Am. J. Bot. Subscribe to E-TOCs
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via ISI Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Posluszny, U.
Right arrow Articles by Fisher, J. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Posluszny, U.
Right arrow Articles by Fisher, J. B.
Agricola
Right arrow Articles by Posluszny, U.
Right arrow Articles by Fisher, J. B.
(American Journal of Botany. 2000;87:1561-1570.)
© 2000 Botanical Society of America, Inc.

Thorn and hook ontogeny in Artabotrys hexapetalus (Annonaceae)1

Usher Posluszny2 and Jack B. Fisher3

2 Department of Botany, University of Guelph, Guelph, Ontario, Canada N1G 2W1; 3 Fairchild Tropical Garden, 11935 Old Cutler Rd., Coral Gables (Miami), Florida 33156 USA; and Department of Biological Sciences, Florida International University, Miami, Florida 33199 USA

Received for publication September 3, 1998. Accepted for publication January 25, 2000.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Artabotrys hexapetalus is widely planted in the tropics and is known as "climbing ylang-ylang," an ornamental liana or woody climber. New natural sprouts, or water shoots, and those induced by the damage of Hurricane Andrew (24 August 1992) were collected and fixed in formalin/acidic acid/alcohol. Seeds from these plants were planted and grown in a greenhouse where seedling morphology was observed and young material collected and fixed. The development of lateral plagiotropic and orthotropic shoots was studied using both epi-illumination light microscopy and scanning electron microscopy. A series of buds develops in the axils of leaves on the orthotropic shoot. At the lateral margins of the axillary shelf, plagiotropic shoots form that will develop into either vegetative shoots, or thorns, or sympodial shoots that bear hooks and flowers. In between the two marginal buds, a series of median vertical buds develop that either remain dormant or grow out as renewal orthotropic shoots. Previous work that suggested that the plagiotropic shoot buds were displaced out of the median vertical series of supernumerary buds is not supported. The sympodial development of plagiotropic branches as inflorescence hooks is documented.

Key Words: Annonaceae • architecture • Artabotrys • development • liana • thorn • tropical


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Artabotrys is a genus of 100 or more species of lianas, or woody climbers, which grow in tropical Africa and the Indomalayan region (Mabberley, 1987 ). They climb by means of recurved hooks borne on lateral branches. The hooks form in linear series and can become swollen and woody after becoming attached to an object. Because the hooks are an obvious feature, they have frequently been described and illustrated, but interpreted variously as modified portions of inflorescences (Treub, 1883 ; Massart, 1896 ; Hallé, 1973 ; Cremers, 1973 ). However, in these published accounts, no attention was paid to the morphology or development of thorns that occur either singly or in pairs at the lower nodes of large stems in some species. Initially we observed these thorns in cultivated specimens of the Asian species A. hexapetalus (L.f.) Bhand. and had difficulty interpreting their morphology in terms of their final position and their derivation from serial axillary buds. Cremers (1973) described the serial lateral buds in stems of A. insignis Engler and Diels, an African species, which has a lateral leafy branch in a position similar to a single thorn in A. hexapetalus. He found that the branch arose from a bud which he suggested was displaced laterally from its original position as a member of a vertical line of serial axillary buds. We found Cremers' (1973) description of lateral ontogenetic displacement difficult to accept, especially if applied to thorn pairs. To resolve this apparent conflict, we studied the structure and development of seedling and adult shoots. We also sought ontogenetic evidence for the interpretation of the hooks as the sympodial branching of a series of inflorescences.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Two, old, established plants of Artabotrys hexapetalus (L.f.) Bhand. growing at Fairchild Tropical Garden, Miami, Florida, USA were examined. This species (syn. A. odoratus R. Br.; A. uncinatus [Lam.] Merrill) is widely planted in the tropics and is known as "climbing ylang-ylang" (Bailey and Bailey, 1976 ). New natural basal sprouts, or water shoots, and those induced by decapitating old stems were collected and fixed in formalin/acidic acid/alcohol. Seeds from these plants were planted and grown in a greenhouse where seedling morphology was observed and young material collected and fixed.

