Abstract
Key message
Trees display contrasting specialized annual shoots during their life-span and along with ontogeny-driven modifications in their branching pattern, they can fulfill different combinations of light exploitation and space exploration functions
Abstract
Tree ontogeny is related to major changes in tree structure and function at different scales, from individual organs to the whole tree. Yet, little is known about the direct effects of tree ontogeny on shoot specialization and branching patterns. Such specific architectural changes occurring with tree growth and aging are of critical importance for understanding the response of trees to their environment. The uppermost branching system of 0.1- to 23-m-tall sugar maple trees was sampled at the end of the growing season. Measurements were made at both the branching system (n = 40) and annual shoot scales (n = 803). An algorithm for automated shoot typology was developed to characterize branching pattern variations. Sugar maple shoots were divided into four types with contrasting sizes and levels of foliage (i.e., relative biomass allocation into leaves, LMF). These morphological differences were interpreted as functional specializations for light exploitation (high LMF) or space exploration and support (low LMF). Only annual trunk shoots exhibited trait value changes during ontogeny such as a minimum allocation to foliage in the current-year shoots for the 5-m-tall trees, which is related to lower light interception capabilities but higher space exploration abilities. However, this relative loss of light interception function is compensated by ontogenetic changes at the branching system scale, which are associated with higher rates of ramification to produce lateral shoots. This study reveals how branching system and annual shoot traits change simultaneously during tree ontogeny to fulfill different functions, particularly light exploitation and space exploration.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baret S, Nicolini E, Le Bourgeois T, Strasberg D (2003) Developmental patterns of the invasive bramble (Rubus alceifolius Poiret, Rosaceae) in Réunion island: an architectural and morphometric analysis. Ann Bot 91:39–48. https://doi.org/10.1093/aob/mcg006
Barthélémy D, Caraglio Y (2007) Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Ann Bot 99:375–407
Barthélémy D, Caraglio Y, Costes E (1997) Architecture, gradients morphogénétiques et âge physiologique chez les végétaux. In: Bouchon J, de Reffye P, Barthélémy D (eds) Modélisation et simulation de l’architecture des végétaux. Science u. INRA, CIRAD-GERDAT-AMAP, Paris, pp 89–136
Bishop DA, Beier CM, Pederson N et al (2015) Regional growth decline of sugar maple (Acer saccharum) and its potential causes. Ecosphere 6:art179. https://doi.org/10.1890/es15-00260.1
Borianne P, Brunel G (2012) Automated valuation of leaves area for large-scale analysis needing data coupling or petioles deletion. In: Proceedings—2012 IEEE 4th international symposium on plant growth modeling, simulation, visualization and applications, PMA 2012. IEEE, pp 50–57
Buissart F, Vennetier M, Delagrange S et al (2018) The relative weight of ontogeny, topology and climate in the architectural development of three North American conifers. AoB Plants. https://doi.org/10.1093/aobpla/ply045
Coble AP, Cavaleri MA, Niinemets Ü (2014) Light drives vertical gradients of leaf morphology in a sugar maple (Acer saccharum) forest. Tree Physiol 34:146–158. https://doi.org/10.1093/treephys/tpt126
Cochard H, Coste S, Chanson B et al (2005) Hydraulic architecture correlates with bud organogenesis and primary shoot growth in beech (Fagus sylvatica). Tree Physiol 25:1545–1552. https://doi.org/10.1093/treephys/25.12.1545
Delagrange S, Messier C, Lechowicz MJ, Dizengremel P (2004) Physiological, morphological and allocational plasticity in understory deciduous trees: importance of plant size and light availability. Tree Physiol 24:775–784. https://doi.org/10.1093/treephys/24.7.775
Delagrange S, Montpied P, Dreyer E et al (2006) Does shade improve light interception efficiency? A comparison among seedlings from shade-tolerant and -intolerant temperate deciduous tree species. New Phytol 172:293–304. https://doi.org/10.1111/j.1469-8137.2006.01814.x
Farnsworth KD, Niklas KJ (1995) Theories of optimization, form and function in branching architecture in plants. Funct Ecol 9:355–363. https://doi.org/10.2307/2389997
Freschet GT, Swart EM, Cornelissen JHC (2015) Integrated plant phenotypic responses to contrasting above- and below-ground resources: key roles of specific leaf area and root mass fraction. New Phytol 206:1247–1260. https://doi.org/10.1111/nph.13352
Godman R, Yawney H, Tubbs C (1990) Sugar maple (Acer saccharum Marsh.). In: Silvics of North America, vol 2. Hardwoods, United States Department of Agriculture (USDA), Forest Service, Agriculture Handbook 654. https://www.fs.usda.gov/treesearch/pubs/1548
Griffon S, de Coligny F (2014) AMAPstudio: an editing and simulation software suite for plants architecture modelling. Ecol Modell 290:3–10. https://doi.org/10.1016/j.ecolmodel.2013.10.037
Henry HAL, Aarssen LW (2001) Inter- and intraspecific relationships between shade tolerance and shade avoidance in temperate trees. Oikos 93:477–487. https://doi.org/10.1034/j.1600-0706.2001.930313.x
Heuret P, Meredieu C, Coudurier T et al (2006) Ontogenetic trends in the morphological features of main stem annual shoots of Pinus pinaster (Pinaceae). Am J Bot 93:1577–1587. https://doi.org/10.3732/ajb.93.11.1577
Horsley SB, Long RP, Bailey SW et al (2002) Health of eastern North American sugar maple forests and factors affecting decline. North J Appl For 19:34–44
Ishii H (2011) How do changes in leaf/shoot morphology and crown architecture affect growth and physiological function of tall trees? In: Meinzer F, Lachenbruch B, Dawson T (eds) Size- and age-related changes in tree structure and function SE—tree physiology, vol 4. Springer, Dordrecht, pp 215–232
Ishii H, Ford ED (2001) The role of epicormic shoot production in maintaining foliage in old Pseudotsuga menziesii (Douglas-fir) trees. Can J Bot 79:251–264. https://doi.org/10.1139/cjb-79-3-251
Koch GW, Stillet SC, Jennings GM, Davis SD (2004) The limits to tree height. Nature 428:851–854. https://doi.org/10.1038/nature02417
Kunstler G, Falster D, Coomes DA et al (2016) Plant functional traits have globally consistent effects on competition. Nature 529:204–207. https://doi.org/10.1038/nature16476
Lauri PE, Normand F (2017) Are leaves only involved in flowering? Bridging the gap between structural botany and functional morphology. Tree Physiol 37:1137–1139. https://doi.org/10.1093/treephys/tpx068
Letort V, Cournède PH, Mathieu A et al (2008) Parametric identification of a functional–structural tree growth model and application to beech trees (Fagus sylvatica). Funct Plant Biol 35:951–963. https://doi.org/10.1071/fp08065
Martre P, Dambreville A (2018) A model of leaf coordination to scale-up leaf expansion from the organ to the canopy. Plant Physiol 176:704–716. https://doi.org/10.1104/pp.17.00986
Massonnet C, Regnard JL, Lauri PÉ et al (2008) Contributions of foliage distribution and leaf functions to light interception, transpiration and photosynthetic capacities in two apple cultivars at branch and tree scales. Tree Physiol 28:665–678. https://doi.org/10.1093/treephys/28.5.665
Mathieu A, Cournede PH, Letort V et al (2009) A dynamic model of plant growth with interactions between development and functional mechanisms to study plant structural plasticity related to trophic competition. Ann Bot 103:1173–1186. https://doi.org/10.1093/aob/mcp054
Matthews SN, Iverson LR (2017) Managing for delicious ecosystem service under climate change: can United States sugar maple (Acer saccharum) syrup production be maintained in a warming climate? Int J Biodivers Sci Ecosyst Serv Manag 13:40–52. https://doi.org/10.1080/21513732.2017.1285815
MFFP (2008) Norme de stratification écoforestière. Quatrième inventaire écoforestier du Québec méridional. Ministère des Forêts, de la Faune et des Parcs du Québec. Direction des inventaires forestiers. Québec
Millet J (2012) L’architecture des arbres des régions tempérées: son histoire, ses concepts, ses usages. Editions MultiMondes, Montreal
Nicolini E, Chanson B (1999) La pousse courte, un indicateur du degré de maturation chez le hêtre (Fagus sylvatica L.). Can J Bot 77:1539–1550. https://doi.org/10.1139/cjb-77-11-1539
Niklas KJ, Cobb ED (2010) Ontogenetic changes in the numbers of short- vs. long-shoots account for decreasing specific leaf area in Acer rubrum (Aceraceae) as trees increase in size. Am J Bot 97:27–37. https://doi.org/10.3732/ajb.0900249
Nock CA, Caspersen JP, Thomas SC (2008) Large ontogenetic declines in intra-crown leaf area index in two temperate deciduous tree species. Ecology 89:744–753. https://doi.org/10.1890/07-0531.1
Onoda Y, Saluñga JB, Akutsu K et al (2014) Trade-off between light interception efficiency and light use efficiency: implications for species coexistence in one-sided light competition. J Ecol 102:167–175. https://doi.org/10.1111/1365-2745.12184
Osada N, Okabe Y, Hayashi D et al (2014) Differences between height- and light-dependent changes in shoot traits in five deciduous tree species. Oecologia 174:1–12. https://doi.org/10.1007/s00442-013-2744-2
Poorter H, Niinemets Ü, Poorter L et al (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588
Poorter H, Niklas KJ, Reich PB et al (2012) Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytol 193:30–50. https://doi.org/10.1111/j.1469-8137.2011.03952.x
Posada JM, Sievänen R, Messier C et al (2012) Contributions of leaf photosynthetic capacity, leaf angle and self-shading to the maximization of net photosynthesis in Acer saccharum: a modelling assessment. Ann Bot 110:731–741. https://doi.org/10.1093/aob/mcs106
Puntieri J, Torres C, Magnin A et al (2018) Structural differentiation among annual shoots as related to growth dynamics in Luma apiculata trees (Myrtaceae). Flora Morphol Distrib Funct Ecol Plants 249:86–96. https://doi.org/10.1016/j.flora.2018.10.005
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Robitaille A (1988) Cartographie des districts écologiques: norme et techniques. Gouvernement du Québec, Bibliothèque et archives nationales du Québec 2013. http://www.mrn.gouv.qc.ca/forets/inventaire/inventaire-systeme.jsp
Rueffler C, Hermisson J, Wagner GP (2012) Evolution of functional specialization and division of labor. Proc Natl Acad Sci 109:E326–E335. https://doi.org/10.1073/pnas.1110521109
Sabatier S, Barthélémy D (2001) Bud structure in relation to shoot morphology and position on the vegetative annual shoots of Juglans regia L. (Juglandaceae). Ann Bot 87:117–123. https://doi.org/10.1006/anbo.2000.1312
Suzuki AA, Suzuki M (2009) Why do lower order branches show greater shoot growth than higher order branches? Considering space availability as a factor affecting shoot growth. Trees Struct Funct 23:69–77. https://doi.org/10.1007/s00468-008-0255-2
Taugourdeau O, Barczi J, Caraglio Y (2012a) Simulation of morphogenetical gradients using a minimal functional–structural plant model (FSPM). In: 2012 IEEE 4th international symposium on plant growth modeling, simulation, visualization and applications. IEEE, pp 379–387
Taugourdeau O, Dauzat J, Griffon S et al (2012b) Retrospective analysis of tree architecture in silver fir (Abies alba Mill.): ontogenetic trends and responses to environmental variability. Ann For Sci 69:713–721. https://doi.org/10.1007/s13595-012-0188-1
Taugourdeau O, Delagrange S, de Reffye P, Messier C (2013) Modelling sugar maple development along its whole ontogeny: modelling hypotheses and calibration methodology. In: Sievänen R, Nikinmaa E, Godin C et al. (eds) Proceedings of the 7th international conference on functional–structural plant models (FSPM2013). Finnish Society of Forest Science, Saariselkä, Finland, 9–14 June 2013, pp 234–236
Thomas SC (2010) Photosynthetic capacity peaks at intermediate size in temperate deciduous trees. Tree Physiol 30:555–573. https://doi.org/10.1093/treephys/tpq005
Tondjo K, Brancheriau L, Sabatier S et al (2018) Stochastic modelling of tree architecture and biomass allocation: application to teak (Tectona grandis L. f.), a tree species with polycyclic growth and leaf neoformation. Ann Bot 121:1397–1410. https://doi.org/10.1093/aob/mcy040
Van de Peer T, Verheyen K, Kint V et al (2017) Plasticity of tree architecture through interspecific and intraspecific competition in a young experimental plantation. For Ecol Manage 385:1–9. https://doi.org/10.1016/j.foreco.2016.11.015
Venables WN, Ripley BD (2002) Modern applied statistics with S. Fourth, Springer
Vennetier M, Girard F, Taugourdeau O et al (2013) Climate change impact on tree architectural development and leaf area. In: Climate change—realities, impacts over ice cap, sea level and risks. InTech
Vincent G, Harja D (2008) Exploring ecological significance of tree crown plasticity through three-dimensional modelling. Ann Bot 101:1221–1231. https://doi.org/10.1093/aob/mcm189
Weraduwage SM, Chen J, Anozie FC et al (2015) The relationship between leaf area growth and biomass accumulation in Arabidopsis thaliana. Front Plant Sci 6:167. https://doi.org/10.3389/fpls.2015.00167
Xiang S, Liu Y, Fang F et al (2009) Stem architectural effect on leaf size, leaf number, and leaf mass fraction in plant twigs of woody species. Int J Plant Sci 170:999–1008. https://doi.org/10.1086/605114
Yagi T (2000) Morphology and biomass allocation of current-year shoots of ten tall tree species in cool temperate Japan. J Plant Res 113:171–183. https://doi.org/10.1007/pl00013928
Yagi T (2004) Within-tree variations in shoot differentiation patterns of ten tall tree species in a Japanese cool-temperate forest. Botany 82:228–243. https://doi.org/10.1177/0890334414548459
Yoshimura K (2011) Hydraulic function contributes to the variation in shoot morphology within the crown in Quercuscrispula. Tree Physiol 31:774–781. https://doi.org/10.1093/treephys/tpr060
Acknowledgements
The authors gratefully thank R. Pouliot for site selection, M. Follett for (climbing the trees for) data collection in mature trees, J. Poirier for scanning leaf samples, S. Martinez Ruiz for biomass measurements, W.F.J. Parsons for manuscript revision, and C. Nock and P. de Reffye for providing valuable advice throughout the project. A postdoctoral fellowship to OT was funded by the Chaire de recherche CNRSG/Hydro-Quebec.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by S. Vospernik.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Taugourdeau, O., Delagrange, S., Lecigne, B. et al. Sugar maple (Acer saccharum Marsh.) shoot architecture reveals coordinated ontogenetic changes between shoot specialization and branching pattern. Trees 33, 1615–1625 (2019). https://doi.org/10.1007/s00468-019-01884-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-019-01884-9