The contribution of dynamic changes in photosynthesis to shade tolerance of two conifer species.

Generally 'shade tolerance' refers to the capacity of a plant to exist at low light levels but characteristics of shade can vary and must be taken into account in defining the term. We studied Abies amabilis Dougl. ex J.Forbes and Tsuga heterophylla (Raf.) Sarg. under a forest canopy in the northwest of the Olympic Peninsula, USA, which has low annual sunshine hours and frequent overcast days. Using BF3 sunshine sensors, we surveyed diffuse and total light received by saplings growing under a range of canopy openness up to 30%. We measured variation in photosynthetic capacity over the growing season and within days and estimated photosynthesis induction in relation to ambient light. Three components of shade tolerance are associated with variation in light climate: (i) Total light on the floor of an 88-year stand of naturally regenerated T. heterophylla was greater on overcast than clear days. Light on overcast days varied throughout the day sometimes with a cyclical pattern. (ii) Photosynthetic capacity, Amax, varied both through the growing season and within days. Amax was generally greater in the latter part of the growing season, being limited by temperature and stomatal conductance, gs, at times during the early part. Saplings in more shaded areas had lower Amax and in the latter part of the growing season Amax was found to decline from mid-afternoon. (iii) Two patterns of photosynthesis induction to increased light were found. In a mean ambient light of 139 µmol m(-2) s(-1), induction had a curvilinear response to a step increase in light with a mean time constant, τ, of 112.3 s. In a mean ambient light of 74 µmol m(-2) s(-1), induction had a two-part increase: one with τ1 of 11.3 s and the other with τ2 of 184.0 s. These are the smallest published values of τ to date. (iv) Both variation in photosynthetic capacity and induction are components of shade tolerance where light varies over time. Amax acclimates to seasonal and diurnal changes in light and varies between microenvironments. The rapid induction processes can cause a rapid response of photosynthesis to changes in diffuse or direct light.

The dynamic relationship between plant architecture and competition.

In this review, structural and functional changes are described in single-species, even-aged, stands undergoing competition for light. Theories of the competition process as interactions between whole plants have been advanced but have not been successful in explaining these changes and how they vary between species or growing conditions. This task now falls to researchers in plant architecture. Research in plant architecture has defined three important functions of individual plants that determine the process of canopy development and competition: (i) resource acquisition plasticity; (ii) morphogenetic plasticity; (iii) architectural variation in efficiency of interception and utilization of light. In this review, this research is synthesized into a theory for competition based on five groups of postulates about the functioning of plants in stands. Group 1: competition for light takes place at the level of component foliage and branches. Group 2: the outcome of competition is determined by the dynamic interaction between processes that exert dominance and processes that react to suppression. Group 3: species differences may affect both exertion of dominance and reaction to suppression. Group 4: individual plants may simultaneously exhibit, in different component parts, resource acquisition and morphogenetic plasticity. Group 5: mortality is a time-delayed response to suppression. Development of architectural models when combined with field investigations is identifying research needed to develop a theory of architectural influences on the competition process. These include analyses of the integration of foliage and branch components into whole-plant growth and precise definitions of environmental control of morphogenetic plasticity and its interaction with acquisition of carbon for plant growth.

Detecting bimodality in plant size distributions and its significance for stand development and competition.

Bimodal distributions in plant size, with a major mode of small and minor mode of large-size plants, have been reported for a range of single species stands in different growing conditions. The occurrence of bimodality has implications for the dynamics of competition within a stand and potentially for stand productivity. However, deduction of the existence of bimodality has been by visual assessment of histograms of a single measure of plant size which can lead to differences of opinion about its existence. We show that the bivariate distribution of plant height and weight is more informative about stand structure than univariate distributions. We demonstrate how sub-populations of small- and large-size plants can be identified using a bivariate mixture distribution fitted using evolutionary computation. For the multiple datasets we analyse, a bimodal distribution fits in preference to unimodal or trimodal distributions. Small- and large-plant sub-populations, respectively, form a lower and upper canopy. The numbers of plants in these canopies change during stand development and vary with initial spacing, contrary to reports for other species. Early in stand development, large plants show spatial separation between themselves but spatial association with small plants, and as stands develop the number of large plants declines markedly but they remain spatially separated between each other. Bivariate analysis of height and weight, and spatial analysis of individuals of different sizes, provides a more comprehensive description of stand structure than that obtained in previous studies.

