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1 Laboratory of Plant Systematics, Botanical Institute, K.U. Leuven, Kardinaal Mercierlaan 92, B-3001 Heverlee, Belgium
Received for publication December 15, 1998. Accepted for publication April 27, 1999.
ABSTRACT
The secondary xylem of Elaeagnus, Hippophae, and Shepherdia is described and illustrated in detail. Shrubs and small trees of Elaeagnaceae have ring-porous or semi-ring-porous wood with simple perforation plates, vascular tracheids, fiber-tracheids, diffuse or rarely paratracheal axial parenchyma, and uni- or biseriate rays in Hippophae and Shepherdia, but wider rays in Elaeagnus. Walls of vessel elements, especially narrow ones, tracheids, or fiber-tracheids sometimes show helical thickenings; in a few instances these intergrade with small bud-like protrusions associated with pits. Scanning electron microscopy illustrates that small to vestigial vestures are present in all species studied, although nonvestured pits are also common. The analogous nature of vestures and helical thickenings is considered. Comparative wood anatomy suggests a rather isolated position of the family Elaeagnaceae; affinities with Rhamnaceae, Proteaceae, and Thymelaeaceae are discussed.
Key Words: Elaeagnaceae • helical thickenings • vestured pits • wood anatomy
The temperate to subtropical family Elaeagnaceae is represented by shrubs and small trees and includes the genera Elaeagnus L. (some cultivated, ornamental species are better known as oleaster), Hippophae L., and Shepherdia Nutt. In the course of research on the distribution of vestures in angiosperms (Jansen, Smets, and Baas, 1998
), wood samples of some Elaeagnaceae were investigated. Vestures are small projections from the secondary cell wall that are most frequently associated with vessel pits. The pit cavity and/or aperture of vestured pits are wholly or partly lined with vestures (IAWA Committee, 1989
). Vestures are generally branched and irregular, reaching up to 1 µm in diameter at their base and up to 3–5 µm in height, but usually they are much smaller.
Most studies including data on the secondary xylem of Elaeagnaceae are based on light microscopy (LM) and do not comment on the presence or absence of vestures (e.g., Greguss, 1959
; Yamauchi, 1976
; Grosser, 1977
; Fahn, Werker, and Baas, 1986
; Schweingruber, 1990
). Bailey (1933)
in his classical paper on vestured pits in dicotyledons included six (unspecified) species covering all three genera of Elaeagnaceae, and he found the pits to be nonvestured. Since the introduction of the scanning electron microscope (SEM) facilitated micromorphological work, new records of families have been reported in which at least one species with vestured pits occurs, e.g., Proteaceae (Meylan and Butterfield, 1974
), Oliniaceae (Mujica and Cutler, 1974
), Crypteroniaceae (Van Vliet, 1975
), Boraginaceae (Miller, 1977
), Clethraceae, Ericaceae, Rhamnaceae, Sabiaceae, Symplocaceae, Theaceae (Ohtani, 1983
), Cistaceae (Baas and Werker, 1981
), Sonneratiaceae (Rao et al., 1987
), Rosaceae (Zhang and Baas, 1992
), Styracaceae (Machado, Angyalossy-Alfonso, and de Morretes, 1997
), and Gentianaceae (Jansen and Smets, 1998
). Clearly SEM is required for unambiguously observing vestured pits, particularly in the case of very small vestures or in very fine pitting.
SEM observations have also illustrated the presence of vestured pits in Hippophae rhamnoides (Zhang and Cao, 1990
). As vestured pits are generally considered to be consistent at the family level, this study investigates whether they can be found in wood of other Elaeagnaceae. In addition, detailed information on the general wood anatomy of the family allows comments on current ideas about its phylogenetic affinities.
MATERIALS AND METHODS
Nine wood samples were collected from small twigs (diameter <1 cm) of herbarium material in the National Botanic Garden of Belgium (BR). Thicker wood samples (diameter >2 cm) of five species were taken from the xylarium of the Royal Museum for Central Africa at Tervuren (Tw).