Fixed material was dehydrated in an ethanol series, stained with acid fuchsin, and observed with epi-illumination using a Zeiss photomicroscope III fitted with Leitz Ultrapak dipping cones (Posluszny, Scott, and Sattler, 1980 ; Charlton et al., 1989 ) or was dehydrated, critical-point dried, sputter coated with gold-palladium, and observed with a Hitachi S570 scanning electron microscope.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Architecture
Seed germination is hypogeal. The first few alternate leaves are initially arranged in a spiral. Later leaves arise distichously at the apex but become spirally arranged by a twisting of the internodes on the orthotropic (= vertical) seedling axis. There is no branching in undamaged seedlings until the tenth to 20th node above the cotyledons, depending upon the vigor of the seedling.

Older seedlings show a complex pattern of bud outgrowth found in many tropical woody plants (Hallé, Oldeman, and Tomlinson, 1978 ). Most lateral buds remain dormant with a prolonged period between initiation and later expansion into a branch or reproductive structure. Such buds are called proleptic and remain inactive in shoots showing complete apical control. Other lateral buds grow continuously from inception, showing no inhibition from the apical meristem of the shoot, and these are called sylleptic. Sylleptic branches often exceed the growth of the main shoot and extend beyond the shoot apex that produced them.

In older seedlings of Artabotrys, a single lateral sylleptic branch arises from the axil of most leaves. The orthotropic leader axis continues to bear leaves in a spiral, due to the twisted internodes, while each lateral plagiotropic (= horizontal) branch has distichous leaves in the horizontal plane.

In saplings and older plants, two to six serial buds occur on the stem directly above the leaf insertion. The uppermost bud is the largest and sometimes (but rarely) produces the sylleptic branch if one develops. The lower buds always remain inactive as dormant buds and always form orthotropic shoots if they develop as a proleptic branch. Thus, proleptic branches become vertical shoots (= leader shoots) and sylleptic branches produce either horizontal shoots or thorns (Fig. 1).



View larger version (26K):
[in this window]
[in a new window]
  		Fig. 1. Diagram of the architecture of a mature plant of A. hexapetalus with three main architectural regions in the main orthotropic axis (OV) and two reiterations: basal thorns (Th), vegetative plagiotropic branches (PV), and reproductive plagiotropic branches with hooks (H). Figure Abbreviations: B, axillary bud; F, F', F'', first, second and third flower on an inflorescence hook; H, inflorescence hook; HL1, the first hook leaf developing on a hook inflorescence; HL2, the second hook leaf developing on a hook inflorescence; Lp, first leaf on either a plagiotropic or orthotropic bud (prophyll); LS, leaf scar; OV, orthotropic shoot or bud; PV, plagiotropic branch; R, renewal shoot; r, removed organ, i.e., rL, removed leaf; Th, thorn.

 
New orthotropic axes or leader shoots develop (1) from dormant buds in distal nodes of the leader after its terminal bud is damaged or stops growing, or (2) from dormant buds in proximal nodes of older shoots or leaders. The orthotropic leaders, whether the original leader or reiterations, all have the same structure as described above for seedlings.

Each leader shows a similar gradient in morphology from proximal to distal nodes. The lowest few nodes lack axillary appendages and have only dormant buds. Then a series of nodes each has (usually) two thorns of slightly unequal size on either side of the serial bud complex (Figs. 2a, 3), or, less commonly, a single thorn (Fig. 2b). The larger thorn or the single thorn can be on either the anodic or cathodic side of the leaf with regard to the genetic spiral of the shoot, with the position constant for a given shoot. Thorns often bear one or two foliage leaves and one or more scale leaves, with the larger thorns having more appendages. At higher nodes, the thorns take on a transitional form with a swollen thorn-like base and continued terminal meristem activity and production of more foliage leaves (Figs. 1, 8). Eventually the thorn apex on these shoots aborts.



View larger version (52K):
[in this window]
[in a new window]
  		Figs. 2–7. Mature morphology of thorns and plagiotropic lateral shoots. Bar = 1 cm. Same magnification in Figures 2a, 2b and 5, 3 and 4, and 6 and 7 . 2(a) Node of an orthotropic shoot with paired thorns, each bearing a leaf. (b) Node of orthotropic shoot with single thorn. 3. Older node with paired thorns and a new orthotropic shoot from a median bud; the lower node of OV has a small thorn and a branch. 4. Node with paired plagiotropic branches. 5. Node with single plagiotropic branch. 6. Young plagiotropic branch with two inflorescence hooks, each with one flower. 7. Older plagiotropic branch with two inflorescence hooks.