Assessment of uncertainty in functional-structural plant models.

BACKGROUND AND AIMS: Constructing functional-structural plant models (FSPMs) is a valuable method for examining how physiology and morphology interact in determining plant processes. However, such models always have uncertainty concerned with whether model components have been selected and represented effectively, with the number of model outputs simulated and with the quality of data used in assessment. We provide a procedure for defining uncertainty of an FSPM and how this uncertainty can be reduced. METHODS: An important characteristic of FSPMs is that typically they calculate many variables. These can be variables that the model is designed to predict and also variables that give indications of how the model functions. Together these variables are used as criteria in a method of multi-criteria assessment. Expected ranges are defined and an evolutionary computation algorithm searches for model parameters that achieve criteria within these ranges. Typically, different combinations of model parameter values provide solutions achieving different combinations of variables within their specified ranges. We show how these solutions define a Pareto Frontier that can inform about the functioning of the model. KEY RESULTS: The method of multi-criteria assessment is applied to development of BRANCHPRO, an FSPM for foliage reiteration on old-growth branches of Pseudotsuga menziesii. A geometric model utilizing probabilities for bud growth is developed into a causal explanation for the pattern of reiteration found on these branches and how this pattern may contribute to the longevity of this species. CONCLUSIONS: FSPMs should be assessed by their ability to simulate multiple criteria simultaneously. When different combinations of parameter values achieve different groups of assessment criteria effectively a Pareto Frontier can be calculated and used to define the sources of model uncertainty.

Defining how aging Pseudotsuga and Abies compensate for multiple stresses through multi-criteria assessment of a functional-structural model.

Many hypotheses have been advanced about factors that control tree longevity. We use a simulation model with multi-criteria optimization and Pareto optimality to determine branch morphologies in the Pinaceae that minimize the effect of growth limitations due to water stress while simultaneously maximizing carbohydrate gain. Two distinct branch morphologies in the Pareto optimal space resemble Pseudotsuga menziesii (Mirb.) Franco and Abies grandis (Dougl. ex D. Don) Lindl., respectively. These morphologies are distinguished by their performance with respect to two pathways of compensation for hydraulic limitation: minimizing the mean path length to terminal foliage (Pseudotsuga) and minimizing the mean number of junction constrictions to terminal foliage (Abies). Within these two groups, we find trade-offs between the criteria for foliage display and the criteria for hydraulic functioning, which shows that an appropriate framework for considering tree longevity is how trees compensate, simultaneously, for multiple stresses. The diverse morphologies that are found in a typical old-growth conifer forest may achieve compensation in different ways. The method of Pareto optimization that we employ preserves all solutions that are successful in achieving different combinations of criteria. The model for branch development that we use simulates the process of delayed adaptive reiteration (DAR), whereby new foliage grows from suppressed buds within the established branch structure. We propose a theoretical synthesis for the role of morphology in the persistence of old Pseudotsuga based on the characteristics of branch morphogenesis found in branches simulated from the optimal set. (i) The primary constraint on branch growth for Pseudotsuga is the mean path length; (ii) as has been previously noted, DAR is an opportunistic architecture; and (iii) DAR is limited by the number of successive reiterations that can form. We show that Pseudotsuga morphology is not the only solution to old-growth constraints, and we suggest how the model results should be used to guide future empirical investigation based on the two contrasting morphologies and how the morphological contrast may relate to physiological processes. Our results show that multi-criteria optimization with Pareto optimality has promise to advance the use of models in theory development and in exploration of functional-structural trade-offs, particularly in complex biological systems with multiple limiting factors.

Physiological and ecological implications of adaptive reiteration as a mechanism for crown maintenance and longevity.

Reiteration is the process whereby architectural units are replicated within a tree. Both immediate (from apical buds) and delayed (from suppressed or adventitious buds) reiteration can be seen in many tree species where architectural units ranging from clusters of shoots to entire branches and stems are replicated. In large old trees and suppressed trees, delayed reiteration occurs without an obvious external stimulus such as defoliation or traumatic loss of the branch apex. This suggests that, in trees that are growth-limited, reiteration is an adaptive mechanism for crown maintenance. We discuss theories about the aging process and how delayed adaptive reiteration may help maintain crown productivity and increase longevity. These include: (1) reducing the respiration/photosynthesis ratio; (2) increasing hydraulic conductance to newly developing foliage; (3) reducing nutrient loss from the tree; and (4) rejuvenating the apical meristem. The ability to reiterate various architectural units may contribute to increasing lifetime reproductive output by prolonging tree longevity. Further studies on the physiological and ecological implications of reiteration are needed to understand its adaptive significance in the life history of trees.

Statistical inference using the g or K point pattern spatial statistics.

Spatial point pattern analysis provides a statistical method to compare an observed spatial pattern against a hypothesized spatial process model. The G statistic, which considers the distribution of nearest neighbor distances, and the K statistic, which evaluates the distribution of all neighbor distances, are commonly used in such analyses. One method of employing these statistics involves building a simulation envelope from the result of many simulated patterns of the hypothesized model. Specifically, a simulation envelope is created by calculating, at every distance, the minimum and maximum results computed across the simulated patterns. A statistical test is performed by evaluating where the results from an observed pattern fall with respect to the simulation envelope. However, this method, which differs from P. Diggle's suggested approach, is invalid for inference because it violates the assumptions of Monte Carlo methods and results in incorrect type I error rate performance. Similarly, using the simulation envelope to estimate the range of distances over which an observed pattern deviates from the hypothesized model is also suspect. The technical details of why the simulation envelope provides incorrect type I error rate performance are described. A valid test is then proposed, and details about how the number of simulated patterns impacts the statistical significance are explained. Finally, an example of using the proposed test within an exploratory data analysis framework is provided.

Simulation of effects of wood microstructure on water transport.

A tracheid-level model was used to quantify the effects of differences in wood microstructure between coastal and interior Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco var. menziesii and var. glauca) wood on larger scale properties like hydraulic conductivity. The model showed that tracheid length, the ease of flow through a bordered pit and effective tracheid diameter can all limit maximum hydraulic conductivity. Among the model parameters tested, increasing bordered pit conductivity and tracheid length resulted in the greatest increase in maximum conductivity in both the inland and coastal ecotypes. A sensitivity analysis of the uncertainty between parameters governing flow through the bordered pit and air-seeding potential showed that, although decreased pit flow resistance increased maximum hydraulic conductivity, increased cavitation led to lower conductivity over time. The benefits of increasing the number of bordered pits depended on the intensity of the meteorological driving function: in drier environmental conditions, wood with fewer pits was more conductive over time than wood with more pits. Switching the bordered pit characteristics between coastal and interior wood indicated that the conductivity time course of coastal and interior wood was primarily governed by differences in the number of bordered pits and not differences in tracheid dimensions. The rate at which tracheids refilled had little effect on the conductivity time course of either coastal or interior wood during the first two summers when the wood was highly saturated, but had a marked influence in subsequent years once the cavitation profile stabilized. Our work highlights the need for more empirical work on bordered pits to determine whether variation in their number and properties is related to changing environmental conditions. In addition, a detailed simulation model of a bordered pit is needed to understand how variation in pit properties affects the relationship between ease of flow through a bordered pit and its potential for facilitating air-seeding.

Development of Erect Leaves in a Modern Maize Hybrid is Associated with Reduced Responsiveness to Auxin and Light of Young Seedlings In Vitro.

Modern corn (Zea mays L.) varieties have been selected for their ability to maintain productivity in dense plantings. We have tested the possibility that the physiological consequence of the selection involves changes in responsiveness to light and auxin.Etiolated seedlings of two older corn hybrids 307 and 3306 elongated significantly more than seedlings of a modern corn hybrid 3394. The level of endogenous auxin and activity of PAT in 307 and 3394 were similar. Hybrid 3394 shows resistance to auxin- and light-induced responses at the seedling, cell and molecular levels. Intact 3394 plants exhibited less responsiveness to the inhibitory effect of R, FR and W, auxin, anti-auxin and inhibitors of PAT. In excised mesocotyl tissue 3394 seedlings also showed essentially low responsiveness to NAA. Cells of 3394 were insensitive to auxin- and light-induced hyperpolarization of the plasma membrane. Expression of ABP4 was much less in 3394 than in 307, and in contrast to 307, it was not upregulated by NAA, R and FR. Preliminary analysis of abp mutants suggests that ABPs may be involved in development of leaf angle in corn.Our results confirm the understanding that auxin interacts with light in the regulation of growth and development of young seedlings and suggest that in corn ABPs may be involved in growth of maize seedlings and development of leaf angle. We hypothesize that ABP4 plays an important role in the auxin- and/or light-induced growth responses. We also hypothesize that in the modern corn hybrid 3394, ABP4 is "mutated," which may result in the observed 3394 phenotypes, including upright leaves.