List of material studied
Elaeagnus argentea Pursh, Austria, Vienna, Forstl. Bundesversuchsanstalt Vienna 0200 (Tw 35080); E. conferta Roxb., China, Guangzhou, F.-W. Xing et al. 042 (BR); E. glabra Thunb., Japan, Honshu, M. Togasi 1651 (BR); E. latifolia Thunb., China, Ngong T'in Lo Shan, Y.-W. Taam 330 (BR); E. montana Makino, Japan, Honshu, H. Kubota 1116 (BR); E. orientalis L., Russia, Gugarac, Dilishan, V. Va
ák BR-S.P. 808 003 (BR); E. triflora Roxb. var. brevilimbatus ‘t Hart, New Guinea, Sattelberg, J. Clemens 468 (BR); E. umbellata Thunb., South-Korea, Forest Research Institute 554 (Tw 43308); Hippophae canadensis L., P. Martens BR-S.P. 808 012 (BR); H. rhamnoides L., Poland, Academy of Agriculture (Tw 47246); H. salicifolia D. Don, India, Kumaon, Kathi, R. Strachey & J.E. Winterbottom 2 (BR); H. thibetana Schldl., India, Kumaon, R. Strachey & J.E. Winterbottom BR-S.P. 808 015 (BR); Shepherdia argentea (Pursh) Nutt., U.S.A., H.C. Sulerud 413 (Tw 21656); S. canadensis (L.) Nutt., Canada, Thieret 4871 (Tw 30305).
For light microscopy, wood sections of the five Tw samples were made following classical microtechnique, stained with safranin, and mounted in Caedax (Jansen et al., 1998
). Macerations of these species were prepared according to Franklin (1945)
. The juvenile wood of the BR herbarium specimens was only used for SEM observations. In order to establish the true nature of vestures, longitudinal surfaces were cleaned with household bleach (15% sodium hypochlorite) for 1 h to remove any protoplasmic debris or vessel contents from the pit chambers since extraneous or coagulated material may be mistaken for vestures (so-called pseudovestures) (Exley, Butterfield, and Meylan, 1974
; Gale, 1982
). After rinsing in water and dehydrating in alcohol, the wood samples were dried at room temperature, sputter coated with gold, and examined with a Jeol JSM-6400 scanning electron microscope at 27 kV.
Terminology of wood anatomical characters follows the recommendations of the IAWA list (IAWA Committee, 1989
). Length of elements was measured in macerations; means were based on 25 measurements of each element. For vessel elements tails were included.
RESULTS
Anatomy of the secondary xylem
The following features are mainly based on the species studied by LM.
Wood is ring-porous to semi-ring-porous, with distinct growth ring boundaries (Figs. 1, 2, 3).
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Fibers are nonseptate, with distinctly bordered pits common in radial and tangential walls. Fibers in earlywood are frequently thinwalled (Fig. 2). Length of fibers is on average 500 µm in Shepherdia, but longer in Hippophae and Elaeagnus (see Table 1). Fiber walls with helical thickenings are found in Elaeagnus umbellata, E. argentea, Hippophae rhamnoides, and Shepherdia argentea.
Axial parenchyma is abundantly present in E. umbellata (Fig. 1) corresponding to the diffuse to diffuse-in-aggregates type. In the other species studied axial parenchyma is only sparsely present and diffuse or scanty paratracheal (Fig. 2, 3). Strand parenchyma is composed of two cells, but parenchyma is sometimes fusiform. Acicular crystals are found in axial parenchyma cells of Elaeagnus conferta and in pith cells of E. orientalis.
Rays are homocellular to weakly heterocellular. Rays of two distinct sizes occur in Elaeagnus (Fig. 4): some rays are uni- or biseriate and others more than fiveseriate. Rays in Hippophae (Fig. 5) and Shepherdia (Fig. 6) are uni- or biseriate, and only seldomly three cells wide. The rays are composed of procumbent cells with marginal cells sometimes square to slightly upright (Figs. 7, 8, 9). Sheath cells are present in parts of some rays of E. argentea (Fig. 4). There are 10–13 rays per millimetre in Shepherdia and Hippophae, while approximately four rays per millimetre occur in Elaeagnus. Ray height is on average 100 µm in Shepherdia argentea, S. canadensis, and Hippophae rhamnoides. Higher rays of 300–400 µm are present in Elaeagnus argentea and E. umbellata (see Table 1). Vessel-ray perforations and storied ray structure are present in Hippophae rhamnoides. Multiseriate rays distend at growth ring boundaries in Elaeagnus umbellata.
Pith-flecks (bands of parenchyma cells intercalated in secondary xylem) are occasionally present in Elaeagnus umbellata.
Fine structural aspects of vestured pits and wall sculpturing
All species studied show vessel pits with small to rudimentary vestures (Figs. 10–18). However, nonvestured pits are also common (Figs. 19, 20). Since most vessels are solitary and generally embedded in fiber tissue, the pits are vessel-fiber pits, and occasionally vessel-parenchyma pits. Apart from vessels and tracheids, vestured pits are also observed in fibers of Elaeagnus argentea, Hippophae rhamnoides, and Shepherdia argentea. Vestured perforation plates and vestured walls are lacking.