 
Initially two (Fig. 4) and then one plagiotropic branch (Fig. 5) develop at each node in the rest of the leader. At more proximal nodes and when growing in shade, lateral vegetative branches tend to grow monopodially, and without the hook inflorescences. More distal nodes and those in full sunlight are sympodial. They produce an inflorescence within two to ten branch nodes from their insertion on the orthotropic stem. This inflorescence bears one to several flowers and bracts and becomes recurved as a hook, terminating the growth of the branch unit (Fig. 6). A lateral renewal bud grows out at the base of the hook and extends the horizontal branch axis (Figs. 6R, 10R), thus producing a series of units, each ending in a downward projecting hook (Fig. 7). The hooks become secondarily thickened like the rest of the branch axis. Those hooks that become attached to another branch or other object become noticeably swollen and woody. Self-grafting can occur between hooks and the internodes they clasp.

Orthotropic shoots grow monopodially, producing lateral appendages as described above (Fig. 8). Infrequently, an orthotropic leader will produce a hook inflorescence (Fig. 9) with a renewal bud continuing the extension of the leader. Otherwise, less vigorous leaders end with a drying up and final abortion of the growing tip.



View larger version (135K):
[in this window]
[in a new window]
  		Figs. 8–12. Figs. 8–9 . Mature orthotropic shoots. Bar = 1 cm. 8. Orthotropic shoot with spirally arranged leaves. Several vegetative plagiotropic shoots (PV) are beginning to grow out in the axils of the leaves. Bar = 1 cm. 9. A rare orthotropic shoot that has developed a hook. Figs. 10–12 . Plagiotropic shoots developing inflorescence hooks and flowers. 10. An inflorescence hook in which the second hook leaf (rHL2) has been removed and a terminal flower is developing. A renewal shoot (R) is developing to the right. 11. A slightly younger stage of inflorescence hook development in which two flower buds can be seen (F', F''). 12. An inflorescence hook with a large terminal flower bud

 
Anatomy of thorns and branches
Thorns can be contrasted with branches of similar thickness and distance from the orthotropic leader. Thorns and branches have equivalent primary and secondary tissues with quantitative differences. The pith is about one-third wider in the branch. Xylem fibers and axial and ray cells are thicker walled in the thorn than the plagiotropic branch. The xylem vessels of thorns are narrow (29–35 µm wide) and mostly single or in groups of 2–3; vessels of branches are wider (69–86 µm) than those in the thorns and mostly in groups of 2–4. From the start of secondary growth, wood of thorns is denser (due to the thicker walled fibers) than those of branches. In older thorns, there is little thickening but much swelling at the base due to a basal collar of secondary xylem and periderm. Paired thorns become widely separated circumferentially on either side of the leaf scar (Fig. 3) after the leader stem thickens with age. The pith tissue of each thorn can be followed through the secondary xylem of the leader into its pith. These pith regions converge next to the inner xylem boundary of the leader, where the thorns were initially close together and adjacent to the leaf trace in the young leader stem. The region of the serial bud complex is often swollen and without external evidence of buds, which become embedded in and covered by periderm.

Reiteration
It should be noted that the arrangement of buds in the axils of leaves on plagiotropic branches is exactly the same as those on the previously described orthotropic branches. In older plagiotropic branches, especially those in full sun, one of the several serial axillary buds is released to form second-order branches in the horizontal plane (along the plagiotropic branch). The overall architecture of a large plant is based on repeated reiteration of the sapling architectural model with release of dormant buds to form new orthotropic leaders (Fig. 1). All leaders produce plagiotropic thorns and branches (Fig. 8). Cultivated plants grow up into neighboring tree crowns to a height of 10–15 m.

Two established plants at FTG in Miami were severely damaged by winds and the fall of supporting tree limbs caused by Hurricane Andrew (August 1992). After 6 mo, there was much new growth on these plants. New orthotropic shoots arose from lateral buds on the nodes of either old leaders (Fig. 3), or old lateral branches, or old thorns near the base of the plant. In some cases, only plagiotropic vegetative branches and few, if any, thorns were produced by leaders growing out at unshaded sites. Such reiterations showed seedling morphology with juvenile features such as lack of thorns and no inflorescence hooks. Thorns were more common at the base of those leaders growing in dense shade.

