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Title: Experimental warming across a tropical forest canopy height gradient reveals minimal photosynthetic and respiratory acclimation

Abstract

Abstract Tropical forest canopies cycle vast amounts of carbon, yet we still have a limited understanding of how these critical ecosystems will respond to climate warming. We implemented in situ leaf‐level + 3°C experimental warming from the understory to the upper canopy of two Puerto Rican tropical tree species, Guarea guidonia and Ocotea sintenisii . After approximately 1 month of continuous warming, we assessed adjustments in photosynthesis, chlorophyll fluorescence, stomatal conductance, leaf traits and foliar respiration. Warming did not alter net photosynthetic temperature response for either species; however, the optimum temperature of Ocotea understory leaf photosynthetic electron transport shifted upward. There was no Ocotea respiratory treatment effect, while Guarea respiratory temperature sensitivity ( Q 10 ) was down‐regulated in heated leaves. The optimum temperatures for photosynthesis ( T opt ) decreased 3–5°C from understory to the highest canopy position, perhaps due to upper canopy stomatal conductance limitations. Guarea upper canopy T opt was similar to the mean daytime temperatures, while Ocotea canopy leaves often operated above T opt . With minimal acclimation to warmer temperatures in the upper canopy, further warming could put these forests at risk of reduced CO 2 uptake, which could weaken the overall carbon sink strength of thismore » tropical forest.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [4]
  1. College of Forest Resources and Environmental Science Michigan Technological University Houghton Michigan USA, Earth and Environmental Science Division Los Alamos National Laboratory Los Alamos New Mexico USA
  2. United States Department of Agriculture, Forest Service International Institute of Tropical Forestry, Jardin Botánico Sur Río Piedras Puerto Rico USA
  3. U.S. Geological Survey, Southwest Biological Science Center Moab Utah USA
  4. College of Forest Resources and Environmental Science Michigan Technological University Houghton Michigan USA
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1805298
Grant/Contract Number:  
89243018S‐SC‐000014; DE‐SC‐0008168; DE‐SC‐0011806; DE‐SC‐0012000; DE‐SC‐0018942
Resource Type:
Publisher's Accepted Manuscript
Journal Name:
Plant, Cell and Environment
Additional Journal Information:
Journal Name: Plant, Cell and Environment Journal Volume: 44 Journal Issue: 9; Journal ID: ISSN 0140-7791
Publisher:
Wiley-Blackwell
Country of Publication:
United Kingdom
Language:
English

Citation Formats

Carter, Kelsey R., Wood, Tana E., Reed, Sasha C., Butts, Kaylie M., and Cavaleri, Molly A. Experimental warming across a tropical forest canopy height gradient reveals minimal photosynthetic and respiratory acclimation. United Kingdom: N. p., 2021. Web. doi:10.1111/pce.14134.
Carter, Kelsey R., Wood, Tana E., Reed, Sasha C., Butts, Kaylie M., & Cavaleri, Molly A. Experimental warming across a tropical forest canopy height gradient reveals minimal photosynthetic and respiratory acclimation. United Kingdom. https://doi.org/10.1111/pce.14134
Carter, Kelsey R., Wood, Tana E., Reed, Sasha C., Butts, Kaylie M., and Cavaleri, Molly A. Tue . "Experimental warming across a tropical forest canopy height gradient reveals minimal photosynthetic and respiratory acclimation". United Kingdom. https://doi.org/10.1111/pce.14134.
@article{osti_1805298,
title = {Experimental warming across a tropical forest canopy height gradient reveals minimal photosynthetic and respiratory acclimation},
author = {Carter, Kelsey R. and Wood, Tana E. and Reed, Sasha C. and Butts, Kaylie M. and Cavaleri, Molly A.},
abstractNote = {Abstract Tropical forest canopies cycle vast amounts of carbon, yet we still have a limited understanding of how these critical ecosystems will respond to climate warming. We implemented in situ leaf‐level + 3°C experimental warming from the understory to the upper canopy of two Puerto Rican tropical tree species, Guarea guidonia and Ocotea sintenisii . After approximately 1 month of continuous warming, we assessed adjustments in photosynthesis, chlorophyll fluorescence, stomatal conductance, leaf traits and foliar respiration. Warming did not alter net photosynthetic temperature response for either species; however, the optimum temperature of Ocotea understory leaf photosynthetic electron transport shifted upward. There was no Ocotea respiratory treatment effect, while Guarea respiratory temperature sensitivity ( Q 10 ) was down‐regulated in heated leaves. The optimum temperatures for photosynthesis ( T opt ) decreased 3–5°C from understory to the highest canopy position, perhaps due to upper canopy stomatal conductance limitations. Guarea upper canopy T opt was similar to the mean daytime temperatures, while Ocotea canopy leaves often operated above T opt . With minimal acclimation to warmer temperatures in the upper canopy, further warming could put these forests at risk of reduced CO 2 uptake, which could weaken the overall carbon sink strength of this tropical forest.},
doi = {10.1111/pce.14134},
journal = {Plant, Cell and Environment},
number = 9,
volume = 44,
place = {United Kingdom},
year = {Tue Jul 06 00:00:00 EDT 2021},
month = {Tue Jul 06 00:00:00 EDT 2021}
}

