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. 2009 Nov 8;105(2):205–220. doi: 10.1093/aob/mcp273

Architectural strategies of Cornus sericea, a native but invasive shrub of Southern Quebec, Canada, under an open or a closed canopy

T Charles-Dominique 1,2,*, C Edelin 1,2, A Bouchard 3
PMCID: PMC2814749  PMID: 19900945

Abstract

Background and Aims

Qualitative and quantitative studies of the pattern of invasive plant development is considered a key aspect in understanding invasiveness. An architectural analysis was therefore performed in order to understand the relationship between shoot architecture and invasiveness in red-osier dogwood, Cornus sericea (Cornaceae).

Methods

The structural and ontogenic characteristics of individuals in invading and non-invading populations in the native range of the species were compared to test the implication of developmental plasticity on invasiveness.

Key Results and Conclusions

The results show that the shrub has a modular architecture governed by strong developmental rules. Cornus sericea is made up of two levels of organization, each with its own intrinsic sequence of differentiation. These intrinsic mechanisms were used as a framework for comparison and it was found that, in response to the light environment, developmental plasticity was elevated, resulting in two architectural strategies. This developmental plasticity concerns the growth direction and the size of the modules, the speed of their time-course changes, their branching and flowering. Under an open canopy, C. sericea rapidly develops large vertical structures and abundant flowering. This strategy leads the plant to be invasive by excluding competitors and disseminating in the landscape. In the understorey, C. sericea slowly develops long horizontal structures which creep across the soil surface, while assimilating structures are poorly developed. This strategy does not lead to invasiveness but may allow the plant to survive in the understorey and reach sunny patches.

Keywords: Cornus sericea, Cornus stolonifera, red-osier dogwood, shrub, invasive, architecture, phenotypic plasticity, development, light, human disturbance

INTRODUCTION

Biological invasions are a threat to biodiversity and cause public health problems and major financial losses (Vitousek et al., 1996; Mack et al., 2000; Pimentel et al., 2000; Olden and Poff, 2003). Although invasive plants are a major problem, little is known of the relative importance of the characteristics of the invading plants, the features of the invaded communities and the landscape context in determining invasion success (Bartuszevige et al., 2006; Theoharides and Dukes, 2007). Four main phases have been recognized in plant invasions: transport, colonization, establishment and landscape spread (Williamson, 1996; Theoharides and Dukes, 2007). These phases are determined by an interplay between human activities, abiotic and biotic environmental conditions and the traits of the invasive species itself. Species traits are involved in each of the four phases, and those such as propagule pressure, vegetative reproduction rate, generation time, dispersal and physiological phenotypic plasticity have been studied in depth, but mainly in exotic species that have become invasive after introduction. Few studies have been performed in invasive native species (Goodwin et al., 1999; Schweitzer and Larson, 1999; Chesson, 2000; Kolar and Lodge, 2001; Sakai et al., 2001; Lockwood et al., 2005). Also, plant structure and developmental pattern are rarely taken into account although they determine ramet type, number, disposal and establishment, i.e. the main parameters conditioning plant spatial competitive abilities (Birnbaum, 1994; Baret et al., 2003a, b, 2004). Qualitatively and quantitatively studying the pattern of invasive plant development is now considered key in understanding invasiveness (Kolar and Lodge, 2001; Sakai et al., 2001; Chambel et al., 2005). In this context, several questions remain unanswered: (a) Do invasive plants change their pattern of development when they become invasive? (b) If so, how are these changes modulated throughout ontogeny? (c) What is the influence of the environment on theses changes? (d) Lastly, what structural properties are involved in invasiveness?

In an attempt to address these questions, we chose to work on shrubs, firstly because they are one of the most invasive life forms on all continents (Archer, 1994) and secondly because their structure is that which has been the least studied. Studies have already been performed in south Québec (Canada), to understand vegetation successions on abandoned farmlands and these shed light on about ten shrub species that spread over pastures and previously cultivated fields (Benjamin et al., 2005). Although most of these species are indigenous, they are invasive and inhibit plant successions, thus forming monospecific communities (Meilleur et al., 1994; Canham et al., 1998). The negative impact of these shrub communities has tended to increase with land abandonment over the last few decades (Cogliastro et al., 2006). The present studies focused on one of these shrub species, the red-osier dogwood (Cornus sericea) which is native to this region. This species is of particular interest for, although it is in an equilibrium in natural wetland habitats (Meilleur and Bouchard, 1989; Richburg et al., 2000), it becomes invasive after habitat perturbations such as pasturage (Middleton, 2002a, b), changes in fire frequency (Richburg et al., 2000; Middleton, 2002b) or an increase in soil salt levels subsequent to salt mining (Mustard and Renault, 2004). It develops monospecific populations of up to 100 000 stems per hectare (Meilleur et al., 1994) and is recognized as one of the main plants that inhibits vegetation succession (Meilleur et al., 1998; Véronneau et al., 1998). The ecological situation in south Québec has been the subject of very considerable study. Numerous authors have analysed the anthropic, biotic and abiotic determinants of vegetation cover on a landscape scale (de Blois et al., 2001, 2002; Cogliastro et al., 2006) and factors implicated in tree colonization on a community scale (Meilleur et al., 1997, 1998; Véronneau et al., 1998; Mercier et al., 1999; Paquette et al., 2007). On an individual scale, we were already in possession of a comprehensive description of adult red-osier dogwood (Meilleur and Bouchard, 1993) but its ontogenesis and variations had never been described. The two behaviours of the red-osier dogwood, which is invasive under an open canopy and in equilibrium under a closed canopy, allow the observation of potential modifications in plant structure and ontogenesis. This approach is used to test the hypothesis of a link between developmental patterns and invasiveness related to differences in light conditions.

A comparative architectural study of red-osier dogwood was conducted in the invasive and non-invasive situations. The architectural analysis defines the nature and relative arrangement of each part of the plant. It reveals, at any given time, the expression of an equilibrium between endogenous growth processes and exogenous constraints exerted by the environment (Edelin, 1977; Barthélémy and Caraglio, 2007). The study of the plant architecture considers both the properties of the structural elements, their patterns of development and the ontogeny of the plant throughout its whole life.

In this study, the vegetation type and light conditions in the invasive and non-invasive situations are briefly described. Then the red-osier dogwood architecture is analysed qualitatively and quantitatively and its ontogenesis defined in both situations. These ontogeneses were compared for discussions on the structural and ontogenic plasticity of red-osier dogwood. Lastly, conclusions concerning the link between architectural plasticity, light conditions and invasiveness in red-osier dogwood were drawn.

MATERIALS AND METHODS

Plant material

Red-osier dogwood (Cornus sericea L., syn. Cornus stolonifera Michx.; Cornaceae) is a woody, deciduous multi-red-stemmed shrub. It has simple opposite leaves 5–10 cm long and its white-petal flowers form terminal clusters. They are auto-sterile and pollination is by insects. Seeds are dispersed by birds. Red-osier dogwood is wide-ranging and proliferates in swamps, low meadows, riparian zones, wetlands, floodplains, forest openings and understoreys (Crane, 1989). It grows from sea level up to 2500 m a.s.l. and tolerates very low temperatures. Red-osier dogwood occurs from Alaska to Newfoundland, south to Virginia in the east, to Kansas in the Great Plains, to northern Mexico, in the Rocky Mountains, and through California on the West Coast (Crane, 1989) and is reported as being a major environmental risk in ten European countries (Anonymous, 2008).

Study sites

The study was conducted in the Montreal area (south-western Québec), a region with a humid continental climate. Annual rainfall is between 940 and 1100 mm (Benjamin et al., 2005; Poulain et al., 2007) and average temperatures are −10 °C in January and 20·8 °C in July.

The first site was called ‘site I’; it is a shrubland where C. sericea forms dense and massive invasive communities (Meilleur et al., 1994, 1998). It constitutes a right-of-way for electricity power lines in Haut-Saint-Laurent Municipalité Régionale de Comté (MRC) located in the south-western part of the province of Quebec, Canada, between the Saint Lawrence River to the north and the state of New York, USA, to the south (45°05'2''N; 74°15'9''W). The regional bedrock is mainly composed of Beekmantown dolomite and Postdam sandstone. These moraine deposits are occupied by eluvial brown soils and podzols (Meilleur et al., 1997). The corridor under the right-of-way was fully cleared in 1977 to a width of 60 m (Mercier et al., 1999).

