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: mo- nopodial 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 Arau- caria , 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 cy- clone -prone habitats and may account for the adaptive radiation in New Caledonia. Future requirements are for quantitative analysis and experimental manipulation.

Introduction Araucaria and Agathis. In view of this diver- sity the following account can only be pre- Trees in the family Araucariaceae, as exem- liminary. We do have an exemplary descrip- plified by the commonly cultivated Araucaria tion of Araucaria in New Caledonia by Veil- heterophylla (Norfolk Island pine), have a dis- lon (1978, 1980), which is closely followed tinctive crown form that makes them easily here. Opportunity to study the problem at recognized. What is the ecological signifi- first-hand has been provided by the cultiva- cance of this form? The question can only be tion of Araucaria in the tropics and sub- answered with knowledge about the devel- tropics outside its natural range. Araucaria opment of the crown. At the same time it is araucana (monkey puzzle) is a frequent Vic- clear that the three genera in the Araucari- torian relict in British and Irish gardens, aceae are distinctly different in the method while the recent IDS excursion to New Cale- of crown construction. Again one might ask donia allowed the study of Agathis and Arau- “what ecological inferences can be gained caria species in natural environments and in from a comparison of Agathis, Araucaria and cultivation. Agathis australis has been studied Wollemia?” Agathis is relatively uniform in extensively in New Zealand. crown form but Araucaria is quite diverse, appropriate for a genus with a considerable Architecture geographic range. The diversity of Araucaria Following the principles laid out in Hallé et includes, on the one hand, the spire-like or al. (1978), the mature canopy of the tree can columnar shape of A. columnaris, a form that be perceived as the sum of two processes. excited the crew of James Cook’s First, there is the architectural model of “Endeavour” when they first saw New Cale- the tree, i.e., the growth plan inherent in its donia, and on the other hand trees with a genetic make-up. The visible expression of candelabra habit, as represented by Araucaria this model at any one moment in time is the araucana of the Chilean Andes. Wollemia, in architecture of the tree. Second, there is the so far as it is known, combines features of partial or total repetition of this model (i.e., 9: Crown structure 51 its reiteration) as a response either to unique feature of the tree, based on his very trauma (physical damage) or some change in extensive and detailed observations (Burrows the immediate environment of the tree that 1986, 1987, 1989, 1990b, 1999, and this vol- disrupts the underlying model. The tree ume). Even with a considerable supply of most precisely conforms to its model as a “reserve” meristems of this kind, a contin- well-grown sapling, but reiteration becomes uum of crown structures is realized. Other progressively more important as the tree ages conifers have similar axillary meristems al- because it makes the developmental plan though these may be relatively short-lived more adaptable to changing circumstances. (Fink 1984). Members of the Araucariaceae may consis- Explore and exploit tently be referred to Massart’s model in the Hallé-Oldeman typology (Hallé et al. 1978) In interpreting the crown architecture of a since the trunk axis is monopodial (i.e., with tree as functionally efficient in both photo- a permanent leader) and exhibits rhythmic synthetic ability and mechanical stability, it growth in the form of regular production of is useful to describe the tree in terms of a branch tiers (pseudowhorls) but with vari- permanent mechanical “framework” (derived able spacing. The trunk axis is vertical and from the architectural model), which bears with radial symmetry (orthotropic), whereas relatively ephemeral photosynthetic units as branches are essentially horizontal and have either leaves or shoots. This approach, devel- dorsiventral symmetry (plagiotropic). Some oped by French morphologists (e.g. Edelin extension of this model in terms of Rauh’s 1977) sees the tree as a series of axes that model is included in Veillon’s descriptions initially “explore” the space available for because in some species the distal ends of making a canopy. These “axes of explora- older axes become erect and radially sym- tion” constitute the framework of the tree, metrical. Apart from the relatively constant which supports the “axes of exploitation,” framework of the tree implied in these de- i.e., the ultimate assimilating units. An ex- scriptions, a family character is the high de- ample would be the familiar Ginkgo biloba in gree of axis polymorphism such that axes of cultivation in temperate countries. The axes different branch orders can have distinctive of exploration are the long-shoots, which morphological features, resulting in a highly have a precise disposition according to Mas- efficient photosynthetic system. In leaf sart’s model, producing a framework re- shape the most immediate contrast is be- vealed in the winter leafless condition. The tween the needle-like or awl-shaped leaves of axes of exploitation are the short-shoots that many Araucaria species and the broad, flat- produce most of the leaves clothing