{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,5]],"date-time":"2026-06-05T20:35:13Z","timestamp":1780691713639,"version":"3.54.1"},"reference-count":40,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,1,10]],"date-time":"2025-01-10T00:00:00Z","timestamp":1736467200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>The ecophysiological and ecohydrological impacts of climate change and progressively increasing atmospheric carbon dioxide (CO<jats:sub>2<\/jats:sub>) concentration on agroecosystems are not well understood compared to the forest ecosystems. In this study, we utilized the presence of old apple and pear trees in the alpine valleys of Northern Italy (maintained for cultural heritage purposes) to investigate climate-scale physiological responses. We developed long-term tree-ring stable isotopic records (\u03b4<jats:sup>13<\/jats:sup>C and \u03b4<jats:sup>18<\/jats:sup>O) from apple (1976-2021) and pear trees (1943-2021). This allowed the reconstruction of key ecophysiological processes like the variations in intrinsic water use efficiency (<jats:italic>i<\/jats:italic>WUE), and we investigated how these trees responded to climate and CO<jats:sub>2<\/jats:sub> changes over decades. Results showed a slight declining trend in carbon discrimination (<jats:italic>\u0394<\/jats:italic><jats:sup>13<\/jats:sup>C) while intercellular CO<jats:sub>2<\/jats:sub> concentration (<jats:italic>C<\/jats:italic>i) for both species has been increasing since the late 1980s. Concurrently both species exhibited a rising trend in <jats:italic>i<\/jats:italic>WUE, with apple trees demonstrating higher efficiency, which appears to be primarily driven by the CO<jats:sub>2<\/jats:sub>-fertilization effect. The concomitant trends in tree-ring \u03b4<jats:sup>18<\/jats:sup>O suggested a relatively stable local hydroclimate during the study period with some species-specific responses. Analyses further revealed that minimum growing season temperature, not precipitation was the most significant factor influencing the rise in <jats:italic>i<\/jats:italic>WUE alongside with CO<jats:sub>2<\/jats:sub> fertilization effect. Analyses of species\u2019 \u03b4<jats:sup>13<\/jats:sup>C coupled with their respective \u03b4<jats:sup>18<\/jats:sup>O confirmed that the rise in <jats:italic>i<\/jats:italic>WUE was due to increased carbon assimilation rather than a decline in evapotranspiration. Moreover, coupled \u03b4<jats:sup>13<\/jats:sup>C\u2013\u03b4<jats:sup>18<\/jats:sup>O analyses suggested increasing trends in carbon assimilation, with apple trees showing higher inter-decadal variations. These long-term records provide a unique opportunity to test and calibrate how these systems respond to recent and anticipated climate change.<\/jats:p>","DOI":"10.3389\/fpls.2024.1471415","type":"journal-article","created":{"date-parts":[[2025,1,10]],"date-time":"2025-01-10T06:12:08Z","timestamp":1736489528000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["Multi-decadal tree-ring stable isotope records of apple and pear trees indicate coherent ecophysiological responses to environmental changes in alpine valleys"],"prefix":"10.3389","volume":"15","author":[{"given":"Nilendu","family":"Singh","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Massimo","family":"Tagliavini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Enrico","family":"Tomelleri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leonardo","family":"Montagnani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,1,10]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1038\/s41558-020-0747-7","article-title":"Diminishing CO2-driven gains in water-use efficiency of global forests","volume":"10","author":"Adams","year":"2020","journal-title":"Nat. Climate Change"},{"key":"B2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.eja.2013.05.007","article-title":"Daily photosynthetic radiation use efficiency for apple and pear leaves: seasonal changes and estimation of canopy net carbon exchange rate","volume":"51","author":"Auzmendi","year":"2013","journal-title":"Eur. J. Agron."},{"key":"B3","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1007\/s00442-014-3031-6","article-title":"A tree-ring perspective on the terrestrial carbon cycle","volume":"176","author":"Babst","year":"2014","journal-title":"Oecologia"},{"key":"B4","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1002\/2016GL071507","article-title":"What drives interannual variation in tree ring oxygen isotopes in the Amazon","volume":"43","author":"Baker","year":"2016","journal-title":"Geophysical Res. Lett."},{"key":"B5","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1071\/FP06228","article-title":"Stable oxygen isotope composition of plant tissue: a review","volume":"34","author":"Barbour","year":"2007","journal-title":"Funct. Plant Biol."