IAWA Journal, Vol. 21 (3), 2000: 293–319

CALLITROID (CALLITRISOID) THICKENING IN by R.D. Heady & P.D. Evans Department of Forestry, The Australian National University, Canberra, Australia

SUMMARY

In softwood tracheids, callitroid thickening is the term given to raised bars located above and below individual bordered pit apertures. Al- though most well developed in the Australasian genus Callitris, callitroid thickening is reported to be absent from six Callitris species and to vary in its frequency and prominence. An SEM study of callitroid thickening was carried out on multiple wood samples of each Callitris species, taken from trees growing in the wild. The aims of the study were to de- termine the occurrence, frequency, visual prominence and morphology of callitroid thickening in all Callitris species and to determine whether it could be used taxonomically. Callitroid thickening was found in all (19) species of the genus, in contrast to previous reports of its absence in some species. In general, callitroid thickening occurred at higher fre- quencies and was more prominent in species from dry habitats than in those from wet habitats. The frequency of thickening varied between and within samples and, for example, it was always more frequent on pits in narrow rather than in wide tracheids. Callitroid thickening var- ied in its morphology, and types consisting of one to four bars, extend- ing completely or only partially across the inner radial wall of the tra- cheid, were observed. Thickening on tracheid-ray pits within cross fields occurred in all species, and with similar frequency and morphology to thickening of bordered pits. Our findings suggest that frequency of calli- troid thickening is useful taxonomically in separating four groups of Callitris species and in assisting in the identification of certain indi- vidual species. Key words: Callitroid thickening, awns, Callitris Vent., cypress pine, bordered pits, cross-field pits.

INTRODUCTION

In softwood tracheids, callitroid (or callitrisoid) thickening is defined as “pairs of thickening bars across the pit border” (Phillips 1948; IAWA Committee 1964). The bars extend across the cell wall in radial longitudinal section (RLS), normal to the tracheid axis, delimiting a “rectangular area” (Cronshaw 1961) with the pit aperture at its centre. When viewed in tangential longitudinal section (TLS) the bars are de- scribed as “awns” (Patton 1927; IAWA Committee 1964).

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Reports in the literature (Phillips 1948; Jane 1970; Barefoot & Hankins 1982) indicate that callitroid thickening is “regularly developed” only in the Australasian genus Callitris Vent. (), a few species of which are important commercial timbers and are commonly known as the cypress pines (Dallimore & Jackson 1966). Similar thickening has been reported to occur occasionally in other Cupressaceae genera, including: Actinostrobus (Kleeberg 1885; Phillips 1948), Juniperus (Phillips 1948) and Tetraclinis (Schweingruber 1990). Callitroid thickening has also been re- ported in the Podocarpaceae: Dacrydium cupressinum Lamb. (Meylan & Butterfield 1978) and Pinaceae: Pseudolarix amabilis Rehd. (Phillips 1948), and several species of the southern pine group of Pinus (Howard & Manwiller 1969). However, these oc- currences outside of the genus Callitris are generally regarded as “rare and inconspic- uous” (Phillips 1948) and callitroid thickening is a defining anatomical feature only for wood of Callitris in the taxonomic keys of Peirce (1937), Phillips (1948), Bare- foot and Hankins (1982) and Wheeler et al. (1985). The literature indicates that callitroid thickening does not occur in all of the 19 species of Callitris listed in Table 1; its absence from C. macleayana, C. muelleri, C. oblonga, C. rhomboidea, C. roei and C. sulcata has been documented by several authors (Patton 1927; Budkevich 1936; Phillips 1948; Greguss 1955, 1972; Venning 1979). As a result, callitroid thickening has been used as the diagnostic character for a dichotomous taxonomic grouping of species within the genus, one group in which thickening occurs, the other group in which it is reported to be absent (Patton 1927; Greguss 1955). In the species reported to possess callitroid thickening, inter-species differences in the frequency of its occurrence, and in its visual prominence, have been noted. Thus thickening in Callitris glauca R.Br. (syn. C. glaucophylla) is said to be “well devel- oped” (Phillips 1948) and occurring on “all pits” (Patton 1927), whereas in Callitris arenosa A. Cunn. (syn. C. columellaris) it is “less strongly developed” (Phillips 1948) and “sparsely present” (Patton 1927). Although descriptions of callitroid thickening always refer to thickening of bor- dered pits (e.g. Phillips 1948; Cronshaw 1961; Greguss 1972), there has also been mention of similar thickening on pits occurring within cross fields. Patton (1927), in a diagram accompanying his text, shows raised borders surrounding pairs of pits in cross fields ofCallitris robusta R. Br. (syn. C. verrucosa). Peirce (1937) found “bands of secondary thickenings” occurring within cross fields of Callitris calcarata R.Br. (syn. C. endlicheri) although he did not mention this form of thickening in his key to genera and description of the wood of Callitris, referring only to “thickening present across the borders of tracheid pit-pairs” (i.e. bordered pits). Venning (1979) did not observe thickening of cross-field pits in any Callitris species. Ilic (1996) described thickening in cross fields of C. endlicheri and C. glaucophylla as giving “the appear- ance of a large border subtending two smaller apertures”. The value of callitroid thickening as a taxonomic indicator of either genus or spe- cies is diminished by a number of omissions and inadequacies in the literature. Two Callitris species, C. monticola and C. neocaledonica, have received no mention as to whether callitroid thickening is present or absent. Also, owing to a recent revision of

Downloaded from Brill.com10/10/2021 04:42:12PM via free access Heady & Evans — Callitroid thickening 295 the taxonomy of the genus (Hill 1998), the occurrence of thickening in C. gracilis, C. preissii, C. tuberculata and C. verrucosa is uncertain. There is also a lack of definitive information regarding the occurrence and morphology of thickening on cross-field pits in all species of the genus. Furthermore, many of the previous studies of Callitris species were based on inadequate or poorly-representative samplings. For example, the report by Greguss (1972) of thickening in C. morrisoni (syn. C. canescens) was based on “sections cut of a [single] bough about 1 cm thick, 3 to 4 years old” rather than multiple specimens of main-stem wood, and Venning (1979) used “branchlets” for her studies. Finally, although the frequency and visual prominence of thickening is reported to vary between species, these parameters have been described in only a very brief and subjective manner for one or two species in the genus. Thus there is clearly a need for a comprehensive survey of callitroid thickening on bordered and cross-field pits in all species ofCallitris . There were two basic aims of this study: 1) to use scanning electron microscopy (SEM) to determine the occurrence, frequency, visual prominence and morphology of callitroid thickening on bordered and cross-field pits in multiple wood samples of all species of Callitris; and, 2) to determine whether callitroid thickening can be used taxonomically to assist in the identification ofCallitris species.