The second site was called ‘site NI’ because of the non-invasive behaviour of C. sericea that fits into the vegetation. Samples at site NI (45°59'4''N; 73°59'9''W) were taken around Cromwell Lake in a forest which belongs to the University of Montréal Laurentides station, and is located 75 km north of Montreal. The soil here is composed of 1–5 m of glacial deposits on a granite base. The site is protected with no interventions apart from road maintenance.

Measurement of vegetation status and canopy openness

A rough qualitative and quantitative characterization was made of the vegetation interacting with C. sericea and its light status in order to substantiate our main hypotheses concerning differences in vegetation successional status. The context of the shrub and tree species in the vegetation surrounding the red-osier dogwood was characterized in 12 different samples of 10-m circular quadrats at each site. Quadrats were centred on red-osier dogwood individuals with at least 20 m maintained between them to avoid pseudoreplication. The presence of shrub and tree species and the number of individuals or patches (for shrubs) were documented by species. At both sites, the dominant species (present in more than one-third of the sites) were documented in order to specify vegetation associations and the proportion of individuals divided into three type classes (conifers, deciduous trees or shrubs). These data were compared with the literature (White, 1965; Légaré et al., 2001; Savage, 2001; Middleton, 2002a) to determine vegetation status. Species were determined using the Flore Laurentienne (Marie-Victorin, 1995).

Lastly, canopy openness was estimated at both locations over 12 different samples at least 20 m apart. Canopy openness was measured by means of a concave spherical densiometer (Forest Densiometers, Arlington, VA, USA). A study previously conducted in Quebec in different biomes showed that the results obtained by this method were closely correlated with the global light index (A. Paquette et al., University of Montréal, Canada, unpubl. res., 2006). Similar results have been obtained for other forest types (Comeau et al., 1998; Englund et al., 2000). Finally a close correlation has been demonstrated between openness measurements taken by hemispherical photographs and the densiometer (Ferment et al., 2001). Therefore the results obtained by this method were used to discuss the effect of the canopy openness and light conditions on plant growth.

Architectural analysis

General principles

The architectural analysis of C. sericea was performed according to the concepts and methods initiated by Hallé and Oldeman (1970), Hallé et al. (1978), modified by Edelin (1984, 1990) and Barthélémy et al. (1989, 1991), and more recently revisited by Barthélémy and Caraglio (2007). The method consists of (a) selecting individuals at various developmental stages from seedling to adult to senescent individuals and (b) qualitatively and quantitatively describing the structure of all stems, in each individual and at each stage of development, in order to identify axis categories which constitute the organism, and to highlight the possible repeated structures within the organism. In a given environment, the species' development pattern is then deduced from a comparison of the architectures shown at each growth stage.

Selection of growth stages

Growth stages are defined a priori on the basis of precise and objective morphological criteria, but which may vary depending on the species studied. Cornus sericea is composed of relays which succeed over time (Meilleur and Bouchard, 1993). Thus, each stage was defined by the emergence of a new relay. Using this criterion for all individuals provided a rigorous framework for comparison; changes in the rate of expression stages prohibited any comparison of plants with the same absolute ages (Wright and McConnaughay, 2002).

Plant age

Plant age was estimated a posteriori for each individual by counting the number of growth units (Barthélémy and Caraglio, 2007). In this species, each growth unit is usually equivalent to 1 year. The age of the oldest individuals, which had lost part of their structures, was estimated by comparison and cross-checking with younger individuals' structures.

Qualitative and quantitative morphological descriptors

To describe plant axes (sensu Barthélémy, 1991), the morphological descriptors prescribed for the architectural analysis were used with the following diagnostic qualitative descriptors being selected: monopodial or sympodial structure, determinate or indeterminate growth, growth direction (plagiotropy/orthotropy), symmetry, shape and reiteration ability. Concerning shape, conicity corresponds to a basal/distal difference in diameter of ≥10 %. Cylindrical-shaped axes were defined when this difference was <10 %. In order to complete and reinforce the morphological observations, quantitative variables were acquired using the following descriptors: length of growth unit and axes, number of leaves per growth unit, number of growth units by axis and basal diameter. The reported diameter is the mean diameter of axes at the end of their development. Lastly, the results were summarized in the form of architectural tables.

Graphic expression of the results

Each plant was drawn, but in results given below, only the drawing that corresponded to the most representative individual selected is shown, such that its properties are similar to the mean quantitative values for the stage. An interpretative scheme of the representative individual was drawn up to explain its structure. On this scheme only the main structural entities were represented. When an event occurred in several individuals at the same stage, but not in the described individual, this is still noted in the text.

Sampling

At site NI, 47 individuals aged 1 year to about 35 years were described and measured, with all individuals encountered in the area being studied. At site I, 82 individuals aged 1–30 years were selected in order to obtain at least 30 measures by axis category and described stage.

Statistical analysis

The different axis categories were separated on the basis of their morphological traits, and this was confirmed by non-parametric statistical tests: Kruskal–Wallis test (null hypothesis, Ho: no difference between groups) or multiple tests of equal or given proportions (with the same null hypothesis). Multiple comparison tests using Bonferroni correction (or Holm correction for proportions) were performed to indicate grouping of axis types. Non-parametric tests were used because homoscedasticity was not verified. Mean values were used for all measured parameters and in order to detect global differences between axis types, and not only differences due to developmental stages, variables for all ontogenic stages were processed together. Significance of tests was reported as ‘*’ for a P-value <0·05, by ‘**’ for a P-value <0·005 and by ‘***’ for a P-value <0·0005. The same procedure was applied to determine the plastic responses when comparing axis types between the two sites.

Then changes in axis category parameters among successive structural units were studied, firstly using a Kruskal–Wallis test (null hypothesis, Ho: no difference between ontogenic stages). If the result was a non-significant difference between the stages, it was concluded that no change had occurred in the parameter. When the result was significant, the effect of the structural unit's rank on the parameters was tested using a non-parametric regression (Ho: rank had no effect on the parameter; Bowman and Azzalini, 1997) and the sign of the slope of the regression line reported. If the effect was significant and the slope was positive, it was concluded that the parameter increased among successive structural units. Otherwise, it was concluded that the parameter decreased among successive structural units. Then the changes in the parameters among successive structural units for the two sites were compared using a non-parametric ANCOVA (Ho: parallel regression surfaces for parameter values between conditions; Young and Bowman, 1995). It was concluded that changes were the same when the tests were non-significant and that changes were different when the tests were significant.

RESULTS

Canopy openness and vegetation status

Site I, where red-osier dogwood is invasive, is dominated by shrubs species such as Rhamnus cathartica which was found in 92 % of the quadrats (0·92) and Salix discolor (0·58). Shrub individuals accounted for 64·5 % of the shrub and tree population (Table 1). This site has a widely open canopy, with on average 90·1 % openness.

Table 1.

Comparison of vegetation composition (in number of individuals per site) and canopy openness (percentage) between site I and site NI

graphic file with name mcp27309.jpg
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Shrubs do not include C. sericea. The number of C. sericea per site does not include the individuals on which the quadrats were centred.

Site NI, where red-osier dogwood fits into the vegetation, is dominated by coniferous trees such as Picea mariana (0·5), Abies balsamea (0·42) and Thuja occidentalis (0·33), and deciduous trees such as Acer rubrum (0·67) and Betula papyrifera (0·42). Dominant species also included a shrub which is also usually found in the understorey: Viburnum cassinoides (0·58). Conifer trees and deciduous trees accounted for 46·5 % and 39·4 % of the global population (Table 1). This site had a closed canopy with on average 27·5 % openness.

Canopy openness and vegetation composition in terms of shrubs and trees were significantly different at the two sites (Table 1). Site I, where red-osier dogwood is invasive, was in a typical early vegetation successional status of disturbed habitats; while site NI, where red-osier dogwood fits in the vegetation, was in a late successional status.