},{"key":"B6","doi-asserted-by":"publisher","first-page":"544","DOI":"10.1111\/nph.2012.197.issue-2","article-title":"Elevated CO2 increases tree-level intrinsic water use efficiency: Insights from carbon and oxygen isotope analyses in tree rings across three forest FACE sites","volume":"197","author":"Battipaglia","year":"2013","journal-title":"New Phytol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"125748","DOI":"10.1016\/j.dendro.2020.125748","article-title":"Compiled records of atmospheric CO2 concentrations and stable carbon isotopes to reconstruct climate and derive plant ecophysiological indices from tree rings","volume":"63","author":"Belmecheri","year":"2020","journal-title":"Dendrochronologia"},{"key":"B8","volume-title":"Team. R: a language and environment for statistical computing","author":"Core","year":"2015"},{"key":"B9","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1104\/pp.106.093278","article-title":"Heavy water fractionation during transpiration","volume":"143","author":"Farquhar","year":"2007","journal-title":"Plant Physiol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1071\/PP9820121","article-title":"On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves","volume":"9","author":"Farquhar","year":"1982","journal-title":"Funct. Plant Biol."},{"key":"B11","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1038\/nclimate2614","article-title":"Water-use efficiency and transpiration across European forests during the Anthropocene","volume":"5","author":"Frank","year":"2015","journal-title":"Nature Climate Change"},{"key":"B12","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1007\/978-3-030-92698-4_19","article-title":"Climate signals in stable isotope tree-ring records","volume-title":"Stable Isotopes in Tree Rings: Inferring Physiological, Climatic and Environmental Responses","author":"Gagen","year":"2022"},{"key":"B13","doi-asserted-by":"publisher","first-page":"1185","DOI":"10.1111\/2041-210X.13847","article-title":"CaptuRING: A do-it-yourself tool for wood sample digitization","volume":"13","author":"Garc\u00eda-Hidalgo","year":"2022","journal-title":"Methods Ecol. Evol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1093\/treephys\/tpu040","article-title":"Stable isotopes in tree rings: towards a mechanistic understanding of isotope fractionation and mixing processes from the leaves to the wood","volume":"34","author":"Gessler","year":"2014","journal-title":"Tree Physiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"503","DOI":"10.1007\/s00468-016-1478-2","article-title":"The increase of atmospheric CO2 affects growth potential and intrinsic water-use efficiency of Norway spruce forests: insights from a multi-stable isotope analysis in tree rings of two Alpine chronosequences","volume":"31","author":"Giammarchi","year":"2017","journal-title":"Trees"},{"key":"B16","doi-asserted-by":"publisher","first-page":"2535","DOI":"10.1111\/nph.v229.5","article-title":"Whole-tree mesophyll conductance reconciles isotopic and gas-exchange estimates of water-use efficiency","volume":"229","author":"Gimeno","year":"2021","journal-title":"New Phytol."},{"key":"B17","doi-asserted-by":"publisher","first-page":"4923","DOI":"10.1111\/gcb.v28.16","article-title":"Overestimated gains in water-use efficiency by global forests","volume":"28","author":"Gong","year":"2022","journal-title":"Global Change Biol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"13","DOI":"10.1007\/s11676-023-01668-5","article-title":"Rising utilization of stable isotopes in tree rings for climate change and forest ecology","volume":"35","author":"Huang","year":"2024","journal-title":"J. Forestry Res."},{"key":"B19","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1111\/j.1469-8137.2007.01967.x","article-title":"The likely impact of elevated [CO2], nitrogen deposition, increased temperature and management on carbon sequestration in temperate and boreal forest ecosystems: a literature review","volume":"173","author":"Hyv\u00f6nen","year":"2007","journal-title":"New Phytol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1981","DOI":"10.1073\/pnas.1018906108","article-title":"Cellulose \u03b418O is an index of leaf-to-air vapor pressure difference (VPD) in tropical plants","volume":"108","author":"Kahmen","year":"2011","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B21","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1111\/nph.2018.217.issue-1","article-title":"The effect of 18O-labelled water vapour on the oxygen isotope ratio of water and assimilates in plants at high humidity","volume":"217","author":"Lehmann","year":"2018","journal-title":"New Phytol."},{"key":"B22","doi-asserted-by":"publisher","first-page":"803","DOI":"10.1111\/nph.18431","article-title":"Do changes in tree-ring \u03b418O indicate changes in stomatal conductance","volume":"236","author":"Lin","year":"2022","journal-title":"New Phytol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"1326","DOI":"10.1111\/nph.v229.3","article-title":"Accounting for mesophyll conductance substantially improves 13C-based estimates of intrinsic water-use efficiency","volume":"229","author":"Ma","year":"2021","journal-title":"New Phytol."},{"key":"B24","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2014286118","article-title":"Global tree intrinsic water use efficiency is enhanced by increased atmospheric CO2 and modulated by climate and plant functional types","volume":"118","author":"Mathias","year":"2021","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B25","doi-asserted-by":"publisher","first-page":"771","DOI":"10.1016\/j.quascirev.2003.06.017","article-title":"Stable isotopes in tree rings","volume":"23","author":"McCarroll","year":"2004","journal-title":"Quaternary Sci. Rev."