Damage to tropical forests caused by cyclones is driven by wind speed but mediated by topographical exposure and tree characteristics.

Each year, an average of 45 tropical cyclones affect coastal areas and potentially impact forests. The proportion of the most intense cyclones has increased over the past four decades and is predicted to continue to do so. Yet, it remains uncertain how topographical exposure and tree characteristics can mediate the damage caused by increasing wind speed. Here, we compiled empirical data on the damage caused by 11 cyclones occurring over the past 40 years, from 74 forest plots representing tropical regions worldwide, encompassing field data for 22,176 trees and 815 species. We reconstructed the wind structure of those tropical cyclones to estimate the maximum sustained wind speed (MSW) and wind direction at the studied plots. Then, we used a causal inference framework combined with Bayesian generalised linear mixed models to understand and quantify the causal effects of MSW, topographical exposure to wind (EXP), tree size (DBH) and species wood density (ρ) on the proportion of damaged trees at the community level, and on the probability of snapping or uprooting at the tree level. The probability of snapping or uprooting at the tree level and, hence, the proportion of damaged trees at the community level, increased with increasing MSW, and with increasing EXP accentuating the damaging effects of cyclones, in particular at higher wind speeds. Higher ρ decreased the probability of snapping and to a lesser extent of uprooting. Larger trees tended to have lower probabilities of snapping but increased probabilities of uprooting. Importantly, the effect of ρ decreasing the probabilities of snapping was more marked for smaller than larger trees and was further accentuated at higher MSW. Our work emphasises how local topography, tree size and species wood density together mediate cyclone damage to tropical forests, facilitating better predictions of the impacts of such disturbances in an increasingly windier world.

Stronger wind, smaller tree: Testing tree growth plasticity through a modeling approach.

Plants exhibit plasticity in response to various external conditions, characterized by changes in physiological and morphological features. Although being non-negligible, compared to the other environmental factors, the effect of wind on plant growth is less extensively studied, either experimentally or computationally. This study aims to propose a modeling approach that can simulate the impact of wind on plant growth, which brings a biomechanical feedback to growth and biomass distribution into a functional-structural plant model (FSPM). Tree reaction to the wind is simulated based on the hypothesis that plants tend to fit in the environment best. This is interpreted as an optimization problem of finding the best growth-regulation sink parameter giving the maximal plant fitness (usually seed weight, but expressed as plant biomass and size). To test this hypothesis in silico, a functional-structural plant model, which simulates both the primary and secondary growth of stems, is coupled with a biomechanical model which computes forces, moments of forces, and breakage location in stems caused by both wind and self-weight increment during plant growth. The Non-dominated Sorting Genetic Algorithm II (NSGA-II) is adopted to maximize the multi-objective function (stem biomass and tree height) by determining the key parameter value controlling the biomass allocation to the secondary growth. The digital trees show considerable phenotypic plasticity under different wind speeds, whose behavior, as an emergent property, is in accordance with experimental results from works of literature: the height and leaf area of individual trees decreased with wind speed, and the diameter at the breast height (DBH) increased at low-speed wind but declined at higher-speed wind. Stronger wind results in a smaller tree. Such response of trees to the wind is realistically simulated, giving a deeper understanding of tree behavior. The result shows that the challenging task of modeling plant plasticity may be solved by optimizing the plant fitness function. Adding a biomechanical model enriches FSPMs and opens a wider application of plant models.

Cross-validation of the high-capacity tensiometer and thermocouple psychrometer for continuous monitoring of xylem water potential in saplings.