Qualitative architectural analysis

Stage 1

At site I, the seedling shows an orthotropic monopodial conical-shaped stem with opposite phyllotaxy and radial symmetry (Fig. 1A). Its growth is rhythmic with growth units, separated by leaf scars, bearing four or five pairs of leaves. After about 3 years (Fig. 1B), the stem is 10 cm tall and it dies terminally. Two kinds of branching occur, both 1-year differed:

  1. Lateral branching along the stem which produces ageotropic short shoots located in an acrotonic position on its growth units. These short shoots have only one or two pairs of leaves disposed in a horizontal plane; their diameter is very small, and they prune when they are 1 or 2 years old.

  2. Subterminal branching which gives rise to one or two opposite new orthotropic stems with the same structure and development as that from which they are derived. Then, at around the 5th year, the 10- to 12-cm-tall plant is an erected sympodium composed of two or three similar ‘modules’ (Hallé and Oldeman, 1970). A module is an axis that has a determinate growth. It is the elementary unit of a sympodium.

Fig. 1.

Fig. 1

Fig. 1

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Ontogenic stage description of plants growing under an open canopy (site I): (A) 1-year-old plant (stage 1); (B) 5-year-old plant (stage 1); (C) 7-year-old plant (stage 2); (D) 13-year-old plant (stage 3); (E) module organization in 13-year-old plants (stage 3); (F) 25-year-old plant (stage 4). Abbreviations: Co, collar; Tap, taproot; Adv, adventitious root; BC, branched complex; mod, module. In schematic views, continuous lines represent structuring axes, spears are delayed axes, dotted lines represent helpers, crosses are dead apices, grey shading indicates BCs and circles are inflorescences.

At site NI, the seedling (Fig. 2A) has the same structure as at site I. It is an orthotropic monopodial conical-shaped stem with opposite phyllotaxy, radial symmetry and rhythmic growth. But, unlike site I, its apex dies without producing subterminal branches; further, after 2 or 3 years, this young plant collapses in its entirety onto the ground.

Fig. 2.

Fig. 2

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Ontogenic stage description of plants growing under a closed canopy (site NI): (A) 3-year-old plant (stage 1); (B) 5-year-old plant (stage 2); (C) 13-year-old plant (stage 3); (D) 15-year-old plant (stage 3); (E) 27-year-old plant (stage 4). Abbreviations: Tap, taproot; Adv, adventitious root; BC, branched complex; mod, module. In schematic views, continuous lines represent structuring axes, spears are delayed axes and crosses are dead apices.

Stage 2

In this stage, at site I, the plant (Fig. 1C) is a regular dichasial sympodium with three levels of erected acrotonic modules which decrease in size from the base to the periphery. Each module is a small monopodium with a main stem bearing lateral short shoots and dying terminally. When it reaches approx. 15–20 cm tall, the sympodium halts its apical development and constitutes as a whole an acrotonic branching system which will be referred to hereinafter as a ‘branched complex’ (BC).

Laterally on this branched complex the plant develops a long, thick and fast-growing orthotropic module which grows out of a dormant bud located basically on a growth unit of a basal module of the branched complex. At this stage this long axis is not yet branched.

At the same stage, at site NI, the collapsed axis of the young plant decays almost entirely except for its basis which remains alive. This part bears laterally a fast-growing orthotropic stem generally derived from one of the dormant cotyledonary buds (Fig. 2B). This basitonic originating axis is the first module of an erected sympodial branched complex composed of orthotropic modules with definite growth, similar to that observed at site I.

Stage 3

At site I, when the plant is about 13 years old, it consists of four branched complexes initiated one after another. The first, derived from the seed and described above, is the smallest. Only its first module is still alive, the others have died and have been naturally pruned away. It bears lateral adventitious roots where the stem is in contact with the soil and acts as a stock for the other branched complexes. Near its base is located the secondly occurred branched complex (BC2). Only two alive modules remain on this sympodium, the others have died and fallen off. Its short shoots have been pruned. The third branched complex (BC3) is a sympodium with three successive series of modules. At the same level on the stock is the 4th branched complex (BC4) which is the newest and largest on the plant. It has four successive series of long modules which are progressively shorter and smaller in diameter. Its modules are small monopodia, which bear short shoots and twigs laterally disposed in an acrotonic position on their growth units (Fig. 1E). The twigs are orthotropic axes with rhythmic growth and opposite phyllotaxy. They have bilateral symmetry, are smaller in diameter, bear fewer leaves, and are shorter than the stems. They are located near the top of the modules' growth units. The short shoots are similar to those described above.

The plant also shows two kinds of recently occurred axes derived from dormant buds located in a basitonic position on the main branched complexes. The first corresponds to a few orthotropic axes that are large in diameter and possess long growth units with numerous internodes. These are the first modules of future branched complexes. The second kind corresponds to short-lived orthotropic axes that are small in diameter and possess short growth units. These often die without branching or sometimes with only one level of small subterminal modules. They are numerous and contribute to increasing the photosynthetic surface of the plant without participating in its edification. They are called ‘helpers’.

At site NI, the plant is also made up of three branched complexes (Fig. 2C and D) increasing in size from one to the other and bearing a few helpers. However, the collapse of the stems, which occurs in the first growth stage, partly alters the regularity of this structure. In each branched complex, only the modules in contact with the soil and producing adventitious roots remain alive. Others, which are more or less erected, die and decay in a few years such that only the most recent ones are still present at the periphery of the plant. Further, the development of new branched complexes does not proceed from the base of the whole plant but from the base of the last branched complex. This behaviour leads to the differentiation of a sympodial stoloniferous axis that creeps across the soil. At this stage the stems produce lateral short shoots but no twigs.

Stage 4

At around 25 years old at site I, the plant is approx. 2·0 m tall and is composed of a stock supporting three or four branched complexes. The stock includes the base of the module derived from the seed and the base of former branched complexes. Because the whole plant is complex to represent, and because the branched complexes are similar in structure, only the newest and the largest is represented and described (Fig. 1F). The plant is a sympodium branched up to the 6th order of subterminal modules. Modules are orthotropic monopodia laterally bearing twigs and short shoots. The twigs are rhythmically ramified and laterally bear short shoots in an acrotonic position. At this stage, the plant flowers profusely; inflorescences are terminal on stems, twigs and short shoots. Helpers occur within the entire structure of the branched complexes. This is considered to be the last stage of development because all types of structure are expressed and also because subsequent branched complexes, emitted from the stock, show the same qualitative and quantitative properties as this described branched complex.

At site NI, and around the same age (27 years), the plant is also made up of branched complexes of increasing size but their maximum height is smaller than at site I. There is no single stock but a stoloniferous, sympodial, irregularly forked axis, already mentioned for the previous stage, with several rooting zones mainly located at the junction between horizontal and erected modules. Its oldest part, derived from the seed, shows necrosis, as do all the lateral modules and the short shoots associated with this sympodial creeping axis. It supports one or two erected or semi-erected distal branched complexes derived one from another. The largest one reaches only five orders of subterminal modules with lateral twigs and short shoots. Only some stems and twigs are able to bear inflorescences terminally.

Table 2A outlines the qualitative properties of stems, twigs and short shoots for the plants present at both sites.

Table 2.

