Crown structure in Araucariaceae

Transcription

1 50 9 Crown structure in Araucariaceae P. B. Tomlinson Harvard Forest, Petersham MA and National Tropical Botanical Garden, Kalaheo, HI, USA Summary: The Araucariaceae is the most ancient extant family of seed plants whose persistence may, in part, be the result of a successful way of making a tree canopy. Deterministic components include: monopodial habit, rhythmic growth, pronounced axis polymorphism, with up to three discrete branch orders, and cones always on ultimate deciduous axes. Opportunistic components include reiteration of trunk axes (total) and first-order branch axes (partial) either from "detached meristems" (cf. Fink, Burrows), as in Araucaria, or de-differentiation of trunk axes, as in Agathis. Wollemia may represent one end of a spectrum of possibilities within Araucaria. The crown can be presented as a repairable framework (of "explorative axes") bearing ultimate long lived but deterministic photosynthetic units (as "exploitative axes"). Many of these features may have existed in ancestors - notably Archeopteris. In its opportunistic mode, total crown repair is possible on an existing trunk, with trunk regeneration restricted in varying degrees. In high winds branches may be stripped from all but the leeward side of the tree to produce a "banner tree", but the canopy can be replaced in toto, maintaining the distinctive shape (e.g. A. columnaris). This property seems adaptive in cyclone-prone habitats and may account for the adaptive radiation in New Caledonia. Future requirements are for quantitative analysis and experimental manipulation. Introduction Trees in the family Araucariaceae, as exemplified by the commonly cultivated Araucaria heterophylla (Norfolk Island pine), have a distinctive crown form that makes them easily recognized. What is the ecological significance of this form? The question can only be answered with knowledge about the development of the crown. At the same time it is clear that the three genera in the Araucariaceae are distinctly different in the method of crown construction. Again one might ask what ecological inferences can be gained from a comparison of Agathis, Araucaria and Wollemia? Agathis is relatively uniform in crown form but Araucaria is quite diverse, appropriate for a genus with a considerable geographic range. The diversity of Araucaria includes, on the one hand, the spire-like or columnar shape of A. columnaris, a form that excited the crew of James Cook s Endeavour when they first saw New Caledonia, and on the other hand trees with a candelabra habit, as represented by Araucaria araucana of the Chilean Andes. Wollemia, in so far as it is known, combines features of Araucaria and Agathis. In view of this diversity the following account can only be preliminary. We do have an exemplary description of Araucaria in New Caledonia by Veillon (1978, 1980), which is closely followed here. Opportunity to study the problem at first-hand has been provided by the cultivation of Araucaria in the tropics and subtropics outside its natural range. Araucaria araucana (monkey puzzle) is a frequent Victorian relict in British and Irish gardens, while the recent IDS excursion to New Caledonia allowed the study of Agathis and Araucaria species in natural environments and in cultivation. Agathis australis has been studied extensively in New Zealand. Architecture Following the principles laid out in Hallé et al. (1978), the mature canopy of the tree can be perceived as the sum of two processes. First, there is the architectural model of the tree, i.e., the growth plan inherent in its genetic make-up. The visible expression of this model at any one moment in time is the architecture of the tree. Second, there is the partial or total repetition of this model (i.e.,

2 9: Crown structure 51 its reiteration) as a response either to trauma (physical damage) or some change in the immediate environment of the tree that disrupts the underlying model. The tree most precisely conforms to its model as a well-grown sapling, but reiteration becomes progressively more important as the tree ages because it makes the developmental plan more adaptable to changing circumstances. Members of the Araucariaceae may consistently be referred to Massart s model in the Hallé-Oldeman typology (Hallé et al. 1978) since the trunk axis is monopodial (i.e., with a permanent leader) and exhibits rhythmic growth in the form of regular production of branch tiers (pseudowhorls) but with variable spacing. The trunk axis is vertical and with radial symmetry (orthotropic), whereas branches are essentially horizontal and have dorsiventral symmetry (plagiotropic). Some extension of this model in terms of Rauh s model is included in Veillon s descriptions because in some species the distal ends of older axes become erect and radially symmetrical. Apart from the relatively constant framework of the tree implied in these descriptions, a family character is the high degree of axis polymorphism such that axes of different branch orders can have distinctive morphological features, resulting in a highly efficient photosynthetic system. In leaf shape the most immediate contrast is between the needle-like or awl-shaped leaves of many Araucaria species and the broad, flattened leaves of Agathis, Wollemia and several Araucaria species. All species in the family have a highly distinctive juvenile morphology that is contrasted with the morphology of adult shoots. Reiteration in the family is expressed either in the replacement of lost orthotropic and plagiotropic axes, together with a dedifferentiaton whereby plagiotropic axes revert to orthotropy as derived trunk axes. Replacement axes are developed from axillary meristems that originate in most leaf axils and may persist throughout the life of the tree. This abundant supply of reserve meristems is considered by Burrows to be a unique feature of the tree, based on his very extensive and detailed observations (Burrows 1986, 1987, 1989, 1990b, 1999, and this volume). Even with a considerable supply of reserve meristems of this kind, a continuum of crown structures is realized. Other conifers have similar axillary meristems although these may be relatively short-lived (Fink 1984). Explore and exploit In interpreting the crown architecture of a tree as functionally efficient in both photosynthetic ability and mechanical stability, it is useful to describe the tree in terms of a permanent mechanical framework (derived from the architectural model), which bears relatively ephemeral photosynthetic units as either leaves or shoots. This approach, developed by French morphologists (e.g. Edelin 1977) sees the tree as a series of axes that initially explore the space available for making a canopy. These axes of exploration constitute the framework of the tree, which supports the axes of exploitation, i.e., the ultimate assimilating units. An example would be the familiar Ginkgo biloba in cultivation in temperate countries. The axes of exploration are the long-shoots, which have a precise disposition according to Massart s model, producing a framework revealed in the winter leafless condition. The axes of exploitation are the short-shoots that produce most of the leaves clothing the tree in summer. This represents the ultimate degree of axis differentiation. Araucaria can be described readily according to this approach, Agathis less easily. Branch orders A consistent terminology for axis orders designates the trunk axis as ax o, with successively higher branch orders as ax 1, ax 2. etc. This immediately designates branch orders by the appropriate suffix and allows the comparison of crown structure in different trees. A distinction has to be made between the topographic order, i.e. the visible

