Coordination theory of leaf nitrogen distribution in a canopy

It has long been observed that leaf nitrogen concentrations decline with depth in closed canopies in a number of plant communities. This phenomenon is generally believed to be related to a changing radiation environment and it has been suggested by some researchers that plants allocate nitrogen in order to optimize total whole canopy photosynthesis. Although optimization theory has been successfully utilized to describe a variety of physiological and ecological phenomena, it has some shortcomings that are subject to criticism (e.g., time constraints, oversimplifications, lack of insights, etc.). In this paper we present an alternative to the optimization theory of plant canopy nitrogen distribution, which we term coordination theory. We hypothesize that plants allocate nitrogen to maintain a balance between two processes, each of which is dependent on leaf nitrogen content and each of which potentially limits photosynthesis. These two processes are defined as W_c, the Rubiscolimited rate of carboxylation, and W_j, the electron transport-limited rate of carboxylation. We suggest that plants allocate nitrogen differentially to, leaves in different canopy layers in such a way that W_c and W_j remain roughly balanced. In this scheme, the driving force for the allocation of nitrogen within a canopy is the difference between the leaf nitrogen content that is required to bring W_c and W_j into balance and the current nitrogen content. We show that the daily carbon assimilation of a canopy with a nitrogen distribution resulting from this internal coordination of W_c and W_j is very similar to that obtained using optimization theory.     

Evolution of life history strategies for an asexual annual plant model

At any given moment in time a plant is partitioning total growth mass into its various component parts such as leaves, roots, reproductive material, etc. The view is taken that the plant has evolved a life history strategy to control this partitioning process. This paper illustrates the utility of optimal control theory for use in determining life history strategies which maximize fitness for a given asexual plant model. The optimal control methods are first used on a model previously analyzed by Professor Dan Cohen, who used a different method. His results of a change from 100% vegetable growth to 100% reproductive growth at a fixed switching time is again obtained. This 100% switching result is shown to be more generally applicable by using a qualitatively described model. However the switching time in general is shown to be a function of both leaf mass and time remaining to the end of the growing season. The allocation to toxin production is also considered. It is shown that under this model an inequality between system parameters must be satisfied before the plant should allocate growth to toxin production. Although the particular model explored here may rarely be realistic in nature, these same methods of optimal control theory can be applied in a similar fashion to many other proposed models of plant resource allocation.     

Optimal Dynamic Allocation of Conservation Funding Among Priority Regions

The optimal allocation of conservation resources between biodiverse conservation regions has generally been calculated using stochastic dynamic programming, or using myopic heuristics. These solutions are hard to interpret and may not be optimal. To overcome these two limitations, this paper approaches the optimal conservation resource allocation problem using optimal control theory. A solution using Pontryagin’s maximum principle provides novel insight into the general properties of efficient conservation resource allocation strategies, and allows more extensive testing of the performance of myopic heuristics. We confirmed that a proposed heuristic (minimize short-term loss) yields near-optimal results in complex allocation situations, and found that a qualitative allocation feature observed in previous analyses (bang-bang allocation) is a general property of the optimal allocation strategy.     

Understanding plant rooting patterns in semi‐arid systems: an integrated model analysis of climate,soil type and plant biomass

Aim A consistent set of root characteristics for herbaceous plants growing in water‐limited environments has been developed based on compilations of global root databases, but an overall analysis of why these characteristics occur is still missing. The central question in this study is whether an ecohydrological model which assumes that rooting strategies reflect maximization of transpiration can predict the variations in rooting strategies of plants in dry environments. Location Arid ecosystems across the globe. Methods A model was used to explore interactions between plant biomass, root–shoot allocation, root distribution, rainfall, soil type and water use by plants. Results Model analyses showed that the predicted shifts in rooting depth and root–shoot allocation due to changes in rainfall, soil type and plant biomass were quite similar to observed shifts. The model predicted that soil type, annual rainfall and plant biomass each had strong effects on the rooting strategies that optimize transpiration, but also that these factors have strong interactive effects. The process by which plants compete for water availability (soil evaporation or drainage) especially affected the depth distribution of roots in the soil, whereas the availability of rainfall mainly affected the optimal root–shoot allocation strategy. Main conclusions The empirically observed key patterns in rooting characteristics of herbaceous plant species in arid environments could be explained in this theoretical study by using the concept of hydrological optimality, represented here by the maximization of transpiration.     