Works referenced in this record:

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

The hot and the cold: unravelling the variable response of plant respiration to temperature
journal, January 2005

  • Atkin, Owen K.; Bruhn, Dan; Hurry, Vaughan M.
  • Functional Plant Biology, Vol. 32, Issue 2
  • DOI: 10.1071/FP03176

Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries: A letter
journal, June 2011


Attaining whole-ecosystem warming using air and deep-soil heating methods with an elevated CO 2 atmosphere
journal, January 2017

  • Hanson, Paul J.; Riggs, Jeffery S.; Nettles, W. Robert
  • Biogeosciences, Vol. 14, Issue 4
  • DOI: 10.5194/bg-14-861-2017

Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis
journal, February 2004


Effects of elevated [CO2] on photosynthesis in European forest species: a meta-analysis of model parameters: Photosynthetic acclimation to elevated CO2
journal, December 1999


The Structure, Distribution, and Biomass of the World's Forests
journal, November 2013


Acclimation and adaptation components of the temperature dependence of plant photosynthesis at the global scale
journal, February 2019

  • Kumarathunge, Dushan P.; Medlyn, Belinda E.; Drake, John E.
  • New Phytologist, Vol. 222, Issue 2
  • DOI: 10.1111/nph.15668

Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature
journal, June 2001


Tropical forest temperature thresholds for gross primary productivity
journal, July 2018

  • Pau, Stephanie; Detto, Matteo; Kim, Youngil
  • Ecosphere, Vol. 9, Issue 7
  • DOI: 10.1002/ecs2.2311

Leaf absorptance of photosynthetically active radiation in relation to chlorophyll meter estimates among woody plant species
journal, May 2004


Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO 2 and climate warming
journal, October 2013

  • Crous, Kristine Y.; Quentin, Audrey G.; Lin, Yan-Shih
  • Global Change Biology, Vol. 19, Issue 12
  • DOI: 10.1111/gcb.12314

Thermal acclimation and the dynamic response of plant respiration to temperature
journal, July 2003


Photosynthetic Response and Adaptation to Temperature in Higher Plants
journal, June 1980


Thylakoid membrane responses to moderately high leaf temperature in Pima cotton
journal, June 2004


Photosynthetic capacity and leaf nitrogen decline along a controlled climate gradient in provenances of two widely distributed Eucalyptus species
journal, June 2018

  • Crous, Kristine Y.; Drake, John E.; Aspinwall, Michael J.
  • Global Change Biology, Vol. 24, Issue 10
  • DOI: 10.1111/gcb.14330

Vertical and seasonal variations in temperature responses of leaf respiration in a Chamaecyparis obtusa canopy
journal, February 2017

