Wind loads and competition for light sculpt trees into self-similar structures

Trees are self-similar structures: their branch lengths and diameters vary allometrically within the tree architecture, with longer and thicker branches near the ground. These tree allometries are often attributed to optimisation of hydraulic sap transport and safety against elastic buckling. Here, we show that these allometries also emerge from a model that includes competition for light, wind biomechanics and no hydraulics. We have developed MECHATREE, a numerical model of trees growing and evolving on a virtual island. With this model, we identify the fittest growth strategy when trees compete for light and allocate their photosynthates to grow seeds, create new branches or reinforce existing ones in response to wind-induced loads. Strikingly, we find that selected trees species are self-similar and follow allometric scalings similar to those observed on dicots and conifers. This result suggests that resistance to wind and competition for light play an essential role in determining tree allometries.Tree branches follow allometric scalings between length, thickness and dry mass. Here, Eloy and colleagues develop a functional-structural model that shows how such allometries in tree architecture can emerge through evolution as a result of competition for light, wind biomechanics, and wind sensing.

[1]  R. Macarthur,et al.  AN EQUILIBRIUM THEORY OF INSULAR ZOOGEOGRAPHY , 1963 .

[2]  Radomír Mech,et al.  Self-organizing tree models for image synthesis , 2009, ACM Trans. Graph..

[3]  K. Niklas Reexamination of a canonical model for plant organ biomass partitioning. , 2003, American journal of botany.

[4]  S. Pacala,et al.  Forest models defined by field measurements : Estimation, error analysis and dynamics , 1996 .

[5]  D. Barthélémy,et al.  Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. , 2007, Annals of botany.

[6]  Gill Mould,et al.  Estimating return period wave heights and wind speeds using a seasonal point process model , 1997 .

[7]  Przemyslaw Prusinkiewicz,et al.  The Algorithmic Beauty of Plants , 1990, The Virtual Laboratory.

[8]  Robert Sedgewick,et al.  Implementing Quicksort programs , 1978, CACM.

[9]  Malcolm Hayward COMPETITION AND EVOLUTION , 1997 .

[10]  Stefan Bornhofen,et al.  Competition and evolution in virtual plant communities: a new modeling approach , 2009, Natural Computing.

[11]  Olivier Hamant,et al.  Widespread mechanosensing controls the structure behind the architecture in plants. , 2013, Current opinion in plant biology.

[12]  Karl J. Niklas,et al.  Mechanical and photosynthetic constraints on the evolution of plant shape , 1984, Paleobiology.

[13]  Drew W. Purves,et al.  Crown Plasticity and Competition for Canopy Space: A New Spatially Implicit Model Parameterized for 250 North American Tree Species , 2007, PloS one.

[14]  S. Ernest,et al.  Relationships between body size and abundance in ecology. , 2007, Trends in ecology & evolution.

[15]  Philippe de Reffye,et al.  A functional model of tree growth and tree architecture , 1997 .

[16]  H. Sinoquet,et al.  Characterization of the Light Environment in Canopies Using 3D Digitising and Image Processing , 1998 .

[17]  A. McDonald,et al.  Net assimilation rate and shoot area development in birch (Betula pendula Roth.) at different steady-state values of nutrition and photon flux density , 1992, Trees.

[18]  Karl J Niklas,et al.  Global Allocation Rules for Patterns of Biomass Partitioning in Seed Plants , 2002, Science.

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

[20]  T. Kira,et al.  A QUANTITATIVE ANALYSIS OF PLANT FORM-THE PIPE MODEL THEORY : I.BASIC ANALYSES , 1964 .

[21]  A. N. Strahler DYNAMIC BASIS OF GEOMORPHOLOGY , 1952 .

[22]  J. White,et al.  CORRELATED CHANGES IN PLANT SIZE AND NUMBER IN PLANT POPULATIONS , 1970 .

[23]  P. Klinkhamer Plant allometry: The scaling of form and process , 1995 .

[24]  Jari Perttunen,et al.  LIGNUM: a model combining the structure and the functioning of trees , 1998 .

[25]  K. Niklas,et al.  Comment on "Critical wind speed at which trees break". , 2016, Physical review. E.

[26]  J. Chave,et al.  Towards a Worldwide Wood Economics Spectrum 2 . L E a D I N G D I M E N S I O N S I N W O O D F U N C T I O N , 2022 .

[27]  J. M. Smith,et al.  Optimization Theory in Evolution , 1978 .

[28]  B. Moulia,et al.  Forest trees filter chronic wind-signals to acclimate to high winds. , 2016, The New phytologist.

[29]  K. Niklas,et al.  A comparison between the record height-to-stem diameter allometries of Pachycaulis and Leptocaulis species. , 2006, Annals of botany.

[30]  Karl J. Niklas,et al.  Invariant scaling relations across tree-dominated communities , 2001, Nature.