3 52 Section 2: Morphology, phylogeny, systematics and ecology sequence of axes within the tree, and the morphological order, where each axis order within the architectural model can be recognized by its distinctive morphological features without regard to its placement in the tree. In Araucaria there are usually only three morphological axis orders (ax 0, ax 1, ax 2 ), the exception being A. cunninghamii, which consistently has four orders (i.e., adds an ax 3 ). Wollemia is distinctive because there are only two orders, ax 0 and ax 1. Agathis essentially produces two branch orders, but repeats first-order branches (ax 1 ) at higher orders of topographic branching. Topographic branching of this kind occurs throughout the family, largely by the processes of reiteration. Units of extension The basic unit of monopodial trunk construction in Araucariaceae may be referred to as the unit of extension. Each unit is represented by a trunk segment and the series of plagiotropic branches (ax 1 ) that constitutes each tier produced by rhythmic growth (Figs. 1-6). A similar method of analysis has been used in the description of Phyllocladus (Tomlinson et al. 1989). In seedling axes, tiers are indistinct because they include only one ax 1 ; but the number of branches per tier increases to a relative constant value as the sapling develops, the value somewhat diagnostic for each species (Veillon 1980). Each unit reflects the alternation of a cycle of extension with a period of dormancy (Figs. 1-4). Agathis and Araucaria differ in the method of construction of these units. In Araucaria (Figs. 1, 2) the renewal of growth of the trunk apex produces an extending leader that initially grows above the previous tier. The leader then produces the tier of branches at the top of the cycle of extension (Fig. 1). The trunk apex then enters the dormant phase and remains quite inconspicuous, even though the branch tier continues its growth and soon starts to produce the next order of branches (ax 2 ) as in Fig. 2 while the trunk apex is dormant. The top of the tree is then represented by the youngest branch tier, rather than an unbranched leader, with the terminal bud enclosed by normal needle-shaped foliage leaves. In Araucaria rhythmic growth of the trunk may be non-seasonal and often irregular, producing several, one or no branch tiers per year, whereas the activity of the higher order branches can proceed quite independently. This disconnection of growth phases in different parts of the tree is not uncommon in tropical trees, but remains little quantified. The unit of extension is represented diagrammatically in Fig. 5 for comparison with Agathis. Agathis, in contrast, shows a different construction of its units of extension because the tier of first-order branches (ax 1 ) is produced at the base of the unit of extension. Here the dormant trunk apex is protected by bud-scales (Fig. 3) developed as a gradual transition from broad foliage leaves to short bud-scales. The initials of the branch tier must be present in the dormant bud, because they extend immediately upon bud burst, each ax 1 usually being subtended by a scale or transitional leaf rather than a foliage leaf. The unit of extension is represented diagrammatically in Fig. 6 for comparison with Araucaria. In vigorous shoots there may be further branches in a distal direction, so that the branch tier is somewhat diffuse or appears to repeat within the extension cycle. The length of the unit of extension varies with the age of the tree and the position of the parent shoot in the outer part of the canopy. Distal increments may be very short, and all leaves on the parent axis are scale leaves, as in Fig. 4. Agathis australis in New Zealand shows that extension units can be produced annually so that branch tiers provide an estimate of shoot and tree age. The crown structure of Agathis is at first sight more complex than Araucaria, but is most precise in the young sapling, as described later.

4 9: Crown structure 53 Figures 1-4: Extension units of Araucaria and Agathis compared. Figs.1, 2, Araucaria nemorosa. Fig. 1, Apex of young sapling showing unit of extension and the morphology of trunk axis and two branch orders. Fig. 2, Older specimen with dormant bud of trunk axis (ax 0 ) and uppermost branch tier with 5 ax 1. Figs. 3, 4, Agathis ovata. Fig. 3, Apex of sapling from above showing dormant bud of trunk axis (ax 0 ) and uppermost tier with 5 ax 1. Fig. 4, Apex of an adult first-order branch (ax 1 ) that has reverted to trunk morphology. Inter-tier intervals are short and most foliage is on the ultimate axes, with essentially decussate phyllotaxis. Figures 5-6: Diagram of shoot extension units in Araucaria (Fig. 5) and Agathis (Fig. 6). Each diagram represents a cycle of growth during production of one unit of extension. A, Apical bud of trunk axis in resting condition. B, Initiation of a cycle of extension by bud burst. C, Completion of the cycle of extension; apical bud enters a new dormant phase. In Araucaria the branch tier is developed toward the end of a cycle of extension (C), but in Agathis it is usually produced at the beginning. In both examples branching is sylleptic, although Agathis presumably initiates branches within the terminal bud.

