Plant Structure-Function Relationships and Woody Tissue Respiration: Upscaling to Forests from Laser-Derived Measurements

Land surface processes dominate the observed global signal of large inter-annual variability in the global carbon cycle , and this signal is itself dominated by responses of tropical forests to climatic variation and extremes. However, our understanding of the functioning of these forests is poorly constrained, not least in terms of the size and climate-sensitivity of gross ecosystem respiratory CO2 emission. Woody tissue CO2 effluxes contribute substantially to gross ecosystem CO2 emissions, thereby influencing the net ecosystem exchange of carbon. Our ability to estimate this component of the forest respiration budget has been limited by our technical capacity to measure vegetation size and structure in sufficient detail and at sufficient scale. The outcome has been to leave large uncertainties in land-surface model performance and prediction. A key challenge in estimating woody tissue CO2 efflux for the ecosystem has been the scaling of measurements made with chambers from the level of an organ to the stand. Appropriate scalars such as woody tissue mass, surface area and volume all require accurate structural information on both size and pattern. For individual trees, pattern is dominated by branching structure and this fundamentally determines how trees partition resources to address the trade-offs inherent in the simultaneous maintenance of structural integrity and metabolism. The detailed structural information needed to address this challenge has until recently been extremely scarce because of the difficulty of acquiring it, even for a single large tree. Recent developments in terrestrial light detection and ranging (LiDAR) technology have made possible a step change in our ability to quantify and describe tree form for continuous forest, for example describing hundreds of adjacent trees at the hectare scale. Connecting this new capability with tree physiology and fundamental theories of plant structure and metabolism offers to change the way we understand plant functional biology and its variation with environment, biogeography and phylogeny.

[1]  O. Atkin F1000Prime Recommendation of [Mori S et al , 2010 .

[2]  Mark G. Tjoelker,et al.  Universal scaling of respiratory metabolism, size and nitrogen in plants , 2006, Nature.

[3]  Philip Lewis,et al.  Fast Automatic Precision Tree Models from Terrestrial Laser Scanner Data , 2013, Remote. Sens..

[4]  D'arcy W. Thompson On Growth and Form , 1945 .

[5]  D. Pury,et al.  Simple scaling of photosynthesis from leaves to canopies without the errors of big‐leaf models , 1997 .

[6]  D. Sprugel Components of woody-tissue respiration in young Abies amabilis (Dougl.) Forbes trees , 1990, Trees.

[7]  K. Anderson‐Teixeira,et al.  Carbon dynamics of mature and regrowth tropical forests derived from a pantropical database (TropForC‐db) , 2016, Global change biology.

[8]  L. Aragão,et al.  Shifts in plant respiration and carbon use efficiency at a large-scale drought experiment in the eastern Amazon. , 2010, The New phytologist.

[9]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[10]  Roberta E. Martin,et al.  Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. , 2015, The New phytologist.

[11]  O. Phillips,et al.  Drought impact on forest carbon dynamics and fluxes in Amazonia , 2015, Nature.

[12]  D. A. King,et al.  Height-diameter allometry of tropical forest trees , 2010 .

[13]  Contributions of carbon cycle uncertainty to future climate projection spread , 2009 .

[14]  P. Levy,et al.  Stem CO2 fluxes in two Sahelian shrub species (Guiera senegalensis and Combretum micranthum) , 1998 .

[15]  T. Kumagai,et al.  Vertical variations in wood CO2 efflux for live emergent trees in a Bornean tropical rainforest. , 2014, Tree physiology.

[16]  Van M. Savage,et al.  A general model for metabolic scaling in self-similar asymmetric networks , 2017, PLoS Comput. Biol..

[17]  T. Feldpausch,et al.  Co-limitation of photosynthetic capacity by nitrogen and phosphorus in West Africa woodlands. , 2010, Plant, cell & environment.

[18]  Patrick Meir,et al.  Light distribution and foliage structure in an oak canopy , 1999, Trees.

[19]  O. Phillips,et al.  Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents , 2016, The New phytologist.

[20]  R. Teskey,et al.  Measurement of stem respiration of sycamore (Platanus occidentalis L.) trees involves internal and external fluxes of CO2 and possible transport of CO2 from roots. , 2007, Plant, cell & environment.

[21]  P. Meir,et al.  The effect of aqueous transport of CO(2) in xylem sap on gas exchange in woody plants. , 1999, Tree physiology.

[22]  Knowlton C. Foote,et al.  The Contribution of Aspen Bark Photosynthesis to the Energy Balance of the Stem , 1978 .

[23]  Lisa Patrick Bentley,et al.  A species‐level model for metabolic scaling of trees II. Testing in a ring‐ and diffuse‐porous species , 2012 .

[24]  M. Herold,et al.  Estimation of above‐ground biomass of large tropical trees with terrestrial LiDAR , 2017 .

[25]  Ian J. Wright,et al.  Fibre wall and lumen fractions drive wood density variation across 24 Australian angiosperms , 2013, AoB Plants.

[26]  Yadvinder Malhi,et al.  The linkages between photosynthesis, productivity, growth and biomass in lowland Amazonian forests , 2015, Global change biology.

[27]  Osvaldo M. R. Cabral,et al.  Leaf area index and above-ground biomass of terra firme rain forest and adjacent clearings in Amazonia , 1993 .

[28]  T. Yoneda Surface area of woody organs of an evergreen broadleaf forest tree in Japan and Southeast Asia , 1993, Journal of Plant Research.

[29]  M. Herold,et al.  Nondestructive estimates of above‐ground biomass using terrestrial laser scanning , 2015 .

[30]  K. Niklas Size‐dependent variations in plant growth rates and the “¾‐power rule” , 1994 .

[31]  M. Pavelka,et al.  Environmental factors influencing the relationship between stem CO2 efflux and sap flow , 2014, Trees.

[32]  Antonio Donato Nobre,et al.  Acclimation of photosynthetic capacity to irradiance in tree canopies in relation to leaf nitrogen concentration and leaf mass per unit area , 2002 .

[33]  J. Peñuelas,et al.  Evaluating the convergence between eddy-covariance and biometric methods for assessing carbon budgets of forests , 2016, Nature Communications.

[34]  Susan E. Trumbore,et al.  Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency , 2004 .

[35]  M. G. Ryan,et al.  Wood CO2 efflux in a primary tropical rain forest , 2006 .

[36]  N. Kunert,et al.  Xylem Sap Flux Affects Conventional Stem CO2 Efflux Measurements in Tropical Trees , 2015 .

[37]  Patrick Meir,et al.  Leaf respiration in two tropical rainforests: constraints on physiology by phosphorus, nitrogen and temperature , 2001 .

[38]  W. Brand,et al.  Optimisation of photosynthetic carbon gain and within-canopy gradients of associated foliar traits for Amazon forest trees , 2010 .

[39]  J. Chambers,et al.  Internal respiration of Amazon tree stems greatly exceeds external CO 2 efflux , 2012 .

[40]  Lisa Patrick Bentley,et al.  An empirical assessment of tree branching networks and implications for plant allometric scaling models. , 2013, Ecology letters.

[41]  R. Betts,et al.  El Nino and a record CO2 rise , 2016 .

[42]  Atul K. Jain,et al.  Using ecosystem experiments to improve vegetation models , 2015 .

[43]  A. P. Abaimov,et al.  Mixed-power scaling of whole-plant respiration from seedlings to giant trees , 2010, Proceedings of the National Academy of Sciences.

[44]  Jean Pierre Henry Balbaud Ometto,et al.  Amazon forest biomass density maps: tackling the uncertainty in carbon emission estimates , 2014, Climatic Change.

[45]  Paul J. Kramer,et al.  Physiology of Woody Plants , 1983 .

[46]  M. G. Ryan,et al.  Woody-tissue respiration for Simarouba amara and Minquartia guianensis, two tropical wet forest trees with different growth habits , 1994, Oecologia.

[47]  J. Amthor Respiration and crop productivity , 2004, Plant Growth Regulation.

[48]  James H. Brown,et al.  A General Model for the Origin of Allometric Scaling Laws in Biology , 1997, Science.

[49]  K. Yoda COMMUNITY RESPIRATION IN A LOWLAND RAIN FOREST IN PASOH, PENINSULAR MALAYSIA , 1983 .

[50]  Prof. Dr. Sherwin Carlquist,et al.  Comparative Wood Anatomy , 2001, Springer Series in Wood Science.

[51]  R. G. Stanley,et al.  Assimilation and release of internal carbon dioxide by woody plant shoots , 1970 .

[52]  B. Nelson,et al.  Improved allometric models to estimate the aboveground biomass of tropical trees , 2014, Global change biology.

[53]  M. G. Ryan,et al.  Annual carbon cost of autotrophic respiration in boreal forest ecosystems in relation to species and climate , 1997 .

[54]  O. Phillips,et al.  The importance of crown dimensions to improve tropical tree biomass estimates. , 2014, Ecological applications : a publication of the Ecological Society of America.

[55]  P. Tomlinson,et al.  Tropical Trees and Forests: An Architectural Analysis , 1978 .

[56]  Prof. Dr. Francis Hallé,et al.  Tropical Trees and Forests , 1978, Springer Berlin Heidelberg.

[57]  O. Phillips,et al.  Branch xylem density variations across the Amazon Basin , 2009 .

[58]  C. Field,et al.  A reanalysis using improved leaf models and a new canopy integration scheme , 1992 .

[59]  S. Pacala,et al.  Tropical nighttime warming as a dominant driver of variability in the terrestrial carbon sink , 2015, Proceedings of the National Academy of Sciences.

[60]  J. Canadell,et al.  Variations in atmospheric CO2 growth rates coupled with tropical temperature , 2013, Proceedings of the National Academy of Sciences.

[61]  O. Phillips,et al.  Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. , 2010, The New phytologist.

[62]  Yadvinder Malhi,et al.  A comparison of plot‐based satellite and Earth system model estimates of tropical forest net primary production , 2015 .

[63]  Nathan G. Swenson,et al.  A general integrative model for scaling plant growth, carbon flux, and functional trait spectra , 2007, Nature.

[64]  M. R. Evans,et al.  Modelling ecological systems in a changing world , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[65]  Yi Lin,et al.  Tree species classification based on explicit tree structure feature parameters derived from static terrestrial laser scanning data , 2016 .

[66]  Tim G Benton,et al.  Predictive ecology: systems approaches , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[67]  K. Niklas,et al.  Theories of optimization, form and function in branching architecture in plants , 1995 .

[68]  D. Hollinger Optimality and nitrogen allocation in a tree canopy. , 1996, Tree physiology.

[69]  F. Woodward,et al.  Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate , 2010, Science.

[70]  Atul K. Jain,et al.  Compensatory water effects link yearly global land CO2 sink changes to temperature , 2017, Nature.

[71]  S. Carlquist Comparative Wood Anatomy: Systematic, Ecological, and Evolutionary Aspects of Dicotyledon Wood , 1990 .

[72]  P. Meir,et al.  Scaling relationships for woody tissue respiration in two tropical rain forests , 2002 .

[73]  E. J. H. Corner,et al.  The Life of Plants , 1981 .