Architectural table of red-osier dogwood

Stem
 Twig
 Short shoot
Site I (1) Site NI (2) Site I (3) Site NI (4) Site I (5) Site NI (6) Grouping
(A) Qualitative properties
Growth direction Orthotropic Orthotropic to oblique Orthotropic Ageotropic –
Symmetry Radial Bilateral Bilateral –
Pruning Long term (3–12 years) Medium term (2–3 years) Short term (1 year) –
Secondary growth Extensive Restricted None –
Shape Conical Cylindrical Cylindrical –
Adventitious rooting ability Yes No No –
Reiteration ability Yes Yes No –
Flowering ability Yes Yes Yes ? –
Branched axis Yes No → yes No –
Branching rhythm Rhythmic → continuous Not ramified → rhythmic Not ramified –
(B) Quantitative properties
Observed flowering frequency 0·1 0·02 0·03 0·01 0·01 0 1; 2–3–4–5; 3–4–5–6
Basal diameter of axis (mm) 2·55 ± 0·98 3·22 ± 1·12 1·01 ± 0·13 1·03 ± 0·08 0·61 ± 0·11 0·58 ± 0·09 1; 2; 3–4; 5–6
Growth unit length (cm) 8·82 ± 7·11 11·23 ± 8·32 1·33 ± 0·44 1·42 ± 0·52 0·25 ± 0·12 0·2 ± 0·07 1; 2; 3–4; 5–6
Leaf no. by growth unit 5·55 ± 1·31 6·38 ± 1·92 3·29 ± 0·77 3·54 ± 1 1·79 ± 0·59 1·63 ± 0·48 1; 2; 3–4; 5–6
No. of growth unit by axis 2·29 ± 0·89 3·1 ± 1·41 1·79 ± 0·79 1·41 ± 0·66 1 ± 0 1 ± 0 1; 2; 3; 4; 5–6
Length of axis (cm) 20·95 ± 21·37 37·41 ± 39·61 2·38 ± 1·5 2·06 ± 1·09 1·79 ± 0·59 1·63 ± 0·48 1; 2; 3–4; 5–6
Maximal observed diameter (mm) 9·55 7·88 1·3 1·23 0·86 0·89 –
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Quantitative architectural analysis

Axis categories

Quantitative analyses were used to distinguish different axis categories (stem, twig and short shoot) in each module. Then the effectiveness of these differences was verified by statistical tests on the quantitative parameters relative to the axis categories. Results for diameter and length are illustrated in Fig. 3 which shows basal diameters and lengths for growth units on the three axis categories at both sites. All the quantitative and qualitative parameters used to distinguish the axes are given in Table 2B. Multiples comparison tests were used to group the diameter and length distributions. This showed that diameters and lengths for the three axis categories were significantly different at both sites (Fig. 3). The same approach was used to distinguish the axis categories as based on quantitative parameters, and the results are outlined in Table 2B. They show, at both sites, that stems, twigs and short shoots belonged to different groups, i.e. growth unit length, number of leaves by growth unit, diameter, number of growth units by axis and flowering frequency on the three axis categories were significantly different. Firstly, these results show that, in addition to possessing different qualitative properties, the axes also had significantly different quantitative properties, and, secondly, that the parameters associated with each axis category were organized in a similar manner: all the axis categories showed a decrease in their quantitative parameters from the stem to the short shoots (Table 2B).

Fig. 3.

Fig. 3

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Quantitative parameters relative to axis categories: mean, standard deviation and extreme values. Grouping is indicated by letters a, b, c and d. ‘S. shoot’ = short shoot.

Moreover, it appears (Table 2B) that distributions of stem parameters were significantly different at site I and site NI, i.e. the stems were thicker, had longer growth units and axes, were composed of a larger number of growth units and bore more leaves at site NI than at site I. Mean diameter was greater at site NI but increased more rapidly at site I; thus, the largest diameter observed was greater at site I than at site NI. Distributions of twigs and short shoots were not significantly different for any quantitative parameters between site I and site NI. The only exception to this concerned the number of leaves borne by twigs; twigs at site NI bore significantly fewer leaves than twigs at site I.

Intrinsic morphogenetic gradients

At both sites, the time-course changes observed in the quantitative properties (diameter, length of growth unit, number of pairs of leaves and number of growth unit by axis) of the different axis categories were studied among successive modules in a branched complex. Then these time-course changes were compared with those of one or two other complexes. Lastly, time-course changes in the quantitative properties of axis categories on the first module were studied from the first branched complex to the last. The procedure is illustrated in Fig. 4 for changes in stem length at site I.

Fig. 4.

Fig. 4

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Time-course changes in stem length in branched complexes and from one branch complex to another in plants growing under an open canopy (site I).

(1) Time-course changes in axis categories properties in branched complexes. A significant decrease in all stem quantitative parameters was observed at both sites (Table 3) for the successive modules on a branched complex (tested on the modules of the 3rd branched complex at site I and the 9th branched complex at site NI to generate sufficient data). At site I, the stem parameters for successive modules were compared from the 3rd to the 1st and 5th branched complexes and showed similar time-course changes (Table 3). The twigs and short shoots on the successive modules within a branched complex (tested on the modules of the 3rd branched complex at site I and the 11th branched complex at site NI) did not show any significant time-course changes in their quantitative parameters at either site (Table 3). The parameters relative to the twigs and short shoots on successive modules among the branched complexes were similar at the two sites (tested on the modules of the 3rd and 4th branched complexes at site I and the 11th and 12th branched complexes at site NI). To sum up, the quantitative parameters for stems on successive modules from the base to the periphery of the complexes decreased in value, while the parameters for twigs and short shoots remained constant.

Table 3.

Time-course changes in the quantitative properties of different axis categories in branched complexes

No. of data by module Length Diameter No. of leaves pairs Growth unit no. by axis
Stem
Site I 3rd BC 30 Decrease** Decrease** Decrease* Decrease***
Parallelism Yes Yes Yes Yes
Site NI 9th BC 30 Decrease* Decrease*** Decrease* Decrease***
Parallelism Not tested Not tested Not tested Not tested
Twig
Site I 3rd BC 30 No evolution No evolution No evolution No evolution
Parallelism Yes Yes Yes Yes
Site NI 11th BC 15 No evolution No evolution No evolution No evolution
Parallelism Yes Yes Yes Yes
Short shoot
Site I 3rd BC 30 No evolution No evolution No evolution –
Parallelism Yes Yes Yes –
Site NI 11th BC 11 No evolution No evolution No evolution –
Parallelism Yes Yes Yes –
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‘Parallelism’ tests whether changes in quantitative parameters are the same by comparing the 3rd BC with the 1st and the 5th BC for stems at site I, the 3rd BC to the 4th BC for twigs and short shoots at site I and the 11th BC to the 12th BC for twigs and short shoots at site NI. Significant differences are indicated: * P < 0·05; ** P <0·005; *** P < 0·0005.

(2) Time-course changes in the properties of axis categories in successive branched complexes. A significant increase was noted at both sites in the quantitative parameters of the stems for the first modules of successive branched complexes (Table 4). The only exception to this was at site NI where the diameter of the first modules of successive branched complexes did not change over time. The twigs and short shoots on the first modules of successive branched complexes (tested on the modules of the 3rd and 4th branched complex at site I and the 11th and 12th branched complex at site NI) did not show any significant time-course changes at either site (Table 4). To sum up, the quantitative parameters of stems on the first modules increased from the first to the last complexes while the quantitative parameters of twigs and short shoots remained constant.

Table 4.

Time-course changes in the quantitative properties of axis categories from one branched complex to another

No. of data by module Length Diameter No. of leaves pairs Growth unit no. by axis
Stem
Site I 1st BC to 5th BC 30 Increase*** Increase*** Increase*** Increase**
Site NI 1st to 12th BC 30 Increase*** No evolution Increase*** Increase***
Twig
Site I 3rd to 4th BC 30 No evolution No evolution No evolution No evolution
Site NI 11th to 12th BC 15 No evolution No evolution No evolution No evolution
Short shoot
Site I 3rd to 4th BC 30 No evolution No evolution No evolution –
Site NI 11th to 12th BC 11 No evolution No evolution No evolution –
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Significant differences are indicated: ** P <0·005; *** P < 0·0005.

Then tests were carried out to see whether changes in quantitative parameters of the stems, for the first modules of successive branched complexes, are the same or not between site I and site NI (see Fig. 5 for slowing of ontogenesis = 1). It was found that length, diameter and number of leaf pairs increased significantly faster (at 10 % level of significance) when plants grew under an open canopy than under a closed canopy; while the number of growth units by stem was unaffected by canopy openness.

Fig. 5.

Fig. 5

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Slowing of ontogenesis in plants growing under open and closed canopies: slowing of ontogenesis corresponds to the number of times the increase in stem parameters under an open canopy was greater than the increase in stem parameters under a closed canopy. The homology hypothesis is the equality of changes in the two sites. The grey shading indicates the range of slowing for which the homology hypothesis was validated (not rejected) for a maximum of parameters.