The pressure chamber, the most popular method used to measure xylem water potential, is a discontinuous and destructive technique and is therefore not suitable for automated monitoring. Continuous non-destructive monitoring could until very recently be achieved only by use of the thermocouple psychrometer (TP). Here we present the high-capacity tensiometer (HCT) as an alternative method for continuous non-destructive monitoring. This provided us with a unique chance to cross-validate the two instruments by installing them simultaneously on the same sapling stem. The HCT and the TP showed excellent agreement for xylem water potential less than -0.5 MPa. Response to day/night cycles and watering was remarkably in phase, indicating excellent response time of both instruments despite substantially different working principles. For xylem water potential greater than -0.5 MPa, the discrepancies sometimes observed between the HCT and TP were mainly attributed to the kaolin paste used to establish contact between the xylem and the HCT, which becomes hydraulically poorly conductive in this range of water potential once dried beyond its air-entry value and subsequently re-wetted. Notwithstanding this limitation, which can be overcome by selecting a clay paste with higher air-entry value, the HCT has been shown to represent a valid alternative to the TP.

Root growth and force chains in a granular soil.

Roots provide basic functions to plants such as water and nutrient uptake and anchoring in soil. The growth and development of root systems contribute to colonizing the surrounding soil and optimizing the access to resources. It is generally known that the variability of plant root architecture results from the combination of genetic, physiological, and environmental factors, in particular soil mechanical resistance. However, this last factor has never been investigated at the soil grain scale for roots. In this paper, we are interested in the effect of the disordered texture of granular soils on the evolution of forces experienced by the root cap during its growth. We introduce a numerical model in which the root is modeled as a flexible self-elongating tube that probes a soil composed of solid particles. By means of extensive simulations, we show that the forces exerted on the root cap reflect interparticle force chains. Our simulations also show that the mean force declines exponentially with root flexibility, the highest force corresponding to the soil hardness. Furthermore, we find that this functional dependence is characterized by a single dimensionless parameter that combines granular structure and root bending stiffness. This finding will be useful to further address the biological issues of mechanosensing and thigmomorphogenesis in plant roots.

Stochastic modelling of tree architecture and biomass allocation: application to teak (Tectona grandis L. f.), a tree species with polycyclic growth and leaf neoformation.

Background and aims: For a given genotype, the observed variability of tree forms results from the stochasticity of meristem functioning and from changing and heterogeneous environmental factors affecting biomass formation and allocation. In response to climate change, trees adapt their architecture by adjusting growth processes such as pre- and neoformation, as well as polycyclic growth. This is the case for the teak tree. The aim of this work was to adapt the plant model, GreenLab, in order to take into consideration both these processes using existing data on this tree species. Methods: This work adopted GreenLab formalism based on source-sink relationships at organ level that drive biomass production and partitioning within the whole plant over time. The stochastic aspect of phytomer production can be modelled by a Bernoulli process. The teak model was designed, parameterized and analysed using the architectural data from 2- to 5-year-old teak trees in open field stands. Key results: Growth and development parameters were identified, fitting the observed compound organic series with the theoretical series, using generalized least squares methods. Phytomer distributions of growth units and branching pattern varied depending on their axis category, i.e. their physiological age. These emerging properties were in accordance with the observed growth patterns and biomass allocation dynamics during a growing season marked by a short dry season. Conclusions: Annual growth patterns observed on teak, including shoot pre- and neoformation and polycyclism, were reproduced by the new version of the GreenLab model. However, further updating is discussed in order to ensure better consideration of radial variation in basic specific gravity of wood. Such upgrading of the model will enable teak ideotypes to be defined for improving wood production in terms of both volume and quality.

Tree stability under wind: simulating uprooting with root breakage using a finite element method.