the tree tened leaves of Agathis, Wollemia and several in summer. This represents the ultimate de- Araucaria species. All species in the family gree of axis differentiation. Araucaria can be have a highly distinctive juvenile morphol- described readily according to this approach, ogy that is contrasted with the morphology Agathis less easily. of adult shoots. Reiteration in the family is Branch orders expressed either in the replacement of lost orthotropic and plagiotropic axes, together A consistent terminology for axis orders with a dedifferentiaton whereby plagiotropic designates the trunk axis as axo, with succes- axes revert to orthotropy as derived trunk sively higher branch orders as ax1, ax2 …. axes. Replacement axes are developed from etc. This immediately designates branch or- axillary meristems that originate in most leaf ders by the appropriate suffix and allows the axils and may persist throughout the life of comparison of crown structure in different the tree. This abundant supply of reserve trees. A distinction has to be made between meristems is considered by Burrows to be a the topographic order, i.e. the visible 52 Section 2: Morphology, phylogeny, systematics and ecology sequence of axes within the tree, and the tree is then represented by the youngest morphological order, where each axis order branch tier, rather than an unbranched within the architectural model can be recog- leader, with the terminal bud enclosed by nized by its distinctive morphological fea- normal needle-shaped foliage leaves. In Arau- tures without regard to its placement in the caria rhythmic growth of the trunk may be tree. In Araucaria there are usually only three non-seasonal and often irregular, producing morphological axis orders (ax0, ax1, ax2), the several, one or no branch tiers per year, exception being A. cunninghamii, which con- whereas the activity of the higher order sistently has four orders (i.e., adds an ax3). branches can proceed quite independently. Wollemia is distinctive because there are only This disconnection of growth phases in dif- two orders, ax0 and ax1. Agathis essentially ferent parts of the tree is not uncommon in produces two branch orders, but repeats tropical trees, but remains little quantified. first-order branches (ax1) at higher orders of The unit of extension is represented dia- topographic branching. Topographic branch- grammatically in Fig. 5 for comparison with ing of this kind occurs throughout the fam- Agathis. ily, largely by the processes of reiteration. Agathis, in contrast, shows a different con- Units of extension struction of its units of extension because the tier of first-order branches (ax ) is pro- The basic unit of monopodial trunk con- 1 duced at the base of the unit of extension. struction in Araucariaceae may be referred to Here the dormant trunk apex is protected by as the “unit of extension.” Each unit is repre- bud-scales (Fig. 3) developed as a gradual sented by a trunk segment and the series of transition from broad foliage leaves to short plagiotropic branches (ax ) that constitutes 1 bud-scales. The initials of the branch tier each tier produced by rhythmic growth must be present in the dormant bud, because (Figs. 1-6). A similar method of analysis has they extend immediately upon bud burst, been used in the description of Phyllocladus each ax usually being subtended by a scale (Tomlinson et al. 1989). In seedling axes, 1 tiers are indistinct because they include only or transitional leaf rather than a foliage leaf. The unit of extension is represented dia- one ax1; but the number of branches per tier increases to a relative constant value as the grammatically in Fig. 6 for comparison with sapling develops, the value somewhat diag- Araucaria. In vigorous shoots there may be nostic for each species (Veillon 1980). Each further branches in a distal direction, so that unit reflects the alternation of a cycle of ex- the branch tier is somewhat diffuse or ap- tension with a period of dormancy (Figs. 1- pears to repeat within the extension cycle. 4). Agathis and Araucaria differ in the The length of the unit of extension varies method of construction of these units. In with the age of the tree and the position of Araucaria (Figs. 1, 2) the renewal of growth the parent shoot in the outer part of the can- of the trunk apex produces an extending opy. Distal increments may be very short, leader that initially grows above the previous and all leaves on the parent axis are scale tier. The leader then produces the tier of leaves, as in Fig. 4. Agathis australis in New branches at the top of the cycle of extension Zealand shows that extension units can be (Fig. 1). The trunk apex then enters the dor- produced annually so that branch tiers pro- mant phase and remains quite inconspicu- vide an estimate of shoot and tree age. The ous, even though the branch tier continues crown structure of Agathis is at first sight its growth and soon starts to produce the more complex than Araucaria, but is most next order of branches (ax2) as in Fig. 2 while precise in the young sapling, as described the trunk apex is dormant. The top of the later. 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 repre- sents a cycle of growth during production of one unit of extension. A, Apical bud of trunk axis in resting con- dition. 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. 54 Section 2: Morphology, phylogeny, systematics and ecology