Branch and foliage morphological plasticity in old-growth Thuja plicata.

At the Wind River Canopy Crane Facility in southeastern Washington State, USA, we examined phenotypic variation between upper- and lower-canopy branches of old-growth Thuja plicata J. Donn ex D. Don (western red cedar). Lower-canopy branches were longer, sprouted fewer daughter branches per unit stem length and were more horizontal than upper-canopy branches. Thuja plicata holds its foliage in fronds, and these had less projected area per unit mass, measured by specific frond area, and less overlap, measured by silhouette to projected area ratio (SPARmax), in the lower canopy than in the upper canopy. The value of SPARmax, used as an indicator of sun and shade foliage in needle-bearing species, did not differ greatly between upper- and lower-canopy branches. We suggest that branching patterns, as well as frond structure, are important components of morphological plasticity in T. plicata. Our results imply that branches of old-growth T. plicata trees have a guerilla growth pattern, responding to changes in solar irradiance in a localized manner.

Light interacts with auxin during leaf elongation and leaf angle development in young corn seedlings.

Modern corn ( Zea mays L.) varieties have been selected for their ability to maintain productivity in dense plantings. We have tested the possibility that the physiological consequence of the selection of the modern hybrid, 3394, for increased crop yield includes changes in responsiveness to auxin and light. Etiolated seedlings in the modern line are shorter than in an older hybrid, 307, since they produce shorter coleoptile, mesocotyl, and leaves (blade as well as sheath). Etiolated 3394 seedlings, as well as isolated mesocotyl and sheath segments, were less responsive to auxin and an inhibitor of polar auxin transport, N-1-naphthylphthalamic acid (NPA). Reduced response of 3394 to auxin was associated with less reduction of elongation growth by light (white, red, far-red, blue) than in 307, whereas the activity of polar auxin transport (PAT) and its reduction by red or far-red light was similar in both genotypes. NPA reduced PAT in etiolated 3394 seedlings much less than in 307. A characteristic feature of 3394 plants is more erect leaves. In both hybrids, light (white, red, blue) increases leaf declination from the vertical, whereas NPA reduces leaf declination in 307, but not in 3394. Our results support findings that auxin and PAT are involved in elongation growth of corn seedlings, and we show that light interacts with auxin or PAT in regulation of leaf declination. We hypothesize that, relative to 307, more erect leaves in the modern hybrid may be primarily a consequence of a reduced amount of auxin receptor(s) and reduced responsiveness to light in etiolated 3394 plants. The more erect leaves in 3394 may contribute to the tolerance of the modern corn hybrid to dense planting.

Modeling tree water flow as an unsaturated flow through a porous medium.

The electric circuit analogy has had a profound influence on how tree physiologists measure, model and think about tree water flow. For example, previous models that attempt to account for changes in saturation use the electric circuit analogy to define capacitance as the change in saturation per change in pressure. Given that capacitance is constant, this relationship implies that subjecting a block of wood to a pressure of -2.5 MPa for 2 min results in the same change in saturation as subjecting the same block to the same pressure for 2 days. Given the definition of capacitance, it is unclear how the electric circuit analogy could be used to predict changes in saturation separately from changes in pressure. The inadequacies in the electric circuit analogy discussed in this paper necessitate a new theory of tree water flow that recognizes the sapwood as being a porous medium and explicitly deals with the full implications of the unsaturated flow occurring in the sapwood. The theory proposed in this paper combines the Cohesion theory with a mathematical theory of multiphase flow through porous media. Based on this theory, both saturated and unsaturated tree water flow models are presented. Previous partial differential equation models of tree water flow based on the electric circuit analogy are shown to be mathematically equivalent to the model of saturated porous flow. The unsaturated model of tree water flow explicitly models the pressure profile and the rates of change in saturation and specific interfacial area (a measure of how the water in the unsaturated sapwood is partitioned between mobile and immobile components). The unsaturated model highlights the differences between saturated and unsaturated flow and the need to measure the variables governing tree water flow at higher spatial and temporal resolutions.