BACKGROUND AND AIMS: Windstorms are the major natural hazard affecting European forests, causing tree damage and timber losses. Modelling tree anchorage mechanisms has progressed with advances in plant architectural modelling, but it is still limited in terms of estimation of anchorage strength. This paper aims to provide a new model for root anchorage, including the successive breakage of roots during uprooting. METHODS: The model was based on the finite element method. The breakage of individual roots was taken into account using a failure law derived from previous work carried out on fibre metal laminates. Soil mechanical plasticity was considered using the Mohr-Coulomb failure criterion. The mechanical model for roots was implemented in the numerical code ABAQUS using beam elements embedded in a soil block meshed with 3-D solid elements. The model was tested by simulating tree-pulling experiments previously carried out on a tree of Pinus pinaster (maritime pine). Soil mechanical parameters were obtained from laboratory tests. Root system architecture was digitized and imported into ABAQUS while root material properties were estimated from the literature. KEY RESULTS: Numerical simulations of tree-pulling tests exhibited realistic successive root breakages during uprooting, which could be seen in the resulting response curves. Broken roots could be visually located within the root system at any stage of the simulations. The model allowed estimation of anchorage strength in terms of the critical turning moment and accumulated energy, which were in good agreement with in situ measurements. CONCLUSIONS: This study provides the first model of tree anchorage strength for P. pinaster derived from the mechanical strength of individual roots. The generic nature of the model permits its further application to other tree species and soil conditions.

Plant growth and architectural modelling and its applications. Preface.

Over the last decade, a growing number of scientists around the world have invested in research on plant growth and architectural modelling and applications (often abbreviated to plant modelling and applications, PMA). By combining physical and biological processes, spatially explicit models have shown their ability to help in understanding plant­environment interactions. This Special Issue on plant growth modelling presents new information within this topic, which are summarized in this preface. Research results for a variety of plant species growing in the field, in greenhouses and in natural environments are presented. Various models and simulation platforms are developed in this field of research, opening new features to a wider community of researchers and end users. New modelling technologies relating to the structure and function of plant shoots and root systems are explored from the cellular to the whole-plant and plant-community levels.

Linking carbon supply to root cell-wall chemistry and mechanics at high altitudes in Abies georgei.

BACKGROUND AND AIMS: The mobile carbon supply to different compartments of a tree is affected by climate, but its impact on cell-wall chemistry and mechanics remains unknown. To understand better the variability in root growth and biomechanics in mountain forests subjected to substrate mass movement, we investigated root chemical and mechanical properties of mature Abies georgei var. smithii (Smith fir) growing at different elevations on the Tibet-Qinghai Plateau. METHODS: Thin and fine roots (0·1-4·0 mm in diameter) were sampled at three different elevations (3480, 3900 and 4330 m, the last corresponding to the treeline). Tensile resistance of roots of different diameter classes was measured along with holocellulose and non-structural carbon (NSC) content. KEY RESULTS: The mean force necessary to break roots in tension decreased significantly with increasing altitude and was attributed to a decrease in holocellulose content. Holocellulose was significantly lower in roots at the treeline (29·5 ± 1·3 %) compared with those at 3480 m (39·1 ± 1·0 %). Roots also differed significantly in NSC, with 35·6 ± 4·1 mg g(-1) dry mass of mean total soluble sugars in roots at 3480 m and 18·8 ± 2·1 mg g(-1) dry mass in roots at the treeline. CONCLUSIONS: Root mechanical resistance, holocellulose and NSC content all decreased with increasing altitude. Holocellulose is made up principally of cellulose, the biosynthesis of which depends largely on NSC supply. Plants synthesize cellulose when conditions are optimal and NSC is not limiting. Thus, cellulose synthesis in the thin and fine roots measured in our study is probably not a priority in mature trees growing at very high altitudes, where climatic factors will be limiting for growth. Root NSC stocks at the treeline may be depleted through over-demand for carbon supply due to increased fine root production or winter root growth.

(Not) Keeping the stem straight: a proteomic analysis of maritime pine seedlings undergoing phototropism and gravitropism.