Initiation and ontogeny of axillary plagiotropic and orthotropic buds
The sequence of development of buds in the axil of leaves on an orthotropic shoot begins with the initiation of plagiotropic bud primordia. At the third node from the apical meristem, either one or two plagiotropic buds can be seen developing on the extreme lateral margins of the axillary shelf (PV in Figs. 13–16), i.e., the space between the third leaf primordium (L3) and the stem. Figures 13 and 14 show the initiation of a single plagiotropic bud, while Figs. 15 and 16 show the initiation of two plagiotropic buds on either side of the axillary shelf. Each plagiotropic bud primordium initiates its prophyll (Lp) in an adaxial position, but as the bud develops, it slowly rotates out and away from the axis (Figs. 16–19). The plagiotropic shoots are sylleptic and grow out rapidly forming a series of foliage leaves including the expanded prophyll (Figs. 19, 20, and 25).



View larger version (149K):
[in this window]
[in a new window]
  		Figs. 13–22. Orthotropic shoot development showing stages in the initiation and early development of axillary buds. 13. SEM of an orthotropic shoot apex (OV) showing leaf primordia (L1, L2, and rL3) developing in a spiral arrangement. In the axil of leaf rL3 an apex of a plagiotropic bud (PV) is present on the left-hand portion of the axillary shelf. Figs. 14–16 . Epi-illumination light micrographs of early stages in the development of plagiotropic apices. 14. A similar stage to that in Fig. 13 . Only a single axillary bud can be seen at the left margin of the axil. 15. An orthotropic shoot in which two plagiotropic apices are present in the axil of leaf rL3, at both right and left lateral margins of the axillary shelf. 16. A slightly older stage than that shown in Fig. 15 ; two plagiotropic shoot apices (PV) are just initiating their prophylls (Lp). Figs. 17–20 . SEMs of early developmental stages of plagiotropic shoots. 17. The single plagiotropic shoot (PV) in the axil of leaf rL4 is just beginning to initiate its prophyll (Lp). 18. A slightly older stage in the development of the prophyll (Lp) of a single plagiotropic shoot. 19. A single plagiotropic shoot which has initiated a prophyll (Lp) and the next leaf (L1). The first serial orthotropic bud (OV) is just initiating its own prophyll (Lp). 20. An axillary complex with two plagiotropic shoots (PV) and a single orthotropic apex (OV, the first of a vertical series). Figs. 21 and 22. Epi-illumination light micrographs showing early development of the serial orthotropic buds. 21. Two orthotropic buds (OV) forming between two well-developed plagiotropic shoots (PV). Two stages in prophyll (Lp) development can be seen. 22. A third orthotropic bud can be seen originating at the end of a vertical series of buds. The two plagiotropic shoots on either side and a leaf (rL) have been removed. Scale bar in Figs. 13 and 17 = 0.1 mm. Scale bar in Figs. 14–16 and 19–21 = 0.1 mm. Scale bar in Fig. 18 = 0.05 mm. Scale bar in Fig. 22 = 0.5 mm

 
The vertical series of orthotropic buds originate on the median portion of the axillary shelf between the lateral plagiotropic buds (OV in Figs. 19 and 20). The first orthotropic bud forms a prophyll adaxial to the main shoot axis (Fig. 19). A second orthotropic bud originates just below the first and a third is initiated just below the second (Figs. 21 and 22). Up to six orthotropic buds, each with an adaxial prophyll, can form in a vertical median series (Figs. 1–5, 21, and 22). The uppermost orthotropic bud can grow out sylleptically if the plant is flushing out new shoots after a disturbance, but normally all of the orthotropic serial buds remain dormant.

Ontogeny of the thorn
The plagiotropic shoot can either form a thorn, grow out vegetatively, or develop into a sympodial hook inflorescence shoot. The formation of thorns usually occurs in the shaded lower portion of the plant and involves the abortion of the apical meristem, loss of leaves, and the sclerification of the stem. Thorns can produce a variable number of leaves (usually one or two) before apical abortion terminates growth. Sometimes the prophyll is a full-size foliage leaf (Fig. 1), but more often the leaves borne by a thorn are reduced in size. The original terminal bud of the thorn axis aborts after producing leaf primordia from an ever-shrinking apical meristem (Fig. 25). The last axillary bud may appear as a false terminal bud.



View larger version (138K):
[in this window]
[in a new window]
  		 Figs. 25–34. Epi-illumination light micrographs showing the development of the plagiotropic thorn and hook shoots. 25. Side view of a plagiotropic shoot that is about to terminate as a thorn. 26. Early stage in the formation of a hook inflorescence. The first hook leaf (HL1) is beginning to develop and curve around the apex (PV). A renewal shoot (R) will form from the axillary bud in the ultimate "normal" foliage leaf (rL). 27. Later stage in the development of the hook inflorescence showing the formation of the second hook leaf (HL2). The two hook leaves are beginning to overgrow the apex. The renewal shoot (R) has already initiated its prophyll (Lp). 28. Oblique top view of a similar stage to that in Fig. 27 showing the two hook leaves prior to overgrowing the apex (PV). 29. Side view of a young hook inflorescence shoot in which the first hook leaf has been removed (rHL1) to show the apex (PV) just before it terminates as a flower. 30. Side view of a later stage in hook inflorescence development in which the hook leaves have overgrown the apex. The renewal shoot (R) is beginning to grow out from the axil of L1 and will replace the original vegetative apex. An axillary bud (B) in the axil of the prophyll (rLp) of a plagiotropic shoot is forming its own prophyll (Lp). 31. Side view of a young hook inflorescence just beginning to close over the apex (PV). 32. Similar stage to that in Fig. 30 showing the apex totally enclosed by the hook leaves. The renewal shoot (R) has a well-developed first leaf (Lp) and the next foliage leaf is beginning to form (L1). Note the numerous trichomes developing on the hook leaves. 33. Side view of hook inflorescence in which one of the hook leaves (rHL1) has been removed so that the initiating floral apex (F) and the continuation renewal shoot (R) can be seen. The renewal shoot has just initiated its first leaf or prophyll (Lp). This stage is shown as a diagram in Fig. 24A . 34. Tip of a hook inflorescence in which both hook leaves (rHL1, rHL2) have been removed. The terminal floral apex (F) and the renewal shoot are visible. The renewal shoot has a well-developed first leaf (Lp) and a second leaf just initiating (L1). The renewal shoot (R) on the left of the figure is similar to the one in Fig. 31 and will continue to extend the plagiotropic shoot beyond the hook inflorescence. Scale bar in Fig. 25 and Figs. 30–35 = 1.0 mm. Scale bar in Figs. 26–29 = 0.1 mm

 
Ontogeny of the hook inflorescence
The development of hook inflorescence shoots occurs higher up on the orthotropic shoot, and the transformation can start right after the first leaf (prophyll, Lp), but more frequently after several foliage leaves, including the prophyll, are formed. The first indication that a hook inflorescence will form is the development of "hook leaves." These leaves are quite noticeably different from the normal foliage leaves. Unlike the foliage leaves, which originate as triangular primordia (Figs. 19 and 20), the hook leaves are rounded, thicker and when still small, form masses of trichomes on their abaxial surface (Figs. 26–32). Two hook leaves form, giving the hook inflorescence a lobster claw-like appearance (Figs. 30–32). The bud in the axil of the last "normal" foliage leaf (Fig. 23L) formed prior to hook leaf formation becomes the renewal shoot (R) that will continue the vegetative growth of the plagiotropic shoot before it also terminates in a hook inflorescence (Figs. 23B, 23C, and 26–32). As the hook leaves enclose the apex of the plagiotropic shoot apex (PV) (Fig. 31), the apex begins to transform into a floral meristem (F) (Figs. 23A, 24A, 33, and 34). The bud in the axil of the first hook leaf acts as a renewal shoot, which will also terminate in a flower and a further renewal shoot (Figs. 23A, 33, and 34). Up to three flowers (F, F', F'') may form on a single hook inflorescence (Figs. 10–12 and 37). The largest and most prominent flower is the terminal flower associated with the second hook leaf (Figs. 6, 12, and 36)



View larger version (22K):
[in this window]
[in a new window]
  		Figs. 23 and 24. Schematic diagrams illustrating stages in the development of the inflorescence hook. 23. (A) First stage of a developing hook inflorescence showing the hook leaves (HL1 and HL2) and the terminal flower (F) with a renewal shoot (R) developing in the axil of the foliage leaf (L). The leaf indicated by a broken line can be a prophyll if hook formation occurs after the second node or it may be a leaf further up the plagiotropic shoot if hook development occurs beyond the third node. (B) Slightly older stage in hook inflorescence development showing the flattened stem prior to curving. (C) Late stage in hook inflorescence development showing curving of the hook back towards the main shoot. 24. (A) More detailed diagram of a stage similar to Fig. 23A . The shaded portion indicates where expansion will occur during hook formation that results in the first hook leaf (HL1) growing beyond the second hook leaf (HL2). (B) Detailed diagram of late-stage hook formation similar to Fig. 23C . The floral bud (F) associated with the second hook leaf (HL2) is the original apical meristem of the plagiotropic shoot. A second floral bud will form at the curved tip associated with the first hook leaf (HL1)

 
The formation of the hook involves a flattening and rapid differential expansion of the inflorescence shoot (Figs. 23B and C, 24B, 35, 36, and 38). The shoot curves back towards the main trunk (attachment of plagiotropic shoot) and in onto itself so that the second hook leaf and its associated flower remain on the outer perimeter of the hook (Figs. 6, 7, 10–12, 23, 24, and 38). The original proximal first hook leaf (HL1 in Fig. 33) becomes displaced to the distal position (seen in Fig. 34) by uneven growth of tissues, as noted by shading in Fig. 24A and B. The first hook leaf usually ends up on the inside of the hook (Figs. 23C, 24B, and 38). If second or third flowers form they will be found on the inside of the hook associated with the first hook leaf (Figs. 6, 10–12, 37, and 38). The hook inflorescence also functions in providing support for the rapidly growing orthotropic shoots. Once a hook clasps onto a stem, it thickens and becomes woody (Fig. 7). No further floral buds form after a hook has become woody.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The position of thorns, foliage branches, and hooks in Artabotrys and other tropical climbers has long intrigued botanists. Bud position and leaf arrangement are puzzling when interpreted by their correspondence to the morphology of related plants (i.e., members of the Annonaceae) (Fries, 1959 ). We have resolved conflicting interpretations by obtaining new information on early ontogeny that more clearly establishes homology obscured by later development. The results support the value of ontogenetic data in determining the homology of highly modified plant organs (Kaplan, 1984 ).

Ontogeny of thorns and branches
Sylleptic thorns and foliage branches, both single and paired, are some lateral distance away from the median axil position, which is where the vertical serial buds are aligned. The buds of thorns and branches are initiated at the marginal flanks of the axil and before the serial buds. Hallé, Oldeman, and Tomlinson (1978) refers to these as bud complexes, which are common in many dicotyledonous families, including the Annonaceae. The earlier initiation of thorns and branches is correlated with their uninterrupted expansion as sylleptic shoots. Artabotrys hexapetalus has the same basic architecture as A. insignis described by Cremers (1973) . However, Cremers hypothesized a realignment of sylleptic branch buds after their initiation within the single median series of buds. Our findings refute such an interpretation since syllepetic thorn and branch buds are initiated on either side of the median axillary position. Later secondary growth only increases the tangential separation of the paired thorns and branches by increased circumference growth of the leader axis.

The earliest formed distal bud of the median series occasionally develops as a sylleptic branch. In this case and when proleptic buds are released (as after decapitation of the leader), the distal bud is the largest and grows out first, similar to the behavior of serial buds of Rhamnaceae (Tourn, Medan, and Tortosa, 1989 ; Tortosa, Aagesen, and Tourn, 1996 ), Bougainvillea, and other species with serial buds (Troll, 1937 ).

The fate of the two kinds of plagiotropic buds (sylleptic thorns and branches) is divergent early in bud ontogeny with future thorns producing smaller and less triangular leaf primordia than those of the foliage branches. Thorn buds vary in the number of leaves produced before the apical meristem shrinks in size and finally becomes sclerotic. Most leaves produced on a thorn are reduced in size and abscise quickly compared to foliage leaves on branches. Similar variability in leaf number and size on thorns was reported in Ulex by Bieniek and Millington (1967) . They found that the apical meristem of a vegetative axillary bud is converted into a thorn by cessation of both meristem activity and leaf initiation. Maturation of the apex of axillary branches occurs in the development of thorns of Gleditsia (Blaser, 1956 ) and this appears to be common in thorn development.

Thorns are most frequent at the base of an orthotropic leader shoot with a transition to foliage and hook inflorescence branches at higher nodes. Intermediate elongated thorns with foliage leaves occur at nodes between the extremes of short thorns and monopodial foliage branches. Thorns are correlated with shaded, low-light conditions, as well as proximal positions on a leader shoot. Conversely, foliage and later hook inflorescence branches are correlated with high-light conditions at the distal nodes. Experimental work on the effect of shade on thorn formation will be reported in a following paper.

Ontogeny of the hook inflorescence
There has been no previous developmental evidence to confirm that the plagiotropic foliage branches become sympodial once they begin to produce the hook inflorescences. In Cremers' (1973) review of the architecture of tropical lianas he notes that there have been two conflicting interpretations of the nature of the hook-forming branches. In an early study of Artabotrys, Blume (1830) concluded that the hook inflorescences differentiated from the tips of the plagiotropic shoots and that they were therefore sympodial, while later work by Treub (1883) on A. suaveolens claimed that the hooks were axillary, ending up in a leaf-opposed position by being carried out of the leaf axil, making the shoots monopodial.

Cremers supported the latter hypothesis because he noted that the last formed foliage leaf and the first hook leaf were on the same side of the axis, which would seemingly be impossible for members of the Annonaceae, as they have distichous phyllotaxy. What he did not realize, as it was only visible in early developmental stages, was that the last foliage leaf (which he termed f2) was in fact quite correctly opposite the first leaf of the hook inflorescence. Repositioning by the differential growth in hook formation made it seem as if the second leaf formed on the hook inflorescence was the next leaf in the phyllotactic sequence. This is clearly illustrated in our dissections of early hook formation (Figs. 26–30) and shown diagrammatically in Figs. 23 and 24. Specifically, Fig. 24A and B illustrate how differential upgrowth carries the first hook leaf (HL1) away from the second hook leaf (HL2), making it appear that the foliage leaf subtending the renewal bud is on the same side as the second hook leaf. Since this is a crucial stage in providing evidence for the sympodial development of the hook inflorescence, a number of young buds were dissected and photographed. This ontogenetic series shows that as the terminal apex becomes a hook inflorescence there is a slowing of vertical growth of the apex so that the ultimate leaf produced (HL2) never overtops the penultimate leaf (HL1) (Figs. 26–32). When the hook begins to develop and curves away from the main stem, the penultimate or first hook leaf and its axillary bud move even farther away from the second hook leaf, further adding to the false impression that HL1 is the ultimate leaf that formed on the apex (Fig. 24B).

The evidence presented in this paper, which helps clarify the controversies of both thorn initiation and formation of the sympodial hook inflorescence, provides a powerful argument for the usefulness of developmental observations in morphological and architectural studies. This is especially true in plants that undergo major secondary developmental shifts and realignments as they reach their mature form.



View larger version (142K):
[in this window]
[in a new window]
  		Figs. 35–38. Figs. 35, 36, and 38 are macrophotographs of late stages of hook inflorescences photographed under a dissecting microscope. Fig. 37 is an epi-illumination light micrograph of a dissected tip of a hook inflorescence. 35. Hook inflorescence prior to curving showing the two hook leaves (HL1 and HL2) in their characteristic claw-like morphology covering the floral meristems. The renewal shoot (R) is well developed and the original first leaf or prophyll (Lp) of the plagiotropic shoot can be seen to the left of the hook inflorescence with a bud (B) developing in its axil. 36. A hook inflorescence before curving with a floral apex (F) clearly visible in the axil of the second hook leaf (HL2). 37. An oblique side view of a dissected hook inflorescence showing the second order floral apex (F') in the axil of first hook leaf (HL1) and the third order floral apex (F") in the axil of a foliage leaf (L1) of the renewal shoot. This post hook formation stage follows on from Fig. 34 where the renewal bud (R) was still in close proximity to the first floral bud (F). 38. A side view of a nearly mature hook inflorescence that has curved to form the characteristic hook. The two hook leaves are still recognizable (HL1 and HL2) and the renewal shoot (R) of the plagiotropic shoot can be seen to the right of the figure. The hook inflorescence has become noticeably lignified at this stage. Scale bar for Figs. 35, 36 and 38 = 1.0 mm. Scale bar for Fig. 37 = 0.1 mm

 

   FOOTNOTES
 
1 The authors thank Sandy Smith for help with the scanning electron microscope, D. DeCosta for illustrations, and C. Lacroix for help in French translation. This research was initiated while the second author was a Short-term Visiting Professor of Botany at the University of Guelph. The first author was supported by an operating grant from the Natural Sciences and Engineering Research Council of Canada (A6260). The second author was supported partly by N.S.F. grant DEB-9224126. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Bailey, L. H., and E. Z. Bailey. 1976 Hortus Third: concise dictionary of plants cultivated in the United States and Canada. MacMillan, New York, New York, USA.

Bieniek, M. E., and W. F. Millington. 1967 Differentiation of lateral shoots as thorns in Ulex europaeus. American Journal of Botany 54: 61–70.

Blaser, H. W. 1956 Morphology of determinate thorn-shoots of Gleditsia. American Journal of Botany 43: 22–28.

Blume, C. L. 1830 Flora Javae: Annonaceae. Fascicle 21–24, 28–33.

Charlton, W. A., A. D. Macdonald, U. Posluszny, and C. P. Wilkins. 1989 Additions to the technique of epi-illumination light microscopy for the study of floral and vegetative apices. Canadian Journal of Botany 67: 1739–1743.

Cremers, G. 1973 Architecture de quelques lianes d'Afrique Tropicale. Candollea 28: 249–280.

Fries, R. E. 1959 Annonaceae. In A. Engler and K. Prantl [eds.], Die natürlichen Pflanzenfamilien 2nd. ed., Bond 17a II. Duncker und Humbolt, Berlin, Germany.

Hallé, F., R. A. A. Oldeman, and P. B. Tomlinson. 1978 Tropical trees and forests: an architectural analysis. Springer-Verlag, Berlin, Germany.

Hallé, N. 1973 Crochets de lianes du Gabon: Ancistrocladus et Anacolosa (Ancistrocladacée). Adansonia, série 2 13: 299–306.

Kaplan, D. P. 1984 The concept of homology and its central role in the elucidation of plant systematic relationships. In T. Duncan and T. F. Stuessy [eds.], Cladistics: perspectives on the reconstruction of evolutionary history, 51–87. Columbia University Press, New York, New York, USA.

Mabberley, D. J. 1987 The plant-book: a portable dictionary of the higher plants. Cambridge University Press, New York, New York, USA.

Massart, J. 1896 Sur la morphologie du bourgeon. Annales du Jardin Botanique de Buitenzorg 13: 121–136.

Posluszny, U., M. G. Scott, and R. Sattler. 1980 Revisions in the technique of epi-illumination light microscopy for the study of floral and vegetative apices. Canadian Journal of Botany 58: 2491–2495.[CrossRef]

Tourn, G. M., D. Medan, and R. D. Tortosa. 1989 Yemas multiples en Ramnaceas: organización del complejo axilar con especial referencia á Ziziphus y Paliurus. Kurtziana 20: 101–111.

Tortosa, R. D., L. Aagesen, and G. M. Tourn. 1996 Morphological studies in the tribe Colletieae (Rhamnaceae): analysis of architecture and inflorescences. Botanical Journal of the Linnean Society 122: 353–367.[CrossRef]

Treub, M. 1883 Sur une nouvelle catégorie de plantes grimpantes. Annales du Jardin Botanique de Buitenzorg 3: 44–75.

Troll, W. 1937 Vergleichenden Morphologie der höheren Pflanzen. 1 Band, 1 Teil. Gebrüder Borntraeger, Berlin, Germany.





This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via ISI Web of Science (2)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Posluszny, U.
Right arrow Articles by Fisher, J. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Posluszny, U.
Right arrow Articles by Fisher, J. B.
Agricola
Right arrow Articles by Posluszny, U.
Right arrow Articles by Fisher, J. B.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS