Evolution of Plant Architecture, Functional Diversification and Divergent Evolution in the Genus Atractocarpus (Rubiaceae) for New Caledonia.

The diversification of ecological roles and related adaptations in closely related species within a lineage is one of the most important processes linking plant evolution and ecology. Plant architecture offers a robust framework to study these processes as it can highlight how plant structure influences plant diversification and ecological strategies. We investigated a case of gradual evolution of branching architecture in Atractocarpus spp. (Rubiaceae), forming a monophyletic group in New Caledonia that has diversified rapidly, predominantly in rainforest understory habitats. We used a transdisciplinary approach to depict architectural variations and revealed multiple evolutionary transitions from a branched (Stone's architectural model) to a monocaulous habit (Corner's architectural model), which involved the functional reduction of branches into inflorescences. We propose an integrative functional index that assesses branching incidence on functional traits influencing both assimilation and exploration functions. We showed that architectural transitions correlate with ecologically important functional traits. Variation in ecologically important traits among closely relatives, as supported by the architectural analysis, is suggestive of intense competition that favored divergence among locally coexisting species. We propose that Pleistocene climatic fluctuations causing expansion and contraction of rainforest could also have offered ecological opportunities for colonizers in addition to the process of divergent evolution.

Trait coordination, mechanical behaviour and growth form plasticity of Amborella trichopoda under variation in canopy openness.

Understanding the distribution of traits across the angiosperm phylogeny helps map the nested hierarchy of features that characterize key nodes. Finding that Amborella is sister to the rest of the angiosperms has raised the question of whether it shares certain key functional trait characteristics, and plastic responses apparently widespread within the angiosperms at large. With this in mind, we test the hypothesis that local canopy openness induces plastic responses. We used this variation in morphological and functional traits to estimate the pervasiveness of trait scaling and leaf and stem economics. We studied the architecture of Amborella and how it varies under different degrees of canopy openness. We analyzed the coordination of 12 leaf and stem structural and functional traits, and the association of this covariation with differing morphologies. The Amborella habit is made up of a series of sympodial modules that vary in size and branching pattern under different canopy openness. Amborella stems vary from self-supporting to semi-scandent. Changes in stem elongation and leaf size in Amborella produce distinct morphologies under different light environments. Correlations were found between most leaf and stem functional traits. Stem tissue rigidity decreased with increasing canopy openness. Despite substantial modulation of leaf size and leaf mass per area by light availability, branches in different light environments had similar leaf area-stem size scaling. The sympodial growth observed in Amborella could point to an angiosperm synapomorphy. Our study provides evidence of intraspecific coordination between leaf and stem economic spectra. Trait variation along these spectra is likely adaptive under different light environments and is consistent with these plastic responses having been present in the angiosperm common ancestor.

Effect of light on the growth and photosynthesis of an invasive shrub in its native range.

Invasive species success may depend on ecophysiological attributes present in their native area or derived from changes that took place in the invaded environment. We studied the growth and photosynthetic capacity of Berberis darwinii shrubs growing under different light conditions (gap, forest edge and below the canopy) in their native area of Patagonia, Argentina. Leaf photosynthesis results determined in the native area were discussed in relation to information provided by studies carried out under the same light conditions in an invaded area in New Zealand. Shoot elongation, leaf production, stem and leaf biomass per shoot and specific leaf area (SLA, cm2 g-1) were determined in five adult plants, randomly selected in each of three light conditions in two forest sites. Net photosynthesis as a function of PPFD (Photosynthetic Photon Flux Density), stomatal conductance (gs), maximum light-saturated photosynthesis rate (Pmax), Pmass (on mass bases) and water-use efficiency (WUEi) were determined in plants of one site. We predicted that functional traits would differ between populations of native and invasive ranges. In their native area, plants growing under the canopy produced the longest shoots and had the lowest values for shoot emergence and foliar biomass per shoot, while their SLA was higher than gap and forest edge plants. Leaf number and stem biomass per shoot were independent of light differences. Leaves of gap plants showed higher Pmax, Pmass and gs but lower WUEi than plants growing at the forest edge. In its native range B. darwinii grows under different light conditions by adjusting shoot and leaf morphology and physiology. Plants of B. darwinii growing under the same light conditions show similar physiology in native and invasive ranges. This means that for B. darwinii, intra-specific variation of the functional traits studied here do not condition successful spread in new areas.

The genus Cecropia: a biological clock to estimate the age of recently disturbed areas in the Neotropics.