BACKGROUND: Plants are subjected to continuous stimuli from the environment and have evolved an ability to respond through various growth and development processes. Phototropism and gravitropism responses enable the plant to reorient with regard to light and gravity. RESULTS: We quantified the speed of maritime pine seedlings to reorient with regard to light and gravity over 22 days. Seedlings were inclined at 15, 30 and 45 degrees with vertical plants as controls. A lateral light source illuminated the plants and stem movement over time was recorded. Depending on the initial angle of stem lean, the apical response to the lateral light source differed. In control and 15° inclined plants, the apex turned directly towards the light source after only 2 h. In plants inclined at 30° and 45°, the apex first reoriented in the vertical plane after 2 h, then turned towards the light source after 24 h. Two-dimensional gel electrophoresis coupled with mass spectrometry was then used to describe the molecular response of stem bending involved in photo- and gravi-tropism after 22 hr and 8 days of treatment. A total of 486 spots were quantitatively analyzed using image analysis software. Significant changes were determined in the protein accumulation of 68 protein spots. Early response gravitropic associated proteins were identified, which are known to function in energy related and primary metabolism. A group of thirty eight proteins were found to be involved in primary metabolism and energy related metabolic pathways. Degradation of Rubisco was implicated in some protein shifts. CONCLUSIONS: Our study demonstrates a rapid gravitropic response in apices of maritime pine seedlings inclined >30°. Little or no response was observed at the stem bases of the same plants. The primary gravitropic response is concomitant with a modification of the proteome, consisting of an over accumulation of energy and metabolism associated proteins, which may allow the stem to reorient rapidly after bending.

Crown structure and wood properties: Influence on tree sway and response to high winds.

Wind can alter plant growth and cause extensive, irreversible damage in forested areas. To better understand how to mitigate the effects of wind action, we investigated the sensitivity of tree aerodynamic behavior to the material and geometrical factors characterizing the aerial system. The mechanical response of a 35-yr-old maritime pine (Pinus pinaster, Pinaceae) submitted to static and dynamic wind loads is simulated with a finite element model. The branching structure is represented in three dimensions. Factor effects are evaluated using a fractional experimental design. Results show that material properties play only a limited role in tree dynamics. In contrast, small morphological variations can produce extreme behaviors such as either very little or nearly critical dissipation of stem oscillations. Slender trees are shown to be relatively more vulnerable to stem breakage than uprooting. Dynamic loading leads to deflections and forces up to 20% higher near the base of the tree than those calculated for a static loading of similar magnitude. Effects of branch geometry on dynamic amplification are substantial yet not linear. The flexibility of the aerial system is found to be critical to reducing the resistance to the airflow and thus to minimizing the risk of failure.

Plant growth modelling and applications: the increasing importance of plant architecture in growth models.

BACKGROUND: Modelling plant growth allows us to test hypotheses and carry out virtual experiments concerning plant growth processes that could otherwise take years in field conditions. The visualization of growth simulations allows us to see directly and vividly the outcome of a given model and provides us with an instructive tool useful for agronomists and foresters, as well as for teaching. Functional-structural (FS) plant growth models are nowadays particularly important for integrating biological processes with environmental conditions in 3-D virtual plants, and provide the basis for more advanced research in plant sciences. SCOPE: In this viewpoint paper, we ask the following questions. Are we modelling the correct processes that drive plant growth, and is growth driven mostly by sink or source activity? In current models, is the importance of soil resources (nutrients, water, temperature and their interaction with meristematic activity) considered adequately? Do classic models account for architectural adjustment as well as integrating the fundamental principles of development? Whilst answering these questions with the available data in the literature, we put forward the opinion that plant architecture and sink activity must be pushed to the centre of plant growth models. In natural conditions, sinks will more often drive growth than source activity, because sink activity is often controlled by finite soil resources or developmental constraints. PMA06: This viewpoint paper also serves as an introduction to this Special Issue devoted to plant growth modelling, which includes new research covering areas stretching from cell growth to biomechanics. All papers were presented at the Second International Symposium on Plant Growth Modeling, Simulation, Visualization and Applications (PMA06), held in Beijing, China, from 13-17 November, 2006. Although a large number of papers are devoted to FS models of agricultural and forest crop species, physiological and genetic processes have recently been included and point the way to a new direction in plant modelling research.