5 54 Section 2: Morphology, phylogeny, systematics and ecology Syllepsis and prolepsis The production of branches that are synchronous with the parent axis in their initiation and extension is referred to as syllepsis, in contrast to prolepsis, in which the branch grows out after a period of bud dormancy, as is common in temperate trees (Hallé et al. 1978). Agathis and Araucaria thus both exhibit sylleptic branching, but only Agathis exhibits the distinctive morphological feature of an extended basal internode (hypopodium), a characteristic feature of this type of branching (Fig. 4). The congested leaf insertion of Araucaria shoots does not permit this morphology, but the continuity of pith between branch and parent axis resulting from syllepsis is clear (Fig. 9). Araucaria Araucaria heterophylla architecture Norfolk Island pine (Figs. 7-11) is used as a type with which other taxa may be compared, because it is familiar in cultivation and, at least in its initial stages of development, it conforms strictly to Massart s model (Fig. 7). The species is used only as a descriptive model; the idea that it in any way represents an evolutionary ancestral type should be avoided. The tree shows most clearly the three axis types, with their individual morphological features, as summarized in Table 1. (a) Trunk axis (ax 0 ): The orthotropic axis is developed by a shoot apical meristem that maintains strict apical control over lateral branch expression (Fig. 8). The persistence and autonomy of the trunk apex results in a seemingly constant phyllotaxis that repeats in each extension unit. There is a pseudowhorled arrangement of branches at each tier, with each ax 1 inserted at a slightly different level. Pith (medulla) of branch and trunk are continuous, a structural consequence of sylleptic branching (Fig. 9). (b) First-order branches (ax 1 ): These are plagiotropic, and at first slightly inclined upward, but bending under their own weight with age. Dorsiventral symmetry results from the continuous series of lateral branches (ax 2 ) in two lateral orthostichies (Fig. 8), the series commencing beyond an initial branch-free zone (cf. Fig. 2). Branching is clearly independent of needle phyllotaxis, and the ax 2 can be opposite, sub-opposite or alternate. (c) Second-order branches (ax 2 ): These are the ultimate branches since they do not branch further. They are at first upwardly inclined and their planes of insertion represent a slight dihedral that may have aerodynamic benefit. They can continue growth for an extended (but not precisely known) period whereupon the apex aborts. Although longlived compared with the leaves of deciduous trees they are ultimately shed because they exhibit little secondary thickening, and so gradually lose a vascular connection to their parent axis. Details of the abscission mechanism are not known. Table 1: Axis differentiation in Araucaria heterophylla ax0 (= trunk) ax1 (1 st order branch) ax2 (2 nd order branch) Symmetry radial dorsiventral radial Growth Indeterminate, rhythmic long-lived, continuous determinate, continuous Branches tiered distichous absent Physiognomy orthotropic plagiotropic plagiotropic Orientation erect ± horizontal ± horizontal to pendulous Reproductive structures absent absent terminal Reiteration complete (ax0) partial (ax1) absent Secondary growth abundant limited ± absent

6 9: Crown structure 55 Figures 7-11: Araucaria heterophylla; architecture and reiteration. Fig. 7, Young tree representing Massart s model very precisely, the three axis types (ax 0, ax 1 and ax 2 ) clearly differentiated. Fig. 8, Crown of a sapling with juvenile foliage; ax 0 (trunk axis) with radial symmetry and early development of young tier of branches toward the end of unit of extension; ax 1 (first-order branches) with dorsiventral symmetry by virtue of two-ranked disposition of unbranched ax 2 (second-order branches). Fig. 9, Transverse sections in sequence through a branch tier to show pith connection between branch and trunk axis. A is uppermost, with a 1 cm interval between A, B and B, C. Fig. 10, Partial reiteration on ax 1, the proliferating shoots each with the repeated morphology of an ax 1. Fig. 11, Complete reiteration of an ax 0 from the decapitated stump of a young tree. In addition there are numerous partial reiterations of ax 1 from the old bases of broken ax 1.