Following on from this the aim was to quantify the slowing of ontogenesis (changes of stem quantitative parameters from one branched complex to another) from site I to site NI. For both parameters, the ontogenesis of site I was artificially slowed down from 1- (no slowing) to 5-fold (the ontogenesis of plants growing under an open canopy is slowed 5-fold) and this slowed ontogenesis compared with the real ontogenesis at site NI (Fig. 5). It appeared that from one complex to another, length increased approx. 1·7 times faster, diameter increased approx. 2·2 times faster and the number of leaves increased approx. 2·5 times faster when plants grew under an open rather than a closed canopy. By considering these three variables together, it was possible to approximate the effective slowing of ontogenesis and this corresponds to the range of slowing for which the three variables are not significantly different in sites I and NI. Considering these three variables together, ontogenesis was 2·1- to 2·6-fold slower in plants growing under a closed canopy compared with an open canopy.

Number of axes by branched complex

Plants under an open canopy possessed branched complexes that bore significantly more axes than those under a closed canopy (Wilcoxon test; Ho = equality of their distribution; P-value = 0·0019). At both sites, the number of axes borne by branched complexes increased by means of exponential growth from one complex to another (Fig. 6). The ratio of the slopes of the linear regressions was calculated after log transformation (for site I, R2 = 0·7505; for site NI, R2 = 0·7927) in order to specify to what degree the increase was more rapid under an open canopy than under a closed canopy. The result was that the number of axes borne by branched complexes increased 10-fold over a time lapse that was approx. 3·22 times shorter under an open canopy than under a closed canopy (ratio = 3·22).

Fig. 6.

Fig. 6

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Time-course changes in the number of axes by branched complex (logarithmic scale)

DISCUSSION

Red-osier dogwood architecture

The comparison of the qualitative and quantitative results given by the architectural analysis of C. sericea between the successive ontogenic stages allows the species ontogenesis to be outlined. It implies three main events:

  1. The setting up of an acrotonic and sympodial branched complex (BC) composed of monopodial modules with three axis categories: the stem, which is a long, thick, long-lived and adventitious root-bearing exploration axis; twigs and short shoots, both of which are thin and short-lived exploitation axes (Johnson and Lakso, 1986; Lauri and Kelner, 2001)

  2. The repetition of these branched complexes by delayed basitonic branching, with a progressive increase in their size and complexity (module number, length, diameter, branching, etc.) up to a stabilization phase

  3. The formation of helpers, which are small, short-lived modules with delayed development from a dormant bud, occurring randomly in space and time. These complement plant architecture by adding small branched complexes on the different parts of the organism during the senescence phase of branched complexes. These helpers correspond to the epicormic branches described by Nicolini et al. (2003) in beech trees.

However, even if this general pattern is always observed, ontogenic modality expressions vary with the plant's environment.

Under an open canopy (Fig. 7), all the modules have a vertical growth direction which results in the edification of vertical branched complexes. A single stock is set up from the axis derived from the seed and from the juxtaposition of the basal part of successive branched complexes. The upper part of the oldest branched complexes dies and undergoes necrosis. This necrosis is accompanied by the emission of helpers on the first modules of the branched complex, extending its lifespan. The branched complex rapidly increases in size and this generates highly branched structures. Flowering occurs approx. 10 years after germination and becomes abundant by rapidly spreading to all axis category apices.

Fig. 7.

Fig. 7

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Ontogenesis under open and closed canopies: numbers correspond to the emission rank of the branched complexes; solid numbers are living branched complexes and open numbers are necrosed branched complexes.

Under a closed canopy (Fig. 7), the branched complexes collapse and thereafter are composed of two parts: (1) a horizontal part made up of one or two modules, which roots and lengthens considerably; (2) a vertical part made up of all the other modules.

The succession of branched complexes is generated from dormant buds of collapsed modules. This gives rise to creeping sympodial, stoloniferous axes whose oldest parts die and disappear. Simultaneous development of several branched complexes can periodically form forks that allow the plant to occupy a broad surface area. The initial stock formed by the axis derived from the seed is rapidly replaced by secondary stocks, set up from adventitious rooting zones, in particular at the junction between horizontal and vertical modules. The helpers can scarcely occur close to these stocks. The branched complexes very slowly increase in size and lead to poorly branched structures. Flowering occurs first on 15 year-old-plants but is sparse and restricted to few axes.

Considerations concerning the shrub form of Cornus sericea

This architectural analysis confirmed that C. sericea is an authentic shrub as defined by Troll (1937) and Rauh (1938). In fact, it is a lignified plant constructed of axes that succeed one another by basitonic branching. Throughout this succession, the axes which are initially small and have a short lifespan grow larger and more branched, until a stabilization phase is reached. This growth pattern has been called ‘establishment growth’ by Tomlinson and Esler (1973). However C. sericea has the particularity of expressing two distinct shrub forms depending on its environment. Under an open canopy, it is a tree-like shrub (Troll, 1937; Rauh, 1939; Küppers, 1989). This term refers to a plant with stems, derived from basitonic branching, which show individual acrotonic behaviour, establishing erect or partially inclined, large branched complexes. Species frequently cited are Sambucus nigra, Coryllus avellana, and several species of Prunus and Rhamnus. When C. sericea grows under this form, each element of its vegetative structure is an orthotropic branched complex constructed by subterminal and sympodial branching similar to plants in Leeuwenberg's architectural model (Hallé et al., 1978). These branched complexes can reach 2·70 m in height (White, 1965).

Under a closed canopy, C. sericea is a stoloniferous shrub. By this term, Rauh (1938) refers to plants that have axes with a more or less long plagiotropic proximal part and an erect distal part, frequently acrotonic. Axes succeed by basitonic branching at the curvature zone between the proximal and the distal parts. Cited species of this shrub form include Symphoricarpus racemosus, Euonymus europaeus and Cornus suecica (Rauh, 1938). In the understorey, C. sericea conforms to this shrub form: every stolon is a collapsed axis corresponding to one of the modules of a branched complex. Erect parts of the plant are not derived from curvature zones but are orthotropic sub-parts of the branched complexes. Under this form, C. sericea rarely exceeds 1 m in height.

This expression of two shrub forms shows that this species is endowed with very considerable phenotypic plasticity. Although a genetic study of C. sericea populations was not performed, it is hypothesized that the populations at the two study sites are genetically homogeneous and that the differences observed can be explained by phenotypic plasticity. This hypothesis is based on the observation that the plants have similar leaves and flowers. Some general observations, not shown in the results, provide evidence that differences lie on plastic responses to its environment. First, it was observed that when individuals in the forest understorey reached fully sunlit areas, they switched to their typical development in an open habitat. Likewise, in open-canopy situations, the individuals least exposed to sunlight showed a creeping behaviour.

Variations induced by environment

Phenotypic plasticity occurs at the two structural units or levels of organizations (Barthélémy, 1991; Barthélémy and Caraglio, 2007): modules and branched complexes. It was noted that many biotic and abiotic factors varied at the two study sites which may explain the shape changes. However, it is believed that the light environment was essentially responsible for the main differences observed in C. sericea behaviour. First, the variations observed at the module scale match the results obtained in eco-physiological studies of shade-induced reactions. For example, King (1998) showed that shade induced a horizontal growth direction of axes in a study of 58 rain forest species. Child et al. (1981) linked the lengthening of modules of Chenopodium album to vegetational shade. Huber and Stuefer (1997) also demonstrated that the stoloniferous herb Potentilla repens produces significantly fewer branches when shaded. In their review of shade-induced variations, Smith and Whitelam (1997) included these above-mentioned variations in the ‘shade avoidance syndrome’ and explain that they are induced by the qualitative and quantitative properties of light. In the understorey, these modifications are due to a decrease in light intensity, a horizontal light direction (Matsuzaki et al., 2007) and a low red : far red ratio (Miner et al., 2005; Valladares et al., 2007).

On the other hand, it was observed in C. sericea, considered on the whole plant scale, that ontogenesis was slowed in the understorey. In their study on Araucaria araucana, Grosfeld et al. (1999) showed that a slowing of ontogenesis is a response to shade. Lastly, the development of large, vertical structures composed of numerous modules as observed in red-osier dogwood growing at man-disturbed sites, has similarly been described in three shrubby species of Viburnum spp. by Picket and Kempf (1980) who linked this behaviour to a response to a high-light environment. It may therefore be concluded that the two different forms of behaviour in C. sericea are effectively induced by the plant's light environment.

Architectural strategies and implications for invasiveness

The results show that the level of organization is modulated by the light environment, and, by considering all these modifications together, it is possible to define two architectural strategies (Fig. 8).