Forest successional processes following disturbance take decades to play out, even in tropical forests. Nonetheless, records of vegetation change in this ecosystem are scarce, increasing the importance of the chronosequence approach to study forest recovery. However, this approach requires accurate dating of secondary forests, which until now was a difficult and/or expensive task. Cecropia is a widespread and abundant pioneer tree genus of the Neotropics. Here we propose and validate a rapid and straightforward method to estimate the age of secondary forest patches based on morphological observations of Cecropia trees. We found that Cecropia-inferred ages were highly correlated with known ages of the forest. We also demonstrate that Cecropia can be used to accurately date disturbances and propose twenty-one species distributed all over the geographical range of the genus as potential secondary forest chronometer species. Our method is limited in applicability by the maximal longevity of Cecropia individuals. Although the oldest chronosequence used in this study was 20 years old, we argue that at least for the first four decades after disturbance, the method described in this study provides very accurate estimations of secondary forest ages. The age of pioneer trees provides not only information needed to calculate the recovery of carbon stocks that would help to improve forest management, but also provides information needed to characterize the initial floristic composition and the rates of species remigration into secondary forest. Our contribution shows how successional studies can be reliably and inexpensively extended without the need to obtain forest ages based on expensive or potentially inaccurate data across the Neotropics.

Remarkable growth pattern in Chrysoglossum ornatum Blume and observations in related species.

The aim of this study was to characterise the remarkable architectural development of the orchid species Chrysoglossum ornatum Blume. Living specimens were collected in two sites in Laos, a country where this species had not been recorded before. Examination of herbarium material of the three other species of Chrysoglossum has confirmed the regularity of this growth pattern at the genus level. Such a vegetative architecture, unique within the plant kingdom, was first described by Barthélémy (1987) for a South American orchid species, Gongora quinquenervis Ruiz and Pav. The nature of this growth pattern within the genus Chrysoglossum and within this particular species, as well as the occurrence of similar patterns in the Orchidaceae is discussed.

Computing competition for light in the GREENLAB model of plant growth: a contribution to the study of the effects of density on resource acquisition and architectural development.

BACKGROUND AND AIMS: The dynamical system of plant growth GREENLAB was originally developed for individual plants, without explicitly taking into account interplant competition for light. Inspired by the competition models developed in the context of forest science for mono-specific stands, we propose to adapt the method of crown projection onto the x-y plane to GREENLAB, in order to study the effects of density on resource acquisition and on architectural development. METHODS: The empirical production equation of GREENLAB is extrapolated to stands by computing the exposed photosynthetic foliage area of each plant. The computation is based on the combination of Poisson models of leaf distribution for all the neighbouring plants whose crown projection surfaces overlap. To study the effects of density on architectural development, we link the proposed competition model to the model of interaction between functional growth and structural development introduced by Mathieu (2006, PhD Thesis, Ecole Centrale de Paris, France). KEY RESULTS AND CONCLUSIONS: The model is applied to mono-specific field crops and forest stands. For high-density crops at full cover, the model is shown to be equivalent to the classical equation of field crop production (Howell and Musick, 1985, in Les besoins en eau des cultures; Paris: INRA Editions). However, our method is more accurate at the early stages of growth (before cover) or in the case of intermediate densities. It may potentially account for local effects, such as uneven spacing, variation in the time of plant emergence or variation in seed biomass. The application of the model to trees illustrates the expression of plant plasticity in response to competition for light. Density strongly impacts on tree architectural development through interactions with the source-sink balances during growth. The effects of density on tree height and radial growth that are commonly observed in real stands appear as emerging properties of the model.

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.

Rhythms and alternating patterns in plants as emergent properties of a model of interaction between development and functioning.

BACKGROUND AND AIMS: To model plasticity of plants in their environment, a new version of the functional-structural model GREENLAB has been developed with full interactions between architecture and functioning. Emergent properties of this model were revealed by simulations, in particular the automatic generation of rhythms in plant development. Such behaviour can be observed in natural phenomena such as the appearance of fruit (cucumber or capsicum plants, for example) or branch formation in trees. METHODS: In the model, a single variable, the source-sink ratio controls different events in plant architecture. In particular, the number of fruits and branch formation are determined as increasing functions of this ratio. For some sets of well-chosen parameters of the model, the dynamical evolution of the ratio during plant growth generates rhythms. KEY RESULTS AND CONCLUSIONS: Cyclic patterns in branch formation or fruit appearance emerge without being forced by the model. The model is based on the theory of discrete dynamical systems. The mathematical formalism helps us to explain rhythm generation and to control the behaviour of the system. Rhythms can appear during both the exponential and stabilized phases of growth, but the causes are different as shown by an analytical study of the system. Simulated plant behaviours are very close to those observed on real plants. With a small number of parameters, the model gives very interesting results from a qualitative point of view. It will soon be subjected to experimental data to estimate the model parameters.

Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny.

BACKGROUND AND AIMS: The architecture of a plant depends on the nature and relative arrangement of each of its parts; it is, at any given time, the expression of an equilibrium between endogenous growth processes and exogenous constraints exerted by the environment. The aim of architectural analysis is, by means of observation and sometimes experimentation, to identify and understand these endogenous processes and to separate them from the plasticity of their expression resulting from external influences. SCOPE: Using the identification of several morphological criteria and considering the plant as a whole, from germination to death, architectural analysis is essentially a detailed, multilevel, comprehensive and dynamic approach to plant development. Despite their recent origin, architectural concepts and analysis methods provide a powerful tool for studying plant form and ontogeny. Completed by precise morphological observations and appropriated quantitative methods of analysis, recent researches in this field have greatly increased our understanding of plant structure and development and have led to the establishment of a real conceptual and methodological framework for plant form and structure analysis and representation. This paper is a summarized update of current knowledge on plant architecture and morphology; its implication and possible role in various aspects of modern plant biology is also discussed.