[31]  A STRUCTURALLY BASED ANALYTIC MODEL FOR ESTIMATION OF BIOMASS AND FUEL LOADS OF WOODLAND TREES , 2009 .

[32]  Z. Bažant,et al.  Fracture and Size Effect in Concrete and Other Quasibrittle Materials , 1997 .

[33]  D D Smith,et al.  Hydraulic trade-offs and space filling enable better predictions of vascular structure and function in plants , 2010, Proceedings of the National Academy of Sciences.

[34]  P. de Reffye,et al.  A dynamic, architectural plant model simulating resource-dependent growth. , 2004, Annals of botany.

[35]  Christophe Eloy,et al.  Leonardo's rule, self-similarity, and wind-induced stresses in trees. , 2011, Physical review letters.

[36]  George Cybenko,et al.  Approximation by superpositions of a sigmoidal function , 1989, Math. Control. Signals Syst..

[37]  Karl J Niklas,et al.  Emergent properties of plants competing in silico for space and light: Seeing the tree from the forest. , 2009, American journal of botany.

[38]  K. Niklas,et al.  Wind-induced stresses in cherry trees: evidence against the hypothesis of constant stress levels , 2000, Trees.

[39]  James H. Brown,et al.  A general model for the structure and allometry of plant vascular systems , 1999, Nature.

[40]  A. R. Ennos,et al.  Wind as an ecological factor. , 1997, Trends in ecology & evolution.

[41]  Raffaella Barone,et al.  General Model , 2005, Encyclopedia of Biometrics.

[42]  Hendrik Poorter,et al.  Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate , 1990, Oecologia.

[43]  Christophe Godin,et al.  Multiscale Framework for Modeling and Analyzing Light Interception by Trees , 2008, Multiscale Model. Simul..

[44]  K. Niklas Size-dependent Allometry of Tree Height, Diameter and Trunk-taper , 1995 .

[45]  Karl J. Niklas,et al.  The Scaling of Plant Height: A Comparison Among Major Plant Clades and Anatomical Grades , 1993 .

[46]  M. Cannell,et al.  Shape of tree stems-a re-examination of the uniform stress hypothesis. , 1994, Tree physiology.

[47]  C. Mattheck,et al.  Teacher tree: The evolution of notch shape optimization from complex to simple , 2006 .

[48]  H. Honda Description of the form of trees by the parameters of the tree-like body: effects of the branching angle and the branch length on the sample of the tree-like body. , 1971, Journal of theoretical biology.

[49]  G Cumming,et al.  Quantitative morphometry of the branching structure of trees. , 1973, Journal of theoretical biology.

[50]  Peter Pfeifer,et al.  A Method for Estimation of Fractal Dimension of Tree Crowns , 1991 .

[51]  André Lacointe,et al.  Carbon allocation among tree organs: A review of basic processes and representation in functional-structural tree models , 2000 .

[52]  P. Prusinkiewicz,et al.  Using L-systems for modeling source-sink interactions, architecture and physiology of growing trees: the L-PEACH model. , 2005, The New phytologist.

[53]  John E. A. Bertram,et al.  Size-dependent differential scaling in branches: the mechanical design of trees revisited , 1989, Trees.

[54]  L. B. Leopold,et al.  Trees and streams: the efficiency of branching patterns. , 1971, Journal of theoretical biology.

[55]  Yan Guo,et al.  Plant growth and architectural modelling and its applications , 2011 .

[56]  E. D. Langre Effects of Wind on Plants , 2008 .

[57]  Bruno Moulia,et al.  Posture control and skeletal mechanical acclimation in terrestrial plants: implications for mechanical modeling of plant architecture. , 2006, American-Eurasian journal of botany.

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

[59]  Hanns-Christof Spatz,et al.  Growth and hydraulic (not mechanical) constraints govern the scaling of tree height and mass. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[60]  F R Adler,et al.  A model of self-thinning through local competition. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Katherine A. McCulloh,et al.  Murray’s Law and the Vascular Architecture of Plants , 2006 .

[62]  C. Bawn Sizing it up , 1975, Nature.

[63]  Eric J. Deeds,et al.  Sizing Up Allometric Scaling Theory , 2008, PLoS Comput. Biol..

[64]  R. Walker β ℕ Revisited , 1974 .

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

[66]  T. McMahon,et al.  Tree structures: deducing the principle of mechanical design. , 1976, Journal of theoretical biology.

[67]  Hendrik Poorter,et al.  How does biomass distribution change with size and differ among species? An analysis for 1200 plant species from five continents , 2015, The New phytologist.

[68]  Andy Hector,et al.  Competition for Light Causes Plant Biodiversity Loss After Eutrophication , 2009, Science.

[69]  D L T,et al.  Networks with Side Branching in Biology , 1998 .