7 56 Section 2: Morphology, phylogeny, systematics and ecology (d) Sexual reproduction: Cones are produced only in older trees and terminate ax 2. Male cones are at the end of extended axes, which are part of the photosynthetic machinery since they can persist long after the cones are shed. Female cones are borne distal to the male on short thick and usually erect ax 2, but are soon lost after seed shed. Sexuality thus has no influence on overall architecture, a feature of Massart s model. (e) Framework: In terms of exploration and exploitation the framework of the tree is represented by the trunk and first-order axes (Fig. 7). This represents little more than a mast and spars - so it is not surprising that they aroused the interest of the crew of James Cook s Endeavour! The framework fills space well, as axes of exploration, but represents a very limited photosynthetic potential. The assimilative capacity of the tree is supplied collectively by the relatively ephemeral ax 2 shoots, with very uniform construction and progressively increasing length (Figs. 7, 11). These are the axes of exploitation. (f) Assimilative ability: Quantitative analysis in terms of exploration demonstrates the collective importance of ax 2 in terms of photosynthetic capacity. In a small tree only 2 m tall the total length of all ax 2 is about 40 times the combined lengths of ax 0 and all ax 1 and represents about 97% of the total number of all axes. Even in such a small specimen the measured total length of all ax 2 is about 600 m. This shows how efficient the tree is in filling space by close packing. These comparisons are valid because the awl-shaped true leaves are relatively uniformly spaced along every axis with internodes between 1.0 and 1.5 mm long. This gives a total value of needles for the 6 m tree. Clearly, the photosynthetic capacity of a mature tree is enormous, and one can estimate values of beyond 100 km for the assembled length of ax 2 in a tall specimen. Araucaria heterophylla - reiteration (a) Partial reiteration branches: In the early stages of development of this species, growing precisely according to its architectural model as older ax 2 are lost (Fig. 7), the inner portion of the crown becomes progressively leafless so that the assimilative portion of the tree should assume the shape of a hollow cone. The proportion of photosynthetic tissue to framework tissues would also progressively decrease as secondary tissues are added to trunk and first-order branches. In-filling of the framework is normally the result of regeneration of ax 1 representing a partial reiteration of the tree form. Initially this occurs from meristems on the older parts of the ax 1, usually on the upper surface of the branch (Fig. 10). These repeat the morphology of an ax 1, but represent, of course, topographically a higher branch order. Similar meristems become active as second-order ax 1 at the base of the original branches that have either been abscised or broken off mechanically. This proliferation of ax 1 produces the long-lived and rather irregular lateral branch complex that characterizes older trees and in-fills the center of the previous hollow cone. Where this is a regular feature conditioned largely by shedding of older branches in a somewhat programmed way, a series of successive crowns develop, each nested within and below the crown above - the nesting crowns to use the terminology of Veillon (1978), who describes them fully (cf. Fig. 19). Araucaria heterophylla in sheltered situations tends to develop a broadly pyramidal crown although older branch complexes often break under their own weight. Broken branches still reiterate so the exploitative capacity of axes is long sustained. (b) Total reiteration trunks: Reiteration of trunk axes (ax 0 ) can occur and is very striking because the total architecture of the model is reproduced, although the result tends to disrupt the symmetrical topology of the canopy. Because the overall architecture

8 9: Crown structure 57 is repeated, such new units can resemble small trees inserted into the canopy. They are particularly noticeable if they develop on the trunk axis of a tall tree whose top has been broken. This process may also account for the infrequent appearance of forked trunks, although a true dichotomy cannot be ruled out. An artificial generation of new ax 0 can be used to supply Christmas trees on a repetitive commercial scale. If a small tree (trunk diameter c. 15 cm) is decapitated close to the ground, it will reiterate one or more treelets that can be culled at any desirable length and the process repeated (Fig. 11). From the same stump, reiterated ax 1 can be produced, presumably from the base of old branch stumps. The general rule that seems to operate is that each axis type reiterates its own kind, ax 0 produce second generation ax 0 whereas ax 1 produces only second generation ax 1 (Table 1). All these reiterated axes seem to result from the consistent presence of axillary meristems (i.e., not buds but small patches of meristematic tissue that are persistent remnants of the original shoot apex). This process has been well documented by Burrows (1986, 1987, 1989, 1990b, 1999) and summarized elsewhere in this volume. The distinctive feature of this process is that a small patch of meristematic tissue has the developmental potential largely determined by its position within the framework of the parent tree. This property may be generalized in conifers, but has been little studied (cf. Fink 1984). This summary provides the background necessary to an understanding of crown form in all Araucaria spp. because the same developmental features are possible in all of them, but their varying expression accounts for contrasted shape in different species. Diversity within Araucaria (a) Section Eutacta (Eutassa): Veillon (1978, 1980) has described canopy modification in New Caledonian species of Araucaria, all members of section Eutacta, to which A. heterophylla belongs. Here we add information about the other three sections, i.e. sect. Araucaria (or Columbea), to which the two South American species belong, sect. Bunya (i.e. A. bidwillii) and sect. Intermedia (A. cunninghamii and A. hunsteinii). In New Caledonia most species are like A. heterophylla but with a much more columnar shape, as in A. columnaris, producing the spire-like physiognomy used as an icon in New Caledonian publicity (Fig. 12). This form essentially is also shown by A. bernieri, A. biramulata, A. humboldtensis, A. laubenfelsii, A. luxurians, A. montana, A. nemorosa, A. schmidii, A. scopulorum and A. subulata. That these species are closely related is indicated by the inability of current molecular systematic techniques to resolve their relationships, at least by the use of rbcl genes (Setoguchi et al. 1998). In many of them partial reiteration of ax 1 at the base of the tree may be limited so that the persistent scars of the branch tiers then form conspicuous rings on the trunk (cf. Figs. 13, 19). A characteristic feature of this canopy form is that the upper portion of the trunk shows the model-conforming physiognomy clearly, with variation determined by the spacing of successive branch tiers. The top of the tree is thus normally narrowly conical. However, where elongation growth slows with age, branch tiers are crowded, and a candelabra form results as the ax 1 grow in length without corresponding trunk growth. Veillon (1980) illustrates this for A. humboldtensis, A. schmidii and A. scopulorum. Otherwise the sparseness or density of the canopy is determined by the rate of production of ax 1 on older parts of the trunk as a result of partial reiteration. Araucaria rulei is distinctive because it conforms almost precisely to the model, and virtually lacks any form of reiteration (Fig. 14). The crown consequently is without infilling. Furthermore the distal extremity of each ax 1 shows radial placement of the ax 2 and a tendency to turn erect. Araucaria muelleri is comparable, reflecting its close systematic position (Setoguchi et al. 1998). Both species are characterized by thick ultimate axes, up to 5 cm diameter