MATERIALS AND METHODS

A total of 169 wood samples, each taken from a different tree, and ranging from three samples each of C. neocaledonica and C. sulcata to 22 samples of C. rhomboidea (Table 1) were obtained using an increment corer. The 5 mm diameter cores were taken from the main stems of trees of unknown age (but of adult appearance for the particular species), growing wild, and from within the known distribution range of each species. Table 1 and Figure 1 show the geographical locations of trees from which

The site numbers: 1 C. baileyi 2 C. canescens 3 C. columellaris 4 C. drummondii 5 C. endlicheri 6 C. glaucophylla 7 C. gracilis 8 C. intratropica 9 C. macleayana 10 C. monticola 11 C. muelleri 12 C. neocaledonica 13 C. oblonga 14 C. preissii 15 C. rhomboidea 16 C. roei 17 C. sulcata Fig. 1. Map of Australia and New Caledonia showing the approxi- 18 C. tuberculata mate wood sampling locations for each Callitris species. 19 C. verrucosa.

Downloaded from Brill.com10/10/2021 04:42:12PM via free access 296 IAWA Journal, Vol. 21 (3), 2000 51 10 84 6 266 782 905 915 583 326 247 129 517 517 856 Num- 1922 2744 2052 1297 2123 2:

Habitat type Habitat . —

4: 5 910 1131 1055 2232 1639 1306 2998 2091 1395 2699 1749 1227 1056 2533 1876 4368 1076 1310 2149 Callitris

4 Dry Dry Dry Wet Wet Wet Wet

Species of Very dry Very dry Very dry Very dry Very dry Very dry Very dry Very dry Very Very wet Very wet Very wet Very wet Very 1:

Numbers of pits on which thickening occurred and for which data

6: 3

Rosewood / Grandchester, QLD Rosewood / Grandchester, & Port Lincoln, SA WA Lake Grace, Bribie Island, QLD WA Ravensthorpe, Pound, SA Wilpena & Coonabarabran, NSW Atherton, QLD & / Groote Eyt., NT Litchfield QLD Tablelands, Windsor Maiala Nat. Park & Gibraltar Range Nat. Park, Glenn Innes, NSW NSW Lithgow, Montagne des Sources, New Caledonia WA Fremantle / Perth, TAS & Bicheno, NSW Batemans Bay, WA Lake Grace / Newdegate, Dumbea du Nord, New Caledonia WA Lake Grace, SA Wilmington, / Tooligie & Euston, NSW Temora, NSW & Rhylstone, NSW NSW Temora, Bend, SA Tailem Avoca / Bicheno, TAS / Bicheno, Avoca

Approximate geographical regions from which the samples were acquired.* — acquired.* were samples the which from regions geographical Approximate 8 5 7 6 6 4 8 5 4 5 2 11 11 5 10 15 16 10 13 22 3:

Sm.

Numbers of bordered pits examined. —

Sm. 5:

Baker & H.G.

Bailey

Blake

Baker & H.G.

Dümmer

Cunn. ex Endl.) F. Muell. Cunn. ex Endl.) F.

1 Thompson & Johnson

Baker Garden

F. Muell. (Parl.) F.Muell.

(F. Muell.) F.Muell. R.Br. ex Rich. R.Br. White R.T.

R.Br. ex R.T. R.Br. (Parl.) F.M. (Parl.) S.T. J. (A. (Parl.) F.Muell. Rich. R.T. Miq. (Parl.) Schlechter C.T. (Endl.) F.Muell. Abbreviations of Australian states and territories are: NSW = New South Wales; NT = Northern Territory; QLD = Queensland; SA = South Australia; TAS = Tasmania; WA = Western Australia. Western = WA Tasmania; = TAS Australia;

C. baileyi C. canescens C. columellaris C. drummondii C. endlicheri C. glaucophylla C. gracilis C. intratropica C. macleayana C. monticola C. muelleri C. neocaledonica C. oblonga C. preissii C. rhomboidea C. roei C. sulcata C. tuberculata C. verrucosa *) Table 1. Wood core sampling and SEM specimen observation information. The columns are numbered as follows: core sampling and SEM specimen observation information. Wood 1. Table — study. the in used species each of samples of bers dry). — wet, Very Dry, Very (Wet, were acquired.

Downloaded from Brill.com10/10/2021 04:42:12PM via free access Heady & Evans — Callitroid thickening 297 samples were obtained. An additional sample of C. sulcata was cut from specimen block R1257-1 obtained from the wood reference collection of the NSW Forestry Commission Laboratories, Sydney, and a sample of C. neocaledonica (neoc-1) was obtained from the Service des Forêts Patrimoine Naturel, Noumea, New Caledonia, thus increasing the number of samples of these two species to four each, and the total number of samples used in the study to 171. Samples were identified to species level. No attempt was made to distinguish the two subspecies in C. gracilis or the three subspecies in C. oblonga which were recent- ly classified by Hill (1998). Since wood anatomy features in heartwood of Callitris are sometimes occluded by resinous extractive deposits, sapwood, which is usually free of such contamination, was always selected in preference to heartwood as the sample material. Plane surfaces for SEM were prepared from wood samples that had been softened by soaking in distilled water at 20 °C for three days. The water-saturated samples were clamped in a small vice and cut with a hand-held, single-edged razor blade while being viewed under a stereo-microscope, a method similar to that outlined by Kucera (1981). Four specimen surfaces, each measuring approximately 4 by 3 mm in RLS and in TLS, were prepared for SEM from each sample. They were cleaned by washing them in several changes of distilled water, dried at atmospheric pressure over silica gel for two days and under vacuum (10-4 Pa) for eight hours, attached to mounting stubs, and sputter coated with a 10 nm layer of gold. Prepared SEM specimens were viewed using a Cambridge Instruments S360 scan- ning electron microscope operating with an accelerating voltage of 15 kV and a work- ing distance of approximately 20 mm. RLS and TLS specimens were mechanically rotated within the SEM so that the longitudinal axes of tracheids were always orientated vertically on the screen. This standardisation of orientation facilitated comparison of the callitroid thickening of different specimens and species. Records were kept of numbers of pits examined and numbers of occurrences of thickening in each RLS specimen (Table 1). These data were used to determine speci- men means for frequency of occurrence of thickening, which in turn were used in analyses of variance to provide estimates of species means and appropriate confidence intervals. Also, since preliminary observations revealed that there were four different morphological forms of callitroid thickening (based on the number of bars and their degree of extension across the wall of the tracheid), all occurrences of thickening were classified into one of four types. An effort was made to view as much of the specimen surface as possible during SEM examination. This was done by viewing the whole surface (approximately 12 mm2) in a series of ordered traverses from left to right and from top to bottom of the specimen at magnifications of between 600 and 3000 times, and recording the occur- rence and type of thickening on all visible pits (typically 100 to 500 pits per speci- men). This procedure also ensured that pits in both wide and narrow tracheids were assessed, and reduced the possibility of individual pits being inadvertently counted more than once.

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Fig. 2. Callitroid thickening in RLS (left) and TLS (right) showing where measurements were made to quantify the morphological variation in thickening between species. 1 = bar separa- tion, 2 = bar width, 3 = bar height, 4 = bar angle.

The presence or absence of thickening on individual pits, and the radial widths of the tracheids in which the pits occurred, was recorded for one pit in each of 25 adja- cent tracheids per specimen. This process was repeated for three to eight specimens of each species. The areas on each specimen where this was carried out were selected randomly, but with the proviso that there were at least 25 adjacent tracheids suitably exposed for SEM examination, and that pits in both narrow and wide tracheids could be included in the process. All linear measurements were made directly on the SEM image using a point-to-point measurement facility. The data were examined to check for a relationship between frequency of occurrence of thickening and tracheid width for each Callitris species. For the study of morphological variation in callitroid thickening, the following four parameters were measured for each species: 1) distances between bars (at their centres), 2) widths of bars, 3) height of individual bars, and 4) bar angles (in relation to the inner radial wall of the tracheid). Measurements were carried out directly on SEM images at magnifications of 1000 to 10,000. Parameter 1 was measured in RLS and parameters 2, 3, and 4 were measured in TLS (Fig. 2). Bar angles (parameter 4) were obtained by using a protractor held against the on-screen image. Means and standard deviations of these measurements were calculated. Light microscopy (LM) of callitroid thickening in all species was carried out to compare results obtained by SEM. LM sections (approximately 20–50 μm thick) were manually cut from water-saturated wood samples using a single-edged razor blade. A Zeiss Axioskop microscope with halogen (transmitted light) illumination and a blue filter was used to examine unstained sections.

RESULTS Occurrence and frequency of thickening Callitroid thickening occurred in all 19 species of Callitris (Fig. 3–21) but the frequency of its occurrence varied between species (Fig. 22), between samples within species, and between different tracheids within individual specimens (Fig. 14 & 19).

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Fig. 3–12. Occurrences of callitroid thickening in Callitris species. – 3: C. baileyi. – 4: C. ca- nescens. – 5: C. columellaris. – 6: C. drummondii. – 7: C. endlicheri. – 8: C. glaucophylla. – 9: C. gracilis. – 10: C. intratropica. – 11: C. macleayana.– 12: C. monticola. — RLS. Tracheid axes are vertical. Scale bars = 20 μm.

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Fig. 13–21. Occurrences of callitroid thickening in Callitris species. – 13: C. muelleri. – 14: C. neocaledonica (arrowed). – 15: C. oblonga (arrowed). – 16: C. preissii. – 17: C. rhomboidea. – 18: C. roei. – 19: C. sulcata (arrowed). – 20: C. tuberculata. – 21: C. verrucosa. — RLS. Tracheid axes are vertical. Scale bars = 20 μm.

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1.0 -

0.8 -

0.6 -

Frequency 0.4 -

0.2 -

0.0 - roei baileyi sulcata preissii gracilis oblonga muelleri verrucosa monticola canescens endlicheri tuberculata intratropica rhomboidea macleayana drummondii columellaris glaucophylla neocaledonica

Fig. 22. Frequency of callitroid thickening in species of Callitris. 95% confidence intervals are shown. The graph is formed from a regression model based on observations made on a total of 34,800 pits in 171 wood samples.

Between species, the mean frequency of occurrence of callitroid thickening on pits as revealed by SEM (hereafter referred to as ʻfrequency of thickeningʼ) varied from 0.8% in C. neocaledonica to 98.7% in C. verrucosa. It was possible to separate four groups of species on the basis of the frequency of their thickening (Fig. 22). The first group contained C. macleayana, C. neocaledonica, C. oblonga and C. sulcata all of which had, on average, less than 10% of their pits possessing thickening. A second group consisted of C. baileyi, C. intratropica, C. monticola, C. muelleri and C. rhom- boidea in which the frequency of thickening was 10–40%. form- ed the third grouping having approximately 40–60% of its pits possessing thick- ening. The remaining species (C. canescens, C. drummondii, C. endlicheri, C. glau- cophylla, C. gracilis, C. preissii, C. roei, C. tuberculata and C. verrucosa) formed the fourth group in which the frequency of thickening was 60% or more. Between- sample variation in frequency of thickening is reflected in the confidence interval associated with the respective mean for each species (Fig. 22). Within specimens, the presence or absence of callitroid thickening was usually consistent within individual tracheids (Fig. 23–28). Variation in frequency of thick- ening within a particular specimen therefore related to differences in its occurrence between groups of tracheids within different areas, and this varied from its absence

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Fig. 23–28. Variability of callitroid thickening within specimens. – 23 & 24: Two different areas on the surface of a single specimen of C. muelleri: 23: all pits devoid of thickening and, 24: all pits with thickening. – 25: Reduced frequency of thickening of pits in wide tracheids in C. verrucosa (pits in the tracheid marked with an arrow do not have callitroid thickening). – 26: Absence of thickening on pits in a wide tracheid (arrowed) in C. verrucosa. – 27: Thickening in C. glaucophylla in both earlywood (EW) and latewood (LW) tracheids. – 28: Thickening occurring in only the narrowest tracheid (arrowed) of C. sulcata. — RLS. Tracheid axes are vertical. Scale bars = 50 μm.

Fig. 29–36. Typical morphology of the four types of callitroid thickening as viewed in RLS (left) and TLS (right). – 29–30: Type 1. – 31 & 32: Type 2. – 33 & 34: Type 3. – 35 & 36: Type 4. — Tracheid axes are vertical. Scale bars = 5 μm. →

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Downloaded from Brill.com10/10/2021 04:42:12PM via free access 304 IAWA Journal, Vol. 21 (3), 2000 on all pits (Fig. 23) to its universal presence (Fig. 24). Thickening occurred with higher frequency in narrow tracheids than in wide ones (Fig. 25). In species with high frequency of thickening it occurred in all but some of the widest tracheids (Fig. 26) and was usually present in both earlywood and latewood (Fig. 27). In species with very low frequency of thickening it was present only on pits in the narrowest tracheids (Fig. 28) and was absent from all others. This correlation between frequency of thick- ening and tracheid width is apparent in Table 2.

Table 2. Average widths of tracheids in all species of Callitris, differentiating between tracheids in which callitroid thickening was present or absent. The main columns indicate species of Callitris, and mean tracheid widths where callitroid thickening was present and absent, respec- tively. Sub-columns indicate: (mean) = mean width of tracheids, (SD) = standard deviation of the mean width of tracheids; (n) = number of tracheids measured.

Tracheid width —————————————————————————————————— Species Thickening present Thickening absent —————————————— ——————————————— (mean) (SD) (n) (mean) (SD) (n) C. baileyi 19.5 5.2 54 29.0 6.3 71 C. canescens 13.0 2.9 112 15.8 2.7 63 C. columellaris 20.7 4.2 82 24.6 6.5 118 C. drummondii 11.6 3.1 87 15.0 3.6 38 C. endlicheri 19.5 5.2 243 25.7 4.9 57 C. glaucophylla 16.8 4.3 217 24.2 4.8 8 C. gracilis 14.5 3.9 106 22.0 4.5 69 C. intratropica 21.7 5.2 91 26.4 5.1 309 C. macleayana 26.6 3.2 8 33.2 7.2 67 C. monticola 10.9 2.6 30 15.7 4.9 120 C. muelleri 12.5 5.1 25 20.9 6.1 125 C. neocaledonica 14.3 4.4 2 37.2 10.2 98 C. oblonga 8.9 2.1 12 16.0 4.1 163 C. preissii 16.8 4.4 108 22.2 3.8 67 C. rhomboidea 15.5 4.4 50 22.7 5.4 200 C. roei 13.1 2.5 77 14.2 2.6 48 C. sulcata 18.3 10.0 6 38.9 7.9 69 C. tuberculata 14.1 3.0 86 18.1 3.3 14 C. verrucosa 16.7 4.7 135 24.8 4.9 15

It can be seen that in all Callitris species the mean width of tracheids in which callitroid thickening was present was smaller than the mean width of tracheids where thickening was absent. For example, Table 2 shows that for C. baileyi where thicken- ing was present, mean tracheid width was 19.5 μm (SD = 5.2, n = 54) whereas for tracheids where thickening was absent, mean width was 29.0 μm (SD = 6.3, n = 71). Table 2 also shows that the mean width of tracheids in which callitroid thickening was present, and the mean width of tracheids in which thickening was absent, varied between species.

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Morphology of thickening Four different morphological forms of callitroid thickening were observed, the particular form being dependent on the number of thickening bars associated with the individual pit, and on whether bars extended fully, or only partially, across the inner radial wall of the tracheid. We have classified the different forms as ʻTypes 1, 2, 3, and 4ʼ (Fig. 29–36). For ʻType 1ʼ thickening, bars did not extend fully across the radial wall from one side to the other (Fig. 29 & 30). For ʻType 2ʼ thickening, two bars were present, both of which extended completely across the radial wall and were attached to both tangential walls (Fig. 31 & 32). For ʻType 3ʼ thickening, single bars occurred both above and below the pit aperture and, in addition, a third bar crossed over the centre of the aperture, parallel to the upper and lower bars (Fig. 33 & 34). For ʻType 4ʼ thickening, two pairs of bars were associated with each individual pit. The second pair of bars were located outside of the pit border and parallel to those adjacent to the pit aperture so that there were two bars above and two bars below the aperture (Fig. 35 & 36). The outer bars of Type 4 were always thinner and less prominent than the inner bars, and they often extended only partially across the radial wall (Fig. 35).

Fig. 37–40. Some variations in the form of Type 1 and Type 3 callitroid thickening. – 37: Type 1 callitroid thickening with two bars both extending to one side wall but not to the other. – 38: Type 1 callitroid thickening consisting of only one bar. – 39: Type 1 callitroid thickening with one full and one partial bar. – 40: Type 3 callitroid thickening with centre bar tapered and incomplete in the region of the pit aperture. — Tracheid axes are vertical. Scale bars = 5 μm.

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There was some variability in these basic types of thickening. In one form of Type 1 thickening, bars extended to one side (tangential) wall but did not extend fully across to the other tangential wall (Fig. 37). In other forms of Type 1, one bar extend- ed fully across the radial wall but the other bar was either entirely lacking (Fig. 38) or did not extend fully from one tangential wall to the other (Fig. 39). Variability also occurred in Type 3 thickening in that the central bar was sometimes incomplete in the region of the pit aperture (Fig. 40). Of all callitroid thickening occurring within the genus, 51.4% was Type 1, 46.3% was Type 2, and 0.8% and 1.5% were of Type 3 and Type 4, respectively (Table 3). However, these percentages varied between species, and it can be seen in Table 3 that Type 1 thickening was most prevalent in C. baileyi, C. columellaris, C. intratropica, C. macleayana, C. monticola, C. muelleri, C. neocaledonica, C. oblonga, C. rhom- boidea and C. sulcata, whereas Type 2 thickening predominated in C. canescens, C. drummondii, C. endlicheri, C. glaucophylla, C. gracilis, C. preissii, C. roei, C. tuberculata and C. verrucosa. Table 3 also shows that thickening of Type 3 was of low frequency (< 4%) in all species, and Type 4 thickening was also generally of low frequency, except in C. glaucophylla and C. verrucosa, where it constituted 11.1% and 8.1% of thickening, respectively. However, within samples, thickening was never exclusively of any particular type, and groupings of pits with heterogeneous mixtures of different thickening types, as well as pits with no thickening, were usually evident (Fig. 41–43). Deviations from these four standard types of thickening were uncommon. How- ever, in tracheids where pits were numerous and closely-spaced vertically, individual bars were sometimes situated midway between the upper bar of thickening occurring on one pit and the lower bar of thickening occurring on the pit situated immediately above it, in an apparent ʻsharing of barsʼ arrangement (Fig. 44). There were also isolated occurrences of bifurcations of individual bars (Fig. 45) and thickening with more than four bars (Fig. 46). Where biseriate pitting occurred, thickening bars were, in some cases, positioned above and below a pair of adjacent pits (Fig. 47). Another form of biseriate pit thickening consisted of single bars above and below each pit, and with a connecting bar between the upper bar of one pit and the lower bar of the other pit, angled between the two pit apertures (Fig. 48). Bordered pits on tangential walls were not common in any Callitris species, but when they occurred, callitroid thickening was sometimes present (Fig. 49).

Fig. 41–52. Various aspects of callitroid thickening. – 41–43: Heterogeneous mixtures of the four standard types of callitroid thickening in tracheids of various Callitris species. Thicken- ing type is annotated as follows: T1 = Type 1, T2 = Type 2, T3 = Type 3, T4 = Type 4, and NT = no thickening. – 44: RLS view of pits with shared bar (SH). – 45: Bifurcated bars (BF) (RLS). – 46: Single pit with eight associated thickening bars (RLS). – 47 & 48: Forms of thickening associated with biseriate pits. – 49: Thickening of pits on tangential wall in C. verrucosa. – 50: Compression wood (RLS) in C. glaucophylla with all pits devoid of callitroid thickening. – 51: Tracheids viewed in TLS longitudinally at 55° angle showing bars extending onto TLS wall. – 52: TLS showing adjacent awns anastomosed (arrowed). — Tracheid axes are vertical. Scale bars = 20 μm.

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Table 3. Proportions of Types 1, 2, 3, and 4 thickening in each species of Callitris as per- centages of all callitroid thickening. The bottom row of the table shows the mean percent- age of each type within the genus.

Species % Type 1 % Type 2 % Type 3 % Type 4 C. baileyi 53.4 42.5 2.6 1.5 C. canescens 42.8 57.1 0.0 0.1 C. columellaris 70.4 29.5 0.1 0.0 C. drummondii 32.4 67.0 0.0 0.6 C. endlicheri 27.0 68.9 2.3 1.8 C. glaucophylla 13.5 74.3 1.1 11.1 C. gracilis 26.7 72.8 0.0 0.5 C. intratropica 76.3 23.3 0.2 0.2 C. macleayana 82.4 13.7 3.9 0.0 C. monticola 66.9 33.1 0.0 0.0 C. muelleri 73.7 25.9 0.4 0.0 C. neocaledonica 80.0 20.0 0.0 0.0 C. oblonga 68.2 31.8 0.0 0.0 C. preissii 38.2 61.7 0.1 0.0 C. rhomboidea 68.7 30.3 0.8 0.2 C. roei 37.0 59.8 2.7 0.5 C. sulcata 91.7 8.3 0.0 0.0 C. tuberculata 15.1 80.8 0.5 3.6 C. verrucosa 13.3 77.0 1.6 8.1 Means: 51.4 46.3 0.8 1.5

Throughout the genus, callitroid thickening was absent from pits in compression wood (Fig. 50). Bars tended to be closer together at their ends than at their centres (excluding the centre bar of Type 3 thickening and the outer bars of Type 4) so that they were slightly curved around the pit aperture. Hence the shape of callitroid thickening in RLS was ʻellipticalʼ. This was particularly noticeable when thickening occurred in very wide tracheids, such as those of C. intratropica (Fig. 10). The mean separation of bars of Types 1 and 2 and the inner bars of Type 4 thickening was 6.3 μm (SD = 1.6, n = 875) whereas the bars above and below the pit aperture in Type 3 thickening were more widely separated, with a mean separation of 11.7 μm (SD = 2.2, n = 147). The bars of all types of thickening were approximately rectangular in cross sec- tion and usually of consistent height and width for most of their length except at their ends, where they were tapered (Fig. 51). Occasionally, an awn from one pit extended fully across the tangential wall and was anastomosed with an awn of a different pit on the opposite side, with the upper awn of one pit connected with the lower awn of the adjacent one (Fig. 52). A warty layer covered the surfaces of the bars of all four types of thickening in all Callitris species. Warts on bars were of similar size and shape to warts on inner tracheid walls, but within the wall area delimited by thickening bars, warts were usually either substantially reduced in size (Fig. 31) or absent (Fig. 33).

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Fig. 53 & 54. Examples of visually distinct and indistinct thickening. – 68: Distinct thickening in C. endlicheri. – 69: Indistinct thickening in C. rhomboidea. — Tracheid axes are vertical. Scale bars = 20 μm.

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Visual prominence of thickening Callitroid thickening varied in its visual prominence, and could be subjectively designated as being ʻdistinctʼ or ʻindistinctʼ in certain species (compare Fig. 53 with Fig. 54). Species in which thickening was always distinct were C. drummondii, C. endlicheri, C. glaucophylla, C. roei, C. tuberculata and C. verrucosa. Thickening was always indistinct in C. intratropica, C. muelleri, C. macleayana, C. neocaledonica, C. oblonga, C. rhomboidea and C. sulcata. SEM examination of the morphology of thickening revealed that the bars of visually distinct thickening were generally wide, with a mean width of 1.4 μm (SD = 0.4, n = 196) and they usually extended fully across the radial wall of the tracheid (i.e., were of Type 2, 3, or 4 thickening). By comparison, bars of indistinct thickening were generally narrow, with a mean width of 0.6 μm (SD = 0.2, n = 21) and they often did not extend fully across the tracheid (i.e., thickening was predominantly of Type 1). A third morphological aspect affect- ing visual prominence of thickening was the angle of inclination of the bars to the radial wall. Bars of visually distinct thickening tended to be upright, with a mean bar angle of 74° (SD = 8.2, n = 196) whereas indistinct thickening consisted of bars that were usually angled more acutely to the radial wall, with mean bar angle of 62° (SD = 11.5, n = 21).

Thickening of cross-field pits Thickening of half-bordered pits in cross fields occurred in all species of Callitris (Fig. 55–73). Inter-species differences in the frequency of occurrence and visual prom- inence of cross-field pit thickening were similar to those for thickening of bordered pits. There were several different morphological forms of cross-field pit thickening. Most commonly, two bars were found, one on either side of a single pit (ʻAʼ in Fig. 74), or pair of pits (ʻBʼ in Fig. 74), with the bars extending fully (ʻCʼ in Fig. 74), or partially (ʻDʼ in Fig. 74), across the radial face of the cross field. Another common type of cross-field pit thickening involved three bars in association with a pair of pits. In this type of thickening, single bars occurred above and below the pit apertures, and a third bar was angled between them (ʻEʼ in Fig. 74). Of less frequent occurrence was a form of thickening in which bars occurred above and below the pit aperture and, in addition, a third bar crossed over the centre of the aperture parallel to the upper and lower bars (Fig. 75). In cross fields containing more than two pits, multiple sets of thickening bars often occurred (Fig. 76). Cross-field pits were always smaller in diameter than bordered pits, and, accordingly, bars of thickening on cross-field pits were smaller than those on bordered pits. This is apparent in Figure 76. Thickening occurred more frequently, and was visually more distinct, in cross fields where rays crossed narrow rather than wide tracheids (Fig. 77). In TLS, the bars of half-bordered

Fig. 55–73. Occurrences of cross-field pit thickening in the different Callitris species. – 55: C. baileyi. – 56: C. canescens. – 57: C. columellaris. – 58: C. drummondii. – 59: C. endlicheri. – 60: C. glaucophylla. – 61: C. gracilis. – 62: C. intratropica. – 63: C. macleayana. – 64: C. monticola. – 65: C. muelleri. – 66: C. neocaledonica. – 67: C. oblonga. – 68: C. preissii. – 69: C. rhomboidea. – 70: C. roei. – 71: C. sulcata. – 72: C. tuberculata. – 73: C. verrucosa. — RLS. Tracheid axes are vertical. Scale bars = 20 μm.

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Fig. 81–83. Pits in axial parenchyma. – 81: RLS view of parenchyma flanked by tracheids showing absence of thickening on the (simple) pits on the inner wall of the parenchyma. – 82: TLS view of half-bordered pit (arrowed) on tangential wall between tracheid and parenchyma showing awns present only on tracheid side and not on parenchyma side of the wall. – 83: Absence of thickening on simple pits in parenchyma crossing a ray. C = cross field (with thickening of cross-field pits); P = axial parenchyma; R = resin content of parenchyma cell; PW = parenchyma end wall; T = tracheid. — Scale bars = 20 μm. pit thickening formed ʻawnsʼ (Fig. 78) similar to those of bordered pit thickening ex- cept that half-bordered pit thickening occurred only on the tracheid side of pits and not on the ray side (Fig. 78 & 79). Where ʻawnsʼ of half-bordered pits were immedi- ately adjacent to awns of bordered pits, anastomosis sometimes occurred between them (Fig. 80).

Fig. 74–80. Aspects of thickening on cross-field pits and rays in Callitris. – 74-75: Various types of thickening of individual cross-field pits (RLS): – 74: (A) two bars, one on either side of a single pit; (B) two bars, one on either side of a pit pair; (C) bars extending fully across the cross field; (D) bars extending partially across the cross field; (E) two bars on either side of a pit pair plus a third bar angled between the pair of pits. – 75: (Arrowed) bars above and below a single pit aperture and a third bar crossing over the aperture parallel to the upper and lower bars. – 76: RLS view of ray, two cells high, with various multiple sets of thickening on pits in individual cross fields (R1 & R2 = individual cells of ray; BP = bordered pits with thickening; note size difference between thickening on bordered pits and thickening on cross-field pits). – 77: Thickening in narrow and wide cross fields. – 78: Ray (TLS) showing awns above and be- low half-bordered pits. – 79: Single cell of a ray (TLS) showing awns present only on tracheid side of the half-bordered pits and not on the ray side. – 80: Anastomosing between awns of thickening on half-bordered pits (CP) and thickening on bordered pits (BP) (TLS). — Scale bars = 50 μm in Fig. 74–77; 10 μm in Fig. 78–80.

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Axial parenchyma Callitroid thickening was absent from the (simple) pits on the inner walls of axial parenchyma cells (Fig. 81), but was sometimes present on the tracheid side of half- bordered pits connecting axial parenchyma and tracheids (Fig. 82). Where axial parenchyma crossed ray parenchyma cells, no thickening occurred on either side of simple pit pairs (Fig. 83).

Light microscopy (LM) Observation of wood samples by LM confirmed the occurrence of callitroid thick- ening in all Callitris species, including those in which previous (LM) studies reported it to be absent: i. e., C. macleayana (Fig. 84), C. muelleri (Fig. 85), C. oblonga (Fig. 86), C. rhomboidea (Fig. 87), C. roei (Fig. 88) and C. sulcata (Fig. 89). With the ex- ception of C. roei, in which thickening was common, its detection by LM in these species required careful observation of many pits, particularly those in narrow rather than wide tracheids. Detection of the four basic types of thickening (Fig. 90–92), thickening on pits in cross fields (Fig. 93 & 94), and verification of the absence of thickening on the simple pits inside parenchyma cells (Fig. 95) was also possible using LM.

DISCUSSION

Two of our findings indicate that generalisations about the systematic value of calli- troid thickening should be modified. Firstly, the value of callitroid thickening as the major taxonomic keying feature of wood of the genus is enhanced, because we have shown that callitroid thickening is universal to all species of Callitris rather than to just ʻsomeʼ of them as previously reported. Thus comments such as: “bands of second- ary thickening across tracheid pit borders in some [Callitris] species” (Peirce 1937), and callitroid thickening has “been observed in all species of commercial importance except Callitris macleayana” (Phillips 1948; Barefoot & Hankins 1982) are no longer correct. Secondly, the universal occurrence of thickening within the genus invalidates the practice of differentiating two groups of Callitris species on the basis of “pres- ence or absence of callitroid thickening” as used by Patton (1927) and Greguss (1955). Our results suggest that “frequency of thickening” is useful taxonomically since it is possible to separate Callitris into four distinct groups of species with 95% confidence using this feature (Fig. 22). Frequency of thickening also has value in separating cer-

Fig. 84–95. Light microscopy images. – 84–89: Occurrence of callitroid thickening in species in which the literature reports it to be absent. – 84: C. macleayana. – 85: C. muelleri. – 86: C. oblonga. – 87: C. rhomboidea. – 88: C. roei. – 89: C. sulcata (arrowed). – 90–92: Various types of callitroid thickening, 90: Type 1 (T1) and Type 2 (T2) thickening in C. glaucophylla; 91: Type 3 thickening (T3) in C. verrucosa; 92: Type 4 (T4) and Type 2 (T2) thickening in C. glaucophylla. – 93: Thickening of cross-field pits (RLS). – 94: Half-bordered pit in TLS (arrowed) showing awns. – 95: TLS view of a half-bordered pit between tracheid (T) and parenchyma (P) showing awns (arrowed) present only on tracheid side and not on parenchyma side of the wall. — Tracheid axes are vertical. Scale bars = 20 μm.

Downloaded from Brill.com10/10/2021 04:42:12PM via free access 316 IAWA Journal, Vol. 21 (3), 2000 tain individual Callitris species. For example, we were able to distinguish C. colu- mellaris, C. glaucophylla and C. intratropica from each other on the basis of their respective frequencies of thickening (if only these three species were under con- sideration). These three species are particularly difficult to separate using conven- tional taxonomic features and they were originally considered as a single species, Callitris columellaris by Blake (1959), who argued that there were no distinctive (botanical) morphological characters to differentiate them. This taxonomic grouping was generally accepted (e.g., Willis 1962; Dallimore & Jackson 1966; Blombery 1967) until Thompson and Johnson (1986) formed polygraphs from five cone char- acters and separated three distinct species, one of which (Callitris glauca R.Br.) was renamed C. glaucophylla and the other two were reinstated as C. columellaris (in a more restricted sense) and C. intratropica. Multiple samples of the wood of these three species were examined in our study, and their frequencies of thickening, shown in Figure 22, indicate that there are differences between them. In C. columellaris, C. glaucophylla and C. intratropica mean frequencies of thickening are 0.48, 0.98 and 0.22, respectively, and the non-overlap of the confidence intervals indicates that the differences between them are statistically significant (p < 0.01). Our study suggests a need for three changes to the anatomical definition of callitroid thickening. Firstly, its description as “pairs of bars of thickening across the pit” (IAWA Committee on Nomenclature 1964) needs to be reviewed in the light of our finding of the regular occurrence of thickening consisting of only one bar (e.g. Fig. 38), three bars (e.g. Fig. 33), and four bars (e.g. Fig. 35). Secondly, we have shown that the outer bars of Type 3 and Type 4 thickening are usually situated on or outside of the pit border (Fig. 33 & 35) and therefore thickening is not always “within the upper and lower margins of the pit border” as implied by Patton (1927) and Cronshaw (1961). Thirdly, based on the similarities between thickening on bordered pits and thickening on cross-field pits, we suggest that the term ʻcallitroid thickeningʼ be extended to include thickening of cross-field pits. This study has shown that the various forms of bordered and cross-field pit thickening are morphologically very similar (compare Figures 29 and 74 (D); Figures 31 and 74 (A); Figures 33 and 75; Figures 47 and 74 (C); and Figures 48 and 74 (E)). The anastomosis that sometimes occurs between awns of bordered pit and half-bordered pit thickening (Fig. 80) also suggests that they are formed at approximately the same time during cell wall differentiation. Thicken- ing of cross-field pits occurs in all species of Callitris and has similar frequencies of occurrence within the different species as does thickening of bordered pits. The observation of Panshin and de Zeeuw (1980) that the bars of callitroid thick- ening are slightly curved into “parenthesis” (i.e. elliptical) shape was confirmed by our study, and it was noted that such an effect was more pronounced in wide tracheids than in narrow ones. However, our study did not fully support Davies and Ingle (1966) who reported that bars in C. glauca (syn. C. glaucophylla) tend to “taper off in thick- ness towards the tangential wall”. When viewing cell walls in RLS, we were able to observe a tapering in bar width at the ends of bars for some Type 1 thickening. How- ever, for Types 2, 3, and 4 thickening, the ends of bars almost always extended around onto the TLS surface (Fig. 51) so that tapered ends (if they occurred) were not in view, and bars generally appeared of constant thickness (e.g. Fig. 53).

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A warty layer was observed on the bars of all four types of thickening suggesting that callitroid thickening is an elaboration of the S3 layer of the secondary wall, as has previously been suggested for thickening consisting of pairs of thickening bars, i.e. Type 2 thickening, by Wardrop (1964). This would also account for the absence of callitroid thickening in our observations of compression wood (Fig. 50) since the S3 layer in compression wood usually is “either absent or poorly developed” (Timell 1986). The covering of thickening bars by a warty layer (Fig. 30) also suggests that bars are formed before the development of warts. Our finding that callitroid thickening occurred in all species of Callitris contra- dicts previous reports of its absence in some species: i.e., in C. macleayana (Patton 1927; Phillips 1948), C. muelleri (Patton 1927; Venning 1979), C. oblonga (Patton 1927; Budkevich 1936; Greguss 1955; Venning 1979), C. rhomboidea (Patton 1927; Greguss 1955), C. roei (Venning 1979) and C. sulcata (Greguss 1955). The question therefore arises as to why these authors did not detect thickening in these species. We can suggest some possible reasons for these discrepancies. Firstly, all of these species except C. roei have thickening that is always visually indistinct, is difficult to see with the light microscope, and therefore may not be detected by cursory inspection. A second possible reason why previous studies did not observe callitroid thickening in the aforementioned species may lie in their very low frequencies of thickening (again with the exception of C. roei), which often necessitates the examination of many pits in each of several wood samples in order to detect it. Finally, previous studies may have failed to detect callitroid thickening because they used wood samples from twigs or branches and examined compression wood, in which thickening does not occur (Fig. 50). This may explain why Venning (1979) did not detect callitroid thickening in C. roei, whereas we found it to be readily visible in this species using either SEM (Fig. 18) or LM (Fig. 88). Our study showed that callitroid thickening was more common in Callitris species adapted to dry habitats than in those from wet habitats. Species with high frequency (> 85%) of thickening – C. canescens, C. endlicheri, C. glaucophylla, C. tubercu- lata and C. verrucosa (Fig. 22) are all native to semi-arid regions of inland Australia (Fig. 1). Conversely, species with low frequency (< 10%) of thickening – C. mac- leayana, C. neocaledonica, C. oblonga and C. sulcata (Fig. 22) occur in environ- ments with high rainfall, i.e. Queensland or New Caledonian rain forest, or, in the case of C. oblonga, in Tasmanian river flood-plains (Fig. 1). Webber (1936) and Carl- quist (1966) found that “all forms of helical sculpturing” (helical thickening) in ves- sels of Angiosperms were more frequent in species from dry habitats than in those from wet habitats. Also, Carlquist and Hoekman (1985) found that helical thicken- ing was more common in latewood (formed under dry conditions) than in earlywood (formed in relatively wetter conditions) of woody southern California flora. Our findings accord with these reports to the extent that higher frequencies of callitroid thickening between species could be related to increased aridity of habitat, and within species higher frequencies of thickening occurred in the narrower tracheids. How- ever, the precise adaptive value of callitroid thickening to Callitris species growing in dry environments is uncertain. Carlquist (1975) has pointed out that helical thicken-

Downloaded from Brill.com10/10/2021 04:42:12PM via free access 318 IAWA Journal, Vol. 21 (3), 2000 ing in secondary xylem tracheids “would theoretically offer mechanical strengthening ideal for countering collapse under conditions of high negative pressure in xylem” and Grosser (1986) has suggested that trabeculae perform a similar “bracing element” function in tracheids of softwoods. It can be hypothesised that callitroid thickening bars mechanically strengthen the tracheid wall against collapse by acting as ʻsupport- ing bracesʼ on either side of the pit aperture, the region where the cell wall is weakest, and where collapse is most likely to occur. Various species of Callitris are adapted to markedly different environmental con- ditions. Thus, it was possible to relate high frequencies of thickening to species from dry habitats and low frequencies of thickening to those from wet habitats, and to suggest that callitroid thickening is an adaptation to dry environmental conditions. A similar relationship between wart morphology and environment was described in our previous study of the warty layer in Callitris (Heady et al. 1994). Our finding that callitroid thickening is more common in Callitris than was previously reported in the literature, indicates that it may also occur more frequently in the other softwood genera in which callitroid thickening has been reported (Actinostrobus, Juniperus, Tetraclinis, Dacrydium, Pseudolarix and Pinus). It is further suggested that, based on the findings here, callitroid thickening in these other genera is more likely to be found in narrow (rather than wide) tracheids, and in species adapted to dry (rather than wet) habitats.

ACKNOWLEDGMENTS

The authors acknowledge technical support and equipment provided by the Electron Microscope Unit (EMU) and the Department of Forestry of The Australian National University (ANU), Can- berra. We are indebted to Ross Cunningham and Christine Donnelly of the ANU Statistical Consult- ing Unit for expert statistical advice, and to Frank Brink of the ANU EMU for assistance with the preparation of the photographic plates. Some of the wood core samples used in the study were obtained by David Jones of The Australian National Botanic Gardens, Canberra; Brendan Lepschi and Tarina Lally of the Department of Conservation and Land Management, Perth, WA; Ken Groves of Margules Poyry Pty Ltd, Canberra; and Bernard Suprin of the Service des Forêts Patrimoine Naturel, New Caledonia. We are also grateful to Stephen Harris of the Tasmanian Parks and Wild- life Service for information on the location of C. oblonga and C. rhomboidea in that state. We would also like to thank Guy Thomas and Rod Holmes, managers of the Maiala and Glen-Innes National Parks, for permission to obtain wood core samples within areas of botanic reserve. Finally, we thank Prof. Elizabeth Wheeler and two anonymous referees for reviewing the manuscript.

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