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Title: Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest

Abstract

Satellite and tower-based metrics of forest-scale photosynthesis generally increase with dry season progression across central Amazônia, but the underlying mechanisms lack consensus. We conducted demographic surveys of leaf age composition, and measured age-dependence of leaf physiology in broadleaf canopy trees of abundant species at a central eastern Amazon site. Using a novel leaf-to-branch scaling approach, we used this data to independently test the much-debated hypothesis—arising from satellite and tower-based observations—that leaf phenology could explain the forest-scale pattern of dry season photosynthesis. Stomatal conductance and biochemical parameters of photosynthesis were higher for recently mature leaves than for old leaves. Most branches had multiple leaf age categories simultaneously present, and the number of recently mature leaves increased as the dry season progressed because old leaves were exchanged for new leaves. These findings provide the first direct field evidence that branch-scale photosynthetic capacity increases during the dry season, with a magnitude consistent with increases in ecosystem-scale photosynthetic capacity derived from flux towers. In conclusion, interaction between leaf age-dependent physiology and shifting leaf age-demographic composition are sufficient to explain the dry season photosynthetic capacity pattern at this site, and should be considered in vegetation models of tropical evergreen forests.

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [6];  [7]; ORCiD logo [8];  [9];  [10];  [11];  [12];  [13];  [14];  [9];  [15];  [3]
  1. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Brown Univ., Providence, RI (United States). Inst. at Brown for Environment and Society
  2. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Brookhaven National Lab. (BNL), Upton, NY (United States). Environmental and Climate Sciences Dept.
  3. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
  4. Univ. of Sao Paulo (Brazil). Center for Nuclear Energy in Agriculture (CENA)
  5. Univ. of California, Irvine, CA (United States). Ecology and Evolutionary Biology and Center for Environmental Biology
  6. Federal Univ. of Western Para, Santarem (Brazil). Inst. for Biodiversity and Forest (UFOPA)
  7. Univ. of Michigan, Ann Arbor, MI (United States). Dept. of Civil and Environmental Engineering
  8. Univ. of Campinas (UNICAMP), Sao Paulo (Brazil). Dept. of Plant Biology
  9. National Inst. of Amazonian Research (INPA), Manaus (Brazil). Tropical Forest Sciences
  10. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology; Michigan State Univ., East Lansing, MI (United States). Dept. of Forestry
  11. Brazilian Agricultural Research Corp. (EMBRAPA), Herbarium of Embrapa Amazônia Oriental (IAN), Santarem (Brazil)
  12. Univ. of Technology, Sydney (Australia). Plant Functional Biology and Climate Change Cluster
  13. Federal Univ. of Western Para, Santarem (Brazil). Inst. for Biodiversity and Forest (UFOPA). Atmospheric Sciences Dept. and Inst. of Engineering and Geosciences
  14. Michigan State Univ., East Lansing, MI (United States). Dept. of Forestry
  15. Federal Univ. of Western Para, Santarem (Brazil). Inst. for Biodiversity and Forest (UFOPA). Society, Nature and Development Dept.
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Science Foundation (NSF); Univ. of Arizona, Tucson, AZ (United States); Brazilian Agricultural Research Corp. (EMBRAPA); Large Scale Biosphere-Atmosphere Program in the Amazon (LBA); Herbarium of Embrapa Amazônia Oriental (IAN)
OSTI Identifier:
1424982
Alternate Identifier(s):
OSTI ID: 1423698
Report Number(s):
BNL-203201-2018-JAAM
Journal ID: ISSN 0028-646X
Grant/Contract Number:  
SC0012704; OISE-0730305; SC0008383
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 218; Journal Issue: 1; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES

Citation Formats

Albert, Loren P., Wu, Jin, Prohaska, Neill, de Camargo, Plinio Barbosa, Huxman, Travis E., Tribuzy, Edgard S., Ivanov, Valeriy Y., Oliveira, Rafael S., Garcia, Sabrina, Smith, Marielle N., Oliveira Junior, Raimundo Cosme, Restrepo-Coupe, Natalia, da Silva, Rodrigo, Stark, Scott C., Martins, Giordane A., Penha, Deliane V., and Saleska, Scott R. Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest. United States: N. p., 2018. Web. doi:10.1111/nph.15056.
Albert, Loren P., Wu, Jin, Prohaska, Neill, de Camargo, Plinio Barbosa, Huxman, Travis E., Tribuzy, Edgard S., Ivanov, Valeriy Y., Oliveira, Rafael S., Garcia, Sabrina, Smith, Marielle N., Oliveira Junior, Raimundo Cosme, Restrepo-Coupe, Natalia, da Silva, Rodrigo, Stark, Scott C., Martins, Giordane A., Penha, Deliane V., & Saleska, Scott R. Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest. United States. doi:10.1111/nph.15056.
Albert, Loren P., Wu, Jin, Prohaska, Neill, de Camargo, Plinio Barbosa, Huxman, Travis E., Tribuzy, Edgard S., Ivanov, Valeriy Y., Oliveira, Rafael S., Garcia, Sabrina, Smith, Marielle N., Oliveira Junior, Raimundo Cosme, Restrepo-Coupe, Natalia, da Silva, Rodrigo, Stark, Scott C., Martins, Giordane A., Penha, Deliane V., and Saleska, Scott R. Sun . "Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest". United States. doi:10.1111/nph.15056. https://www.osti.gov/servlets/purl/1424982.
@article{osti_1424982,
title = {Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest},
author = {Albert, Loren P. and Wu, Jin and Prohaska, Neill and de Camargo, Plinio Barbosa and Huxman, Travis E. and Tribuzy, Edgard S. and Ivanov, Valeriy Y. and Oliveira, Rafael S. and Garcia, Sabrina and Smith, Marielle N. and Oliveira Junior, Raimundo Cosme and Restrepo-Coupe, Natalia and da Silva, Rodrigo and Stark, Scott C. and Martins, Giordane A. and Penha, Deliane V. and Saleska, Scott R.},
abstractNote = {Satellite and tower-based metrics of forest-scale photosynthesis generally increase with dry season progression across central Amazônia, but the underlying mechanisms lack consensus. We conducted demographic surveys of leaf age composition, and measured age-dependence of leaf physiology in broadleaf canopy trees of abundant species at a central eastern Amazon site. Using a novel leaf-to-branch scaling approach, we used this data to independently test the much-debated hypothesis—arising from satellite and tower-based observations—that leaf phenology could explain the forest-scale pattern of dry season photosynthesis. Stomatal conductance and biochemical parameters of photosynthesis were higher for recently mature leaves than for old leaves. Most branches had multiple leaf age categories simultaneously present, and the number of recently mature leaves increased as the dry season progressed because old leaves were exchanged for new leaves. These findings provide the first direct field evidence that branch-scale photosynthetic capacity increases during the dry season, with a magnitude consistent with increases in ecosystem-scale photosynthetic capacity derived from flux towers. In conclusion, interaction between leaf age-dependent physiology and shifting leaf age-demographic composition are sufficient to explain the dry season photosynthetic capacity pattern at this site, and should be considered in vegetation models of tropical evergreen forests.},
doi = {10.1111/nph.15056},
journal = {New Phytologist},
issn = {0028-646X},
number = 1,
volume = 218,
place = {United States},
year = {2018},
month = {3}
}

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Cited by: 6 works
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    Works referencing / citing this record:

    Precipitation regionalization of the Brazilian Amazon: Precipitation regionalization of the Brazilian Amazon
    journal, September 2014

    • Santos, Eliane Barbosa; Lucio, Paulo Sérgio; Silva, Cláudio Moisés Santos e.
    • Atmospheric Science Letters, Vol. 16, Issue 3
    • DOI: 10.1002/asl2.535

    Regulation and activation of phytoene synthase, a key enzyme in carotenoid biosynthesis, during photomorphogenesis
    journal, November 2000


    Forest structure and carbon dynamics in Amazonian tropical rain forests
    journal, June 2004


    Increasing day-length induces spring flushing of tropical dry forest trees in the absence of rain
    journal, July 2002


    Spectral changes with leaf aging in Amazon caatinga
    journal, January 1998


    Climate change, phenology, and phenological control of vegetation feedbacks to the climate system
    journal, February 2013


    What drives the seasonality of photosynthesis across the Amazon basin? A cross-site analysis of eddy flux tower measurements from the Brasil flux network
    journal, December 2013


    Modeling the interannual variability and trends in gross and net primary productivity of tropical forests from 1982 to 1999
    journal, October 2005


    Leaf flush drives dry season green-up of the Central Amazon
    journal, September 2016


    Herbivory as a selective agent on the timing of leaf production in a tropical understory community
    journal, December 1988


    Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model
    journal, November 2000

    • Cox, Peter M.; Betts, Richard A.; Jones, Chris D.
    • Nature, Vol. 408, Issue 6809
    • DOI: 10.1038/35041539

    Interannual extremes in the rate of rise of atmospheric carbon dioxide since 1980
    journal, June 1995

    • Keeling, C. D.; Whorf, T. P.; Wahlen, M.
    • Nature, Vol. 375, Issue 6533
    • DOI: 10.1038/375666a0

    The worldwide leaf economics spectrum
    journal, April 2004

    • Wright, Ian J.; Reich, Peter B.; Westoby, Mark
    • Nature, Vol. 428, Issue 6985
    • DOI: 10.1038/nature02403

    Amazon forests maintain consistent canopy structure and greenness during the dry season
    journal, February 2014

    • Morton, Douglas C.; Nagol, Jyoteshwar; Carabajal, Claudia C.
    • Nature, Vol. 506, Issue 7487
    • DOI: 10.1038/nature13006

    Dry-season greening of Amazon forests
    journal, March 2016

    • Saleska, Scott R.; Wu, Jin; Guan, Kaiyu
    • Nature, Vol. 531, Issue 7594
    • DOI: 10.1038/nature16457

    Seasonality of temperate forest photosynthesis and daytime respiration
    journal, June 2016

    • Wehr, R.; Munger, J. W.; McManus, J. B.
    • Nature, Vol. 534, Issue 7609
    • DOI: 10.1038/nature17966

    Simulated resilience of tropical rainforests to CO2-induced climate change
    journal, March 2013

    • Huntingford, Chris; Zelazowski, Przemyslaw; Galbraith, David
    • Nature Geoscience, Vol. 6, Issue 4
    • DOI: 10.1038/ngeo1741

    Photosynthetic seasonality of global tropical forests constrained by hydroclimate
    journal, March 2015

    • Guan, Kaiyu; Pan, Ming; Li, Haibin
    • Nature Geoscience, Vol. 8, Issue 4
    • DOI: 10.1038/ngeo2382

    Leaf age affects the seasonal pattern of photosynthetic capacityand net ecosystem exchange of carbon in a deciduous forest
    journal, June 2001


    Shade acclimation of rainforest leaves to colonization by lichens
    journal, December 2002


    Climatic and biotic controls on annual carbon storage in Amazonian ecosystems
    journal, July 2000


    Development of Leaf Photosynthetic Parameters in Betula pendula Roth Leaves: Correlations with Photosystem I Density
    journal, May 2004


    Cloud cover limits net CO2 uptake and growth of a rainforest tree during tropical rainy seasons
    journal, January 2003

    • Graham, E. A.; Mulkey, S. S.; Kitajima, K.
    • Proceedings of the National Academy of Sciences, Vol. 100, Issue 2
    • DOI: 10.1073/pnas.0133045100

    Large seasonal swings in leaf area of Amazon rainforests
    journal, March 2007

    • Myneni, R. B.; Yang, W.; Nemani, R. R.
    • Proceedings of the National Academy of Sciences, Vol. 104, Issue 12
    • DOI: 10.1073/pnas.0611338104

    Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest
    journal, February 2009

    • Malhi, Y.; Aragao, L. E. O. C.; Galbraith, D.
    • Proceedings of the National Academy of Sciences, Vol. 106, Issue 49
    • DOI: 10.1073/pnas.0804619106

    Seasonal and interannual variability of climate and vegetation indices across the Amazon
    journal, August 2010

    • Brando, P. M.; Goetz, S. J.; Baccini, A.
    • Proceedings of the National Academy of Sciences, Vol. 107, Issue 33
    • DOI: 10.1073/pnas.0908741107

    Rainforest-initiated wet season onset over the southern Amazon
    journal, July 2017

    • Wright, Jonathon S.; Fu, Rong; Worden, John R.
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 32
    • DOI: 10.1073/pnas.1621516114

    Cloud cover in Landsat observations of the Brazilian Amazon
    journal, January 2001


    Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest
    journal, February 2013

    • Domingues, Tomas F.; Martinelli, Luiz A.; Ehleringer, James R.
    • Plant Ecology & Diversity, Vol. 7, Issue 1-2
    • DOI: 10.1080/17550874.2012.748849

    Sunlight mediated seasonality in canopy structure and photosynthetic activity of Amazonian rainforests
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