Xylem hydraulic physiology: The functional backbone of terrestrial plant productivity

Land plants are completely dependent on a passive system of water transport for their survival. The great bulk of the xylem tissue is non-living and consequently has no short term capacity to acclimate or adjust to changes in hydraulic demand. Yet there exists an extraordinary degree of coordination between the hydraulic and photosynthetic systems of plants that defies developmental explanation. The connection between hydraulic capacity and photosynthetic assimilation arises as a product of the shared stomatal pathway for water and CO₂ exchange in the leaf. A combination of optimization in both water use and structural xylem investment has led to a situation in vascular plants where the form and function of all individuals is moulded by the link between hydraulic and photosynthetic systems. Unlike competing models of hormonal control of gas exchange, hydraulic limitation of productivity under optimal and drought conditions accounts for much of the observed variation in plant gas exchange in natural systems. The plant water transport system places a hard physical limit to plant productivity and survival. Identifying the developmental control of key xylem traits will yield the potential for achieving new performance capabilities in plants.     

Drought effect on plant biomass allocation: A meta‐analysis

Drought is one of the abiotic stresses controlling plant function and ecological stability. In the context of climate change, drought is predicted to occur more frequently in the future. Despite numerous attempts to clarify the overall effects of drought stress on the growth and physiological processes of plants, a comprehensive evaluation on the impacts of drought stress on biomass allocation, especially on reproductive tissues, remains elusive. We conducted a meta‐analysis by synthesizing 164 published studies to elucidate patterns of plant biomass allocation in relation to drought stress. Results showed that drought significantly increased the fraction of root mass but decreased that of stem, leaf, and reproductive mass. Roots of herbaceous plants were more sensitive to drought than woody plants that reduced reproductive allocation more sharply than the former. Relative to herbaceous plants, drought had a more negative impact on leaf mass fraction of woody plants. Among the herbaceous plants, roots of annuals responded to drought stress more strongly than perennial herbs, but their reproductive allocation was less sensitive to drought than the perennial herbs. In addition, cultivated and wild plants seemed to respond to drought stress in a similar way. Drought stress did not change the scaling exponents of the allometric relationship between different plant tissues. These findings suggest that the allometric partitioning theory, rather than the optimal partitioning theory, better explains the drought‐induced changes in biomass allocation strategies.     

Phytoremediation: an overview of metallic ion decontamination from soil

In recent years, phytoremediation has emerged as a promising ecoremediation technology, particularly for soil and water cleanup of large volumes of contaminated sites. The exploitation of plants to remediate soils contaminated with trace elements could provide a cheap and sustainable technology for bioremediation. Many modern tools and analytical devices have provided insight into the selection and optimization of the remediation process by plant species. This review describes certain factors for the phytoremediation of metal ion decontamination and various aspects of plant metabolism during metallic decontamination. Metal-hyperaccumulating plants, desirable for heavily polluted environments, can be developed by the introduction of novel traits into high biomass plants in a transgenic approach, which is a promising strategy for the development of effective phytoremediation technology. The genetic manipulation of a phytoremediator plant needs a number of optimization processes, including mobilization of trace elements/metal ions, their uptake into the root, stem and other viable parts of the plant and their detoxification and allocation within the plant. This upcoming science is expanding as technology continues to offer new, low-cost remediation options.     

Sex and size in cosexual plants

There are conceptual and practical difficulties in measuring the exact shape of fitness-gain curves and sex allocation, and these hamper empirical testing of some of the basic predictions of sex allocation theory for plants. Nevertheless, our knowledge of the processes that shape fitness-gain curves allows us to formulate hypotheses to test predictions of sex allocation theory. One such hypothesis is that plants adjust their gender according to size. The connection between plant size and gender was generally thought to be weak. Recent data, however, suggest that size-dependent sex allocation (SDS) is a common phenomenon in hermaphrodites and other cosexual plants.     