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and to types 1, 2, 3, and 4 of Ohtani and Ishida (1976)
. In Shepherdia canadensis and S. argentea (Figs. 14, 16, 17) small, irregular, and branched vestures occur. In Shepherdia vestures on one side of a rather elongated pit border sometimes occur opposite vestures on the other side of the pit border (Fig. 14). In a few instances they are joined together. Most vestured pits belong to type 2 and subtype 3 following the vesture typification of Nair and Mohan Ram (1989)
, because the vestures do not protrude, or very weakly so, into the pit chamber. They arise from the margin of the pit aperture pointing to its center. Accordingly, the pit apertures are often irregularly shaped. Moreover, the same vestures are visible on the pit aperture from both inner and outer vessel wall surfaces (Fig. 16). Note that when the pit channel is short, the distinction between inner pit aperture on the lumen end and outer pit aperture on the pit chamber end becomes obscure. Vestures are more common in narrow vessel elements or tracheids than in wide vessel elements (Figs. 19, 20), although this tendency cannot be generalized. In Elaeagnus orientalis, furthermore, small vessel-ray pits (2–3 µm) are frequently vestured, while larger vessel-ray pits (5–6 µm) often lack vestures (Fig. 21).
Helical thickenings are found in vessel elements of Elaeagnus glabra, E. orientalis, E. umbellata, Hippophae rhamnoides, H. salicifolia, Shepherdia argentea (Fig. 22), and S. canadensis. They are also common on walls of tracheids or fibers, except for Shepherdia canadensis. Prominent helical thickenings are restricted to Hippophae rhamnoides. The ridges are sometimes branching and usually discontinuous (i.e., not completing a full spiral, Fig. 23). Helical thickenings in Shepherdia argentea are frequently swirled, especially near perforation plates. None of the species studied has thickenings in all vessels. Note that, as for vestures, helical thickenings are more common in narrow vessel elements than in wide ones.
Furthermore, bud-like protrusions locally occur on vessel walls of Elaeagnus glabra and E. umbellata (Fig. 24). These structures are 2–4 µm in height and occur close to pits. Short helical thickenings intergrading with these protrusions near vessel pits may also be present (Fig. 25).
DISCUSSION
General wood anatomy of Elaeagnaceae
Our LM observations agree very well with the wood anatomical data of Elaeagnaceae found in literature; secondary xylem of Elaeagnaceae is ring-porous to semi-ring-porous, with simple perforation plates, tracheids, fiber-tracheids, and sometimes helical thickenings. Most variation is found in the rays and axial parenchyma. Wood of Hippophae and Shepherdia is similar by the presence of numerous uni- or biseriate rays and scanty axial parenchyma cells. The rays in Elaeagnus, however, are wider, higher, and occur less frequently. Axial parenchyma is also more numerous in Elaeagnus. Storied ray structure is characteristic for wood of Hippophae rhamnoides, but we could not determine whether storied rays also occur in other species of Hippophae, since these wood samples were too small for the preparation of sections.
Vestured pits and helical thickenings in Elaeagnaceae
SEM observations demonstrate that vestured pits are clearly present in all Elaeagnaceae studied. Hence, this feature is apparently characteristic of the entire family. It is not surprising that the small to rudimentary vestures remained unnoticed in earlier LM studies (Bailey, 1933
; Greguss, 1959
; Yamauchi, 1976
; Grosser, 1977
; Fahn, Werker, and Baas, 1986
; Schweingruber, 1990
) because they can hardly be detected by LM.
The bud-like protrusions occasionally found in some species of Elaeagnus have already been described by Yamauchi (1976)
as "papillae" or "papillary spiral thickenings." We observed these protuberances in Elaeagnus glabra and Elaeagnus umbellata. Similar bud-like protrusions were found in Ligustrum and Syringa (Oleaceae) by Parameswaran and Gomes (1981)
, Baas and Zhang (1986)
, and Baas et al. (1988)
. Parameswaran and Gomes (1981)
made an ultrastructural study of the bud-like protrusions in Ligustrum lucidum and found that dark amorphous zones within the protuberances indicate that they are more lignified than other parts of the secondary cell wall. Furthermore, they concluded that "these decorative developments associated with the vessel pits can be compared with other common features like vestures and warts, even though their size and origin obviate an immediate homology with the latter." We share the opinion of Baas and Zhang (1986)
that the bud-like protrusions are local helical thickenings near pit apertures because they are often intergrading with short and faint thickenings. In other words, the bud-like protrusions are a result of the uneven nature of the thickenings, which are most pronounced near pit apertures.