Bud and growth-unit structure in seedlings and saplings of Nothofagus alpina (Nothofagaceae).

In temperate trees, axis length growth generally results from the differentiation of organs at the end of a growing season and the extension of such "preformed organs" in the next growing season. Neoformation, i.e., the simultaneous differentiation and extension of organs, has been studied for only a few species. Here we evaluated bud composition and growth unit (GU) size for seedlings and saplings of Nothofagus alpina, a valuable South American forest tree. Trunk GUs of seedlings and saplings included preformed and neoformed organs, whereas main-branch GUs of saplings were entirely preformed. The size of a GU was more closely related to the number of preformed green leaves than to the number of cataphylls of its preceding bud. Proximal buds of a trunk GU had more cataphylls and less green-leaf primordia than distal buds. Individual leaf area increased from proximal to distal positions on trunk GUs. For trunk and main-branch GUs, the length/width ratio was maximum for leaves in intermediate positions. The development of large neoformed leaves at the end of the growing season could increase the photosynthetic capacity of this species in late summer, when the activity of preformed organs is likely to be decreasing.

Ontogenetic trends in the morphological features of main stem annual shoots of Pinus pinaster (Pinaceae).

Phase change refers to the transition between juvenile and adult vegetative phases. The study of trees throughout their entire life span requires retrospective analyses and validates the use of a chronosequence by sequencing observations at different and successive stages. The main axis growth pattern of 62 maritime pines (Pinus pinaster) selected in a chronosequence of three stands consisting of 8-, 22-, and 48-yr-old trees was analyzed retrospectively. Comparison of measured features (length, number of axillary products, reproductive organs) at common ages from the three stands supported the validity of using these data to form a continuous chronosequence. Endogenous trends in tree development are revealed free from variability due to annual growth conditions. Two main phases of development corresponding respectively to the juvenile vegetative and adult reproductive stages were identified, and the transition between both occurred in 9-yr-old trees. The relevance of these two phases and more generally the notion of phase changes are discussed in light of observed trends in the values of studied growth and branching parameters that may either show gradual variations (such as length of annual shoot) or a distinctive expression in one or the other phase (such as presence of female cones).

Analysing branching pattern in plantations of young red oak trees (Quercus rubra L., Fagaceae).

Branching patterns of the growth units of monocyclic or bicyclic annual shoots on the main axis of 5-year-old red oaks were studied in a plantation in south-western France. For each growth unit, the production of axillary structures associated with each node was described in the form of a sequence. For a given category of growth units, homogeneous zones (i.e. zones in which composition in terms of type of axillary production does not change substantially) were identified on such sequences using a dedicated statistical model called a hidden semi-Markov chain. For instance, on the first growth unit of bicyclic annual shoots, a zone with 1-year-delayed branches was found systematically below a zone with buds and one-cycle-delayed branches. Branching patterns shown by the growth unit of monocyclic annual shoots and on the second growth unit of bicyclic annual shoots were very similar. Branches with a 1-year delay in development tended to be polycyclic at the top of the growth unit and monocyclic lower down. The number of nodes shown by the branched zone of the growth unit of monocyclic annual shoots was stable, irrespective of the total number of nodes of the growth unit. In contrast, the second growth unit of bicyclic annual shoots exhibited a correlation between the number of nodes in the branching zone and the total number of nodes. The contribution made by this method to understanding plant functioning is discussed.

Synchronization of growth, branching and flowering processes in the South American tropical tree Cecropia obtusa (Cecropiaceae).

Cecropia obtusa Trécul (Cecropiaceae) is a pioneer species associated with the initial phases of regeneration of tropical South American forests. A comparison of the succession of morphological events associated with each node (inflorescences or branches developed or aborted and underlying internode length) making up the axes of 30 trees helped to establish a link between their architecture and the regularity and synchronicity of their expression of growth, flowering, and branching processes over time on an individual and stand level. For a given individual, new nodes are emitted at the same rate on all the axes, irrespective of their branching order. Flowering and branching alternate, and these processes occur in all the axes of the tree synchronously. On a stand level, flowering and branching occur regularly every 35 nodes or so, which apparently corresponds to an annual rhythm. Under nonlimiting conditions, a single branch tier would be emitted each year, and it is thus possible to determine a posteriori the age of a crown accurately. The merits of the method, the possibility of estimating the age of natural Cecropia obtusa regrowth by observing tree architecture, and the possible applications in the field of ecology are discussed.