Pollen limitation meets resource allocation: towards a comprehensive methodology

The standard method of measuring pollen limitation is to add pollen to a number of flowers, preferably to a whole plant, and to compare fruit and seed set with that of naturally pollinated flowers on other plants. In 25 yr of research, this method has yielded valuable data, but it is difficult to use in large plants. This has caused a bias in the available data towards smaller, herbaceous plants with relatively few flowers. I argue that, in order to widen our knowledge of how pollen limitation affects plants, we should go beyond whole-plant pollen addition and change our concept of how a flowering plant functions. The traditional method does not take into account the variation in and dynamics of resource allocation and pollen availability. The concept of integrated physiological units (IPUs) does, but, although it has been applied to pollination biology, it has not received the attention it deserves. I use this article to present its merits again, to propose a step-by-step methodology for studying pollen limitation, and to examine factors influencing possible plant strategies.     

Plant defence and stochastic risk of herbivory

Summary The influence of risk of herbivory and its variation in time on the optimal defence strategy in plants is analysed by a simple optimization model. We contrast two possible defence strategies; a constitutive defence with an invariant defence level in time and an idealized induced defence, that is, a strategy that adjusts the defence level to the prevailing risk of herbivory. We also take into account effects of the efficiency of the defence. If there is no variation in risk of herbivory over years, constitutive and induced defence should have the same expected optimal defence level and both strategies are equally fit. The optimal defence level increases as the maximum fecundity and the adult to juvenile survival ratio of the plants both increase. If the risk of herbivory varies stochastically, the expected optimal level of the constitutive defence is either increased or unaffected by the variation, whereas the induced defence strategy may result in both higher or lower expected optimal defence levels as variance increases. This outcome is dependent on the mean risk of herbivory. It also depends on the defence efficiency, i.e. the shape (convex, concave or linear) of the defence function that relates the probability of survival if encountered by a herbivore to defence level. Thus, the defence level of plants interacting with variable herbivore populations cannot be unambiguously predicted unless the defence strategy (constitutive or induced), mean risk of herbivory, the form of the defence function and plant life history are known.     

Optimal defense strategy against herbivory in plants: Conditions selecting for induced defense, constitutive defense, and no-defense

To examine the conditions selecting for induced defense, constitutive defense, and no-defense, we developed a model of plant defense strategy against herbivory. In the model, a plant consists of two modules between which signal inducing defense compounds can be translocated. We assume three strategies: plants produce defense compounds responding to herbivory (induced defense), they have the compounds beforehand (constitutive defense), and they never produce the compounds (no-defense). We found that no-defense is optimal if the amount of biomass lost due to herbivory is small because of the growth cost of having defense compounds. The constitutive defense is optimal if the amount of biomass lost is not so small and the probability of herbivory is high. If the biomass loss is not so small but the probability of herbivory is low, the induced defense or no-defense is optimal. When the induced defense is optimal, the probability of herbivory necessarily increases in plants once herbivory has occurred. If the probability stays the same, no-defense is optimal. Thus, the behavior of herbivores, i.e., whether they remain around a plant and attack it repeatedly, affects the evolution of the induced defense.     

Allocation strategies for nitrogen and phosphorus in forest plants

The allocation of limiting elements, such as nitrogen (N) and phosphorus (P), in plants is an important basis for structural stability and functional optimization in natural plant communities. However, because of the lack of systematic investigation data, the mechanisms of optimal nutrient allocation in plants in natural forests are still unclear. Using consistent measurements of N and P contents in 930 plant species, we explored the allocation strategies for N and P in different plant organs and plant functional groups (PFGs) in natural communities. The N and P contents and N:P ratio were the highest in the leaf (the most active organ) at the organ level. At the PFG level, the N and P contents were higher in herbs than in woody plants, but the trend was opposite for the N:P ratio. The elemental plasticity of root was higher than that of leaf. Furthermore, at the large scale, the allometric exponents of N and P were less than 1 and showed no difference, indicating strong conservatism of the scaling relationship in plants. In summary, higher element content in more active organs, higher element plasticity in underground organs, and conservative allometric allocation among different organs and among different PFGs jointly constitute the optimal strategies for the allocation of limiting elements.     