Parameterizing a model of Douglas fir water flow using a tracheid-level model.

The theory of tree water flow proposed in Aumann & Ford (submitted) is assessed by numerically solving the model developed from this theory under a variety of functional parameterizations. The unknown functions in this nonlinear partial differential equation model are determined using a tracheid-level model of water flow in a block of Douglas fir tracheids. The processes of flow, cavitation, pit aspiration/deaspiration, flow through the cell wall and ray exudation in a block of approximately 79 000 tracheids are modeled. Output from the tracheid model facilitates determination of the hydraulic conductivities in the sapwood as a function of saturation and interfacial area between liquid and gaseous phases of water, the function governing the rate of change in saturation, and the function governing the rate of change in interfacial area. The models show complementary things. The tracheid model shows that capacitance, or the change in saturation per change in pressure, is not constant. When all refilling is stopped, it takes over 180 days for the hydraulic conductivity in the vertical direction to reach 1/4 of its maximal value, showing the robustness of the transpiration stream for conducting water. The shape of the functions determined with the tracheid model change with different tracheid-level assumptions. When these functions are used in the differential equation model, it is shown that cell-wall conductivity plays an important part in the lag in flow observed in many conifers. The flow velocities and rates of change in saturation predicted by the differential equation model agree with those measured in Douglas fir. Both models support the theory of tree water flow presented in Aumann & Ford (submitted) and undermine the theory that water flow in trees is analogous to the flow of current in electric circuits.

Variation in specific needle area of old-growth Douglas-fir in relation to needle age, within-crown position and epicormic shoot production.

Variation in specific needle area (SNA; cm2 projected fresh needle area g-1 oven-dried needle weight) was investigated in relation to needle age, within-crown position and epicormic shoot production in 450-year-old Douglas-fir (Pseudotsuga menziesii Mirb. (Franco) var. menziesii) trees. Specific needle area decreased with increasing needle age. The magnitude and rate of change in SNA with needle age were greatest for lower-crown branches, and decreased toward the middle- and upper-crown branches. For all branches, there was no difference between regular and epicormic shoots in the relationship between SNA and needle age. Specific needle area decreased with increasing distance from branch base, and this relationship was significant for the majority of needle age classes of the upper- and middle-crown branches. In the lowercrown branches, SNA did not vary with distance from branch base for the majority of needle age classes. For all branches, there was no difference between regular and epicormic shoots in the relationship between SNA and distance from branch base for the majority of needle age classes. These results indicate that renewal of foliage by epicormic shoot production maintains needle quality. Branch SNA increased linearly with decreasing height in the crown at a mean rate of 0.951 +/- 0.110 cm2 g-1 per vertical meter. Total needle area of branches was estimated from total needle dry weight taking into account within-branch variation in SNA. Analyses of allometric relationships between branch size and foliage amount (needle area and needle dry weight) showed that branch length was a better predictor of foliage amount than branch diameter for old Douglas-fir trees. Total needle dry weight and needle area of the sample trees, estimated from branch length and branch height and taking into account vertical within-crown variation in branch SNA, ranged from 42.4 to 154.2 kg and from 246.2 to 816.0 m2 per tree, respectively.

The concept of closure in calculating carbon balance of forests: accounting for differences in spatial and temporal scales of component processes.

The concept of closure, which has been used extensively to calculate the heat and water budgets of forests, has led to advances in the understanding of how heat and water balances are controlled. The successful construction of closed heat and water budgets of forests can be attributed to the large scale of input and output fluxes relative to changes in storage, the comparative ease with which such fluxes can be measured, and the regularity with which forests cycle through discharge and recharge on diurnal and annual cycles. The applicability of simple, closed budget analysis for carbon balance of forests is less certain because changes in internal storage, which are of major significance, occur at different time scales for growth and decomposition. We conclude that carbon balance might best be modeled as an open system. For long-term predictions, the most important processes to consider are acclimation and adaptation, which occur at different spatial and temporal scales. Construction of a modeling procedure to accommodate this variation is discussed.