Understanding the impact of root morphology on overturning mechanisms: a modelling approach.

BACKGROUND AND AIMS: The Finite Element Method (FEM) has been used in recent years to simulate overturning processes in trees. This study aimed at using FEM to determine the role of individual roots in tree anchorage with regard to different rooting patterns, and to estimate stress distribution in the soil and roots during overturning. METHODS: The FEM was used to carry out 2-D simulations of tree uprooting in saturated soft clay and loamy sand-like soil. The anchorage model consisted of a root system embedded in a soil block. Two root patterns were used and individual roots removed to determine their contribution to anchorage. KEY RESULTS: In clay-like soil the size of the root-soil plate formed during overturning was defined by the longest roots. Consequently, all other roots localized within this plate had no influence on anchorage strength. In sand-like soil, removing individual root elements altered anchorage resistance. This result was due to a modification of the shape and size of the root-soil plate, as well as the location of the rotation axis. The tap root and deeper roots had more influence on overturning resistance in sand-like soil compared with clay-like soil. Mechanical stresses were higher in the most superficial roots and also in leeward roots in sand-like soil. The relative difference in stresses between the upper and lower sides of lateral roots was sensitive to root insertion angle. Assuming that root eccentricity is a response to mechanical stresses, these results explain why eccentricity differs depending on root architecture. CONCLUSIONS: A simple 2-D Finite Element model was developed to better understand the mechanisms involved during tree overturning. It has been shown how root system morphology and soil mechanical properties can modify the shape of the root plate slip surface as well as the position of the rotation axis, which are major components of tree anchorage.

AmapSim: a structural whole-plant simulator based on botanical knowledge and designed to host external functional models.

BACKGROUND AND AIMS: AmapSim is a tool that implements a structural plant growth model based on a botanical theory and simulates plant morphogenesis to produce accurate, complex and detailed plant architectures. This software is the result of more than a decade of research and development devoted to plant architecture. New advances in the software development have yielded plug-in external functions that open up the simulator to functional processes. METHODS: The simulation of plant topology is based on the growth of a set of virtual buds whose activity is modelled using stochastic processes. The geometry of the resulting axes is modelled by simple descriptive functions. The potential growth of each bud is represented by means of a numerical value called physiological age, which controls the value for each parameter in the model. The set of possible values for physiological ages is called the reference axis. In order to mimic morphological and architectural metamorphosis, the value allocated for the physiological age of buds evolves along this reference axis according to an oriented finite state automaton whose occupation and transition law follows a semi-Markovian function. KEY RESULTS: Simulations were performed on tomato plants to demonstrate how the AmapSim simulator can interface external modules, e.g. a GREENLAB growth model and a radiosity model. CONCLUSIONS: The algorithmic ability provided by AmapSim, e.g. the reference axis, enables unified control to be exercised over plant development parameter values, depending on the biological process target: how to affect the local pertinent process, i.e. the pertinent parameter(s), while keeping the rest unchanged. This opening up to external functions also offers a broadened field of applications and thus allows feedback between plant growth and the physical environment.

A generic 3D finite element model of tree anchorage integrating soil mechanics and real root system architecture.

Understanding the mechanism of tree anchorage in a forest is a priority because of the increase in wind storms in recent years and their projected recurrence as a consequence of global warming. To characterize anchorage mechanisms during tree uprooting, we developed a generic finite element model where real three-dimensional (3D) root system architectures were represented in a 3D soil. The model was used to simulate tree overturning during wind loading, and results compared with real data from two poplar species (Populus trichocarpa and P. deltoides). These trees were winched sideways until failure, and uprooting force and root architecture measured. The uprooting force was higher for P. deltoides than P. trichocarpa, probably due to its higher root volume and thicker lateral roots. Results from the model showed that soil type influences failure modes. In frictional soils, e.g., sandy soils, plastic failure of the soil occurred mainly on the windward side of the tree. In cohesive soils, e.g., clay soils, a more symmetrical slip surface was formed. Root systems were more resistant to uprooting in cohesive soil than in frictional soil. Applications of this generic model include virtual uprooting experiments, where each component of anchorage can be tested individually.