  • Araki, Masatake G.; Gyokusen, Koichiro; Kajimoto, Takuya
  • Tree Physiology, Vol. 37, Issue 10
  • DOI: 10.1093/treephys/tpx012

Terrestrial Carbon–Cycle Feedback to Climate Warming
journal, December 2007


Complete or overcompensatory thermal acclimation of leaf dark respiration in African tropical trees
journal, December 2020

  • Mujawamariya, Myriam; Wittemann, Maria; Manishimwe, Aloysie
  • New Phytologist, Vol. 229, Issue 5
  • DOI: 10.1111/nph.17038

Annual wood production in a tropical rain forest in NE Costa Rica linked to climatic variation but not to increasing CO 2
journal, February 2010


High-temperature tolerance of a tropical tree, Ficus insipida: methodological reassessment and climate change considerations
journal, January 2010

  • Krause, G. Heinrich; Winter, Klaus; Krause, Barbara
  • Functional Plant Biology, Vol. 37, Issue 9
  • DOI: 10.1071/FP10034

Changes in the Shadow: The Shifting Role of Shaded Leaves in Global Carbon and Water Cycles Under Climate Change
journal, May 2018

  • He, Liming; Chen, Jing M.; Gonsamo, Alemu
  • Geophysical Research Letters, Vol. 45, Issue 10
  • DOI: 10.1029/2018GL077560

Reconciling the optimal and empirical approaches to modelling stomatal conductance: RECONCILING OPTIMAL AND EMPIRICAL STOMATAL MODELS
journal, January 2011


Scaling foliar respiration in two contrasting forest canopies
journal, February 2003


The control of stomata by water balance: Tansley review
journal, August 2005


An Introduction to Environmental Biophysics
book, January 1998


Diameter growth performance of tree functional groups in Puerto Rican secondary tropical forests
journal, March 2014


Convergence in the temperature response of leaf respiration across biomes and plant functional types
journal, March 2016

  • Heskel, Mary A.; O’Sullivan, Odhran S.; Reich, Peter B.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 14
  • DOI: 10.1073/pnas.1520282113

Differences in leaf thermoregulation and water use strategies between three co-occurring Atlantic forest tree species: Leaf energy balance of Atlantic forest trees
journal, May 2018

  • Fauset, Sophie; Freitas, Helber C.; Galbraith, David R.
  • Plant, Cell & Environment, Vol. 41, Issue 7
  • DOI: 10.1111/pce.13208

Height is more important than light in determining leaf morphology in a tropical forest
journal, June 2010

  • Cavaleri, Molly A.; Oberbauer, Steven F.; Clark, David B.
  • Ecology, Vol. 91, Issue 6
  • DOI: 10.1890/09-1326.1

High rates of photosynthesis in the tropical pioneer tree, Ficus insipida Willd.
journal, July 1995


Canopy gradients in leaf functional traits for species that differ in growth strategies and shade tolerance
journal, May 2017

  • Coble, Adam P.; Fogel, Marilyn L.; Parker, Geoffrey G.
  • Tree Physiology, Vol. 37, Issue 10
  • DOI: 10.1093/treephys/tpx048

Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis
journal, April 2009


Adaptation and acclimation both influence photosynthetic and respiratory temperature responses in Corymbia calophylla
journal, April 2017

  • Aspinwall, Michael J.; Vårhammar, Angelica; Blackman, Chris J.
  • Tree Physiology, Vol. 37, Issue 8
  • DOI: 10.1093/treephys/tpx047

Urgent need for warming experiments in tropical forests
journal, March 2015

  • Cavaleri, Molly A.; Reed, Sasha C.; Smith, W. Kolby
  • Global Change Biology, Vol. 21, Issue 6
  • DOI: 10.1111/gcb.12860

Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest
journal, February 2014


Light acclimation optimizes leaf functional traits despite height-related constraints in a canopy shading experiment
journal, January 2015