},{"key":"B26","doi-asserted-by":"publisher","first-page":"1049","DOI":"10.1111\/j.1365-2486.2010.02222.x","article-title":"Long-term increases in intrinsic water-use efficiency do not lead to increased stem growth in a tropical monsoon forest in western Thailand","volume":"17","author":"Nock","year":"2011","journal-title":"Global Change Biol."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1778","DOI":"10.1111\/gcb.14910","article-title":"Long-term physiological and growth responses of Himalayan fir to environmental change are mediated by mean climate","volume":"26","author":"Panthi","year":"2020","journal-title":"Global Change Biol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"597","DOI":"10.1111\/j.1466-8238.2010.00608.x","article-title":"Increased water-use efficiency during the 20th century did not translate into enhanced tree growth","volume":"20","author":"Pe\u00f1uelas","year":"2011","journal-title":"Global Ecol. Biogeogr."},{"key":"B29","doi-asserted-by":"publisher","first-page":"904","DOI":"10.1093\/treephys\/tpaa043","article-title":"Disentangling the effects of atmospheric CO2 and climate on intrinsic water-use efficiency in South Asian tropical moist forest trees","volume":"40","author":"Rahman","year":"2020","journal-title":"Tree Physiol."},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1029\/2005JG000033","article-title":"Carbon and oxygen isotope ratios of tree ring cellulose along a precipitation transect in Oregon, United States","volume":"110","author":"Roden","year":"2005","journal-title":"J. Geophysical Res.: Biogeosci."},{"key":"B31","doi-asserted-by":"crossref","first-page":"3700","DOI":"10.1111\/gcb.12717","article-title":"Spatial variability and temporal trends in water-use efficiency of European forests","volume":"20","author":"Saurer","year":"2014","journal-title":"Global Change Biology"},{"key":"B32","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1007\/s004420000466","article-title":"Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity: a conceptual model","volume":"125","author":"Scheidegger","year":"2000","journal-title":"Oecologia"},{"key":"B33","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.dendro.2017.05.002","article-title":"A guideline for sample preparation in modern tree-ring stable isotope research","volume":"44","author":"Schollaen","year":"2017","journal-title":"Dendrochronologia"},{"key":"B34","doi-asserted-by":"publisher","first-page":"2606","DOI":"10.1111\/pce.14630","article-title":"Updating the dual C and O isotope-Gas-exchange model: A concept to understand plant responses to the environment and its implications for tree rings","volume":"46","author":"Siegwolf","year":"2023","journal-title":"Plant Cell Environ."},{"key":"B35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.jfe.2008.03.001","article-title":"Valuing environmental goods and services derived from the forests","volume":"15","author":"Stenger","year":"2009","journal-title":"J. For. Economics"},{"key":"B36","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1038\/ngeo2313","article-title":"No growth stimulation of tropical trees by 150 years of CO2 fertilization but water-use efficiency increased","volume":"8","author":"Van Der Sleen","year":"2015","journal-title":"Nat. Geosci."},{"key":"B37","doi-asserted-by":"publisher","first-page":"2413","DOI":"10.1111\/nph.v229.5","article-title":"Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO2","volume":"229","author":"Walker","year":"2021","journal-title":"New Phytol."},{"key":"B38","doi-asserted-by":"publisher","first-page":"730","DOI":"10.1029\/2018EA000529","article-title":"CO2 fertilization confounds tree-ring records of regional hydroclimate at northeastern Qinghai-Tibetan Plateau","volume":"6","author":"Wang","year":"2019","journal-title":"Earth Space Sci."},{"key":"B39","doi-asserted-by":"publisher","first-page":"803","DOI":"10.1016\/j.quascirev.2003.06.011","article-title":"Northern European trees show a progressively diminishing response to increasing atmospheric carbon dioxide concentrations","volume":"23","author":"Waterhouse","year":"2004","journal-title":"Quaternary Sci. Rev."},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2016.00799","article-title":"Stable water use efficiency under climate change of three sympatric conifer species at the alpine treeline","volume":"7","author":"Wieser","year":"2016","journal-title":"Front. Plant Sci."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2024.1471415\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,10]],"date-time":"2025-01-10T06:12:13Z","timestamp":1736489533000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2024.1471415\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,1,10]]},"references-count":40,"alternative-id":["10.3389\/fpls.2024.1471415"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2024.1471415","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,10]]},"article-number":"1471415"}}