Abstract
In Amazonian non-flooded forests with a moderate dry season, many trees do not form anatomically definite annual rings. Alternative indicators of annual rings, such as the oxygen (δ18Owc) and carbon stable isotope ratios of wood cellulose (δ13Cwc), have been proposed; however, their applicability in Amazonian forests remains unclear. We examined seasonal variations in the δ18Owc and δ13Cwc of three common species (Eschweilera coriacea, Iryanthera coriacea, and Protium hebetatum) in Manaus, Brazil (Central Amazon). E. coriacea was also sampled in two other regions to determine the synchronicity of the isotopic signals among different regions. The annual cyclicity of δ18Owc variation was cross-checked by 14C dating. The δ18Owc showed distinct seasonal variations that matched the amplitude observed in the δ18O of precipitation, whereas seasonal δ13Cwc variations were less distinct in most cases. The δ18Owc variation patterns were similar within and between some individual trees in Manaus. However, the δ18Owc patterns of E. coriacea differed by region. The ages of some samples estimated from the δ18Owc cycles were offset from the ages estimated by 14C dating. In the case of E. coriacea, this phenomenon suggested that missing or wedging rings may occur frequently even in well-grown individuals. Successful cross-dating may be facilitated by establishing δ18Owc master chronologies at both seasonal and inter-annual scales for tree species with distinct annual rings in each region.
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References
Alvares CA, Stape JL, Sentelhas PC, de Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Zeitschr 22:711–728. doi:10.1127/0941-2948/2013/0507
Anchukaitis KJ, Evans MN, Wheelwright NT, Schrag DP (2008) Stable isotope chronology and climate signal calibration in Neotropical montane cloud forest trees. J Geophys Res 113:G03030. doi:10.1029/2007JG000613
Andreu-Hayles L, Santos GM, Herrera-Ramírez DA, Martin-Fernández J, Ruiz-Carrascal D, Boza-Espinoza TE, Fuentes AF, Jørgensen PM (2015) Matching dendrochronological dates with the Southern Hemisphere 14C bomb curve to confirm annual tree rings in Pseudolmedia rigida from Bolivia. Radiocarbon 57:1–13. doi:10.2458/azu_rc.57.18192
Ballantyne AP, Baker PA, Chambers JQ, Villalba R, Argollo J (2011) Regional differences in South American monsoon precipitation inferred from the growth and isotopic composition of tropical trees. Earth Interact 15:1–35. doi:10.1175/2010EI277.1
Barbour MM (2007) Stable oxygen isotope composition of plant tissue: a review. Funct Plant Biol 34:83–94. doi:10.1071/FP06228
Brienen RJW, Lebrija-Trejos E, Zuidema PA, Martínez-Ramos M (2010) Climate-growth analysis for a Mexican dry forest tree shows strong impact of sea surface temperatures and predicts future growth declines. Glob Chang Biol 16:2001–2012. doi:10.1111/j.1365-2486.2009.02059.x
Brienen RJW, Helle G, Pons TL, Guyot JL, Gloor M (2012) Oxygen isotopes in tree rings are a good proxy for Amazon precipitation and El Nino-Southern Oscillation variability. Proc Natl Acad Sci USA 109:16957–16962. doi:10.1073/pnas.1205977109
Bronk Ramsey C (2009) Bayesian analysis of radiocarbon dates. Radiocarbon 51:337–360
Chambers JQ, Higuchi N, Schimel JP (1998) Ancient trees in Amazonia. Nature 391:135–136. doi:10.1038/34325
Chambers JQ, Negron-Juarez RI, Marra DM, Di Vittorio A, Tews J, Roberts D, Ribeiro GHPM, Trumbore SE, Higuchi N (2013) The steady-state mosaic of disturbance and succession across an old-growth Central Amazon forest landscape. Proc Natl Acad Sci USA 110:3949–3954. doi:10.1073/pnas.1202894110
Clark DA (2007) Detecting tropical forests’ responses to global climate and atmospheric change: current challenges and a way forward. Biotropica 39:4–19. doi:10.1111/j.1744-7429.2006.00227.x
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 USA 100:5852–5857. doi:10.1073/pnas.0935903100
da Silva RP, dos Santos J, Tribuzy ES, Chambers JQ, Nakamura S, Higuchi N (2002) Diameter increment and growth patterns for individual tree growing in Central Amazon, Brazil. For Ecol Manage 166:295–301. doi:10.1016/S0378-1127(01)00678-8
Dansgard BW (1964) Stable isotopes in precipitation. Tellus 16:436–468. doi:10.1111/j.2153-3490.1964.tb00181.x
Davidson EA, de Araújo AC, Artaxo P, Balch JK, Brown IF, Bustamante MMC, Coe MT, DeFries RS, Keller M, Longo M et al (2012) The Amazon basin in transition. Nature 481:321–328. doi:10.1038/nature10717
DeNiro MJ, Epstein S (1979) Relationship between the oxygen isotope ratios of terrestrial plant cellulose, carbon dioxide, and water. Science 204:51–53. doi:10.1126/science.204.4388.51
Evans MN, Schrag DP (2004) A stable isotope-based approach to tropical dendroclimatology. Geochim Cosmochim Acta 68:3295–3305. doi:10.1016/j.gca.2004.01.006
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Biol 40:503–537. doi:10.1146/annurev.pp.40.060189.002443
Ferrio JP, Voltas J (2005) Carbon and oxygen isotope ratios in wood constituents of Pinus halepensis as indicators of precipitation, temperature and vapour pressure deficit. Tellus 57B:164–173. doi:10.1111/j.1600-0889.2005.00137.x
Fichtler E, Clark DA, Worbes M (2003) Age and long-term growth of trees in an old-growth tropical rain forest, based on analyses of tree rings and 14C. Biotropica 35:306–317. doi:10.1646/03027
Green JW (1963) Wood cellulose. In: Whistler RL (ed) Methods in carbohydrate chemistry, vol 3. Academic Press, New York, pp 9–21
Helle G, Schleser GH (2004) Beyond CO2-fixation by Rubisco-an interpretation of 13C/12C variations in tree rings from novel intra-seasonal studies on broad-leaf trees. Plant Cell Environ 27:367–380. doi:10.1111/j.0016-8025.2003.01159.x
Holdridge LR (1947) Determination of world plant formations from simple climatic data. Science 105:367–368. doi:10.1126/science.105.2727.367
Hua Q, Barbetti M, Rakowski AZ (2013) Atmospheric radiocarbon for the period 1950–2010. Radiocarbon 55:2059–2072. doi:10.2458/azu_js_rc.v55i2.16177
IAEA/WMO (2015) Global network of isotopes in precipitation. The GNIP Database (URL http://www.iaea.org/water/). Accessed 19 April 2013
Japan Meteorological Agency (2015) ClimatView (URL http://www.data.jma.go.jp/gmd/cpd/monitor/climatview/frame.php). Accessed 18 February 2015
Kagawa A, Sano M, Nakatsuka T, Ikeda T, Kubo S (2015) An optimized method for stable isotope analysis of tree rings by extracting cellulose directly from cross-sectional laths. Chem Geol 393–394:16–25. doi:10.1016/j.chemgeo.2014.11.019
Kurokawa H, Yoshida T, Nakamura T, Lai J, Nakashizuka T (2003) The age of tropical rain-forest canopy species, Borneo ironwood (Eusideroxylon zwageri), determined by 14C dating. J Trop Ecol 19:1–7. doi:10.1017/S0266467403003018
Leavitt SW (2010) Tree-ring C-H-O isotope variability and sampling. Sci Total Environ 408:5244–5253. doi:10.1016/j.scitotenv.2010.07.057
Leavitt SW, Long A (1991) Seasonal stable-carbon isotope variability in tree rings: possible paleoenvironmental signals. Chem Geol Isot Geosci Sect 87:59–70. doi:10.1016/0168-9622(91)90033-S
Li ZH, Labbé N, Driese SG, Grissino-Mayer HD (2011) Micro-scale analysis of tree-ring δ18O and δ13C on α-cellulose spline reveals high-resolution intra-annual climate variability and tropical cyclone activity. Chem Geol 284:138–147. doi:10.1016/j.chemgeo.2011.02.015
Loader NJ, Robertson I, Barker AC, Switsur VR, Waterhouse JS (1997) An improved technique for the batch processing of small wholewood samples to α-cellulose. Chem Geol 136:313–317. doi:10.1016/S0009-2541(96)00133-7
Loader NJ, Robertson I, McCarroll D (2003) Comparison of stable carbon isotope ratios in the whole wood, cellulose and lignin of oak tree-rings. Palaeogeogr Palaeoclimatol Palaeoecol 196:395–407. doi:10.1016/S0031-0182(03)00466-8
Martı́nez-Ramos M, Alvarez-Buylla ER (1998) How old are tropical rain forest trees? Trends Plant Sci 3:400–405. doi:10.1016/S1360-1385(98)01313-2
Matsui E, Salati E, Ribeiro MNG, Reis CM, Tancredi ACSNF, Gat JR (1983) Precipitation in the central Amazon Basin: the isotopic composition of rain and atmospheric moisture at Belém and Manaus. Acta Amaz 13:307–369
McCarroll D, Loader NJ (2004) Stable isotopes in tree rings. Quat Sci Rev 23:771–801. doi:10.1016/j.quascirev.2003.06.017
Mooney HA, Field C, Vásquez Yanes C, Chu C (1983) Environmental controls on stomatal conductance in a shrub of the humid tropics. Proc Natl Acad Sci USA 80:1295–1297
Mullane M, Waterhouse J, Switsur V (1988) On the development of a novel method for the determination of stable oxygen isotope ratios in cellulose. Int J Radiat Appl Instrumentation Part A Appl Radiat Isot 39:1029–1035. doi:10.1016/0883-2889(88)90136-0
Noguchi H, Suwa R, de Souza CAS, da Silva RP, dos Santos J, Higuchi N, Kajimoto T, Ishizuka M (2014) Examination of vertical distribution of fine root biomass in a tropical moist forest of the central Amazon, Brazil. Jpn Agric Res Q 48:231–235
Ogata Y, Nobuchi T, Fujita M, Sahri MH (2002) Asynchronous wood formation in young Acacia mangium planted in Malaysia. J Wood Sci 48:89–94. doi:10.1007/BF00767283
Ohashi S, Okada N, Nobuchi T, Siripatanadilok S, Veenin T (2009) Detecting invisible growth rings of trees in seasonally dry forests in Thailand: isotopic and wood anatomical approaches. Trees Struct Funct 23:813–822. doi:10.1007/s00468-009-0322-3
Ohashi S, Okada N, Abdul Azim AA, Siripatanadilok S, Veenin T, Yahya AZ, Nobuchi T (2014) Vessel feature changes as a tool for detecting annual rings in tropical trees. Trees Struct Funct 28:137–149. doi:10.1007/s00468-013-0936-3
Pearson S, Hua Q, Allen K, Bowman DMJS (2011) Validating putatively cross-dated Callitris tree-ring chronologies using bomb-pulse radiocarbon analysis. Aust J Bot 59:7–17. doi:10.1071/BT10164
Pons TL, Helle G (2011) Identification of anatomically non-distinct annual rings in tropical trees using stable isotopes. Trees Struct Funct 25:83–93. doi:10.1007/s00468-010-0527-5
Poussart PF, Schrag DP (2005) Seasonally resolved stable isotope chronologies from northern Thailand deciduous trees. Earth Planet Sci Lett 235:752–765. doi:10.1016/j.epsl.2005.05.012
Poussart PF, Evans MN, Schrag DP (2004) Resolving seasonality in tropical trees: multi-decade, high-resolution oxygen and carbon isotope records from Indonesia and Thailand. Earth Planet Sci Lett 218:301–316. doi:10.1016/S0012-821X(03)00638-1
Poussart PM, Myneni SCB, Lanzirotti A (2006) Tropical dendrochemistry: a novel approach to estimate age and growth from ringless trees. Geophys Res Lett 33:L17711. doi:10.1029/2006GL026929
Roberts J, Cabral OMR, De Aguiar LF (1990) Stomatal and boundary-layer conductances in an Amazonian terra firme rain forest. J Appl Ecol 27:336–353. doi:10.2307/2403590
Roden JS, Lin G, Ehleringer JR (2000) A mechanistic model for interpretation of hydrogen and oxygen isotope ratios in tree-ring cellulose. Geochim Cosmochim Acta 64:21–35. doi:10.1016/S0016-7037(99)00195-7
Rozanski K, Araguás-Araguás L, Gonfiantini R (1993) Isotopic patterns in modern global precipitation. In: Swart PK, Lohmann KC, Mckenzie J, Savin S (eds) Climate change in continental isotopic records. American Geophysical Union, Washington, DC, pp 1–36
Salati E, Dall’Olio A, Matsui E, Gat JR (1979) Recycling of water in the Amazon basin: an isotopic study. Water Resour Res 15:1250–1258. doi:10.1029/WR015i005p01250
Sternberg LDSL, Deniro MJ, Savidge RA (1986) Oxygen isotope exchange between metabolites and water during biochemical reactions leading to cellulose synthesis. Plant Physiol 82:423–427. doi:10.1104/pp.82.2.423
Stuiver M, Polach HA (1977) Discussion; reporting of 14C data. Radiocarbon 19:355–363
Suwa R, Sakai T, dos Santos J, da Silva RP, Kajimoto T, Ishizuka M, Higuchi N (2013) Significance of topographic gradient in stem diameter–height allometry for precise biomass estimation of a tropical moist forest in the central Amazon. Jpn Agric Res Q 47:109–114
ter Steege H, Pitman NCA, Sabatier D, Baraloto C, Salomão RP, Guevara JE, Phillips OL, Castilho CV, Magnusson WE, Molino JF et al (2013) Hyperdominance in the Amazonian tree flora. Science 342:1243092. doi:10.1126/science.1243092
Verheyden A, Helle G, Schleser GH, Dehairs F, Beeckman H, Koedam N (2004a) Annual cyclicity in high-resolution stable carbon and oxygen isotope ratios in the wood of the mangrove tree Rhizophora mucronata. Plant Cell Environ 27:1525–1536. doi:10.1111/j.1365-3040.2004.01258.x
Verheyden A, Kairo JG, Beeckman H, Koedam N (2004b) Growth rings, growth ring formation and age determination in the mangrove Rhizophora mucronata. Ann Bot 94:59–66. doi:10.1093/aob/mch115
Verheyden A, De Ridder F, Schmitz N, Beeckman H, Koedam N (2005a) High-resolution time series of vessel density in Kenyan mangrove trees reveal a link with climate. New Phytol 167:425–436. doi:10.1111/j.1469-8137.2005.01415.x
Verheyden A, Roggeman M, Bouillon S, Elskens M, Beeckman H, Koedam N (2005b) Comparison between δ13C of α-cellulose and bulk wood in the mangrove tree Rhizophora mucronata: implications for dendrochemistry. Chem Geol 219:275–282. doi:10.1016/j.chemgeo.2005.02.015
Vetter RE, Botosso PC (1989) Remarks on age and growth rate determination of Amazonian trees. IAWA J 10:133–145. doi:10.1163/22941932-90000481
Vlam M, Baker PJ, Bunyavejchewin S, Zuidema PA (2014) Temperature and rainfall strongly drive temporal growth variation in Asian tropical forest trees. Oecologia 174:1449–1461. doi:10.1007/s00442-013-2846-x
Worbes M (1997) The forest ecosystem of the floodplains. In: Junk WJ (ed) The Central Amazon floodplain. Springer, Berlin, pp 223–265
Worbes M (1999) Annual growth rings, rainfall-dependent growth and long-term growth patterns of tropical trees from the Caparo Forest Reserve in Venezuela. J Ecol 87:391–403. doi:10.1046/j.1365-2745.1999.00361.x
Worbes M, Junk WJ (1999) How old are tropical trees? The persistence of a myth. IAWA J 20:255–260
Xu X, Trumbore SE, Zheng S, Southon JR, McDuffee KE, Luttgen M, Liu JC (2007) Modifying a sealed tube zinc reduction method for preparation of AMS graphite targets: reducing background and attaining high precision. Nucl Instruments Methods Phys Res Sect B 259:320–329. doi:10.1016/j.nimb.2007.01.175
Xu C, Sano M, Nakatsuka T (2011) Tree ring cellulose δ18O of Fokienia hodginsii in northern Laos: a promising proxy to reconstruct ENSO? J Geophys Res 116:D24109. doi:10.1029/2011JD016694
Acknowledgments
We thank Mr. F. Q. Reis, Mr. F. R. de Araujo, and Dr. V. Carneiro for identification of the tree species. The field investigations and sample preparations were assisted by Mr. M. Sakurai, Dr. J. dos Santos, Dr. A. J. N. Lima, Mr. L. K. de Ourique, Mr. G. H. P. M. Ribeiro, Ms. E. Barboza, Dr. C. C. do Nascimento, and Ms. P. Baggio. Dr. R. Suwa and Dr. H. Noguchi gave us useful comments regarding the discussion and interpretation of the results. We are also grateful to Dr. H. ter Steege for giving us valuable advice on selecting species. Permission to collect samples was granted by the Chico Mendes Institute of Biodiversity Conservation and this study was financially supported by the Science and Technology Research Partnership for Sustainable Development program of the Japan Science and Technology Agency and the Japan International Cooperation Agency.
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S. O., F. M. D., A. K., T. K., S. E. T., M. I., and N. H. designed the experiment. S. O. and F. M. D. conducted the fieldwork. S. O. and A. K. performed wood anatomical and stable isotope analyses, and S. E. T. and X. X. performed radiocarbon analysis. S. O., F. M. D., A. K., and T. K. wrote the manuscript; other authors provided editorial advice.
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Communicated by Russell Monson.
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Ohashi, S., Durgante, F.M., Kagawa, A. et al. Seasonal variations in the stable oxygen isotope ratio of wood cellulose reveal annual rings of trees in a Central Amazon terra firme forest. Oecologia 180, 685–696 (2016). https://doi.org/10.1007/s00442-015-3509-x
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DOI: https://doi.org/10.1007/s00442-015-3509-x