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Anatomy and Morphology |
2Institut National de la Recherche Agronomique (INRA), UMR AMAP, Montpellier, F-34000 France; 3INRA, Unité de recherche Écologie fonctionnelle et Physique de l'Environnement (EPHYSE), 69 route d'Arcachon, Cestas, F-33612 France; and 4INRA, Unité de Recherches Forestières Méditerranéennes (URFM), avenue Vivaldi, Avignon, F-84000 France
Received for publication November 30, 2005. Accepted for publication September 28, 2006.
ABSTRACT
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).
Key Words: annual shoot • chronosequence • growth • morphology • ontogeny • phase changes • Pinaceae • Pinus pinaster
Since the pioneer work of Goethe (1970)
, that defined the basic principles of plant morphology, observations of many authors on numerous plant species (e.g., Hallé et al., 1978
; White, 1979
; Barthélémy, 1991
, 2003
; Bell, 1991
; Room et al., 1994
) have confirmed that plants are modular organisms that develop by the repetition of elementary botanical entities or constructional units. In seed plants, considering their huge specific diversity, the number of these entities is actually relatively small; they correspond, in increasing order of complexity or integration, to metamer (also called phytomer), growth unit, sympodial unit (also called modules), annual shoot, axis, architectural unit, and whole reiterated organism (Barthélémy, 1991
, 2003
; Barthélémy and Caraglio, 2006
). The range of biological entities, from the most elementary to the most global, represents a set of nested levels of organization. During ontogeny, they progressively derive from one another by three main and fundamental morphogenetic processes of growth, branching, and reiteration. Whatever the botanical entity (or level of organization) concerned, its repetition always induces either progressive or abrupt changes in their features. Changes can be morphological, anatomical, and physiological (Zimmerman et al., 1985
; Greenwood, 1995
; Jones, 1999
; Claßen-Bockhoff, 2001
; Kaplan, 2001
; Barthélémy, 2003
; Poethig, 2003
).
Because of its economic importance for agronomic production, plant reproduction, and vegetative propagation, acquisition during ontogeny of reproductive capacities has been profusely studied (Goebel, 1900
; Doorenbos, 1954
; Wareing, 1961
; Borchert, 1976
; Jones, 1999
; Poethig, 2003
). Four phases of plant development have been proposed: the embryonic phase, in which the shoot and root meristem are established; the juvenile phase, in which there is no sexual reproduction; the adult vegetative phase, in which reproductive competency is established; and finally the adult reproductive phase (Poethig, 2003
). The transition between phases is referred to as phase change (Jones, 1999
). The acquisition by a plant of reproductive competency is, however, not the only marker of the reproductive adult phase. Some well-known examples, such as ivy (Hedera helix L., Araliaceae), show that this transition occurs along with modifications of many other morphological, anatomical, and/or functional features such as the aptitude of root adventitious emission or propagation by cuttings or the form, the anatomy, and the content of anthocyanes, and the phyllotaxy of the leaves (Doorenbos, 1954
; Brink, 1962
; Poethig, 1990
). Nevertheless, most studies of first flowering or the differentiation of reproductive organs do not simultaneously document changes in several other vegetative morphological features (Atherton et al., 1998
).
Trends in features of the metamers comprising small, unbranched plants of short life span can be easily studied across the entire ontogeny. In comparison, the study of trees imposes several limitations. First of all, in order to understand an organism as a branched system, characters must be studied on the whole axes that constitute the tree architecture. Second, the structure of the tree can be considered at various levels of organization (one axis can be considered as a succession of metamers, growth units, or annual shoots), each one characterized by several variables. Third, their longevity prevents the study of trends across the life span, and retrospective analyses are necessary. This last point requires the identification and subsequent observation of morphological and anatomical markers (e.g., leaf scars or ring scars of cataphylls that delimit growth units), which allows the retrospective reconstitution of the plant's development. During growth and development of the tree, some necessary structural information may disappear with time due to (1) the natural fading of morphological markers and/or (2) the natural self-pruning of branches. Studying the development of a tree species along with its ontogeny thus means working with a chronosequence by sequencing observations at different and successive stages. In this context and before the study and analysis of branches and comprehensive tree architecture may be undertaken, the validation of the chronosequence method for main stem parameters is an important prerequisite. Due to these intrinsic and methodological limitations in higher woody plants, little is known in trees about the successive, qualitative, and quantitative changes in different morphological features, simultaneously taking into account growth, branching, and flowering processes at different levels of organization (growth unit and annual shoot), and considering the whole aerial architecture of the plant (trunk and crown).