Plant invaders outperform congeneric natives on amino acids

As a key nitrogen (N) source, soil amino acids play an important role in plant N nutrition. However, how amino acids differentially influence the N use strategies of native and invasive plants remains unclear. We performed a potted experiment using five pairs of native and invasive plant congeners, which were subject to 23 N treatments (i.e., 20 protein primary amino acids, nitrate, ammonium, and control), each with 10 replicates. We determined their growth, biomass allocation, N use efficiency, and the growth advantage of plant invaders over their natives. Native and invasive plants used the same 18 amino acid N sources (i.e., a similar amino acid economics spectrum). The growth of plant invaders was invariably better than the growth of native plants, and this superior growth of invaders was linked to their higher root biomass allocation and greater N use efficiency. Additionally, invasive plants had a greater growth advantage on amino acid N than on inorganic N, so was this advantage greater on neutral amino acids than on acidic amino acids. These findings suggest that the differences in amino acid use strategies between invasive and native congeners could help to explain plant invasiveness, as indicated by a growth advantage.     

Plant Biomass Allocation across a Precipitation Gradient: An Approach to Seasonally Dry Tropical Forest at Yucatán, Mexico

It has been assumed that plant biomass partitioning to stems and roots at the ecosystem level follows a single strategy according to which the stem biomass scales isometrically with root biomass, a hypothesis known as ??isometric scaling??. In this study, we examined an alternative theory used for plants: plant biomass is allocated preferentially to the plant organ that harvests the limiting growth resource, a theory known as the ??balanced growth hypothesis??. Our objective was to test these two alternative hypotheses across a water availability gradient. We quantified the stem and root biomass in a seasonally dry tropical forest (SDTF) in three regions of the Yucatán peninsula along a precipitation gradient. Reduced major axis analysis showed that the slopes of the relationship between stem and root biomass across the study regions were statistically similar and significantly different from 1.0 (common slope?=?2.5), which contrasts with the ??isometric scaling?? hypothesis. The allometric coefficient was different between regions along the precipitation gradient, which showed that plant biomass allocation to stems is higher in high than in low water availability regions where biomass is allocated in greater proportions to roots. The stem:root ratio increases following the low to high water availability gradient. Our results showed that plant biomass allocation in the SDTF follows a simple allometric strategy in which greater plant biomass is allocated to stems irrespective of water availability, suggesting to the forest level that plant biomass allocation strategy is invariant across the water availability gradient.     

Variation in lifetime male fitness in Ipomopsis aggregata: tests of sex allocation theory

Sex allocation theory assumes that a shift in allocation of resources to male function both increases male fitness and decreases female fitness. Moreover, the shapes of these fitness gain functions determine whether hermaphroditism or another breeding system is evolutionarily stable. In this article, I first outline information needed to measure these functions in flowering plants. I then use paternity analysis to describe the shapes of the fitness gain functions in natural populations of the hermaphroditic herb Ipomopsis aggregata. I also explore the relationships of male fitness (number of seeds sired) and female fitness (number of seeds produced) to the number of flowers produced by a plant. Plants with greater investment of biomass in the androecium, compared to the gynoecium and seeds, showed increased success at siring seeds, assumed by the models. That sex allocation trait, however, explained only 9% of the variance in estimates of male fitness. The shapes of the fitness gain functions were consistent with theoretical expectations for a hermaphroditic plant, but the model predicted a more female-biased evolutionarily stable strategy (ESS) allocation than was observed. These results lend only partial support the classical sex allocation model.     