Syllepsis and prolepsis maintains strict apical control over lateral branch expression (Fig. 8). The persistence The production of branches that are syn- and autonomy of the trunk apex results in a chronous with the parent axis in their initia- seemingly constant phyllotaxis that repeats tion and extension is referred to as syllepsis, in each extension unit. There is a pseudo- in contrast to prolepsis, in which the branch whorled arrangement of branches at each grows out after a period of bud dormancy, as tier, with each ax1 inserted at a slightly dif- is common in temperate trees (Hallé et al. ferent level. Pith (medulla) of branch and 1978). Agathis and Araucaria thus both ex- trunk are continuous, a structural conse- hibit sylleptic branching, but only Agathis quence of sylleptic branching (Fig. 9). exhibits the distinctive morphological fea- ture of an extended basal internode (b) First-order branches (ax1): These are pla- (hypopodium), a characteristic feature of giotropic, and at first slightly inclined up- this type of branching (Fig. 4). The con- ward, but bending under their own weight gested leaf insertion of Araucaria shoots does with age. Dorsiventral symmetry results not permit this morphology, but the conti- from the continuous series of lateral nuity of pith between branch and parent branches (ax2) in two lateral orthostichies axis resulting from syllepsis is clear (Fig. 9). (Fig. 8), the series commencing beyond an initial branch-free zone (cf. Fig. 2). Branching Araucaria is clearly independent of needle phyllotaxis, and the ax can be opposite, sub-opposite or Araucaria heterophylla – architecture 2 alternate. Norfolk Island pine (Figs. 7-11) is used as a type with which other taxa may be com- (c) Second-order branches (ax2): These are the pared, because it is familiar in cultivation ultimate branches since they do not branch and, at least in its initial stages of develop- further. They are at first upwardly inclined ment, it conforms strictly to Massart’s and their planes of insertion represent a model (Fig. 7). The species is used only as a slight dihedral that may have aerodynamic descriptive model; the idea that it in any benefit. They can continue growth for an way represents an evolutionary ancestral extended (but not precisely known) period type should be avoided. The tree shows most whereupon the apex aborts. Although long- clearly the three axis types, with their indi- lived compared with the leaves of deciduous trees they are ultimately shed because they vidual morphological features, as summa- exhibit little secondary thickening, and so rized in Table 1. gradually lose a vascular connection to their

(a) Trunk axis (ax0): The orthotropic axis is parent axis. Details of the abscission mecha- developed by a shoot apical meristem that nism are not known.

Table 1: Axis differentiation in Araucaria heterophylla

ax0 (= trunk) ax1 (1st order branch) ax2 (2nd 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 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 juve- nile 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. 56 Section 2: Morphology, phylogeny, systematics and ecology

(d) Sexual reproduction: Cones are produced Araucaria heterophylla - reiteration only in older trees and terminate ax2. Male (a) Partial reiteration – branches: In the early cones are at the end of extended axes, which stages of development of this species, grow- are part of the photosynthetic machinery ing precisely according to its architectural since they can persist long after the cones are model as older ax are lost (Fig. 7), the inner shed. Female cones are borne distal to the 2 portion of the crown becomes progressively male on short thick and usually erect ax , 2 “leafless” so that the assimilative portion of but are soon lost after seed shed. Sexuality the tree should assume the shape of a hollow thus has no influence on overall architecture, cone. The proportion of photosynthetic tis- a feature of Massart’s model. sue to framework tissues would also progres- (e) Framework: In terms of “exploration” and sively decrease as secondary tissues are added “exploitation” the framework of the tree is to trunk and first-order branches. In-filling represented by the trunk and first-order axes of the framework is normally the result of (Fig. 7). This represents little more than a regeneration of ax1 representing a partial mast and spars - so it is not surprising that reiteration of the tree form. Initially this oc- they aroused the interest of the crew of curs from meristems on the older parts of James Cook’s “Endeavour”! The framework the ax1, usually on the upper surface of the fills space well, as “axes of exploration,” but branch (Fig. 10). These repeat the morphol- represents a very limited photosynthetic po- ogy of an ax1, but represent, of course, to- tential. The assimilative capacity of the tree pographically a higher branch order. Similar is supplied collectively by the relatively meristems become active as second-order ax1 at the base of the original branches that have ephemeral ax2 shoots, with very uniform construction and progressively increasing either been abscised or broken off mechani- length (Figs. 7, 11). These are the “axes of cally. This proliferation of ax1 produces the long-lived and rather irregular lateral branch exploitation”. complex that characterizes older trees and (f) Assimilative ability: Quantitative analysis in-fills the center of the previous hollow in terms of exploration demonstrates the cone. Where this is a regular feature condi- collective importance of ax2 in terms of pho- tioned largely by shedding of older branches tosynthetic capacity. In a small tree only 2 m in a somewhat programmed way, a series of tall the total length of all ax2 is about 40 successive crowns develop, each nested times the combined lengths of ax0 and all ax1 within and below the crown above - the and represents about 97% of the total num- “nesting crowns” to use the terminology of ber of all axes. Even in such a small specimen Veillon (1978), who describes them fully (cf. the measured total length of all ax2 is about Fig. 19). Araucaria heterophylla in sheltered 600 m. This shows how efficient the tree is situations tends to develop a broadly py- in filling space by close packing. These com- ramidal crown although older branch com- parisons are valid because the awl-shaped plexes often break under their own weight. true leaves are relatively uniformly spaced Broken branches still reiterate so the ex- along every axis with internodes between 1.0 ploitative capacity of axes is long sustained. and 1.5 mm long. This gives a total value of (b) Total reiteration – trunks: Reiteration of 6 1.2 × 10 needles for the 6 m tree. Clearly, trunk axes (ax0) can occur and is very strik- the photosynthetic capacity of a mature tree ing because the total architecture of the is enormous, and one can estimate values of model is reproduced, although the result beyond 100 km for the assembled length of tends to disrupt the symmetrical topology of ax2 in a tall specimen. the canopy. Because the overall architecture 9: Crown structure 57 is repeated, such new units can resemble tion about the other three sections, i.e. sect. small trees inserted into the canopy. They Araucaria (or Columbea), to which the two are particularly noticeable if they develop on South American species belong, sect. Bunya the trunk axis of a tall tree whose top has (i.e. A. bidwillii) and sect. Intermedia (A. cun- been broken. This process may also account ninghamii and A. hunsteinii). In New Caledo- for the infrequent appearance of forked nia most species are like A. heterophylla but trunks, although a true dichotomy cannot be with a much more columnar shape, as in A. ruled out. columnaris, producing the spire-like physiog- nomy used as an icon in New Caledonian An artificial generation of new ax0 can be used to supply Christmas trees on a repeti- publicity (Fig. 12). This form essentially is tive commercial scale. If a small tree (trunk also shown by A. bernieri, A. biramulata, A. diameter c. 15 cm) is decapitated close to the humboldtensis, A. laubenfelsii, A. luxurians, A. ground, it will reiterate one or more treelets montana, A. nemorosa, A. schmidii, A. scopulo- that can be culled at any desirable length and rum and A. subulata. That these species are the process repeated (Fig. 11). From the same closely related is indicated by the inability of stump, reiterated ax1 can be produced, pre- current molecular systematic techniques to sumably from the base of old branch stumps. resolve their relationships, at least by the use The general rule that seems to operate is that of rbcL genes (Setoguchi et al. 1998). In many each axis type reiterates its own kind, ax0 pro- of them partial reiteration of ax1 at the base duce second generation ax0 whereas ax1 pro- of the tree may be limited so that the persis- duces only second generation ax1 (Table 1). tent scars of the branch tiers then form con- All these reiterated axes seem to result from spicuous rings on the trunk (cf. Figs. 13, 19). the consistent presence of axillary meristems A characteristic feature of this canopy form (i.e., not buds but small patches of meris- is that the upper portion of the trunk shows tematic tissue that are persistent remnants the model-conforming physiognomy clearly, of the original shoot apex). This process has with variation determined by the spacing of been well documented by Burrows (1986, successive branch tiers. The top of the tree is 1987, 1989, 1990b, 1999) and summarized thus normally narrowly conical. However, elsewhere in this volume. The distinctive where elongation growth slows with age, feature of this process is that a small patch branch tiers are crowded, and a candelabra of meristematic tissue has the developmental form results as the ax1 grow in length with- potential largely determined by its position out corresponding trunk growth. Veillon within the framework of the parent tree. (1980) illustrates this for A. humboldtensis, A. This property may be generalized in conifers, schmidii and A. scopulorum. Otherwise the but has been little studied (cf. Fink 1984). sparseness or density of the canopy is deter-

This summary provides the background nec- mined by the rate of production of ax1 on essary to an understanding of crown form in older parts of the trunk as a result of partial all Araucaria spp. because the same develop- reiteration. Araucaria rulei is distinctive be- mental features are possible in all of them, cause it conforms almost precisely to the but their varying expression accounts for model, and virtually lacks any form of reit- contrasted shape in different species. eration (Fig. 14). The crown consequently is without infilling. Furthermore the distal ex- Diversity within Araucaria tremity of each ax1 shows radial placement