In France, maritime pine (Pinus pinaster Ait) represents 16% of national pulp and wood production with 1 361 030 ha of forest (Inventaire Forestier National [IFN], 2004
). Various quantitative approaches were developed and usually considered only some features of the main axis parameters (total height) and particular trees (average, dominant). For example, numerous studies exist on height growth in particular in even-aged forest stands for site index curves modeling (Kremer and Roussel, 1982
; Monserud, 1984
; Danjon and Hervé, 1994
; Espinosa et al., 1999
; Alvarez Gonzalez et al., 2005
). On the other hand, many studies have been performed on maritime pine to determine organogenesis, growth patterns, and annual shoot structure at different stages of development (Doak, 1935
; Bugnon and Bugnon, 1951
; Debazac, 1963
, 1966b
; Kremer and Roussel, 1982
; Kremer et al., 1990
). The results of these works provide a better interpretation of the morphological markers that can be used retrospectively to deduce the development of a tree (annual and intra-annual growth stops, branch and cone scars, etc.). Loup (1990)
qualitatively studied the architectural development of the maritime pine and established its "architectural unit," whereas other studies (Prat, 1936
; Wareing, 1958
; Edelin, 1977
) qualitatively described morphogenetic gradients for some species of Pinus.
Initiated by a preliminary study published by Coudurier et al. (1995)
, we are beginning here a series of papers with the general aim of establishing a full quantitative description of the architectural development of maritime pine for a given silvicultural schedule from germination to 48 years old. This first paper describes the various components of main stem development in terms of growth, branching, and production of reproductive organs, by considering annual shoot and growth unit levels of organization (Barthélémy and Caraglio, 2006
) and using data from three stands selected to represent a chronosequence. For common ontogenetical years, we check the overlap between the three stands for growth, branching, and flowering variables, thereby validating the use of chronosequences (Heuret et al., 2000
; Passo et al., 2002
). Phase changes and the concept of juvenility considering the concomitance of the trends expressed on morphological entities during ontogeny are also discussed.
MATERIALS AND METHODS
Background on maritime pine architecture
Maritime pine, like all species of Pinus, develops according to Rauh's architectural model (Hallé and Oldeman, 1970
; Edelin, 1977
; Hallé et al., 1978
). All the axes are orthotropic, with rhythmic and indefinite growth. An annual shoot (As), i.e., each axis portion extended over one year, is made up of one or several growth units (Gu) (Fig. 1a, b), each Gu corresponding to the portion of stem established during an uninterrupted elongation event. Except for the first years (less than three) after germination, each Gu is clearly composed of three main zones: (Doak, 1935
; Prat, 1936
; Bugnon and Bugnon, 1951
; Debazac, 1963
, 1966a
; Kremer and Roussel, 1982
, 1986
) (1) a zone of scale leaves (cataphylls); (2) a zone of short shoots (dwarf branches called brachyblasts with two needles); and (3) a bud zone (Fig. 1a) from which a tier of branches develops in the same year as the bearing shoot or the year after (Bugnon and Bugnon, 1951
; Debazac, 1963
). Because of this strong acrotony, branching is rhythmic and lateral axes are grouped in pseudo-whorls.