A finite element model for investigating effects of aerial architecture on tree oscillations.

A finite element model was developed to study the influence of aerial architecture on the structural dynamics of trees. The model combines a complete description of the axes of the aerial architecture of the plant with numerical techniques suitable for dynamic nonlinear analyses. Trees were modeled on the basis of morphological measurements that were previously made on three 4-year-old Pinus pinaster Ait. saplings originating from even-aged stands. Calculated and measured oscillations were compared to evaluate model behavior. The computations allowed the characteristics of the fundamental mode of vibration to be estimated with satisfactory accuracy. Inclusion of a topological description of the aerial system in a mechanical model provided insight into the effect of tree architecture on tree dynamic behavior. Simplifications of the branching pattern in the model led to overestimations of the natural swaying frequency of saplings by 10 to 20%. Inadequate values of stem and root anchorage stiffness resulted in errors of 10 to 20%. Modeling results indicated that aerodynamic drag of needles is responsible for 80% of the damping in the studied trees. Additionally, damping of stem movement is reduced by one half when branch oscillations are not considered. It appears that the efficiency of the dissipative mechanisms depends directly on crown topology.

Root architecture and wind-firmness of mature Pinus pinaster.

This study aims to link three-dimensional coarse root architecture to tree stability in mature timber trees with an average of 1-m rooting depth. Undamaged and uprooted trees were sampled in a stand damaged by a storm. Root architecture was measured by three-dimensional (3-D) digitizing. The distribution of root volume by root type and in wind-oriented sectors was analysed. Mature Pinus pinaster root systems were organized in a rigid 'cage' composed of a taproot, the zone of rapid taper of horizontal surface roots and numerous sinkers and deep roots, imprisoning a large mass of soil and guyed by long horizontal surface roots. Key compartments for stability exhibited strong selective leeward or windward reinforcement. Uprooted trees showed a lower cage volume, a larger proportion of oblique and intermediate depth horizontal roots and less wind-oriented root reinforcement. Pinus pinaster stability on moderately deep soils is optimized through a typical rooting pattern and a considerable structural adaptation to the prevailing wind and soil profile.

A mechanical analysis of the relationship between free oscillations of Pinus pinaster Ait. saplings and their aerial architecture.

The aim of this study was to investigate the influence of aerial architecture on the dynamic characteristics of young maritime pines (Pinus pinaster Ait.) using a mechanistic approach. For this purpose, three 4-year-old saplings with prominent differences in their branching patterns were submitted to free oscillation tests. The tests were carried out with different methods and directions of mechanical loading in order to initiate the movement of each sapling. The oscillations of the different architectural elements, i.e. stem and branches of different topological order, were measured with inclinometers and strain gauges fixed to saplings. Successive pruning of the architectural elements was carried out to evaluate their relative influence on the dynamic characteristics of the trees. The aerial systems were digitized before the mechanical tests in order to use 3D visualization techniques and to make architectural analyses of the crown structure. Two distinct modes of deformation were detected during free oscillations. The natural swaying frequency ranged from 0.6-0.8 Hz for the saplings tested at the same period of the year. The frequency variations were partly explained by the morphological differences of the experimental subjects. The motions of the axes were found to depend on their topology, i.e. the movement of the axes of a given branching order was forced by the movement of their respective bearing axis. The axes of third branching order had a significant and negative effect on the damping of the natural deformation mode. Results point out the major role played by foliage, qualitatively and quantitatively, on the damping of tree motions and on coupling the motions of the crown components.