Climate and plant trait strategies determine tree carbon allocation to leaves and mediate future forest productivity

Forest leaf area has enormous leverage on the carbon cycle because it mediates both forest productivity and resilience to climate extremes. Despite widespread evidence that trees are capable of adjusting to changes in environment across both space and time through modifying carbon allocation to leaves, many vegetation models use fixed carbon allocation schemes independent of environment, which introduces large uncertainties into predictions of future forest responses to atmospheric CO₂ fertilization and anthropogenic climate change. Here, we develop an optimization‐based model, whereby tree carbon allocation to leaves is an emergent property of environment and plant hydraulic traits. Using a combination of meta‐analysis, observational datasets, and model predictions, we find strong evidence that optimal hydraulic–carbon coupling explains observed patterns in leaf allocation across large environmental and CO₂ concentration gradients. Furthermore, testing the sensitivity of leaf allocation strategy to a diversity in hydraulic and economic spectrum physiological traits, we show that plant hydraulic traits in particular have an enormous impact on the global change response of forest leaf area. Our results provide a rigorous theoretical underpinning for improving carbon cycle predictions through advancing model predictions of leaf area, and underscore that tree‐level carbon allocation to leaves should be derived from first principles using mechanistic plant hydraulic processes in the next generation of vegetation models.     

The use of transgenic plants in the bioremediation of soils contaminated with trace elements

The use of plants to clean-up soils contaminated with trace elements could provide a cheap and sustainable technology for bioremediation. Field trials suggested that the rate of contaminant removal using conventional plants and growth conditions is insufficient. The introduction of novel traits into high biomass plants in a transgenic approach is a promising strategy for the development of effective phytoremediation technologies. This has been exemplified by generating plants able to convert organic and ionic forms of mercury into the less toxic, volatile, elemental mercury, a trait that occurs naturally only in some bacteria and not at all in plants. The engineering of a phytoremediator plant requires the optimization of a number of processes, including trace element mobilization in the soil, uptake into the root, detoxification and allocation within the plant. A number of transgenic plants have been generated in an attempt to modify the tolerance, uptake or homeostasis of trace elements. The phenotypes of these plants provide important insights for the improvement of engineering strategies. A better understanding, both of micronutrient acquisition and homeostasis, and of the genetic, biochemical and physiological basis of metal hyperaccumulation in plants, will be of key importance for the success of phytoremediation.     

Heuristic optimization of the general life history problem: A novel approach

Summary The general life history problem concerns the optimal allocation of resources to growth, survival and reproduction. We analysed this problem for a perennial model organism that decides once each year to switch from growth to reproduction. As a fitness measure we used the Malthusian parameterr, which we calculated from the Euler-Lotka equation. Trade-offs were incorporated by assuming that fecundity is size dependent, so that increased fecundity could only be gained by devoting more time to growth and less time to reproduction. To calculate numerically the optimalr for different growth dynamics and mortality regimes, we used a simplified version of the simulated annealing method. The major differences among optimal life histories resulted from different accumulation patterns of intrinsic mortalities resulting from reproductive costs. If these mortalities were accumulated throughout life, i.e. if they were senescent, a bangbang strategy was optimal, in which there was a single switch from growth to reproduction: after the age at maturity all resources were allocated to reproduction. If reproductive costs did not carry over from year to year, i.e. if they were not senescent, the optimal resource allocation resulted in a graded switch strategy and growth became indeterminate. Our numerical approach brings two major advantages for solving optimization problems in life history theory. First, its implementation is very simple, even for complex models that are analytically intractable. Such intractability emerged in our model when we introduced reproductive costs representing an intrinsic mortality. Second, it is not a backward algorithm. This means that lifespan does not have to be fixed at the begining of the computation. Instead, lifespan itself is a trait that can evolve. We suggest that heuristic algorithms are good tools for solving complex optimality problems in life history theory, in particular questions concerning the evolution of lifespan and senescence.     

Multiple switches between vegetative and reproductive growth in annual plants

A model of growth and reproduction in annual plants was developed by Cohen (1971, J. Theor. Biol.33, 299–307) to determine the allocation strategy which maximizes seed yield. The model divides the plant into vegetative and reproductive parts and predicts that yield is maximized by a strategy consisting of a switch from purely vegetative to strictly reproductive growth. We generalize Cohen's model to include vegetative and reproductive loss terms. Both growth and loss rates are allowed to vary with time. Using optimal control theory we find that seed yield is maximized by a strategy consisting of multiple switches between vegetative and reproductive growth, for certain ranges of the model parameters. In natural systems a predictable vegetative loss burst may be necessary to promote multiple switches.