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) with a shallow groundwater table and a hardpan horizon at a depth varying from 0.5 to 1.0 m. The understorey is mainly Molinia coerulea L. (Moench) (Poaceae) and Ulex nanus Forst. (Fabaceae), or Pteridium aquilinum L (Kuhn) (Dennstaedtiaceae). In order to avoid tree and sample heterogeneity, three 8-, 22-, and 48-yr-old stands of maritime pine were selected on the basis of their phytoecological and silvicultural similarities: (1) all were seeded (wild progeny) and thinned regularly and (2) the trees, chosen on the basis of their height and diameter, were selected to represent only dominant or codominant trees in order to minimize tree status effects. Although maritime pine stems are often leaning or flexuous, only straight trees were selected. Tree stems were neither forked nor deformed. The stands and the selected trees are described in Table 1.
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), the first Gu on an annual shoot is generally longer than the second or third for that year, while the last Gu on a particular annual shoot generally carries branches with larger basal diameters than those carried by the most proximal or intermediate Gus (Bugnon and Bugnon, 1951
; Debazac, 1963
; Kremer and Roussel, 1982
; Kremer et al., 1990
). Complementary observation of Gus and annual shoot on branches also helps to reconstitute trunk Gus. But the simplest and most robust method is to cut transverse sections of the trunk between two pseudo whorls and count the number of rings for each growth unit: the result is the same for all growth units in an annual shoot. Branches and female cones were both inserted at the top of the bearing Gu (Fig. 1c), which can cause confusion when interpreting the scars they leave. A branch scar differs from that of a female cone by the presence of commissures on both sides of the insertion point. After pruning, cone scars have a circular shape; they are less persistent than those due to branches and are very difficult to observe in the oldest part of the tree.
Protocol and parameters measured
The limits of the Gus and the annual shoots were identified with the morphological markers previously described. In case of any doubt, transverse sections were made to verify the accuracy of the morphological markers. Nevertheless, because of the difficulties inherent in accurately determining the limits of a growth unit and an annual shoot in the oldest parts of the trees, the first annual shoots considered on the trunk were those corresponding to the second, third, and seventh years post-germination in trees aged 8, 22, and 48 yr, respectively. Branches and female cones were counted from the seventh and 16th years of growth in the 22- and 48-yr-old trees, respectively (Table 1).
The following data were recorded for each growth unit: circumference measured just below the zone with short shoots or within 10 cm of the base of the Gu when this limit was no longer visible, overall length, the presence of needles, the presence or absence of branches, their number, and the presence or absence of female cones and their number (no male cones were observed on the trunks in our study).
Scale leaves and short shoot zones were precisely measured in the Gus that had appeared over the last 5 years. The monocyclic or polycyclic status of an annual shoot was deduced from the constitutive number of its Gus. Annual shoot length was obtained by summing the lengths of all their constitutive growth units. Measurements were taken in the summer, meaning that the characteristics of the elongating last annual shoot were not taken into account.
Methods of analysis
The topology, i.e., the relative position of the different botanical units described (axis, annual shoot, growth units), was coded using AMAPmod software (Godin et al., 1997
; Godin and Caraglio, 1998
; Godin, 2000
). This gave a precise spatial location for each structure during the analysis. The age attributed to the meristem may differ depending on the approach used for its determination (chronological age, ontogenetical age, or physiological age) (Barthélémy, 2003
; Barthélémy and Caraglio, 2006
). The morphological characteristics of each botanical entity are represented here according to its ontogenetical age, i.e., the time elapsed since seed germination.
Three main types of growth unit were considered: monocyclic annual shoots called "Gu.mono" and bicyclic annual shoots with their first and second growth units called "Gu.bi1" and "Gu.bi2," respectively (Fig. 1a, b). Since the level of polycyclism varies from one year to another, the number of different types of growth unit (Gu.mono, Gu.bi1, and Gu.bi2) may be small in a given year. In the graphs, only means and 95% confidence limits calculated using more than five values are shown. Corresponding distributions were compared using the nonparametric Mann–Whitney–Wilcoxon (MWW) test, which is valid even if the data are not normally distributed. This test can therefore be used to compare distributions with relatively small sample sizes (Saporta, 1990
). The relative lengths of Gu.bi1 and Gu.bi2 in the same bicyclic annual shoot (As.bi) were studied using the L.Gu.bi2/L.As.bi ratio, which corresponds to the length of Gu.bi2 divided by the overall length of the bicyclic annual shoot to which it belongs. In the same manner we studied the ratio given by length of the scale leaves zone to length of the Gu.