9 58 Section 2: Morphology, phylogeny, systematics and ecology Figures 12-15: Araucaria spp., variation in crown structure. Fig. 12, A. columnaris. Spire-like form with continued replacement of relatively short-lived ax 1. Fig. 13, A. rulei, base of trunk of a young tree, the hoops representing the expanded base of the members of each branch tier but without reiterated ax 1. Fig. 14, A. rulei, model confirming tree without reiteration; the distal extremity of each ax 1 shows radial symmetry reminiscent of Rauh s model. Fig. 15, A. cunninghamii, top of the crown of a young tree with plumose first-order (ax 1 ) branch complexes. A third-order (ax 3 ) branch system is regularly added and combined with radial symmetry of ax 1 and orthotropy produces a relatively closed canopy.

10 9: Crown structure 59 overall (de Laubenfels 1972). Veillon (1980) describes A. muelleri and A. rulei as Rauh s model, but there is never any distal reversion of an ax 1 to an ax 0 capable of repeating the tree s total architecture. Araucaria montana is similar, but more extensively reiterates and can produce numerous secondary trunks (Fig. 18). Araucaria cunninghamii (hoop pine) may be included in section Eutacta but is distinctive in crown form because it consistently produces a third-order series of axes on each first-order branch complex. The complexes become sub-erect and the overall bushy effect is striking as the crown is in-filled within the architectural model (Fig. 15). This morphology could justify inclusion in Rauh s model although there is little reversion of ax 0 to ax 1 and reiteration is limited. The distinctive physiognomy of this species accords well with its phylogeny, since it is the sister species to all other members of section Eutacta (Setoguchi et al. 1998). Araucaria biramulata can produce ax 3, but not consistently so and without pronounced influence on architecture. (b) Section Columbea: The South American species develop their distinctive flat-topped candelabra habit with age, but show the total range of Araucaria opportunistic shoot development. Araucaria araucana has been described in detail by Grosfeld et al. (1999) with a refreshing approach by quantifying several aspects of growth. Trees are unusual in being dioecious. They conform to Massart s model but again with some elements of Rauh s model in the tendency of ax 1 to dedifferentiate and become erect distally with a change to radial symmetry. Otherwise the characteristic morphological distinction between trunk, first and second order branches (i.e., ax 0, ax 1, ax 2 ) is maintained. A distinctive feature is that male cones are lateral on ax 2 and so constitute a further branch order (ax 3 ). Female cones, on the other hand are terminal on ax 2, but growth is continued by the development of a lateral branch successively below each cone. This sympodial development is very unusual in conifers. These authors also compare crown form in contrasted habitats. The characteristic physiognomy is expressed in forest stands, with the progressive loss of lower branches. One may contrast this with cultivated specimens in benign environments in which branches are especially long-lived and the trunk retains dead branches (Fig. 16). Although they have the developmental potential to produce new ax 1 by partial reiteration, trees do not develop nesting crowns and the canopy is not therefore infilled. Grosfeld et al. (1999) document several mechanisms for developing new trunk axes (ax 0 ) that mainly come from existing trunks, but root suckers are also reported (cf. Veblen 1982). Cut stumps can initiate new trunks (cf. Fig. 11) while basal sprouts (cf. Wollemia) and distal trunk reiteration (cf. Fig. 18) are reported. The ability of fallen trunks to reiterate new trunks is also remarkable. The form of the tree is an expression of the rate of trunk elongation in relation to branch elongation. Both are rhythmic but are not synchronized. The apical meristem of the trunk may remain dormant for up to nine years, even though the branches may be growing annually. The somewhat surprising conclusion is that despite having a very precise physiognomy the tree is very plastic in its growth expression it is capable of persisting in a suppressed state in a poor environment for up to 150 years, whereas in a favorable environment the architecture is deployed continually, with regular annual increments of both trunk and branch. The candelabra form of adult trees that provides such a striking icon for the Southern Andes is a result of the return to slow trunk growth with age (Veblen et al. 1995). Growth expression seems to be the most significant adaptive parameter, with minimum recruitment of new axes as a traumatic response.