Vestured pits are sometimes more pronounced in small vessel elements and in tracheids; nonvestured pits appear to be more common in wide elements, although this tendency does not appear to be a general rule. A similar tendency is that narrow (latewood) vessels show more pronounced helical thickenings than wide (earlywood) vessels; this is shown in this study and that by Greguss (1959)
for Elaeagnaceae, and also for other taxa by Parham and Kaustinen (1973)
, Meylan and Butterfield (1978)
, Ohtani and Ishida (1978)
, Carlquist (1982)
, and Nair (1987)
. Note that there is a parallel to the conditions for vestured vessel walls ("warts") and position of vessels within a growth ring (Ohtani and Ishida, 1973
; Parham and Baird, 1974
). Ohtani and Fujikawa (1971)
discovered that warts in some coniferous woods gradually increase in diameter from earlywood to latewood. Moreover, Ohtani and Ishida (1976) found that "when spiral thickening meets pit aperture, in some cases, the end of spiral thickening enters into the pit chamber from the pit aperture and branches at the tip like vestures in appearance." These observations of vestures and helical thickenings invite speculation as to their mode of origin and suggest an analogous nature.
Vesture formation has been related to prolongation of the activity of the protoplast just before its death (Scurfield and Silva, 1970
; Scurfield, Silva, and Ingle, 1970
); for a survey of the ontogeny of vestures, see Jansen, Smets, and Baas (1998)
. According to Preston (1974)
helical thickenings are homologous with the other layers of the secondary wall, and he suggested that they could represent an attempt to continue secondary wall formation when the cell is dying. The structural and chemical composition of vestures and helical thickenings is obviously different. Vestures can be distinguished from the cell wall by their different density and nonfibrillar composition as they appear homogeneous in transmission electron microscopic photographs (Schmid and Machado, 1964
; Schmid, 1965
). Most investigators who studied the chemical composition of vestures concluded that they largely consist of lignin, hemicellulose and a small quantity of pectin, but do not contain cellulose (Côté and Day, 1962
; Schmid, 1965
; Scurfield and Silva, 1970
; Baird, Parham, and Johnson, 1974
; Ohtani, Meylan, and Butterfield, 1984a
). Furthermore, vestures are removed from the secondary wall by treatment with acetic acid and hydrogen peroxide, which are used for maceration at 90°C until loss of color (Scurfield and Silva, 1970
; Ohtani, Meylan, and Butterfield, 1984a
). Helical thickenings on the other hand are similar to cell wall material in composition and remain visible after maceration (see Fig. 22). Nevertheless, it must be stressed that the nature and ontogeny of both structures are not yet fully clarified; modern ultrastructural research on this topic is lacking.
Note that Carlquist (1982)
hypothesized a similar function of vestures and helical thickenings, but Baas, Werker, and Fahn (1983)
do not consider both structures to have any functional significance. Finally, it is interesting to mention that helical thickenings are more widespread in woody species of temperate and subtropical distribution (Baas, 1973
; van der Graaf and Baas, 1974
; Carlquist, 1975
), while vestures are more common in tropical and subtropical plant families (Schmid and Machado, 1964
). Until now, the presence of vestures that are associated with helical thickenings was restricted to a few genera in the Fabaceae (Ohtani and Ishida, 1976
; Meylan and Butterfield, 1978
; Ohtani, Meylan and Butterfield, 1984b
).
Systematic relationships of Elaeagnaceae
Vestured pits are regarded as a taxonomic feature characterizing large natural groups such as the orders Fabales (exceptions are the tribes Cassieae and Cercideae; Quirk and Miller, 1985
), Myrtales (Van Vliet and Baas, 1984
), and Gentianales (Jansen and Smets, in press
), or families such as Dipterocarpaceae (Gottwald and Parameswaran, 1966
; Brazier, 1979
) and Vochysiaceae (Quirk, 1980
). Accordingly, the systematic value of vestured pits is high at the ordinal or familial level for these taxa. However, far less taxonomic value can be assigned to vestured pits in taxa such as Oleaceae (Baas and Zhang, 1986
; Baas et al., 1988
) and Boraginaceae (Miller, 1977
; Gottwald, 1982, 1983
) since the presence/absence of the character is not in congruence with any classification system of these families.