Fig. 8.

Fig. 8

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Red-osier dogwood architectural strategies.

The first architectural strategy is expressed under an open canopy, and lies on extensive spatial occupation and flowering. Extensive spatial occupation is achieved by the setting up of vertical, highly developed structures. According to Meilleur et al. (1994), these properties of red-osier dogwood prevent neighbouring tree species from germinating and developing. A study on Microstegium vimineum (Claridge and Franklin, 2002) also established a link between competitive abilities and investments in spatial occupation structures. Under an open canopy, the second trait that allows red-osier dogwood to be a strong competitor is the rapid rate of its establishment growth (2·1–2·6 times faster than in the understorey). In fact in a disturbed environment, light competition between species rapidly increases (Valladares et al., 2003), such that the best competitor is the one which first emits its efficient structures of spatial occupation (Bazzaz, 1979; Schlichting and Smith, 2002; Valladares et al., 2007). Miner et al. (2005) emphasized the role played by the speed of growth by underlining that the population can only survive if individual responses are faster than environmental changes. As seen before, red-osier dogwood under an open canopy sets up a dense crown but with low lateral development. The setting up of highly branched structures is accompanied by high-flowering frequency. The plant spreads in the landscape only because of its abundant flowering that is >5 times higher than in understorey. It is believed that all these properties, expressed in invaded sites, are responsible for the observed invasive behaviour of red-osier dogwood (Meilleur et al., 1994, 1998; Véronneau et al., 1998; Richburg et al., 2000; Middleton, 2002a, b).

The second architectural strategy expressed under a closed canopy lies on shade avoidance and survival. Plants emit long and horizontal axes that root and give rise to many stocks. This allows the plant to achieve great lateral exploration. As in the crown of a tree, the branching occurs preferentially in the more exposed areas to sunlight (Takenaka, 1994). At the same time, the vertical structures set up show little development (number of modules and branching) and produce few inflorescences. In this manner the plant sets up low-cost vertical structures and develops horizontal structures so that it can migrate to a more favourable area. This architectural strategy may be considered as a waiting status (Heuret et al., 2000) until opening occurs and the plant can express its full developmental potential. Individuals were observed that switched their development from this understorey architectural strategy to the open canopy strategy at the interface between closed and open canopy stands. Moreover, this hypothesis is consistent with the fact that C. sericea is known as a species well adapted to invading cleared areas after water-level fluctuations (Hudon et al., 2006). Here, the expression of the two functions of developmental plasticity were observed: in favourable environmental conditions, plasticity allows the plant to maximize its capacities while, in unfavourable environmental conditions, plasticity allows the plant to survive (Novoplansky, 2002). In this manner, the plant can survive in a great variety of habitats and invades disturbed habitats (Sultan, 2003, 2004).

CONCLUSIONS

The architectures of invasive and non-invasive red-osier dogwood were compared to distinguish species invariant characteristics from traits expressed when the plant becomes invasive. Concerning species invariant characteristics, C. sericea is a modular plant which expresses two levels of organization associated with their morphogenetic gradient: the module and the branched complex. These two levels of organization associated with their morphogenetic gradient underline the importance of ontogenesis in the variations noted for the qualitative and quantitative properties of plant parts. The results confirm that this ontogenic effect must be described and considered if the effect of phenotypic plasticity is to be evaluated (Diggle, 2002; Wright and McConnaughay, 2002; Young et al., 2005; Guédon et al., 2007). Although the developmental sequence in C. sericea is similar in invasive and non-invasive plants, this sequence is highly modulated by the light environment. Plastic responses in different ways concern the different scales of the plant and highlight the necessity to study the plant simultaneously at the internode, growth unit, axis and whole plant scales (Barnola, 1970; Barthélémy and Caraglio, 2007). Architectural analysis is a pertinent method for studying and summarizing ontogenetic variations at different plant scales. These variations determine two architectural strategies. Non-invasive red-osier dogwood prefers a slow, lateral manner of development. This is a waiting status, allowing the plant to reach a more favourable environment. Invasive red-osier dogwood rapidly expresses vertical, highly developed structures that produce many inflorescences and exclude other species. This strategy prevents or slows vegetation succession.

This study should be strengthened by further analyses: (a) by field experiments on the link between competition and architectural strategy; (b) a genetic study of invasive and non-invasive plants; and (c) an extension of this study to other invasive shrubs that employ varied architectural manners of development in order to understand plant invasion processes.

ACKNOWLEDGEMENTS

We thank Richard Carignan, Eric Valiquette and staff at the SBL (Station de biologie des Laurentides de l'Université de Montréal) for their logistical support. Thanks are extended to Daniel Barthélémy, Yves Caraglio, Thomas Le Bourgeois, Hervé Rey, Alain Meilleur and Alain Cogliastro for helpful suggestions in manuscript preparation. This work was supported by the Natural Sciences and Engineering Research Council of Canada to André Bouchard and by the Centre National de la Recherche Scientifique to Claude Edelin and Tristan Charles-Dominique.