11 60 Section 2: Morphology, phylogeny, systematics and ecology (c) Section Bunya: In A. bidwillii all features of the basic crown structure of Araucaria exist, but reiterative processes are limited and obvious nesting crowns are not developed (Fig. 17). The most distinctive feature is the rhythmic growth of ax 1 resulting in zones of short leaves alternating with more extended series of long leaves. Radial symmetry characterizes each branch complex (Fig. 17). Open grown trees may resemble A. araucana in a distinctly pyramidal habit. (d) Section Intermedia: Although A. hunsteinii (klinki pine) co-occurs with A. cunninghamii (hoop pine) in Papua New Guinea, the two are strongly contrasted in crown form since the former only produces two branch orders, as in the standard Araucaria model. Canopy development in A. hunsteinii involves extensive production of secondary ax 1 and distinctive nesting crowns do occur (Edelin 1986). Rhythmic growth of ax 1, comparable to that in A. bidwillii, is pronounced. Adaptive ecology The previous descriptive summary shows that deployment in varying degrees of a common set of developmental features can produce appreciable diversity of physiognomic expression. This diversity suggests how crown form may be functional in the successful survival of trees in natural habitats. Trees of the columnar Eutacta type (Fig. 12) seem well adapted to cyclone- or hurricane-prone environments. Araucaria columnaris retains its narrow crown by the regular shedding and replacement of ax 1 (Fig. 19), but in addition shows dramatic response to storm winds. Figure 20 illustrates a cultivated specimen in South Florida one year after Hurricane Andrew (1993) had stripped away all the ax 1 on the windward side, but leaving most axes on the leeward side to produce a banner tree. The initial result is to reduce wind drag almost completely and the tree remained upright. Canopy reconstruction begins immediately from old branch bases throughout the whole of the trunk so that the canopy is replaced within two years. Araucaria heterophylla in the same location was identical in its response. This suggests that the columnar habit of so many New Caledonian species (e.g., Figs. 12, 19) is most advantageous in allowing trees to become tall in exposed, and especially coastal, habitats. Trees in upland habitats (e.g. A. rulei, Fig. 14) never grow tall, but are probably wind resistant because of their open canopy. Reiteration is most likely to produce new ax o (Fig. 18) but these do not increase the density of the crown. Araucaria hunsteinii as described by Havel (1965) seems well adapted to forest conditions because a columnar, model-conforming stage allows the tree to grow in partial shade in secondary succession or in gaps within a well-developed forest canopy. Once extended above this canopy, the tree retains a columnar shape by extensive partial reiteration. This extension corresponds to the process of crown metamorphism described by Edelin (1986), in which there is a progressive change to radial symmetry of higher ax 1, i.e. in upper tiers. This recalls the same process obvious in A. bidwillii (Fig. 17). Agathis Crown structure in Agathis is very uniform and any species will show most features. Although assigned to Massart s model (Hallé et al. 1978) it is contrasted with Araucaria in the construction of extension units (Fig. 6) and the absence of marked shoot polymorphism. Broad leaves, extended internodes and development of bud scales are the most conspicuous features of shoot morphology. Architecture The monopodial trunk axis shows spiral phyllotaxis, radial symmetry (Fig. 3) and rhythmic growth, with an extended resting period between each cycle of elongation. The dormant period is marked subsequently by the scars of the bud-scales so that units of extension are clearly separated throughout the tree. The trunk produces regular branch tiers, each tier with a pseudowhorl of five to

12 9: Crown structure 61 Figures 16-20: Araucaria spp. Model conforming and reiterated trees. Fig. 16, A. araucana, avenue of trees with limited reiteration of ax 1 on ax 1, the branch complexes long-lived. Fig. 17, A. bidwillii, open grown tree almost without reiteration, the ax 1 long-lived and with radial symmetry. Fig. 18, A. muelleri, tree with extreme reiteration of trunk axes (ax 0 ) as a combination of the leaning primary trunk and possibly some trauma. Fig. 19, A. columnaris; young planted specimens with the uppermost ( primary ) crown without reiteration and three distinct nesting crowns, especially in the right-hand specimens; figure of Dr. J-M. Veillon for scale. Fig. 20, A. columnaris, banner tree representing the effect of Hurricane Andrew (1993) in Miami, Florida; all ax 1 have been lost on the windward side, but persist on the leeward side. Crown structure is being totally restored throughout the trunk by partial reiteration of new ax 1.

13 62 Section 2: Morphology, phylogeny, systematics and ecology seven ax 1. Syllepsis is obvious because of the long basal internode below the first leaf pair on the branch (Figs. 3 and 4). In some species (e.g. A. ovata) the trunk axis tends to produce only scale leaves. In the juvenile stage first-order branches (ax 1 ) are plagiotropic with dorsiventral symmetry and approximately horizontal orientation. In contrast to the spiral phyllotaxis of the trunk, leaves are irregularly decussate, although often sub-opposite rather than strictly opposite. The two-ranked symmetry of the mature branch is a result of the twisting of each internode so that leaf pairs are horizontal, followed by petiolar torsion so that the adaxial surface of each leaf becomes uppermost. This arrangement is common to many tropical trees and also occurs in the gymnosperm Gnetum gnemon. First-order branches (ax 1 ) repeat the rhythmic growth of the ax 0 and retain dorsiventral symmetry in branching because the resulting branch pairs are horizontal. The insertion of each branch is narrow and with limited secondary xylem; consequently the horizontal branch complex is determinate. It is eventually abscised in a precise way to leave a characteristic embossed scar (Licitis-Lindbergs 1956). The young tree thus maintains a narrow conical form, especially in the forest understorey, by virtue of the short life span or slow growth of the plagiotropic axes. The only change is the increase in leaf width to the adult form. This early narrow-crowned form is referred to by foresters as the ricker phase (a word of Saxon origin) and is important in establishing a long trunk without knots. Crown repair in the juvenile phase seems limited to occasional reiterated ax 1, as in Araucaria, and derived from an axillary meristem (Burrows 1987) persisting in the base of a pre-existing branch. A more significant change in older trees is dedifferentiation of ax 1 so that they turn erect distally, show a return to a spiral phyllotaxis and adopt the radial symmetry and tiered branches of a trunk axis (ax 0 ). In open-grown trees dedifferentiation occurs early and the crown assumes the appearance of a population of treelets attached to the original trunk (Fig. 21). Each treelet repeats the architecture of the adult trunk form. Maturity is demonstrated by the onset of sexuality with both male and female cones on short lateral axes within each cycle of extension growth. Very young female cones are contemporaneous with and almost indistinguishable from vegetative buds that also occur below the resting terminal bud. As major lateral axes are developed by this transition from plagiotropy to orthotropy, via an upward curvature beyond the branch insertion, the crown becomes broader, as in A. australis. Agathis ovata is distinguished by the straightness and upward slope of these axes. The process can be repeated at higher topographic branch orders so that the canopy becomes in-filled. Treelets of this dedifferentiated type retain abundant growth and their attachment to the parent trunk is robust. The oldest of these persistent axes represent the massive limbs of the mature tree (Fig. 22). This description, based on A. australis, corresponds to that for A. dammara by Edelin (1986) although the term crown metamorphism is used by him, implying a gradual change as the tree ages. Ecology The crown shape of the mature Agathis can be interpreted as a result of the metamorphosis from the juvenile to the adult state and is supported by extensive population analysis (Ogden & Stewart 1995). The ricker stage is maintained in the shaded condition of the forest understorey. Once the tree breaks through to full sunlight, dedifferentiation of ax 1 becomes pronounced, essentially as a population of explorative trunks on the main axis (Fig. 21). The population of ax 1 produced on these ax 0 represents the relatively short-lived exploitative ultimate branch complexes. The analysis of A. macrophylla on Vanikoro by Whitmore