(a) Section Eutacta (Eutassa): Veillon (1978, of the ax2 and a tendency to turn erect. Arau- 1980) has described canopy modification in caria muelleri is comparable, reflecting its New Caledonian species of Araucaria, all close systematic position (Setoguchi et al. members of section Eutacta, to which A. 1998). Both species are characterized by heterophylla belongs. Here we add informa- thick ultimate axes, up to 5 cm diameter 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 contin- ued replacement of relatively short-lived ax 1. Fig. 13 , A. rulei, base of trunk of a young tree, the “hoops” repre- senting 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. 9: Crown structure 59 overall (de Laubenfels 1972). Veillon (1980) sively below each cone. This sympodial de- describes A. muelleri and A. rulei as Rauh’s velopment is very unusual in conifers. model, but there is never any distal reversion These authors also compare crown form in of an ax to an ax capable of repeating the 1 0 contrasted habitats. The characteristic physi- tree’s total architecture. Araucaria montana is ognomy is expressed in forest stands, with similar, but more extensively reiterates and the progressive loss of lower branches. One can produce numerous secondary trunks may contrast this with cultivated specimens (Fig. 18). in benign environments in which branches Araucaria cunninghamii (hoop pine) may be are especially long-lived and the trunk re- included in section Eutacta but is distinctive tains dead branches (Fig. 16). Although they in crown form because it consistently pro- have the developmental potential to produce duces a third-order series of axes on each new ax1 by partial reiteration, trees do not first-order branch complex. The complexes develop nesting crowns and the canopy is become sub-erect and the overall bushy ef- not therefore infilled. fect is striking as the crown is in-filled within the architectural model (Fig. 15). This Grosfeld et al. (1999) document several morphology could justify inclusion in Rauh’s mechanisms for developing new trunk axes (ax0) that mainly come from existing trunks, model although there is little reversion of ax0 but root suckers are also reported (cf. Veblen to ax1 and reiteration is limited. The distinc- tive physiognomy of this species accords 1982). Cut stumps can initiate new trunks well with its phylogeny, since it is the sister (cf. Fig. 11) while basal sprouts (cf. Wollemia) species to all other members of section Eu- and distal trunk reiteration (cf. Fig. 18) are tacta (Setoguchi et al. 1998). Araucaria bira- reported. The ability of fallen trunks to reit- erate new trunks is also remarkable. The mulata can produce ax3, but not consistently so and without pronounced influence on form of the tree is an expression of the rate architecture. of trunk elongation in relation to branch elongation. Both are rhythmic but are not (b) Section Columbea: The South American synchronized. The apical meristem of the species develop their distinctive flat-topped trunk may remain dormant for up to nine candelabra habit with age, but show the to- years, even though the branches may be tal range of Araucaria opportunistic shoot growing annually. development. Araucaria araucana has been described in detail by Grosfeld et al. (1999) The somewhat surprising conclusion is that with a refreshing approach by quantifying despite having a very precise physiognomy several aspects of growth. Trees are unusual the tree is very plastic in its growth expres- in being dioecious. They conform to Mas- sion – it is capable of persisting in a sup- sart’s model but again with some elements pressed state in a poor environment for up to of Rauh’s model in the tendency of ax1 to de- 150 years, whereas in a favorable environ- differentiate and become erect distally with ment the architecture is deployed continu- a change to radial symmetry. Otherwise the ally, with regular annual increments of both characteristic morphological distinction be- trunk and branch. The candelabra form of tween trunk, first and second order branches adult trees that provides such a striking icon

(i.e., ax0, ax1, ax2) is maintained. A distinc- for the Southern Andes is a result of the re- tive feature is that male cones are lateral on turn to slow trunk growth with age (Veblen ax2 and so constitute a further branch order et al. 1995). Growth expression seems to be

(ax3). Female cones, on the other hand are the most significant adaptive parameter, terminal on ax2, but growth is continued by with minimum recruitment of new axes as a the development of a lateral branch succes- traumatic response. 60 Section 2: Morphology, phylogeny, systematics and ecology

(c) Section Bunya: In A. bidwillii all features of years. Araucaria heterophylla in the same loca- the basic crown structure of Araucaria exist, tion was identical in its response. but reiterative processes are limited and ob- This suggests that the columnar habit of so vious nesting crowns are not developed (Fig. many New Caledonian species (e.g., Figs. 12, 17). The most distinctive feature is the 19) is most advantageous in allowing trees to rhythmic growth of ax1 resulting in zones of become tall in exposed, and especially short leaves alternating with more extended coastal, habitats. Trees in upland habitats series of long leaves. Radial symmetry char- (e.g. A. rulei, Fig. 14) never grow tall, but are acterizes each branch complex (Fig. 17). probably wind resistant because of their Open grown trees may resemble A. araucana open canopy. Reiteration is most likely to in a distinctly pyramidal habit. produce new axo (Fig. 18) but these do not (d) Section Intermedia: Although A. hunsteinii increase the density of the crown. (klinki pine) co-occurs with A. cunninghamii Araucaria hunsteinii as described by Havel (hoop pine) in Papua New Guinea, the two (1965) seems well adapted to forest condi- are strongly contrasted in crown form since tions because a columnar, model-conforming the former only produces two branch orders, stage allows the tree to grow in partial shade as in the standard Araucaria model. Canopy in secondary succession or in gaps within a development in A. hunsteinii involves exten- well-developed forest canopy. Once ex- tended above this canopy, the tree retains a sive production of secondary ax1 and distinc- tive nesting crowns do occur (Edelin 1986). columnar shape by extensive partial reitera- tion. This extension corresponds to the proc- Rhythmic growth of ax1, comparable to that in A. bidwillii, is pronounced. ess of crown metamorphism described by Edelin (1986), in which there is a progressive Adaptive ecology change to radial symmetry of higher ax1, i.e. The previous descriptive summary shows in upper tiers. This recalls the same process that deployment in varying degrees of a obvious in A. bidwillii (Fig. 17). common set of developmental features can produce appreciable diversity of physiog- Agathis nomic expression. This diversity suggests Crown structure in Agathis is very uniform how crown form may be functional in the and any species will show most features. successful survival of trees in natural habi- Although assigned to Massart’s model (Hallé tats. Trees of the columnar Eutacta type (Fig. et al. 1978) it is contrasted with Araucaria in 12) seem well adapted to cyclone- or hurri- the construction of extension units (Fig. 6) cane-prone environments. Araucaria colum- and the absence of marked shoot polymor- naris retains its narrow crown by the regular phism. Broad leaves, extended internodes shedding and replacement of ax1 (Fig. 19), and development of bud scales are the most but in addition shows dramatic response to conspicuous features of shoot morphology. storm winds. Figure 20 illustrates a culti- vated specimen in South Florida one year Architecture after Hurricane Andrew (1993) had stripped The monopodial trunk axis shows spiral away all the ax1 on the windward side, but phyllotaxis, radial symmetry (Fig. 3) and leaving most axes on the leeward side to pro- rhythmic growth, with an extended resting duce a “banner” tree. The initial result is to period between each cycle of elongation. The reduce wind drag almost completely and the dormant period is marked subsequently by tree remained upright. Canopy reconstruc- the scars of the bud-scales so that units of tion begins immediately from old branch extension are clearly separated throughout bases throughout the whole of the trunk so the tree. The trunk produces regular branch that the canopy is replaced within two tiers, each tier with a pseudowhorl of five to 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 reitera- tion 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 dis- tinct “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. 62 Section 2: Morphology, phylogeny, systematics and ecology

seven ax1. Syllepsis is obvious because of the trunk axis (ax0). In open-grown trees dedif- long basal internode below the first leaf pair ferentiation occurs early and the crown as- on the branch (Figs. 3 and 4). In some species sumes the appearance of a population of (e.g. A. ovata) the trunk axis tends to produce treelets attached to the original trunk (Fig. only scale leaves. 21). Each treelet repeats the architecture of In the juvenile stage first-order branches the adult trunk form. Maturity is demon- strated by the onset of sexuality with both (ax1) are plagiotropic with dorsiventral sym- metry and approximately horizontal orienta- male and female cones on short lateral axes tion. In contrast to the spiral phyllotaxis of within each cycle of extension growth. Very the trunk, leaves are irregularly decussate, young female cones are contemporaneous although often sub-opposite rather than with and almost indistinguishable from strictly opposite. The two-ranked symmetry vegetative buds that also occur below the of the mature branch is a result of the twist- resting terminal bud. ing of each internode so that leaf pairs are As major lateral axes are developed by this horizontal, followed by petiolar torsion so transition from plagiotropy to orthotropy, that the adaxial surface of each leaf becomes via an upward curvature beyond the branch uppermost. This arrangement is common to insertion, the crown becomes broader, as in many tropical trees and also occurs in the A. australis. Agathis ovata is distinguished by gymnosperm Gnetum gnemon. the straightness and upward slope of these

First-order branches (ax1) repeat the rhyth- axes. The process can be repeated at higher mic growth of the ax0 and retain dorsiventral topographic branch orders so that the can- symmetry in branching because the resulting opy becomes in-filled. “Treelets” of this de- branch pairs are horizontal. The insertion of differentiated type retain abundant growth each branch is narrow and with limited sec- and their attachment to the parent trunk is ondary xylem; consequently the horizontal robust. The oldest of these persistent axes branch complex is determinate. It is eventu- represent the massive “limbs” of the mature ally abscised in a precise way to leave a char- tree (Fig. 22). This description, based on A. acteristic embossed scar (Licitis-Lindbergs australis, corresponds to that for A. dammara 1956). The young tree thus maintains a nar- by Edelin (1986) although the term “crown row conical form, especially in the forest metamorphism” is used by him, implying a understorey, by virtue of the short life span gradual change as the tree ages. or slow growth of the plagiotropic axes. The Ecology only change is the increase in leaf width to The crown shape of the mature Agathis can the adult form. This early narrow-crowned be interpreted as a result of the metamor- form is referred to by foresters as the “ricker” phosis from the juvenile to the adult state phase (a word of Saxon origin) and is impor- and is supported by extensive population tant in establishing a long trunk without analysis (Ogden & Stewart 1995). The knots. “ricker” stage is maintained in the shaded Crown repair in the juvenile phase seems condition of the forest understorey. Once limited to occasional reiterated ax1, as in the tree breaks through to full sunlight, de-

Araucaria, and derived from an axillary mer- differentiation of ax1 becomes pronounced, istem (Burrows 1987) persisting in the base essentially as a population of explorative of a pre-existing branch. A more significant “trunks” on the main axis (Fig. 21). The change in older trees is dedifferentiation of population of ax1 produced on these ax0 ax1 so that they turn erect distally, show a represents the relatively short-lived exploita- return to a spiral phyllotaxis and adopt the tive ultimate branch complexes. The analysis radial symmetry and tiered branches of a of A. macrophylla on Vanikoro by Whitmore 9: Crown structure 63

Figures 21 -22: Agathis australis . Crown form. Fig. 21, Open -grown tree with numerous dedifferentiated first - order 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 “open - grown” tree, as in Figure 21.

(1966) supports these interpretations. Wollemia Crown repair from latent meristems is un- necessary since it has become a feature of the This newly-described tree shares features repeated expression of the architectural found in both Araucaria and Agathis, but is model, even though such latent meristems unique in several respects. Published descrip- appear to exist (Burrows 1987). Once estab- tions (Hill 1997; Jones et al. 1995) indicate a lished above the forest canopy the frame- trunk axis (ax0) with rhythmic monopodial work is permanent and the tree is usually growth producing plagiotropic axes (ax1) in impregnable to all except the most violent regular tiers, i.e., Massart’s model in the storms and, of course, the woodsman’s saw. Hallé-Oldeman system (Hallé et al. 1978). Edelin (1986) notes how A. dammara co- The juvenile phase is distinctive because the exists with dipterocarps in lowland Malesian pseudowhorls are relatively close set and dor- forests, and presumes that this is the result siventrality of ax1 is precise, with two ranks of a similar crown metamorphism. of narrow leaves. This suggests decussate 64 Section 2: Morphology, phylogeny, systematics and ecology phyllotaxis with secondary leaf orientation, in A. cunninghamii (Burrows 1990b). Trauma- as in Agathis. The adult phase is distinctive tized roots in A. cunnninghamii can produce because the first-order branches (ax1) remain new shoots (Burrows 1990a). If basal sprout- unbranched, i.e., without ax2 so that the ing is an architectural feature, as implied by trunk bears only one series of branches. The Hill (1997), then Wollemia would indeed be decussate arrangement of the adult foliage unique. seems responsible for the four ranks of broad Wollemia survives in deep, moist, sheltered leaves, recalling Agathis ovata (Fig. 4). Both canyons that apparently provide refugia male and female cones are said to terminate from dry, windy and fire-prone environ- the branches so that ax1 are determinate by ments. Subsequent cultivation and progres- sexuality, a condition possibly unique for sive monitoring should provide the opportu- conifers. It is not stated whether cone- nity to resolve some of the many uncertain- bearing axes subsequently can continue ties that still exist in our understanding of vegetative growth by sympodiality, as can this distinctive tree. occur in the otherwise determinate ax2 of some Araucaria species (e.g. Grosfeld et al. Conclusions 1999; Veillon 1978). These preliminary observations show that First-order axes (ax1), as in Araucaria, al- the three genera of Araucaria have contrasted though long-lived are eventually shed, strip- canopy structures although based on a range ping the trunk of all foliage. How can a can- of shared common features. In this sense ? opy be maintained Two methods of reitera- they represent three reference points in an tion seem to occur. In the first there is devel- architectural continuum. The contrasted opment of a second and subsequent genera- features seem adaptive in the distinctive en- tions of first-order axes by partial reiteration, vironment occupied by each genus. Further in the manner of Araucaria columnaris, but research is needed, especially in the quantita- without the development of obvious tive understanding of shoot disposition, the “nesting crowns.” Secondly, and more sig- precise observation of phenological patterns nificantly, there is dedifferentiation of first- and the details of shoot phyllotaxis. The un- order branches so that ax essentially revert 1 derlying basis for much of the adaptive con- to ax and so replicate the whole adult archi- 0 struction lies in the remarkable ability of all tecture of the tree. This suggests the same trees to sequester meristematic tissue as mechanism as in Agathis but without pro- “axillary meristems,” emphasized by Bur- ducing a broad crown, presumably because rows et al. (1988). This has very important higher order branches are not produced. The economic implications, as elite trees are se- framework of the tree may thus largely be lected and propagated for plantation pur- the result of reiteration, which is based on poses or stump sprouts generated for decora- the same mechanism for sequestering axil- tive purposes (Fig. 11). Propagation of spe- lary meristems as is found in the rest of the cies that are endangered, of which Wollemia family (Burrows 1999). is an outstanding icon, depends on extensive A distinctive feature of Wollemia is the devel- knowledge of the inherent mechanisms that opment of basal shoot suckers that can form control canopy form throughout the family. a palisade of apparently derivative trunks, although it is not known if these are stem- References or root-borne. Hill (1997) suggests this as a Burrows, G.E. 1986. Axillary meristem ontogeny in unique feature since it is rare in conifers (e.g. Araucaria cunninghamii Aiton ex D. Don. Australian Sequoia), but basal suckering is reported for Journal of Botany 34: 357-375. the South American species (Grosfeld et al. Burrows, G.E. 1987. Leaf axil anatomy in the Araucari- 1999; Veblen 1982) and the potential exists aceae. Australian Journal of Botany 35: 631-640. 9: Crown structure 65

Burrows, G.E. 1989. Developmental anatomy of axillary Hill, K.D. 1997. Architecture of the Wollemi pine meristems of Araucaria cunninghamii released from (Wollemia nobilis, Araucariaceae), a unique combina- apical dominance following shoot apex decapitation tion of model and reiteration. Australian Journal of in vitro and in vivo. Botanical Gazette 150: 369-377. Botany 45: 817-826. Burrows, G.E. 1990a. Anatomical aspects of root bud Jones, W.G.; Hill, K.D.; Allen, J.M. 1995. Wollemia nobi- development in hoop pine (Araucaria cunninghamii). lis, a new living genus and species in the Araucari- Australian Journal of Botany 38: 87-78. aceae. Telopea 6: 173-176. Burrows, G.E. 1990b. The role of axillary meristems in Licitis-Lindbergs, R. 1956. Branch abscission and disinte- coppice and epicormic bud initiation in Araucaria gration of the female cones of Agathis australis Salisb. cunninghamii. Botanical Gazette 151: 293-301. Phytomorphology 6: 151-167. Burrows, G.E. 1999. Wollemi pine (Wollemia nobilis, Ogden, J.; Stewart, G.H. 1995. Community dynamics of Araucariaceae) possesses the same unusual leaf axil the New Zealand conifers. In Enright, N.J.; Hill, R.S. anatomy as other investigated members of the fam- (eds.). Ecology of the southern conifers. Smithsonian ily. Australian Journal of Botany 47: 61-68. Institution Press, Washington, D.C.: pp.81-119. Burrows, G.E.; Doley, D.D.; Haines, R.J.; Nikles, D.G. Setoguchi, H.; Osawa, T.A.; Pintaud J-C.; Jaffré T.; 1988. In vitro propagation of Araucaria cunninghamii Veillon J-M. 1998. Phylogenetic relationships within and other species of the Araucariaceae via axillary Araucariaceae based on rbcL gene sequences. American meristems. Australian Journal of Botany 36: 665-676. Journal of Botany 85: 1507-1517. de Laubenfels, D.J. 1972. Gymnospermes. In Aubréville, Tomlinson, P.B.; Takaso, T.; Rattenbury, J.A. 1989. A.; Leroy, J-F. (eds.). Flore de la Nouvelle-Calédonie et Developmental shoot morphology in Phyllocladus Dépendances 4. Muséum National d’Histoire (Podocarpaceae). Botanical Journal of the Linnean Soci- Naturelle, Paris: pp. 1-168. ety 99: 223-248. Edelin, C. 1977. Images de l’architecture des Conifères. Veblen, T.T. 1982. Regeneration patterns in Araucaria Thesis. Université des Sciences et Techniques du araucana forests in Chile. Journal of Biogeography 9: Languedoc, Montpellier. 11-28. Edelin, C. 1986. Stratégie de reiteration et édification de Veblen, T.T.; Burns, B.R.; Kitzberger, T.; Lara, A.; la cime chez les conifères. In L’Arbre: compte-rendu du Villalba, R. 1995. The ecology of the conifers of Colloque international L’Arbre. Naturalia Monspelien- South America. In Enright, N.J.; Hill, R.S. (eds.). sia, Institut de Botanique, Montpellier: pp. 139-158. Ecology of the southern conifers. Smithsonian Institu- Fink, S. 1984. Some cases of delayed or induced develop- tion Press, Washington, D.C.: pp. 120-155. ment of axillary buds from persisting detached mer- Veillon, J-M. 1978. Architecture of the New Caledonian istems in conifers. American Journal of Botany 71: 44- species of Araucaria. In Tomlinson, P.B.; 51. Zimmermann, M.H. (eds.). Tropical trees as living Grosfeld, J.; Barthélémy, D.; Brion, C. 1999. Architec- systems. Cambridge University Press, Cambridge: pp. tural variations of Araucaria araucana (Molina) K. 233-245. Koch (Araucariaceae) in its natural habitat. In Kur- Veillon, J-M. 1980. Architecture des espèces néo- mann, M.H.; Hemsley, A.R. (eds.). The evolution of calédoniennes du genre Araucaria. Candollea 35: 609- plant architecture. Royal Botanic Gardens, Kew: pp. 640. 109-122. Whitmore, T.C. 1966. The social status of Agathis in a Hallé, F.; Oldeman, R.A.A.; Tomlinson, P.B. 1978. Tropi- rainforest in Melanesia. Journal of Ecology 54: 285-301. cal trees and forests: an architectural analysis. Springer Verlag, Berlin. Havel, J.J. 1971. The Araucaria forests of New Guinea and their regenerative capacity. Journal of Ecology 59: 203-214.