Empirical evidence for resilience of tropical forest photosynthesis in a warmer world
journal, October 2020


Convergent acclimation of leaf photosynthesis and respiration to prevailing ambient temperatures under current and warmer climates in Eucalyptus tereticornis
journal, June 2016

  • Aspinwall, Michael J.; Drake, John E.; Campany, Courtney
  • New Phytologist, Vol. 212, Issue 2
  • DOI: 10.1111/nph.14035

Foliage physiology and biochemistry in response to light gradients in conifers with varying shade tolerance
journal, August 1999

  • Bond, Barbara J.; Farnsworth, Blake T.; Coulombe, Robert A.
  • Oecologia, Vol. 120, Issue 2
  • DOI: 10.1007/s004420050847

Similar temperature dependence of photosynthetic parameters in sun and shade leaves of three tropical tree species
journal, February 2020


Experimental branch warming alters tall tree leaf phenology and acorn production
journal, July 2010


Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves
journal, November 2009


The energetic and carbon economic origins of leaf thermoregulation
journal, August 2016

  • Michaletz, Sean T.; Weiser, Michael D.; McDowell, Nate G.
  • Nature Plants, Vol. 2, Issue 9
  • DOI: 10.1038/nplants.2016.129

High tolerance of tropical sapling growth and gas exchange to moderate warming
journal, October 2017


The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species
journal, November 2014

  • Drake, John E.; Aspinwall, Michael J.; Pfautsch, Sebastian
  • Global Change Biology, Vol. 21, Issue 1
  • DOI: 10.1111/gcb.12729

Photosynthetic acclimation to warming in tropical forest tree seedlings
journal, April 2017

  • Slot, Martijn; Winter, Klaus
  • Journal of Experimental Botany, Vol. 68, Issue 9
  • DOI: 10.1093/jxb/erx071

Photosynthetic heat tolerance of shade and sun leaves of three tropical tree species
journal, July 2018

  • Slot, Martijn; Krause, G. Heinrich; Krause, Barbara
  • Photosynthesis Research, Vol. 141, Issue 1
  • DOI: 10.1007/s11120-018-0563-3

Warming puts the squeeze on photosynthesis – lessons from tropical trees
journal, April 2017

  • Dusenge, Mirindi Eric; Way, Danielle A.
  • Journal of Experimental Botany, Vol. 68, Issue 9
  • DOI: 10.1093/jxb/erx114

The dynamics of photosynthetic acclimation to changes in light quanlity and quality in three Australian rainforest tree species
journal, January 1993

  • Turnbull, Matthew H.; Doley, David; Yates, David J.
  • Oecologia, Vol. 94, Issue 2
  • DOI: 10.1007/BF00341320

General patterns of acclimation of leaf respiration to elevated temperatures across biomes and plant types
journal, December 2014


Photosynthetic temperature responses of tree species in Rwanda: evidence of pronounced negative effects of high temperature in montane rainforest climax species
journal, February 2015

  • Vårhammar, Angelica; Wallin, Göran; McLean, Christopher M.
  • New Phytologist, Vol. 206, Issue 3
  • DOI: 10.1111/nph.13291

High-resolution temperature responses of leaf respiration in snow gum ( Eucalyptus pauciflora ) reveal high-temperature limits to respiratory function : Temperature dependence of leaf respiration
journal, January 2013

  • O'Sullivan, Odhran S.; Weerasinghe, K. W. Lasantha K.; Evans, John R.
  • Plant, Cell & Environment, Vol. 36, Issue 7
  • DOI: 10.1111/pce.12057

A simple new equation for the reversible temperature dependence of photosynthetic electron transport: a study on soybean leaf
journal, January 2004

  • June, Tania; Evans, John R.; Farquhar, Graham D.
  • Functional Plant Biology, Vol. 31, Issue 3
  • DOI: 10.1071/FP03250