14 9: Crown structure 63 Figures 21-22: Agathis australis. Crown form. Fig. 21, Open-grown tree with numerous dedifferentiated firstorder branches (ax 1 ) which turn erect and repeat the whole architecture of the tree; the crown is thus made of numerous upwardly curved treelets. Fig. 22, Majestic forest-grown tree ( Lord of the Forest ) with a massive extended branch-free bole. The level of insertion of the larger branches represents the level at which the ricker tree originally broke through the former forest canopy, i.e. reverted to the physiognomy of an opengrown tree, as in Figure 21. (1966) supports these interpretations. Crown repair from latent meristems is unnecessary since it has become a feature of the repeated expression of the architectural model, even though such latent meristems appear to exist (Burrows 1987). Once established above the forest canopy the framework is permanent and the tree is usually impregnable to all except the most violent storms and, of course, the woodsman s saw. Edelin (1986) notes how A. dammara coexists with dipterocarps in lowland Malesian forests, and presumes that this is the result of a similar crown metamorphism. Wollemia This newly-described tree shares features found in both Araucaria and Agathis, but is unique in several respects. Published descriptions (Hill 1997; Jones et al. 1995) indicate a trunk axis (ax 0 ) with rhythmic monopodial growth producing plagiotropic axes (ax 1 ) in regular tiers, i.e., Massart s model in the Hallé-Oldeman system (Hallé et al. 1978). The juvenile phase is distinctive because the pseudowhorls are relatively close set and dorsiventrality of ax 1 is precise, with two ranks of narrow leaves. This suggests decussate

15 64 Section 2: Morphology, phylogeny, systematics and ecology phyllotaxis with secondary leaf orientation, as in Agathis. The adult phase is distinctive because the first-order branches (ax 1 ) remain unbranched, i.e., without ax 2 so that the trunk bears only one series of branches. The decussate arrangement of the adult foliage seems responsible for the four ranks of broad leaves, recalling Agathis ovata (Fig. 4). Both male and female cones are said to terminate the branches so that ax 1 are determinate by sexuality, a condition possibly unique for conifers. It is not stated whether conebearing axes subsequently can continue vegetative growth by sympodiality, as can occur in the otherwise determinate ax 2 of some Araucaria species (e.g. Grosfeld et al. 1999; Veillon 1978). First-order axes (ax 1 ), as in Araucaria, although long-lived are eventually shed, stripping the trunk of all foliage. How can a canopy be maintained? Two methods of reiteration seem to occur. In the first there is development of a second and subsequent generations of first-order axes by partial reiteration, in the manner of Araucaria columnaris, but without the development of obvious nesting crowns. Secondly, and more significantly, there is dedifferentiation of firstorder branches so that ax 1 essentially revert to ax 0 and so replicate the whole adult architecture of the tree. This suggests the same mechanism as in Agathis but without producing a broad crown, presumably because higher order branches are not produced. The framework of the tree may thus largely be the result of reiteration, which is based on the same mechanism for sequestering axillary meristems as is found in the rest of the family (Burrows 1999). A distinctive feature of Wollemia is the development of basal shoot suckers that can form a palisade of apparently derivative trunks, although it is not known if these are stemor root-borne. Hill (1997) suggests this as a unique feature since it is rare in conifers (e.g. Sequoia), but basal suckering is reported for the South American species (Grosfeld et al. 1999; Veblen 1982) and the potential exists in A. cunninghamii (Burrows 1990b). Traumatized roots in A. cunnninghamii can produce new shoots (Burrows 1990a). If basal sprouting is an architectural feature, as implied by Hill (1997), then Wollemia would indeed be unique. Wollemia survives in deep, moist, sheltered canyons that apparently provide refugia from dry, windy and fire-prone environments. Subsequent cultivation and progressive monitoring should provide the opportunity to resolve some of the many uncertainties that still exist in our understanding of this distinctive tree. Conclusions These preliminary observations show that the three genera of Araucaria have contrasted canopy structures although based on a range of shared common features. In this sense they represent three reference points in an architectural continuum. The contrasted features seem adaptive in the distinctive environment occupied by each genus. Further research is needed, especially in the quantitative understanding of shoot disposition, the precise observation of phenological patterns and the details of shoot phyllotaxis. The underlying basis for much of the adaptive construction lies in the remarkable ability of all trees to sequester meristematic tissue as axillary meristems, emphasized by Burrows et al. (1988). This has very important economic implications, as elite trees are selected and propagated for plantation purposes or stump sprouts generated for decorative purposes (Fig. 11). Propagation of species that are endangered, of which Wollemia is an outstanding icon, depends on extensive knowledge of the inherent mechanisms that control canopy form throughout the family. References Burrows, G.E Axillary meristem ontogeny in Araucaria cunninghamii Aiton ex D. Don. Australian Journal of Botany 34: Burrows, G.E Leaf axil anatomy in the Araucariaceae. Australian Journal of Botany 35:

