestrial carbon cycle, future plant geography and climate-carbon cycle feedbacks using five Dynamic Global Vegetation Models (DGVMs). Glob Change Biol 14:2015–2039. https://doi.org/10.1111/j.1365-2486.2008.01626.x
Slik JWF, Arroyo-Rodríguez V, Aiba S-I et al (2015) An estimate of the number of tropical tree species. Proc Natl Acad Sci 112:7472–7477. https://doi.org/10.1073/pnas.1423147112
Stephenson NL, Das AJ, Condit R et al (2014) Rate of tree carbon accumulation increases continuously with tree size. Nature 507:90–93. https://doi.org/10.1038/nature12914
Steppe K, Sterck F, Deslauriers A (2015) Diel growth dynamics in tree stems: linking anatomy and ecophysiology. Trends Plant Sci 20:335–343. https://doi.org/10.1016/j.tplants.2015.03.015
Sun F, Kuang Y, Wen D et al (2010) Long-term tree growth rate, water use efficiency, and tree ring nitrogen isotope composition of Pinus massoniana L. in response to global climate change and local nitrogen deposition in Southern China. J Soils Sediments 10:1453–1465. https://doi.org/10.1007/s11368-010-0249-8
Teskey R, Wertin T, Bauweraerts I et al (2015) Responses of tree species to heat waves and extreme heat events. Plant Cell Environ 38:1699–1712. https://doi.org/10.1111/pce.12417
Thomas RB, Strain BR (1991) Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiol 96:627–634. https://doi.org/10.1104/pp.96.2.627
Tyree MT, Davis SD, Cochard H (1994) Biophysical perspectives of xylem evolution: is there a tradeoff of hydraulic efficiency for vulnerability to dysfunction? IAWA J 15:335–360. https://doi.org/10.1163/22941932-90001369
Van Nieuwstadt MGL, Sheil D (2005) Drought, fire and tree survival in a Borneo rain forest, East Kalimantan, Indonesia. J Ecol 93:191–201. https://doi.org/10.1111/j.1365-2745.2005.00954.x
van der Sleen P, Groenendijk P, Vlam M et al (2014) No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased. Nat Geosci 8:24–28. https://doi.org/10.1038/ngeo2313
van der Sleen P, Groenendijk P, Vlam M et al (2017a) Trends in tropical tree growth: re-analyses confirm earlier findings. Glob Change Biol 23:1761–1762. https://doi.org/10.1111/gcb.13572
van der Sleen P, Zuidema PA, Pons TL (2017b) Stable isotopes in tropical tree rings: theory, methods and applications. Funct Ecol 31:1674–1689. https://doi.org/10.1111/1365-2435.12889
Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298. https://doi.org/10.2307/1939481
Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15. https://doi.org/10.1890/08-0127.1
Vlam M, Baker PJ, Bunyavejchewin S et al (2014) Understanding recruitment failure in tropical tree species: insights from a tree-ring study. For Ecol Manag 312:108–116. https://doi.org/10.1016/j.foreco.2013.10.016
Volland F, Pucha D, Bräuning A (2016) Hydro-climatic variability in southern ecuador reflected by tree-ring oxygen isotopes. Erdkunde 70:69–82. https://doi.org/10.3112/erdkunde.2016.01.05
Way DA, Oren R (2010) Differential responses to changes in growth temperature between trees from different functional groups and biomes: a review and synthesis of data. Tree Physiol 30:669–688. https://doi.org/10.1093/treephys/tpq015
Williams LJ, Bunyavejchewin S, Baker PJ (2008) Deciduousness in a seasonal tropical forest in western Thailand: interannual and intraspecific variation in timing, duration and environmental cues. Oecologia 155:571–582. https://doi.org/10.1007/s00442-007-0938-1
Williams AP, Funk C, Michaelsen J et al (2012) Recent summer precipitation trends in the Greater Horn of Africa and the emerging role of Indian Ocean sea surface temperature. Clim Dyn 39:2307–2328. https://doi.org/10.1007/s00382-011-1222-y
Willium K, Percival F, Merino J, Mooney HA (1987) Estimation of tissue construction cost from heat of combustion and organic nitrogen content. Plant Cell Environ 10:725–734. https://doi.org/10.1111/1365-3040.ep11604754
Wils THG, Robertson I, Eshetu Z et al (2010) Towards a reconstruction of Blue Nile baseflow from Ethiopian tree rings. Holocene 20:837–848. https://doi.org/10.1177/0959683610365940
Wilson BF, Howard RA (1968) A computer model for cambial activity. For Sci 14:77–90
Wolfe BT, Kursar TA (2015) Diverse patterns of stored water use among saplings in seasonally dry tropical forests. Oecologia 179:925–936. https://doi.org/10.1007/s00442-015-3329-z
Worbes M (2002) One hundred years of tree-ring research in the tropics—a brief history and an outlook to future challenges. Dendrochronologia 20:217–231. https://doi.org/10.1078/1125-7865-00018
Worbes M, Junk WJ (1989) Dating tropical trees by means of 14C from bomb tests. Ecology 70:503–507. https://doi.org/10.2307/1937554
Yazaki K, Kuroda K, Nakano T et al (2015) Recovery of physiological traits in saplings of invasive Bischofia tree compared with three species native to the Bonin Islands under successive drought and irrigation cycles. PLoS One. https://doi.org/10.1371/journal.pone.0135117
Zhou G, Peng C, Li Y et al (2013) A climate change-induced threat to the ecological resilience of a subtropical monsoon evergreen broad-leaved forest in Southern China. Glob Change Biol 19:1197–1210. https://doi.org/10.1111/gcb.12128
Zimmermann MH (1978) Hydraulic architecture of some diffuse-porous trees. Can J Bot 56:2286–2295. https://doi.org/10.1139/b78-274
Zuidema PA, Vlam M, Chien PD (2011) Ages and long-term growth patterns of four threatened Vietnamese tree species. Trees Struct Funct 25:29–38. https://doi.org/10.1007/s00468-010-0473-2
Zuidema PA, Brienen RJW, Schöngart J (2012) Tropical forest warming: looking backwards for more insights. Trends Ecol Evol 27:193–194. https://doi.org/10.1016/j.tree.2011.12.007
Zuidema PA, Baker PJ, Groenendijk P et al (2013) Tropical forests and global change: filling knowledge gaps. Trends Plant Sci 18:413–419. https://doi.org/10.1016/j.tplants.2013.05.006
Acknowledgements
The first author sincerely acknowledges the Research Grants-Doctoral programme in Germany 2015–2016 provided by the German Academic Exchange Service (DAAD) (Grant no. 57129429). We thank Dr. Christoph Mayr for his suggestions at the development stage of this manuscript.
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Rahman, M., Islam, M., Gebrekirstos, A. et al. Trends in tree growth and intrinsic water-use efficiency in the tropics under elevated CO2 and climate change. Trees 33, 623–640 (2019). https://doi.org/10.1007/s00468-019-01836-3
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DOI: https://doi.org/10.1007/s00468-019-01836-3