Temperate and Tropical Forest Canopies are Already Functioning beyond Their Thermal Thresholds for Photosynthesis
journal, January 2018

  • Mau, Alida; Reed, Sasha; Wood, Tana
  • Forests, Vol. 9, Issue 1
  • DOI: 10.3390/f9010047

Summary for Policymakers
book, March 2014


Height-related changes in leaf photosynthetic traits in diverse Bornean tropical rain forest trees
journal, November 2014


Effects of rising temperatures and [CO 2 ] on the physiology of tropical forest trees
journal, February 2008

  • Lloyd, Jon; Farquhar, Graham D.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1498
  • DOI: 10.1098/rstb.2007.0032

Photosynthetic and Respiratory Acclimation of Understory Shrubs in Response to in situ Experimental Warming of a Wet Tropical Forest
journal, September 2020

  • Carter, Kelsey R.; Wood, Tana E.; Reed, Sasha C.
  • Frontiers in Forests and Global Change, Vol. 3
  • DOI: 10.3389/ffgc.2020.576320

Predicting effects of climate change on productivity and persistence of forest trees
journal, May 2020

  • Kramer, Russell D.; Ishii, H. Roaki; Carter, Kelsey R.
  • Ecological Research, Vol. 35, Issue 4
  • DOI: 10.1111/1440-1703.12127

Canopy position affects photosynthesis and anatomy in mature Eucalyptus trees in elevated CO2
journal, September 2020


Exceptional Sensitivity of Rubisco Activase to Thermal Denaturation in Vitro and in Vivo
journal, November 2001

  • Salvucci, Michael E.; Osteryoung, Katherine W.; Crafts-Brandner, Steven J.
  • Plant Physiology, Vol. 127, Issue 3
  • DOI: 10.1104/pp.010357

Phloem Loading: How Leaves Gain Their Independence
journal, January 2006


Effects of seasonal change and experimental warming on the temperature dependence of photosynthesis in the canopy leaves of Quercus serrata
journal, April 2016

  • Yamaguchi, Daisuke P.; Nakaji, Tatsuro; Hiura, Tsutom
  • Tree Physiology, Vol. 36, Issue 10
  • DOI: 10.1093/treephys/tpw021

Effects of foliage clumping on the estimation of global terrestrial gross primary productivity: FOLIAGE CLUMPING EFFECT ON GLOBAL GPP
journal, March 2012

  • Chen, Jing M.; Mo, Gang; Pisek, Jan
  • Global Biogeochemical Cycles, Vol. 26, Issue 1
  • DOI: 10.1029/2010GB003996

Strong thermal acclimation of photosynthesis in tropical and temperate wet-forest tree species: the importance of altered Rubisco content
journal, January 2017

  • Scafaro, Andrew P.; Xiang, Shuang; Long, Benedict M.
  • Global Change Biology, Vol. 23, Issue 7
  • DOI: 10.1111/gcb.13566

Variation in foliar respiration and wood CO2 efflux rates among species and canopy layers in a wet tropical forest
journal, January 2015


Plant respiration and photosynthesis in global-scale models: incorporating acclimation to temperature and CO 2
journal, September 2012


Only sun-lit leaves of the uppermost canopy exceed both air temperature and photosynthetic thermal optima in a wet tropical forest
journal, May 2021


Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species
journal, June 2003


Temperature responses of leaf net photosynthesis: the role of component processes
journal, January 2012


Canopy position affects the relationships between leaf respiration and associated traits in a tropical rainforest in Far North Queensland
journal, April 2014


Plant carbon metabolism and climate change: elevated CO 2 and temperature impacts on photosynthesis, photorespiration and respiration
journal, July 2018

  • Dusenge, Mirindi Eric; Duarte, André Galvao; Way, Danielle A.
  • New Phytologist, Vol. 221, Issue 1
  • DOI: 10.1111/nph.15283

Growth response and acclimation of CO2 exchange characteristics to elevated temperatures in tropical tree seedlings
journal, July 2013