LITERATURE CITED

  1. Anonymous. 2008 Bulletin d'information no. 4. Paris: European and Mediterranean Plant Protection Organization. [Google Scholar]
  2. Archer S. Woody plant encroachment into southwestern grasslands and savannas: rates, patterns and proximate causes. In: Vavra M, Laycock WA, Pieper RD, editors. Ecological implications of livestock herbivory in the West. Denver, CO: Society for Range Management; 1994. pp. 13–68. [Google Scholar]
  3. Baret S, Nicolini E, Humeau L, Le Bourgeois T, Strasberg D. Use of architectural and morphometric analysis to predict the flowering pattern of the invasive Rubus on Réunion island (Indian Ocean) Canadian Journal of Botany. 2003a;81:1293–1301. [Google Scholar]
  4. Baret S, Nicolini E, Le Bourgeois T, Strasberg D. Development patterns of the invasive bramble (Rubus alceifolius Poiret, Rosaceae) in Réunion Island: an architectural and morphometric analysis. Annals of Botany. 2003b;91:39–48. doi: 10.1093/aob/mcg006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baret S, Maurice S, Le Bourgeois T, Strasberg D. Altitudinal variation in fertility and vegetative growth in the invasive plant Rubus alceifolius Poiret (Rosaceae), on Réunion island. Plant Ecology. 2004;172:265–273. [Google Scholar]
  6. Barnola P. Recherches sur le déterminisme de la basitonie chez le framboisier (Rubus idaeus L.) Annales des Sciences Naturelles, Botanique, Paris. 1970;11:129–152. [Google Scholar]
  7. Barthélémy D. Levels of organization and repetition phenomena in seeds plants. Acta Biotheoretica. 1991;39:309–323. [Google Scholar]
  8. Barthélémy D, Caraglio Y. Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of Botany. 2007;99:375–407. doi: 10.1093/aob/mcl260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Barthélémy D, Edelin C, Hallé F. Architectural concepts for tropical trees. In: Holm-Nielsen LB, Balslev H, editors. Tropical forests: botanical dynamics, speciation and diversity. London: Academic Press; 1989. pp. 89–100. [Google Scholar]
  10. Barthélémy D, Edelin C, Hallé F. Canopy architecture. In: Raghavendra AS, editor. Physiology of trees. Chichester: John Wiley and Sons; 1991. pp. 1–20. [Google Scholar]
  11. Bartuszevige AM, Gorchov DL, Raab L. The relative importance of landscape and community features in the invasion of an exotic shrub in a fragmented landscape. Ecography. 2006;29:213–222. [Google Scholar]
  12. Bazzaz FA. The physiological ecology of plant succession. Annual Review of Ecology and Systematics. 1979;10:351–371. [Google Scholar]
  13. Benjamin K, Domon G, Bouchard A. Vegetation composition and succession of abandoned farmland: effects of ecological, historical and spatial factors. Landscape Ecology. 2005;20:627–647. [Google Scholar]
  14. Birnbaum P. Histoire de l'invasion d'une plante introduite, Miconia calvescens, dans une île polynésienne, Tahiti. Journal d'agriculture traditionnelle et de botanique appliquée. 1994;36:283–295. [Google Scholar]
  15. de Blois S, Domon G, Bouchard A. Environmental, historical, and contextual determinants of vegetation cover: a landscape perspective. Landscape Ecology. 2001;16:421–436. [Google Scholar]
  16. de Blois S, Domon G, Bouchard A. Factors affecting plant species distribution in hedgerows of southern Quebec. Biological Conservation. 2002;105:355–367. [Google Scholar]
  17. Bowman AW, Azzalini A. Applied smoothing techniques for data analysis: the Kernel approach with S-Plus illustrations. Oxford: Oxford University Press; 1997. [Google Scholar]
  18. Canham CD, Hill JD, Berkowitz AR, Ostfeld RS. Ecological perspectives on tree invasion in rights-of-way: quantifying variation among communities in resistance to tree invasion. In: Doucet GJ, Séguin C, Giguère M, editors. Fifth International Symposium on Environmental Concerns in Right-of-way Management. 1998. pp. 81–86. Montréal: Vice présidence Environnement Hydro-Québec. [Google Scholar]
  19. Chambel MR, Climent J, Alia R, Valladares F. Phenotypic plasticity: a useful framework for understanding adaptation in forest species. Investigacion agraria – Sistemas y recursos forestales. 2005;14:334–344. [Google Scholar]
  20. Chesson P. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics. 2000;31:343–366. [Google Scholar]
  21. Child R, Morgan DC, Smith H. Control of development in Chenopodium album L. by shadelight – the effect of light quality (red:far red ratio) on morphogenesis. New Phytologist. 1981;89:545–555. [Google Scholar]
  22. Claridge K, Franklin SB. Compensation and plasticity in an invasive plant species. Biological Invasions. 2002;4:339–347. [Google Scholar]
  23. Cogliastro A, Benjamin K, Bouchard A. Effects of full and partial clearing, with and without herbicide, on weed cover, light availability, and establishment success of white ash on shrub communities of abandoned pastureland in southwestern Quebec, Canada. New Forests. 2006;32:197–210. [Google Scholar]
  24. Comeau PG, Gendron F, Letchford T. A comparison of several methods for estimating light under a paper birch mixedwood stand. Canadian Journal of Forest Research. 1998;28:1843–1850. [Google Scholar]
  25. Crane MF. Cornus sericea. 1989 http://www.fs.fed.us/database/feis/plants/shrub/corser/all.html. (accessed 10 July 2009) [Google Scholar]
  26. Diggle PK. A developmental morphologist's perspective on plasticity. Evolutionary Ecology. 2002;16:267–283. [Google Scholar]
  27. Edelin C. 1977 Images de l'architecture des conifères. PhD Thesis, Université Montpellier II, France. [Google Scholar]
  28. Edelin C. 1984 L'architecture monopodiale: l'exemple de quelques arbres d'Asie Tropicale. PhD Thesis, Université Montpellier II, France. [Google Scholar]
  29. Edelin C. The monopodial architecture: the case of some tree species from tropical Asia. Forest Research Institute Malaysia Research Pamphlet. 1990;105:1–222. [Google Scholar]
  30. Englund SR, O'Brien JJ, Clark DB. Evaluation of digital and film hemispherical photography and spherical densiometry for measuring forest light environments. Canadian Journal of Forest Research. 2000;30:1999–2005. [Google Scholar]
  31. Ferment A, Picard N, Gourlet-Fleury S, Baraloto C. A comparison of five indirect methods for characterizing the light environment in a tropical forest. Annals of Forest Science. 2001;58:877–891. [Google Scholar]
  32. Goodwin BJ, McAllister AJ, Fahrig L. Predicting invasiveness of plant species based on biological information. Conservation Biology. 1999;13:422–426. [Google Scholar]
  33. Grosfeld J, Barthélémy D, Brion C. Architectural variations of Araucaria araucana (Molina) K. Koch (Araucariaceae) in its natural habitat. In: Kurmann MH, Hemsley AR, editors. The evolution of plant architecture. London: Royal Botanic Gardens, Kew; 1999. pp. 109–122. [Google Scholar]
  34. Guédon Y, Caraglio Y, Heuret P, Lebarbier E, Meredieu C. Analyzing growth components in trees. Journal of Theoretical Biology. 2007;248:418–447. doi: 10.1016/j.jtbi.2007.05.029. [DOI] [PubMed] [Google Scholar]
  35. Hallé F, Oldeman RAA. Essai sur l'architecture et la dynamique de croissance des arbres tropicaux. Paris: Masson; 1970. [Google Scholar]
  36. Hallé F, Oldeman RAA, Tomlinson PB. Tropical trees and forests – an architectural analysis. Berlin: Springer; 1978. [Google Scholar]
  37. Heuret P, Barthélémy D, Nicolini E, Atger C. Analyse des composantes de la croissance en hauteur et de la formation du tronc chez le chêne sessile (Quercus petraea (Matt.) Liebl., Fagaceae) en sylviculture dynamique. Canadian Journal of Botany. 2000;78:361–373. [Google Scholar]
  38. Huber H, Stuefer JF. Shade-induced changes in the branching pattern of a stoloniferous herb: functional response or allometric effect? Oecologia. 1997;110:478–486. doi: 10.1007/s004420050183. [DOI] [PubMed] [Google Scholar]
  39. Hudon C, Wilcox D, Ingram J. Modeling wetland plant community response to assess water-level regulation scenarios in the lake-Ontario–St. Lawrence river basin. Environmental Monitoring and Assessment. 2006;113:303–328. doi: 10.1007/s10661-005-9086-4. [DOI] [PubMed] [Google Scholar]
  40. Johnson RS, Lakso AN. Carbon balance model of a growing apple shoot. II. Simulated effects of light and temperature on long and short shoots. Journal of the American Society for Horticultural Science. 1986;111:164–169. [Google Scholar]
  41. King DA. Relationship between crown architecture and branch orientation in rain forest trees. Annals of Botany. 1998;82:1–7. [Google Scholar]
  42. Kolar CS, Lodge DM. Progress in invasion biology: predicting invaders. Trends in Ecology and Evolution. 2001;16:199–204. doi: 10.1016/s0169-5347(01)02101-2. [DOI] [PubMed] [Google Scholar]
  43. Küppers M. Ecological significance of above-ground architectural patterns in woody plants: a question of cost-benefit relationships. Tree. 1989;4:375–379. doi: 10.1016/0169-5347(89)90103-1. [DOI] [PubMed] [Google Scholar]
  44. Lauri P-É,, Kelner J-J. Shoot type demography and dry matter partitioning: a morphometric approach in apple (Malus × domestica) Canadian Journal of Botany. 2001;79:1270–1273. [Google Scholar]
  45. Légaré S, Bergeron Y, Leduc A, Paré D. Comparison of the understory vegetation in boreal forest types of southwest Quebec. Canadian Journal of Botany. 2001;79:1019–1027. [Google Scholar]
  46. Lockwood JL, Cassey P, Blackburn T. The role of propagule pressure in explaining species invasions. Trends in Ecology and Evolution. 2005;20:223–228. doi: 10.1016/j.tree.2005.02.004. [DOI] [PubMed] [Google Scholar]
  47. Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA. Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications. 2000;10:689–710. [Google Scholar]
  48. Marie-Victorin F. Flore laurentienne. 3rd edn. Montréal: Presses de l'Université de Montréal; 1995. [Google Scholar]
  49. Matsuzaki J, Masumori M, Tange T. Phototropic bending of non-elongating and radially growing woody stems results from asymmetrical xylem formation. Plant, Cell and Environment. 2007;30:646–653. doi: 10.1111/j.1365-3040.2007.01656.x. [DOI] [PubMed] [Google Scholar]
  50. Meilleur A, Bouchard A. 1989 Contrôle biologique de la végétation incompatible sous les lignes de transport d'électricité d'Hydro-Québec – Phase I – Synthèse bibliographique et dispositifs expérimentaux. Rapport annuel pour la vice-présidence environnement, Hydro-Québec, Université de Montréal, Québec. [Google Scholar]
  51. Meilleur A, Bouchard A. 1993 Contrôle biologique de la végétation incompatible sous les lignes de transport d'électricité d'Hydro-Québec – Phase III – Travaux expérimentaux sur les arbustes. Rapport annuel pour la vice-présidence environnement, Hydro-Québec, Université de Montréal, Québec. [Google Scholar]
  52. Meilleur A, Véronneau H, Bouchard A. Shrub communities as inhibitors of succession in southern Quebec. Environmental Management. 1994;18:907–921. [Google Scholar]
  53. Meilleur A, Véronneau H, Bouchard A. Shrub propagation techniques for biological control of invading tree species. Environmental Management. 1997;21:433–442. doi: 10.1007/s002679900040. [DOI] [PubMed] [Google Scholar]
  54. Meilleur A, Véronneau H, Bouchard A. Les critères de sélection des espèces arbustives comme contrôle de la végétation indésirable dans les emprises. In: Doucet GJ, Séguin C, Giguère M, editors. Fifth International Symposium on Environmental Concerns in Right-of-way Management. 1998. pp. 127–135. Montréal: Vice présidence Environnement Hydro-Québec. [Google Scholar]
  55. Mercier C, Brisson J, Bouchard A. Demographic colonization in a 20-year-old right-of-way. Environmental Management. 1999;28:777–787. doi: 10.1007/s002670010261. [DOI] [PubMed] [Google Scholar]
  56. Middleton B. Nonequilibrium dynamics of sedge meadows grazed by cattle in southern Wisconsin. Plant Ecology. 2002a;161:89–110. [Google Scholar]
  57. Middleton B. Winter burning and the reduction of Cornus sericea in sedge meadows in Southern Wisconsin. Restoration Ecology. 2002b;10:723–730. [Google Scholar]
  58. Miner BG, Sultan SE, Morgan SG, Padilla DK, Relyea RA. Ecological consequences of phenotypic plasticity. Trends in Ecology and Evolution. 2005;20:685–692. doi: 10.1016/j.tree.2005.08.002. [DOI] [PubMed] [Google Scholar]
  59. Mustard J, Renault S. Effects of NaCl on water relations and cell wall elasticity and composition of red-osier dogwood (Cornus stolonifera) seedlings. Physiologia Plantarum. 2004;121:265–271. doi: 10.1111/j.1399-3054.2004.00322.x. [DOI] [PubMed] [Google Scholar]
  60. Nicolini E, Chanson B, Bonne F. Stem growth and epicormic branch formation in understorey beech trees (Fagus sylvatica L.) Annals of Botany. 2003;87:737–750. [Google Scholar]
  61. Novoplansky A. Developmental plasticity in plants: implications of noncognitive behavior. Evolutionary Ecology. 2002;16:177–188. [Google Scholar]
  62. Olden JD, Poff LR. Toward a mechanistic understanding and prediction of biotic homogenization. American Naturalist. 2003;162:442–460. doi: 10.1086/378212. [DOI] [PubMed] [Google Scholar]
  63. Paquette A, Bouchard A, Cogliastro A. A less restrictive technique for the estimation of understory light under variable weather conditions. Forest Ecology and Management. 2007;242:800–804. [Google Scholar]
  64. Pickett STA, Kempf JS. Branching patterns in forest shrubs and understory trees in relation to habitat. New Phytologist. 1980;86:219–228. [Google Scholar]
  65. Pimentel D, Lach L, Zuniga R, Morrison D. Environmental and economic costs of nonindigenous species in the United States. BioScience. 2000;50:53–65. [Google Scholar]
  66. Poulain AJ, Roy V, Amyot M. Influence of temperate mixed and deciduous tree covers on Hg concentrations and photoredox transformations in snow. Geochimica et Cosmochimica Acta. 2007;71:2448–2462. [Google Scholar]
  67. Rauh W. Über die Verzweigung ausläuferbildender Sträucher mit besonderer Berücksichtigung ihrer Beziehungen zu den Stauden. Hercynia. 1938;1:187–231. [Google Scholar]
  68. Rauh W. Über Gesetzmäßigkeit der Verzweigung und deren Bedeutung für die Wuchsformen der Pflanzen. Mitteilungen der deutschen dendrologischen Gesellschaft. 1939;52:86–111. [Google Scholar]
  69. Richburg JA, Dibble AC, Patterson WA. Woody invasive species and their role in altering fire regimes of the Northeast and Mid-Atlantic states. In: Galley KEM, Wilson TP, editors. The First National Congress on Fire Ecology, Prevention, and Management. Tallahassee, FL: Tall Timbers Research Station; 2000. pp. 104–111. [Google Scholar]
  70. Sakai AK, Allendorf FW, Holt JS, et al. The population biology of invasive species. Annual Review of Ecology and Systematics. 2001;32:305–332. [Google Scholar]
  71. Savage C. 2001 Recolonization forestière dans les Basses Laurentides au sud du domaine climacique de l'érablière à bouleau jaune. M.Sc. Thesis, Université de Montréal, Québec. [Google Scholar]
  72. Schlichting CD, Smith H. Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes. Evolutionary Ecology. 2002;16:189–211. [Google Scholar]
  73. Schweitzer JA, Larson KC. Greater morphological plasticity of exotic honeysuckle species may make them better invaders than native species. Journal of the Torrey Botanical Society. 1999;126:15–23. [Google Scholar]
  74. Smith H, Whitelam GC. The shade avoidance syndrome: multiple responses mediated by multiple phytochromes. Plant, Cell and Environment. 1997;20:840–844. [Google Scholar]
  75. Sultan SE. Phenotypic plasticity in plants: a case study in ecological development. Evolution & Development. 2003;5:25–33. doi: 10.1046/j.1525-142x.2003.03005.x. [DOI] [PubMed] [Google Scholar]
  76. Sultan SE. Promising directions in plant phenotypic plasticity. Perspectives in Plant Ecology, Evolution and Systematics. 2004;6:227–233. [Google Scholar]
  77. Takenaka A. A simulation model of tree architecture development based on growth response to local light environment. Journal of Plant Research. 1994;107:321–330. [Google Scholar]
  78. Theoharides KA, Dukes JS. Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytologist. 2007;176:256–273. doi: 10.1111/j.1469-8137.2007.02207.x. [DOI] [PubMed] [Google Scholar]
  79. Tomlinson PB, Esler AE. Establishment growth in woody monocotyledons native to New Zealand. Principes. 1973;19:83–99. [Google Scholar]
  80. Troll W. Vergleichende Morphologie der höheren Pflanzen. Berlin: Springer; 1937. [Google Scholar]
  81. Valladares F, Gianoli E, Gomez JM. Ecological limits to plant phenotypic plasticity. New Phytologist. 2007;176:749–763. doi: 10.1111/j.1469-8137.2007.02275.x. [DOI] [PubMed] [Google Scholar]
  82. Valladares F, Hernandez LG, Dobarro I, Garcia-Perez C, Sanz R, Pugnaire FI. The ratio of leaf to total photosynthetic area influences shade survival and plastic response to light of green stem leguminous shrub seedlings. Annals of Botany. 2003;91:1–8. doi: 10.1093/aob/mcg059. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Véronneau H, Meilleur A, Bouchard A. Méthodes expérimentales favorisant les espèces arbustives comme contrôle de la végétation indésirable dans les emprises de lignes de transport d'électricité. In: Doucet GJ, Séguin C, Giguère M, editors. Fifth International Symposium on Environmental Concerns in Right-of-way Management. 1998. pp. 203–209. Montréal: Vice présidence Environnement Hydro-Québec. [Google Scholar]
  84. Vitousek PM, d'Antonio CM, Loope LL, Westbrooks R. Biological invasions as global environmental change. American Scientist. 1996;84:468–478. [Google Scholar]
  85. White KL. Shrub-carrs of southeastern Wisconsin. Ecology. 1965;46:286–304. [Google Scholar]
  86. Williamson MH. Biological invasions. London: Chapman & Hall; 1996. [Google Scholar]
  87. Wright SD, McConnaughay KDM. Interpreting phenotypic plasticity: the importance of ontogeny. Plant Species Biology. 2002;17:119–131. [Google Scholar]
  88. Young SG, Bowman AW. Nonparametric analysis of covariance. Biometrics. 1995;51:920–931. [Google Scholar]
  89. Young TP, Petersen DA, Clary JJ. The ecology of restoration: historical links, emerging issues and unexplored realms. Ecology Letters. 2005;8:662–673. [Google Scholar]

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