RESULTS
Primary growth
Height growth and length of annual shoot—Average height growth was slow over the first 4 yr, then increased sharply and tended to level out after approximately 20 yr, conferring a classical sigmoid form to the cumulative height plot. All three stands showed a similar pattern (Fig. 3a). There was no significant difference between 8- and 22-yr-old trees for common ontogenetical ages. The 22-yr-old trees were slightly taller, however, than those aged 48 yr in common ontogenetical ages (95% confidence intervals on the mean are shown in Fig. 3a). Data were compared with theoretical values provided by the stand dominant-height model developed by Lemoine (1991)
. Initialized with 24.1 m for "dominant stand height at 40 years," this theoretical plot was comparable (nonsignificant difference) with the development of the 22-yr-old trees after nearly the first 10 yr of growth. Initialization with 23.1 m for dominant stand height at 40 yr was necessary to give a plot comparable to the development of the 48-yr-old trees.
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Level of polycyclism
The annual shoots were mainly bicyclic in all three stands (Fig. 4). Tricyclic and tetracyclic shoots were rare (26 As, 2.67% of the total observed As) and occurred only at the base of the trunk, before the first 14 yr of tree growth (92% in the first 7 yr of tree growth). The linear regression indicated that the level of bicyclism tended to increase from 0.59% to 0.85% during ontogeny (slope of the linear regression = 0.0058, with R2 = 0.373 significant at the 99% threshold). This trend was marked by annual fluctuations. For example, a large proportion of monocyclic annual shoots was observed for the 10th and 14th years of growth in the 22-yr-old trees (75% and 70%, respectively), and for the 28th and 38th years in the 48-yr-old trees (70% and 80%, respectively).
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Length of scale leaves zone according to type of Gu
The scale leaves zone in Gu.bi1 increased from nearly 10% of the Gu in the eighth year to 25% in the 48th (Fig. 6). Gu.mono was not significantly different from Gu.bi1 in the years in which sufficient data were available for the comparison. No marked trend could be determined for the relative size of the scale leaves zone on Gu.bi2. This ratio, which can account for up to two-thirds of the Gu.bi2 length, was generally always larger for Gu.bi2 than for Gu.bi1 and Gu.mono. The variability of this parameter was far higher for Gu.bi2 than for Gu.bi1 and Gu.mono (95% confidence intervals on the mean). Needles in Gu.mono and Gu.bi1 were generally located on the three last years of growth, and there was no difference between the stands. Needle life span on Gu.bi2 was somewhat shorter: two yr on average for the different stands.
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Branch diameter according to position on the trunk and type of Gu
When all three stands and common years were considered, Gu.mono and Gu.bi2 failed to show any significant difference (88% of the cases) for the diameter of branches carried in a given year while the diameter of branches on Gu.bi1 was smaller (Fig. 7c). These differences are slight towards the base of the tree, earlier than the 10th year of growth, and increased towards the top of the tree. In the 22-yr-old trees, the branches with larger diameters were extended on Gu.mono and Gu.bi2 when the tree was approximately 15 yr old. From this position to the base of the trunk, the diameter of the branches, which were therefore increasingly old, gradually decreased. Branch diameter decreased more sharply at the top of the trees. The same trend was observed for the 48-yr-old trees in which the largest branch diameters were located on the annual shoot extended when trees were nearly 30 yr old.
The reproductive and cone production process
In maritime pines, sexuality is lateral. Female cones appear under branches (Fig. 1c), whereas male cones occur in great numbers between the scale leaf zone and the short shoot zone (Fig. 1d). A fertile Gu is in general female or male and on very rare occasions hermaphroditic (Kremer et al., 1990
).
Time course changes in the percentage of female Gu according to their type
During ontogeny, the frequency of female Gu.bi1 increased greatly from the ninth to the 40th years of growth when the proportion reached nearly 90% (Fig. 8a). This trend was marked by substantial annual fluctuations. In the 22- and 48-yr-old trees, the presence of female cones on Gu.mono was generally less frequent than on Gu.bi1. No female cones were observed on Gu.bi2 in 22-yr-old trees (except on one year) and in 48-yr-old trees over the first 35 yr of growth. Some fertile Gu.bi2 (25%) were counted from 35 yr onwards.
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Relation between cones and branches
For each stand, if we consider the sum of cones and branches, no significant difference was observed age by age among GU.mono, GU.bi1, and GU.bi2 (only one significant difference appears at 40 yr for 48-yr-old trees). As GU.bi2 are always branched and carry only few cones, the trend observed for this new character is very close to the average number of branches for GU.bi2 whatever the type of GU considered.
DISCUSSION
The use of morphological markers in the retrospective reconstruction of tree development
Studies published on pine tree species often use a limited set of features for stem analyses (Lemoine, 1991
; Danjon and Hervé, 1994
). For example, many authors state that Gus.bi2 are shorter than Gus.bi1 or that the branches they bear have a relatively larger basal diameter (Bugnon and Bugnon, 1951
; Debazac, 1963
; Kremer and Roussel, 1982
; Kremer et al., 1990
). Our study demonstrates that these criteria are globally true, but not in all parts of the tree as their expression may vary with ontogenetical age. For example, in this and previous work (Coudurier et al., 1995
) we showed that Gus.bi2 are not always shorter than Gus.bi1 at the base of the stem and this criterion must thus be used with caution in the oldest and proximal parts of the tree. Thus, from a practical standpoint, our study provides a quantification of the morphological and ontogenetic gradients and trends on the main stem, i.e., some characters used for morphological analysis show varying degrees of effectiveness depending on the part of the stem under study. Furthermore, for retrospective reconstruction of tree growth and development, other diagnostic features may be added, e.g., the increase in unbranched status and of the relative part of the sterile zone of Gu.bi1 after the occurrence of reproductive process.
Phase change
Most studies on flowering ability do not simultaneously document changes in vegetative morphological characters (Atherton et al., 1998
). In particular, careful analysis of the vegetative body of the plant, which is necessary to ascertain when adult features are first expressed, is rarely reported. Therefore, the precise relationship between vegetative and reproductive development is unknown for all but a few models and most often structurally simple organisms (Jones, 1999
).
As for other species, main stem development during ontogeny of maritime pines can clearly be divided into two phases. In our case, the passage of a sterile juvenile phase to a fertile mature phase is associated with different morphological changes. Some characters such as tricyclism, tetracyclism, or cone production are expressed only during one of the two phases. Other features, such as length of As or Gu, express trends or intensity changes on both sides of the limit (Fig. 9).
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The progressive increase in vigor associated with the early establishment phase is noted in most seedlings of woody plants (Jones, 1999
; Barthélémy and Caraglio, 2006
). In some species such as oak, beech, or fir, it has been shown that this establishment phase, or the appearance of flowering, may be delayed under restrictive conditions (Gatsuk et al., 1980
; Nicolini, 1997
; Heuret et al., 2000
; Nicolini et al., 2000
). The study reported here showed that trees aged eight and 22 years exhibited similar behaviors in common ontogenetical age with regard to growth and branching variables, and no shift was observed. As far as cone production is concerned, it should be noted that very little was expressed in the 8-yr-old trees (except one individual in the seventh year), in the same manner as for the first 8 yr in the 22-yr-old trees. These results show that during this first stage these two populations followed a similar pattern of development with common characteristics at similar ontogenetical ages.
Subsequent tree development (based on 22- and 48-yr-old trees and stands data)
After maximum height extension rate, which was reached after approximately 9 yr, the frequency of annual shoots bearing female cones increased rapidly while annual shoot length decreased gradually in the trees aged 22 and 48 yr. This reduction was mainly due to a reduction in the length of Gu.mono and Gu.bi1. Second growth unit of a bicyclic annual shoot (Gu.bi2) also decreased in length, but these were always very short compared to Gu.bi1 and hence participated little in the overall length of the annual shoot. Annual shoots were mainly bicyclic while tri- or tetracyclic annual shoots were absent. The frequency of branched Gu.bi1 and the number of branches they carried also gradually decreased. As the sum of the number of cones and the number of branches is the same for all shoots, this reduction in the number of branches may be associated with the increase in the number of female cones occupying the same position as branches. It is noteworthy that for the eighth and 12th years of growth, corresponding growth units were significantly longer in 22-yr-old trees than in 48-yr-old trees. These stands were no longer different after the 12th year of growth. Also, the 22-yr-old trees consistently remained on average 1 m taller than the 48-yr-old trees at the same ontogenetical ages. This pattern was also underlined when a comparison was made with data provided by the stand dominant-height model developed by Lemoine (1991)
in which a site index of 23.1 m at 40-yr-old was necessary to fit the cumulative height growth of 48-yr-old trees while those aged 22 yr required a site index of 24.1 m. If these differences cannot be explained by site fertility, they may be explained by intensive prethinnings; i.e., two prethinnings were carried out after 4 and 9 yr in the 22-yr-old trees whereas no information was available concerning the age at which prethinnings were done in the 48-yr-old trees.
After the initial stage of maturation the expression of sexuality in approximately the ninth year of growth demonstrates the passage from a juvenile vegetative to a mature reproductive stage. The time of appearance of first female cones agreed with the observations of Alazard (1979)
or Danjon (1994) and with data on other species such as Pinus sylvestris (Wareing, 1959
). Our results nevertheless show that this transition was also associated with a set of morphological modifications. Most notable was the progressive reduction in annual shoot length. This loss of vigor with aging is commonly observed in woody species (Wareing, 1959
; Kozlowski, 1971
). Here it was shown that the starting moment of this process (i.e., the reduction in annual shoot length) coincided with the first manifestation of the reproductive process. This type of correlation may also be clearly highlighted in common beech (Nicolini and Chanson, 1999
), where the decrease in annual shoot length begins just after the first expression of flowering, corresponding in this case to the beginning of the architectural metamorphosis by a reiteration process.
The idea of youth criteria was sometimes extended to characters being expressed before flowering but not, however, necessarily in concomitance. For example, in 8-yr-old trees, euphylle (true leaves located at the same site as dwarf branches) were observed in the very first years (1–3) of growth in the same manner as in many conifers (Kozlowski, 1971
), but these disappeared before the expression of female sexuality. Marcescence in the common beech is expressed in young trees but also disappears before first flowering (Nicolini and Chanson, 1999
). Kremer et al. (1990)
reports 6 yr of juvenile phase in maritime pine but this corresponds to the capacity of the plant's shoots to carry out neoformation without any reference to flowering. It is also important to underline in these cases that although these characters are markers of the juvenile phase, their disappearance does not automatically signify entrance into the mature vegetative phase. In our study, it may be retained, in accordance with the definition given by Jones (1999)
, that the juvenile period is sterile. Furthermore, concomitance between the expression of flowering and some morphological modifications such as the decrease in polycyclism or the decrease in annual shoot length was observed by statistical analysis in a large sample.
Use of chronosequence
During ontogeny and considering the set of variables examined in this study, it would appear that the three sampled stands exhibited similar behaviors in common ontogenetical years with regard to growth, branching, and female cone production. Despite the minor differences in height between the 22-yr-old and 48-yr-old trees, no shift was observed and none of the variables measured varied in intensity in common ontogenetical ages. Thus, the three tree populations growing under similar forestry conditions showed similar ontogenetical trends and features despite the fact that they grew at different times and had been subject to different climatic variations. This result, which is often an assumption in tree development modeling (de Reffye et al., 1991
), was thus verified in our study. It confirms that it is possible to reconstitute the main axis growth of maritime pine along the ontogeny by sequencing observations made on trees at distinct stages of the same silvicultural scenario. This assumption may be called into question by the current concerns of global climatic change (e.g., increases in atmospheric CO2, nitrogen deposits, average temperature). This result associated with other studies, for example on oak (Heuret et al., 2000
), shows that a chronosequence can be used to characterize tree development over a long period of time, and this is particularly advantageous for studying the development of branches that undergo natural pruning and are thus absent from the basal part of old trees. It is important to note that in our case tree developmental trajectory was analyzed in only dominant and codominant trees for one type of site condition. The variability observed for the different studied variables is thus linked to our sample design and does not take into account the comprehensive and potential natural specific plasticity that should be studied separately in further works.
Based on stand chronosequence analyses, the methodology we used may also be applied in order to compare sources or genetic improvement levels as well as treatments. It may also serve as a basis for methods of comparing branching and axillary products (Guédon et al., 2003
). As with previous works on plant architecture, our results show that plant development from germination to death is carried out by a succession of events and/or stages characterized by morphological, anatomical, and physiological changes, which define its ontogeny (Barthélémy et al., 1997
; Barthélémy, 2003
). For common ontogenetical ages, trees from the three measured stands showed similar values for the analyzed morphological parameters. This provides a rationale for building an architectural quantitative model based on measurements taken in stands of different ages. In particular this will enable us to compare time course changes in morphological characters along the branches (as well as higher branching order axes) positioned at different levels along the trunk. We do not have any common measurement between samples due to the limited extension of branches and to the natural pruning of oldest branches developed during the first years of growth of the trees. As stated by Barthélémy et al. (1997)
, Barthélémy (2003)
and Barthélémy and Caraglio (2006)
, the "physiological age of a meristem" relates to the degree of differentiation of the structures it produced and may generally be characterized and defined by a particular combination of the values of several morphological (and/or anatomical and/or functional parameters) of a given botanical entity derived from the activity of this meristem. In our case this is illustrated (Fig. 9) for the main stem of maritime pine trees belonging to three different stands of a chronosequence. At the level of the comprehensive architecture of a plant, the "morphogenetic gradients" notion was also defined (Barthélémy et al., 1997
; Barthélémy, 2003
; Barthélémy and Caraglio, 2006
) in order to explain the inherent and intrinsic organizational rules of plant structure and revealed to be a powerful concept to explain the observed structure and series of modifications of botanical entities during the ontogeny of any plant species. The core of further studies will thus be, on the basis of these first results, to validate, to calibrate, and to quantify these notions by considering the comprehensive set of axes of maritime pine trees belonging to the same chronosequence used here for main stem development analysis.
FOOTNOTES
1 The authors wish to thank B. Lemoine and D. Guyon for their logistic assistance; Mr. Fignac from GROUPAMA who allowed us to work on the Marcheprime maritime pine stand; J. Beauvery, B. Chanson, M. Fournier, F. Lagane, C. Loup, and P. Rossetto for their help in collecting field data; F. Houllier, J. Puntieri, and J. Bachelier for critical and valuable comments on the manuscript; and F. Ramirez and M. Jones for their assistance. This study was conducted as part of the GIP-ECOFOR program Ecosystème Forestier Landais. 
5 Author for correspondence (heuret{at}cirad.fr
), INRA, Unité mixte de recherche botAnique et bioinforMatique de l'Architecture des Plantes (AMAP), TA40/PS2, Bd. de la Lironde, 34398 Montpellier cedex 5, France. Tel: 33. (0)4.67.61.55.98, Fax: 33. (0)4.67.61.56 68
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with their 95% confidence limits, and comparisons (Mann–Whitney Wilcoxon test) of the corresponding distributions are in the upper part of each graph: a dash indicates no significant difference; an asterisk indicates distributions are significantly different at the 95% threshold