  • Cheesman, Alexander W.; Winter, Klaus
  • Journal of Experimental Botany, Vol. 64, Issue 12
  • DOI: 10.1093/jxb/ert211

Foliar and ecosystem respiration in an old-growth tropical rain forest
journal, April 2008


Stand microclimate and physiological activity of tree leaves in an oak-hornbeam forest: I. Stand microclimate
journal, December 1989

  • Eliáš, P.; Kratochvílová, Irena; Janouš, D.
  • Trees, Vol. 3, Issue 4
  • DOI: 10.1007/BF00225356

How do leaf and ecosystem measures of water-use efficiency compare?
journal, June 2017

  • Medlyn, Belinda E.; De Kauwe, Martin G.; Lin, Yan-Shih
  • New Phytologist, Vol. 216, Issue 3
  • DOI: 10.1111/nph.14626

Plasticity in leaf traits of 38 tropical tree species in response to light; relationships with light demand and adult stature
journal, April 2006


Long-term decline of the Amazon carbon sink
journal, March 2015

  • Brienen, R. J. W.; Phillips, O. L.; Feldpausch, T. R.
  • Nature, Vol. 519, Issue 7543
  • DOI: 10.1038/nature14283

Vertical variation in leaf gas exchange parameters for a Southeast Asian tropical rainforest in Peninsular Malaysia
journal, May 2012

  • Kosugi, Yoshiko; Takanashi, Satoru; Yokoyama, Naoto
  • Journal of Plant Research, Vol. 125, Issue 6
  • DOI: 10.1007/s10265-012-0495-5

Stomatal Conductance and Photosynthesis
journal, June 1982


Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data
journal, September 2002


Within-Canopy Experimental Leaf Warming Induces Photosynthetic Decline Instead of Acclimation in Two Northern Hardwood Species
journal, December 2018

  • Carter, Kelsey R.; Cavaleri, Molly A.
  • Frontiers in Forests and Global Change, Vol. 1
  • DOI: 10.3389/ffgc.2018.00011

Why Mountain Passes are Higher in the Tropics
journal, May 1967

  • Janzen, Daniel H.
  • The American Naturalist, Vol. 101, Issue 919
  • DOI: 10.1086/282487

In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species
journal, October 2017

  • Slot, Martijn; Winter, Klaus
  • Plant, Cell & Environment, Vol. 40, Issue 12
  • DOI: 10.1111/pce.13071

Temperature acclimation of photosynthesis: mechanisms involved in the changes in temperature dependence of photosynthetic rate
journal, December 2005

  • Hikosaka, Kouki; Ishikawa, Kazumasa; Borjigidai, Almaz
  • Journal of Experimental Botany, Vol. 57, Issue 2
  • DOI: 10.1093/jxb/erj049

The projected timing of climate departure from recent variability
journal, October 2013

  • Mora, Camilo; Frazier, Abby G.; Longman, Ryan J.
  • Nature, Vol. 502, Issue 7470
  • DOI: 10.1038/nature12540

Cold‐blooded forests in a warming world
journal, October 2020


Height-related growth declines in ponderosa pine are not due to carbon limitation
journal, January 2009


An In Situ Leaf and Branch Warming Experiment in the Amazon: Warming Experiment in the Amazon
journal, January 2011


A worldwide analysis of within-canopy variations in leaf structural, chemical and physiological traits across plant functional types
journal, October 2014

  • Niinemets, Ülo; Keenan, Trevor F.; Hallik, Lea
  • New Phytologist, Vol. 205, Issue 3
  • DOI: 10.1111/nph.13096

Short-term acclimation to warmer temperatures accelerates leaf carbon exchange processes across plant types
journal, May 2017

  • Smith, Nicholas G.; Dukes, Jeffrey S.
  • Global Change Biology, Vol. 23, Issue 11
  • DOI: 10.1111/gcb.13735

Canopy position affects the temperature response of leaf respiration in Populus deltoides
journal, June 2002