16 9: Crown structure 65 Burrows, G.E Developmental anatomy of axillary meristems of Araucaria cunninghamii released from apical dominance following shoot apex decapitation in vitro and in vivo. Botanical Gazette 150: Burrows, G.E. 1990a. Anatomical aspects of root bud development in hoop pine (Araucaria cunninghamii). Australian Journal of Botany 38: Burrows, G.E. 1990b. The role of axillary meristems in coppice and epicormic bud initiation in Araucaria cunninghamii. Botanical Gazette 151: Burrows, G.E Wollemi pine (Wollemia nobilis, Araucariaceae) possesses the same unusual leaf axil anatomy as other investigated members of the family. Australian Journal of Botany 47: Burrows, G.E.; Doley, D.D.; Haines, R.J.; Nikles, D.G In vitro propagation of Araucaria cunninghamii and other species of the Araucariaceae via axillary meristems. Australian Journal of Botany 36: de Laubenfels, D.J Gymnospermes. In Aubréville, A.; Leroy, J-F. (eds.). Flore de la Nouvelle-Calédonie et Dépendances 4. Muséum National d Histoire Naturelle, Paris: pp Edelin, C Images de l architecture des Conifères. Thesis. Université des Sciences et Techniques du Languedoc, Montpellier. Edelin, C Stratégie de reiteration et édification de la cime chez les conifères. In L Arbre: compte-rendu du Colloque international L Arbre. Naturalia Monspeliensia, Institut de Botanique, Montpellier: pp Fink, S Some cases of delayed or induced development of axillary buds from persisting detached meristems in conifers. American Journal of Botany 71: Grosfeld, J.; Barthélémy, D.; Brion, C Architectural variations of Araucaria araucana (Molina) K. Koch (Araucariaceae) in its natural habitat. In Kurmann, M.H.; Hemsley, A.R. (eds.). The evolution of plant architecture. Royal Botanic Gardens, Kew: pp Hallé, F.; Oldeman, R.A.A.; Tomlinson, P.B Tropical trees and forests: an architectural analysis. Springer Verlag, Berlin. Havel, J.J The Araucaria forests of New Guinea and their regenerative capacity. Journal of Ecology 59: Hill, K.D Architecture of the Wollemi pine (Wollemia nobilis, Araucariaceae), a unique combination of model and reiteration. Australian Journal of Botany 45: Jones, W.G.; Hill, K.D.; Allen, J.M Wollemia nobilis, a new living genus and species in the Araucariaceae. Telopea 6: Licitis-Lindbergs, R Branch abscission and disintegration of the female cones of Agathis australis Salisb. Phytomorphology 6: Ogden, J.; Stewart, G.H Community dynamics of the New Zealand conifers. In Enright, N.J.; Hill, R.S. (eds.). Ecology of the southern conifers. Smithsonian Institution Press, Washington, D.C.: pp Setoguchi, H.; Osawa, T.A.; Pintaud J-C.; Jaffré T.; Veillon J-M Phylogenetic relationships within Araucariaceae based on rbcl gene sequences. American Journal of Botany 85: Tomlinson, P.B.; Takaso, T.; Rattenbury, J.A Developmental shoot morphology in Phyllocladus (Podocarpaceae). Botanical Journal of the Linnean Society 99: Veblen, T.T Regeneration patterns in Araucaria araucana forests in Chile. Journal of Biogeography 9: Veblen, T.T.; Burns, B.R.; Kitzberger, T.; Lara, A.; Villalba, R The ecology of the conifers of South America. In Enright, N.J.; Hill, R.S. (eds.). Ecology of the southern conifers. Smithsonian Institution Press, Washington, D.C.: pp Veillon, J-M Architecture of the New Caledonian species of Araucaria. In Tomlinson, P.B.; Zimmermann, M.H. (eds.). Tropical trees as living systems. Cambridge University Press, Cambridge: pp Veillon, J-M Architecture des espèces néocalédoniennes du genre Araucaria. Candollea 35: Whitmore, T.C The social status of Agathis in a rainforest in Melanesia. Journal of Ecology 54: