FEATURES of the SECONDARY XYLEM THAT FACILITATE BRANCH ABSCISSION in JUVENILE WOLLEMIA NOBILIS R.D. Heady1 and G.E. Burrows2

IAWA Journal, Vol. 29 (3), 2008: 225–236

FEATURES OF THE SECONDARY XYLEM THAT FACILITATE BRANCH ABSCISSION IN JUVENILE WOLLEMIA NOBILIS

R.D. Heady1 and G.E. Burrows2

SUMMARY Wollemi pine (Wollemia nobilis) does not shed individual leaves but instead cleanly self-prunes the whole first-order branch with all the leaves still attached. A zone of stranded xylem at the branch base, the site of branch abscission, is described here in relation to the profusion of bordered pits and ray parenchyma cells that occur in this region. We propose that the much higher occurrence frequencies of these two features, compared to those in the stem and in the outer regions of the branch, results in a zone of radially-orientated weakness which facilitates branch abscission. We also suggest that since the stranded xylem region has a smaller cross-sectional area than the outer regions of the branch, the prevalence of bordered pits promotes water flow, and thus may alleviate the effects of this region on water supply to the foliage. Our observations represent, to the best of our knowledge, the first report of the involvement of bordered pits and ray parenchyma in branch abscission. Key words: Wollemia nobilis, Wollemi pine, branch abscission, ray parenchyma cells, bordered pits, self-pruning, xylem.

INTRODUCTION

Branches of the endangered species Wollemia nobilis (Araucariaceae), or Wollemi pine as it is commonly known, are reported to have three unusual features. Firstly, all of its branches are “first-order” only – the branches do not branch again. Secondly, Wollemi pine does not shed individual leaves but instead self-prunes the whole branch with all the leaves still attached. Thirdly, when branches are shed, they are cleanly abscised from the tree (Hill 1997; Offord et al. 1999; Burrows et al. 2007). Millington and Chaney (1973) report that many families of angiosperms and gymnosperms contain species which shed lateral branches, a process known as cladoptosis, and they list thirty families of angiosperms in which it occurs to some degree. In the gymnosperms, cladoptosis occurs in some of the species of five families of the Coniferales: Taxodiaceae, Pinaceae, Cupressaceae, Podocarpaceae and Araucariaceae (Millington & Chaney 1973). However, this process “is usually limited to twigs and small branches in the crown of trees” (Millington & Chaney 1973) and shedding of entire first-order foliar branches (such as occurs inW. nobilis) is rare. Licitis-Lindbergs

1) Fenner School of Environment and Society, The Australian National University, Canberra, ACT 0200, Australia. 2) Institute for Land, Water and Society, Charles Sturt University, Locked Bag 588, Wagga Wagga, NSW 2678, Australia.

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(1956) and Wilson et al. (1998) have described shedding of first-order branches in Kauri (Agathis australis) and have pointed out that this is a very desirable feature in trees used for timber since it results in wood that is virtually knot free. Burrows et al. (2007) have shown that branch abscission in W. nobilis occurs in a region of constricted and stranded xylem in the branch base. The main features of this region are a “narrow diameter xylem cylinder within the stem cortex, xylem dividing into strands in the abscission zone, and strands rejoining in the much larger diameter apparent branch base”. Burrows et al. (2007) also described the proximal end of abscised W. nobilis branches as having a smooth separation layer with a small xylem protrusion. In this paper we describe some of the anatomical features of the wood of W. nobilis saplings and compare equivalent features in the abscission region of the branch base with those of the stem and the more distal regions of the branch. We discuss possible advantages for the unusually high frequencies of ray parenchyma cells and bordered pits that are present in the abscission region and suggest that they constitute a weakening of the xylem which facilitates abscission when self-pruning occurs. We then attempt to correlate these findings with an investigation of the anatomy of the proximal ends of some abscised branches.

MATERIALS AND METHODS

Since Wollemia nobilis is an endangered species and access to material growing in the wild is severely restricted by law, our sampling was confined to three 6–7-year-old, seed-derived and cultivated plants grown in 75 L pots under 50% shade cloth at Mount Annan Botanic Garden, NSW, Australia. These plants were approximately 2 m tall and at their base the main stems were 2–3 cm in diameter. Lengths of main stem for study, each complete with 4–6 branches, were taken from these trees and used for examination of xylem structure in the abscission zone. We also used twelve individual branches which had abscised from similar trees grown at the same source for observation of the branch bases post-abscission. Material for light microscopy (LM) was softened prior to cutting by soaking it in water for 48 h. The wetted wood was then clamped in a vice, viewed under a dissecting microscope, and transverse (TS), tangential longitudinal (TLS), and radial longitudinal (RLS) sections were shaved off using a hand-held, single-edged razor blade. The shaved sections were then stained in a safranin solution and dried in an alcohol series before mounting on glass slides. Water-softened material for scanning electron microscope (SEM) examination was cut using a hand-held razor blade and cleaned by washing in several changes of distilled water. The cut sections were then dried at atmospheric pressure over silica gel for 48 h and under vacuum (10-4 Pa) for 24 h, attached to mounting stubs and sputter-coated with a 10 nm layer of gold. A Cambridge Instruments S360 SEM was used to image the various wood features. Measurements of the dimensions of anatomical features such as ray height and ray width were carried out directly using an on-SEM-screen, point- to-point measurement facility. Other features such as ray volume and xylem area were

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determined from pre-recorded SEM images by using the ʻdensity slice facilityʼ of the NIH Scion Image program on a personal computer. Maximums, minimums, means and standard deviations were calculated, and they are represented below using the format: [minimum-mean-maximum (SD = , n = )] in which ʻSDʼ indicates the standard devia- tion and ʻnʼ the number of measurements (IAWA Committee 2004).

Figures 1–3. Branch attachment in juvenile Wollemi pine. – 1: Section of stem with branch. The bark and cortical tissues are intact. – 2: Bark tissues partially removed to reveal the xylem of the stem and branch base. Note that, in this sample, the branch xylem attaches to the stem xylem approximately 35 mm below the apparent branch base. – 3: Sections of xylem from the Upper (U), Strands (S) and Lower (L) regions of the branch base, all at the same magnification. — Scale bars = 20 mm for Fig. 1 & 2; 1 mm for Fig. 3.

RESULTS

Branch attachment in juvenile Wollemia nobilis is shown in Figures 1–3. The branch xylem exits from the main stem in a small-diameter cylindrical form termed the “Lower” zone. The cross-sectional area of the xylem in this region, excluding the small central pith, was 0.43-0.53-0.60 mm2 (SD = 0.065, n = 5). Note that “n = 5” indicates that five branches were measured. This zone of xylem continued upwards at about 3–5° to the main stem and was completely enclosed within the cortex and bark of the stem. The length of the Lower region of xylem was 21–28 mm. The xylem then gradually separated into 5–14 discrete or semi-discrete strands (Fig. 3). This “Strands” zone was partially flattened to about 2 mm high and 4.5 mm wide, and the cross-sectional area of the xylem was 1.46-2.00-2.53 mm2 (SD = 0.425, n = 5). There was an area of parenchymatous pith inside the ring of strands and parenchyma also separated the individual strands.

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The Strands zone continued for 18–37 mm and in its mid to distal region it was bent out from the stem at about 45°. At its distal end the xylem gradually reformed into the single cylindrical form termed the “Upper” zone. This was oval in transverse section, had a diameter of approximately 3 mm, and the xylem (excluding the central pith) had a cross-sectional area 2.39-3.11-4.23 mm2 (SD = 0.698, n = 5). The transverse sections in Figure 3 are shown at the same magnification and provide a visual comparison of the area of xylem in each of the different zones. Ray tissue was at least two and a half times more prevalent in the Lower and Strands zones than in the stem and the Upper zone of branches. Ray volume, expressed as a percentage (i.e. the proportion of ray tissue relative to all other tissue in the xylem) in the Lower region was 11.7-15.9-21.6 (SD = 3.3, n = 9) and in the Strands region it was 13.6-16.4-22.2 (SD = 2.4, n =10), whereas in the Upper it was 3.4-4.9-6.3 (SD = 0.8, n =11), and in the stem xylem it was 4.3-5.8-8.7 (SD =1.5, n = 9). Note that “n =” refers to the number of images, each of area 0.068 mm2 that were measured – it does not refer to the number of rays measured. Table 1 shows that the larger ray volume in the Strands region than in the Upper region was mainly a function of ray cell frequency and the number of cells present in individual rays. The heights and widths of individual ray cells in the Upper, Strands, and Lower regions and in the stem were all similar.

Table 1. Comparison of the average values of various xylem features in the stem, and in the Lower, Strands, and Upper zones of the branch bases of juvenile Wollemi pine trees.

Feature Lower Strands Upper Stem 1 Xylem area (mm2) 0.53 2.00 3.11 N/A 2 Ray volume (%) 15.9 16.4 4.9 5.8 3 Ray height (μm) 72.8 64.6 39.9 45.6 4 Ray cell width (μm) 17.3 16.3 15.5 17.9 5 Ray cell height (μm) 31.1 32.6 31.5 27.3 6 Ray cell frequency (mm2) 331 351 178 168 7 Number of cells in ray 2.3 2.0 1.3 1.7

Far more bordered pits per unit area were present in the Lower and Strands zones than occurred in the stem or in the Upper zone. It was not possible to make an accu- rate count of the number of bordered pits in particular areas because pits occurred in both radial and tangential walls. However, an approximate indication is apparent by comparing Figures 4 and 5. A count of bordered pits in these two areas, which are of the same size, found 179 pits in the Strands region and 8 pits in the Upper region; i.e. approximately 22 times more bordered pits in the Strands than in the Upper region. In the Strands region, pitting was prolific on both tangential (Fig. 4) and radial walls (Fig. 6), whereas in the Upper region pitting was absent from tangential walls (Fig. 5) and was present (though not prolific) on radial walls (Fig. 7). Figure 8 shows typical abundant pitting of the Strands region. Figures 9 and 10 show the proximal ends of abscised branches in which strands of xylem protrude from the general abscission zones. Similar xylem protrusions were

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Figure 4 & 5. Comparison of TLS views of secondary xylem from the Strands and Upper regions. – 4: Small area (approx. 0.068 mm2) of the Strands zone showing abundant pitting in both the radial and tangential walls of tracheids. Nineteen ray cells can be seen. – 5: Same-sized area of Upper zone xylem showing sparse RLS pitting and six ray cells. — Scale bars = 100 μm.

present in all of the twelve abscised branches that were examined. The lengths of the protrusions ranged from a few microns up to 3.3 mm, but varied between branches, and between and within the individual strands (Fig. 11) on the various branches. The broken ends of tracheids and xylem strands were rough and irregular. All breaks occurred in xylem that was heavily pitted (Fig. 12–17). There also appeared to be a correlation

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Figure 6 & 7. Comparison of RLS views of secondary xylem from the Strands and Upper regions. – 6: Area of the Strands zone showing three rays, all greater than one cell in height. Bordered pits (arrows) are present in the tracheid walls. – 7: Area of Upper zone xylem with two rays, each one cell in height. No bordered pits are present in the tracheids. Both images are at the same magnification. — Scale bars = 100μ m.

between the breaks and rays in the xylem; many of the breaks occurred in radial files along a row of ray parenchyma cells (Fig. 12–15). There was also a pronounced splitting of the broken xylem in the radial longitudinal plane (Fig. 12). Figures 16 and 17 show the broken ends of tracheids.

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Figure 8. TLS of Strands zone showing abundant pitting of tracheids in both radial and tangential longitudinal planes. The ray at right of center is seven cells in height. — Scale bar = 50 μm.

DISCUSSION

Table 1 and Figure 3 indicate that the Upper region of the branch base had a larger average cross-sectional area of xylem (3.11 mm2) than the Lower and Strands regions (0.53 mm2 and 2.00 mm2 respectively). Thus the Lower and Strands regions of the branch base represent a potential constriction to water flowing from the stem to the Upper region and the more distal parts of the branch and thus the foliage.

→ Figures 9–17. SEM images of the proximal ends of branches that had abscised from juvenile Wollemi pine stems. – 9: Proximal end of branch showing a smooth abscission zone through the bark and cortex, and irregular protrusions of xylem strands. – 10: End-on view of branch base showing seven strands of xylem, each raised above the remainder of the general abscission zone. – 11: A single strand of xylem with a rough, uneven, broken surface. – 12: Irregular broken ends of part of a xylem strand. There is extensive splitting of the xylem in the radial longitudinal plane and breaks appear to follow along the lines of rays. – 13: Broken ends of tracheids which have prolific bordered pitting. The breaks appear to follow the lines of ray parenchyma cells. – 14: Break in xylem appears to follow along a ray. – 15: Break (arrows) follows line of parenchyma cells at base of ray. – 16: Tracheids with frayed ends. – 17: Cleanly broken tracheids. The tracheids have prolific bordered pitting. — Scale bars = 5 mm for Fig. 9 & 10; 500μ m for Fig. 11; 200 μm for Fig. 12; 100 μm for Fig. 13 & 16; 50 μm for Fig. 14, 15 & 17.

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Table 1 also shows that average ray volume in the stem and in the Upper zone was 5.8 and 4.9% respectively. These values are in line with the ray volume range of 3.4 to 11.7% reported for the coniferous woods of the United States by Panshin and DeZeeuw (1980) and a range of 6 to 10% for conifers grown in Yugoslavia (Petric & Scukanec 1973). However, average ray volumes for the Lower and Strands zones (15.9 and 16.4% respectively) are much higher than those reported by the above authors and higher than any of those reported for other regions of adult or juvenile W. nobilis stem wood by Heady et al. (2002). This poses the question as to the purpose of the unusually high proportion of ray parenchyma cells in these regions. Ray parenchyma cells are well known to play an important role in the storage and radial transport of reserve materials (Ziegler 1964; Lev-Yadun & Aloni 1995). How- ever, this would not seem to be a logical function for the rays in the Lower and Strands regions of the branch base xylem since it would be far more practical to store materials in other regions of the stem or outer branch. Rays also play a part in gas exchange (Back 1969; Kučera 1985) but we can see no logical reason for this in a region of stranded xylem, and we saw no evidence of the pore spaces that accompany this role. We propose, instead, that since the rays are aligned at right angles to the axis of the tree (i.e. in the plane of the proposed break) the wood of the Strands zone is ef- fectively weakened in the radial plane by the ray parenchyma cells, and this suggests that they assist abscission. Table 1 shows that ray volume in the Strands region (where abscission occurs) is more than three times greater than that in the Upper region of the branch (where breakage is not wanted). Cross-field pitting of the rays is of the “arau- carioid” type, with individual pits crowded together, leaving very little unused space within each cross field (Fig. 6). The apertures of cross-field pits represent a weakness of the ray parenchyma cell wall which, in turn, reduces radial breaking strength and facilitates abscission. It can also be pointed out that the cross-field pit-pairs of rays in W. nobilis are half-bordered (bordered on the tracheid side and simple on the ray parenchyma side). Thus, on the ray side, cross-field pits do not have pit borders to give them structural rigidity. Pickard (1981) says that the membrane areas of unbordered pits produce a serious weakening of the cell wall. This is normally not of concern to rays since they are not subjected to water flows, embolisms, and possible wall collapse, as is the case for tracheids. However, this inherent weakness of the ray cell wall could be a useful feature when transverse fracture (in the Strands region) is needed. It appeared that abscission often occurred along the lines of ray parenchyma cells (Fig. 12–15) and Figure 15 shows a break in tracheids at the base of a ray. Another likely role for an increased number of ray cells in an area where branch abscission takes place would be to play a part in the compartmentalization of damage from the abscission break and the formation of callus, which in turn can differentiate a wound cambium (Kuroda & Shimaji 1984; Lev-Yadun & Aloni 1995). A greater proportion of ray cells, each with a larger number of cross-field pits, would be likely to facilitate a wider and more complete formation of callus to the affected area of stem, and thus speed-up the healing process after abscission has taken place. In all softwoods, tracheids are linked together by bordered pits in their radial walls, the ends of tracheids are tapered, and their tips are not all in the same plane. Therefore

Downloaded from Brill.com10/07/2021 05:34:18AM via free access 234 IAWA Journal, Vol. 29 (3), 2008 Heady & Burrows — Branch abscission in Wollemia 235 they present only an axial plane in the wood, not a radial plane, even at their termina- tions. Thus tracheids do not represent a transverse weakness in wood as is the case for rays. However, the stranding of the branch base xylem in W. nobilis possibly represents a means of facilitating rupture of the smaller, and therefore proportionally weaker, individual strands of xylem as the break takes place, rather than breaking all of the xylem at one time. The much higher proportion of bordered pits in the Strands zone than in the Upper zone and outer branch could also facilitate abscission in this region. Sperry et al. (2006) have pointed out that “xylem conduits, in addition to transporting water efficiently while avoiding cavitation, must also protect themselves against implosion” and indicate that “negative sap pressure puts the conduit wall under compression, drawing it inward”. Furthermore, Hacke et al. (2004) reported that the presence of pits in tracheids low- ered the pressure necessary for implosion to occur “by about 30% relative to a solid wall of the same dimensions, with apertures causing 25% and chambers causing 5% of the effect”. Thus, unusually large numbers of bordered pits in the Strands zone is a possible means of weakening the tracheid cell wall in that region. We also found that bordered pits were prolific in both tangential longitudinal and radial longitudinal walls (Fig. 8) which is very unusual for any coniferous wood since bordered pits normally occur only in radial walls. Pittermann et al. (2006) suggest that “the localization of pits to radial walls may also be an adaptation to minimize their effect on weakening the axis”. Therefore it seems likely that the Strands region of W. nobilis branches, where both tangential longitudinal and radial longitudinal walls of the tracheids are profusely perforated by multiple bordered pits, would be much more likely to rupture than the Upper region of the branch, which has many-times fewer pits in its tracheid walls. It appears that xylem breakage occurs in tracheids which are profusely perforated by bordered pits (Fig. 16–17). While it is possible that increased proportions of rays and bordered pits is conducive to branch abscission, we must also consider their effect on water flow to the leaves of the branch in the 5–13 years of active growth that occur (Hill 1997; Offord et al. 1999) prior to the branch being abscised. Since the Lower and Strands regions represent a reduced cross-sectional area of xylem for water flow (relative to the outer branch) (Table 1) and rays play no part in conducting water axially, the increased proportion of rays to tracheids would suggest that the high proportion of ray tissue further reduces water flow to the foliage. However, we propose that the profusion of bordered pits in the Lower and Strands zones might reduce resistance to water flow when the branch is growing and the major requirement is to supply sufficient water to the leaves. Pickard (1981) points out that much of the resistance to water flow between tracheids of softwoods resides in the membrane (margo) of the bordered pit pairs. We suggest that the proliferation of bordered pits in the Lower and Strands regions of the W. nobilis branch base presents a substantial increase in area of membrane exposed to water flow and therefore possibly alleviates any potential water supply restriction to the foliage. It is likely that the mechanism that finally causes the abscission is the weight of the branch. As branches grow and lengthen (they are all first-order branches) they place an ever-increasing turning moment on the branch base which eventually leads to the

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rupture in the Strands region, where xylem strength is weakest. Abscission does not occur in the Lower region, even though the amount of ray tissue (Table 1) and numbers of bordered pits are similar to that of the Strands region. This is because the Lower region is aligned almost parallel to the stem whereas the approximate mid-point of the Strands region is angled at about 45° to the stem (Fig. 2) and so is subjected to a greater turning moment. Figures 9 to 17 show that the xylem of abscised branches protrudes out from the general surface of the abscission zone, and the ends of tracheids and xylem strands are ruptured in a rough, uneven manner. Nevertheless self-pruning in juvenile W. nobilis can be considered to be relatively ʻcleanʼ in that the separation area on the tree stem immediately below the base of the branch has smooth bark and cortex (Burrows et al. 2007), and breaks in the xylem are recessed up to 3.3 mm below the stem surface. For such an arrangement, branch abscission is likely to cause minimal injury to the tree and facilitate a fast and comprehensive healing of the break which is therefore less likely to admit pathogens into the wound. We conclude that there are two entirely different mechanical and physiological requirements for the branch abscission region, each with totally different requirements, but the requirements of each particular situation must be taken into account by the other. One situation occurs when the leaves of a particular branch are no longer necessary and the tree ʻrequiresʼ a clean abscission of the branch (with leaves attached) in order to allow a faster healing of the wound, thus minimising entry of pathogens and reduc- ing the risk of infection. In this situation a lowering of the branchʼs radial breaking strength in a region close to the base of the branch is the requirement, and we suggest that this is facilitated by multiple-fold increases in the number of bordered pits and ray parenchyma cells which cause a weakness in the xylem. A different situation occurs when the branch is growing and the major requirement is to supply sufficient water to the leaves. In this situation the region of narrow diameter xylem at the base of the branch with a high proportion of ray parenchyma could be a major restriction to water flow to the foliage unless some means of promoting flow was built into this region. We suggest that this situation could be alleviated by the vastly increased number of bordered pits in the region, which lowers the resistance to water flow.

ACKNOWLEDGEMENTS

We thank the ANU Electron Microscope Unit for providing the excellent facilities for imaging, Cathy Offord, Patricia Meagher, and Amanda Rollason of the Royal Botanic Gardens, Sydney for supply- ing the wood samples used in this research, and Professor Pieter Baas of the Nationaal Herbarium Nederland for very useful comments on the original manuscript.

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