The small family Elaeagnaceae has been included in Daphnales by Bentham and Hooker (1862–1892); in Thymeales by Engler (1964)
; in Rhamnales by Hutchinson (1973)
; in Proteales by Cronquist (1981, 1988)
and Dahlgren (1989)
; and in a separate order Elaeagnales by Takhtajan (1969, 1997)
and Dahlgren (1980)
. Most authors believed Elaeagnaceae to be more or less closely related to Proteaceae, Rhamnaceae, Thymelaeaceae, or Penaeaceae. Elaeagnaceae can be distinguished from these families by the golden or silvery hairy indumentum, the nature of the fruit, and the basally attached ovule. A recent classification of angiosperms (APG, 1998
) places Elaeagnaceae in a comparatively widely circumscribed Rosales (including Moraceae, Rhamnaceae, Rosaceae, Urticaceae, Ulmaceae, and their allies), while Proteaceae are included in Proteales, Penaeaceae in Myrtales, and Thymelaeaceae in Malvales. Table 2 gives a survey of diagnostic wood anatomical characters of these families. The data in this table are summarized from literature. Note that we omitted the monospecific family Dirachmaceae, which is included in Rosales sensu APG, since wood anatomical data of Dirachma are not found in literature.
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; simple perforation plates, vessels grouped solitary, in multiples or clustered, alternate vessel pitting, helical thickenings, nonseptate fibers (except for Moraceae and few taxa of Rhamnaceae, Rosaceae, and Urticaceae), heterocellular rays (sometimes of two distinct sizes), and sheath cells occur to a certain extent in most families. However, other wood anatomical characters of Elaeagnaceae, namely vestured pits, vascular tracheids, and fiber-tracheids, occur only sparsely in the Rosales sensu APG. Prismatic crystals are also much less common in wood of Elaeagnaceae compared to the abundant occurrence in Moraceae, Rhamnaceae, Ulmaceae, and Urticaceae. Hence, the combination of these features suggests a rather isolated position of Elaeagnaceae in the Rosales sensu APG, although the question is what evolutionary and taxonomic significance to attach to these differences.
Vestured pits have been reported in at least one species of Rhamnaceae (Ohtani, 1983
), but nonvestured representatives are most frequent (Meylan and Butterfield, 1974
; Ohtani and Ishida, 1976
; Schirarend, 1991
). Remark that Schirarend (1991)
could not establish by LM whether true vestures or pseudovestures are present in six genera of Rhamnaceae. Moreover, the occurrence of vascular tracheids in Rhamnaceae is restricted to three genera. Unlike fiber-tracheids in Elaeagnaceae, libriform fibers are characteristic of Rhamnaceae (Schirarend, 1991
). Therefore, wood anatomical features do not suggest a close affinity between Elaeagnaceae and Rhamnaceae, although an association between both families is confirmed by seed anatomy (Corner, 1976
) and uredinological data (Holm, 1979
; Savile, 1979
). In the combined morphological and molecular tree of Nandi, Chase, and Endress (1998)
both families are also included in the same clade. Note that Elaeagnaceae (and Rhamnaceae) are considered to lack vestured pits in their nonmolecular data matrix.
A close association of Elaeagnaceae with Rosaceae, which is wood anatomically rather diverse, has not been considered earlier. Although ground tissue fibers in Rosaceae are mostly with distinctly bordered pits (fiber-tracheids as in Elaeagnaceae), the presence of vestured pits is restricted to some Spiraea species. Tracheids in Rosaceae are also limited to a few genera (Zhang, 1992
; Zhang and Baas, 1992
). Other anatomical or morphological data reveal no strong affinity between both families.
Proteaceae have also been related to Elaeagnaceae sharing features such as perigynous flowers, an undifferentiated perianth (it is unclear in Elaeagnaceae whether the perianth is sepalar or petalar), and a single carpel (e.g., Dahlgren, 1989
). Vestured pits are found, as far as we know, in six genera of the Proteaceae (Butterfield and Meylan, 1974
; Lanyon, 1979
; Patel, 1992
). Nonvestured pits are reported in Proteaceae by Butterfield and Meylan (1974)
, Ohtani and Ishida (1976)
, Lanyon (1979)
, Nair and Mohan Ram (1989)
, and Patel (1992)
. Other wood anatomical features that are similar in both families are helical thickenings and vascular tracheids. Moreover, there are conspicuous similarities in the rays of Elaeagnus and Proteaceae, which are often of two distinct sizes, the uniseriate rather few, the multiseriate very wide. There is also a tendency for tangential arrangement of vessel elements, and this is often closely connected with the scalariform axial parenchyma (Chattaway, 1948
). Differences in the wood of the two families are the fiber type; while libriform fibers are most common in Proteaceae, Elaeagnaceae have fiber-tracheids. Also, silica bodies reported in a few Proteaceae by Mennega (1966)
and ter Welle (1976)
are lacking in Elaeagnaceae. Contrary to the aberrant position of Proteaceae according to APG (1998)
, wood anatomy suggests that Elaeagnaceae and Proteaceae are more or less related. Cronquist (1968)
states that both families might have undergone a series of parallel changes from more or less similar ancestors.
Vestured pits and fiber-tracheids are common in Penaeaceae (Carlquist and Debuhr, 1977
). A close association of Elaeagnaceae with Penaeaceae (Rao, 1974
) seems unlikely, because Penaeaceae, which show intraxylary phloem, have traditionally been referred to the Myrtales. Intraxylary phloem is also found in nine genera of the Thymelaeaceae (Van Vliet and Baas, 1984
), but the position of this family in the Myrtales is disputable (Cronquist, 1984
; Dahlgren and Thorne, 1984
). Vestured pits are observed in three genera of Thymelaeaceae (Scurfield, Silva, and Ingle, 1970
; Ohtani and Ishida, 1976
; Rao and Dayal, 1992
; Ohtani, Meylan, and Butterfield, 1984b
). Although all the pits on the vessel wall are nonvestured in species of Daphne, all the pits on the fiber-tracheid wall are vestured (Ohtani and Ishida, 1976
). The vestures in Daphne are remarkably similar to the vestures found in Elaeagnaceae; they are small, simple or forked, and arise from the margin of the pit aperture pointing to its center (Ohtani and Ishida, 1976
: Figs. 49, 50). Other similarities between both families are the occurrence of tracheids, fiber-tracheids, and helical thickenings. Furthermore, Cronquist (1981, 1988)
states that Elaeagnaceae look remarkably like some Thymelaeaceae; they share perigynous flowers, and tetramery is common in Thymelaeaceae and dominant in Elaeagnaceae. Unlike Elaeagnaceae, Thymelaeaceae are not tanniferous, and they characteristically accumulate daphnin and allied compounds (Cronquist, 1984
).
Conclusion
This study demonstrates that SEM observations are required for the detection of vestures in Elaeagnaceae and probably also in other families. The lists of taxa with vestured pits presented by Bailey (1933)
, Carlquist (1982, 1988)
, Metcalfe and Chalk (1983)
, and Jansen, Smets, and Baas (1998)
remain preliminary and should be interpreted with caution.
FOOTNOTES
1 The authors thank Anja Vandeperre for her share in the microtechnical work and the reproduction of photographs, and the curators of the xylarium of Tervuren (Tw) and the herbarium of the National Botanic Garden of Belgium (BR) for the supply of wood samples. Steven Jansen holds a scholarship of the Research Council of the K.U.Leuven. Frederic Piesschaert is a research assistant of the Fund for Scientific Research (F.W.O.) Flanders. This research is supported by a grant from the Research Council of the K.U.Leuven (OT/97/23) and by grants from the Fund for Scientific Research—Flanders (F.W.O., Belgium): project numbers 2.0038.91 and G. 0143.95. 
LITERATURE CITED
APG. 1998 An ordinal classification for the families of flowering plants. Annals of the Missouri Botanical Garden 85: 531–553. [CrossRef][ISI]
Baas, P. 1973 The wood anatomical range in Ilex (Aquifoliaceae) and its ecological and phylogenetic significance. Blumea 21: 193–258.
———, P. E. Esser, M. E. T. van der Westen, and M. Zandee. 1988 Wood anatomy of the Oleaceae. International Association of Wood Anatomists Bulletin, New Series 9: 103–182.
———, and E. Werker. 1981 A new record of vestured pits in Cistaceae. International Association of Wood Anatomists Bulletin, New Series 2: 41–42.
———, ———, and A. Fahn. 1983 Some ecological trends in vessel characters. International Association of Wood Anatomists Bulletin, New Series 4: 141–159.
———, and X. Zhang. 1986 Wood anatomy of trees and shrubs from China. I. Oleaceae. International Association of Wood Anatomists Bulletin, New Series 7: 195–220.
Bailey, I. W. 1933 The cambium and its derivative tissues. VIII. Structure, distribution, and diagnostic significance of vestured pits in dicotyledons. Journal of the Arnold Arboretum 14: 259–273.
Baird, W. M., R. A. Parham, and M. A. Johnson. 1974 Development and composition of the warty layer in Balsam Fir. II. Composition. Wood and Fiber 6: 211–222.
Bentham, G., and J. D. Hooker. 1862–1892 Genera plantarum. London, UK.
Brazier, J. D. 1979 Classifying the Dipterocarpaceae: the wood technologist's view. Mémoires du Museum National d'Histoire Naturelle, Paris B 26: 76–80.
Butterfield, B. G., and B. A. Meylan. 1974 Vestured vessel and fibre pits in Persoonia toru A.Cunn. (Proteaceae). International Association of Wood Anatomists 1974/1: 10–15.
Carlquist, S. 1975 Ecological strategies of xylem evolution. University of California Press, Berkeley, California, USA.
———. 1982 Wood anatomy of Onagraceae: further species; root anatomy; significance of vestured pits and allied structures in dicotyledons. Annals of the Missouri Botanical Garden 69: 755–769. [CrossRef][ISI]
———. 1988 Comparative wood anatomy: systematic, ecological, and evolutionary aspects of dicotyledon wood. Springer-Verlag, Berlin, Germany.
———, and L. Debuhr. 1977 Wood anatomy of Penaeaceae (Myrtales): comparative, phylogenetic and ecological implications. Botanical Journal of the Linnean Society 75: 211–227.
Chattaway, M. M. 1948 The wood anatomy of the Proteaceae. Australian Journal of Scientific Research B 1: 279–302.
Corner, E. J. H. 1976 The seeds of dicotyledons, vols. 1 and 2. Cambridge University Press, Cambridge, UK.
Côté, W. A., and A. C. Day. 1962 Vestured pits—fine structure and apparent relationship with warts. Technical Association of the Pulp and Paper Industry 45: 906–910.
Cronquist, A. 1968 The evolution and classification of the flowering plants. Houghton Mifflin, Boston, MA.
———. 1981 An integrated system of classification of flowering plants. Columbia University Press, New York, New York, USA.
———. 1984 A commentary on the definition of the order Myrtales. Annals of the Missouri Botanical Garden 71: 780–782. [CrossRef][ISI]
———. 1988 The evolution and classification of flowering plants, 2nd ed. New York Botanical Garden, New York, New York, USA.
Dahlgren, G. 1989 The last Dahlgrenogram: system of classification of the dicotyledons. In K. Tan [ed.], Plant taxonomy, phytogeography, and related subjects, 249–260. Davis and Hedge Festschrift, Edinburgh University Press, Edinburgh, UK.
Dahlgren, R. 1980 A revised system of classification of the angiosperms. Botanical Journal of the Linnean Society 80: 91–124. [ISI]
———, and R. F. Thorne. 1984 The order Myrtales: circumscription, variation, and relationships. Annals of the Missouri Botanical Garden 71: 633–699. [CrossRef][ISI]
Engler, A. 1964 Syllabus der Pflanzenfamilien, 12th ed., edited and revised by H. Melchior, Berlin, Germany.
Exley, R. R., B. G. Butterfield, and B. A. Meylan. 1974 Preparation of wood specimens for the scanning electron microscope. Journal of Microscopy 101: 21–30.
Fahn, A., E. Werker, and P. Baas. 1986 Wood anatomy and identification of trees and shrubs from Israel and adjacent regions. Israel Academy of Sciences, Jerusalem, Israel.
Franklin, G. L. 1945 Preparation of thin sections of synthetic resins and wood-resin composites, and a new macerating method for wood. Nature 155: 51.
Gale, R. 1982 Some pitfalls in wood identification, with reference to Nothofagus. International Association of Wood Anatomists Bulletin, New Series 3: 179–184.
Gottwald, H. 1982 First description of the wood anatomy of Antrophora, Lepidocordia and Pteleocarpa (Boraginaceae). International Association of Wood Anatomists Bulletin, New Series 3: 161–165.
———. 1983 Wood anatomical studies of Boraginaceae (s.l.). 1. Cordioideae. International Association of Wood Anatomists Bulletin, New Series 4: 161–178.
———, and N. Parameswaran. 1966 Das secundäre Xylem der Familie Dipterocarpaceae, anatomische Untersuchungen zur Taxonomie und Phylogenie. Botanische Jahrbücher für Systematik 85: 410–508.
Greguss, P. 1959 Holzanatomie der europäischen Laubhölzer und Sträucher. Akademiai Kiado, Budapest, Hungary.
Grosser, D. 1977 Die Hölzer Mitteleuropas. Ein mikrophotographischer Lehratlas. Springer-Verlag, Berlin, Germany.
Holm, L. 1979 Some problems in angiosperm taxonomy in light of the rust data. In I. Hedberg [ed.], Parasites as plant taxonomists, 177–181. Upsala, Sweden.
Hutchinson, J. 1973 The families of flowering plants. Clarendon Press, Oxford, UK.
IAWA Committee. 1989 IAWA list of microscopic features for hardwood identification. International Association of Wood Anatomists New Series 10: 219–332.
Jansen, S., P. Kitin, H. De Pauw, M. Idris, H. Beeckman, and E. Smets. 1998 Preparation of wood specimens for transmitted light microscopy and scanning electron microscopy. Belgian Journal of Botany 131: 41–49. [ISI]
———, and E. Smets. 1998 Vestured pits in some woody Gentianaceae. International Association of Wood Anatomists Journal 19: 35–42.
———, and ———. In press. Morphology, distribution, and systematic value of vestures in the Gentianales. In Plant systematics and diversity for the 21st century, Proceedings of the Wenner Gren International Symposium. Portland Press, London, UK.
———, ———, and P. Baas. 1998 Vestures in woody plants: a review. International Association of Wood Anatomists Journal 19: 347–382.
Lanyon, J. W. 1979 The wood anatomy of three proteaceous timbers Placospermum coriaceum, Dilobeia thouarsii and Garnieria spathulaefolia. International Association of Wood Anatomists Bulletin 1979/2–3: 27–33.
Machado, S. R., V. Angyalossy-Alfonso, and B. L. de Morretes. 1997 Comparative wood anatomy of root and stem in Styrax camporum (Styracaceae). International Association of Wood Anatomists Journal 18: 13–25.
Mennega, A. M. W. 1966 Wood anatomy of the genus Euplassa and its relation to other Proteaceae of the Guianas and Brazil. Acta Botanica Neerlandica 15: 177–129.
Metcalfe, C. R., and L. Chalk. 1983 Anatomy of the dicotyledons, vol. II. Wood structure and conclusion of the general introduction, 2nd ed. Clarendon Press, Oxford, UK.
Meylan, B. A., and B. G. Butterfield. 1974 Occurrence of vestured pits in the vessels and fibres of New Zealand woods. New Zealand Journal of Botany 12: 3–18.
———, and ———. 1978 Occurrence of helical thickenings in the vessels of New Zealand woods. New Phytologist 81: 139–146.
Miller, R. B. 1977 Vestured pits in Boraginaceae. International Association of Wood Anatomists Bulletin 1977/3: 43–48.
Mujica, M. B., and D. F. Cutler. 1974 Taxonomic implications of anatomical studies on the Oliniaceae. Kew Bulletin 29: 93–123. [CrossRef]
Nair, M. N. B. 1987 Occurrence of helical thickenings on the vessel element walls of dicotyledonous woods. Annals of Botany 60: 23–32.
———, and H. Y. Mohan Ram. 1989 Vestured pits and vestured vessel member walls in some Indian dicotyledonous woods. Botanical Journal of the Linnean Society 100: 323–336.
Nandi, O. I., M. W. Chase, and P. K. Endress. 1998 A combined cladistic analysis of angiosperms using rbcL and non-molecular data sets. Annals of the Missouri Botanical Garden 85: 137–177.
Ohtani, J. 1983 SEM investigation on the micromorphology of vessel wall sculptures. Research Bulletins of the College Experiment Forests, College of Agriculture, Hokkaido University 40: 323–386.
———, and S. Fujikawa. 1971 Study of warty layer by the scanning electron microscopy. I. The variation of warts on the tracheid wall within an annual ring of coniferous woods. Journal of the Japanese Wood Research Society 17: 89–95.
———, and S. Ishida. 1973 An observation of the sculptures of the vessel wall of Fagus crenata Bl. using scanning electron microscopy. Research Bulletins of the College Experiment Forests, College of Agriculture, Hokkaido University 30: 125–144.
———, and ———. 1976 Study on the pit of wood cells using scanning electron microscopy. 5. Vestured pits in Japanese dicotyledonous woods. Research Bulletins of the College Experiment Forests, College of Agriculture, Hokkaido University 33: 407–435.
———, and ———. 1978 An observation on the spiral thickenings in the vessel members in Japanese dicotyledonous woods using scanning electron microscopy. Research Bulletins of The College Experiment Forests, College of Agriculture, Hokkaido University 35: 433–464.
———, B. A. Meylan, and B. G. Butterfield. 1984a Vestures or warts—proposed terminology. International Association of Wood Anatomists Bulletin, New Series 5: 3–8.
———, and ———. 1984b A note on vestures on helical thickenings. International Association of Wood Anatomists Bulletin, New Series 5: 9–11.
Parameswaran, N., and A. V. Gomes. 1981 Fine structural aspects of helical thickenings and pits in vessels of Ligustrum lucidum Ait. (Oleaceae). International Association of Wood Anatomists Bulletin, New Series 2: 179–185.
Parham, R. A., and W. M. Baird. 1974 Warts in the evolution of angiosperm wood. Wood Science and Technology 8: 1–10.
———, and H. Kaustinen. 1973 On the morphology of spiral thickenings. International Association of Wood Anatomists Bulletin 1973/2: 8–17.
Patel, R. N. 1992 Wood anatomy of the dicotyledons indigeneous to New Zealand. 22. Proteaceae. New Zealand Journal of Botany 30: 415–428. [ISI]
Preston, R. D. 1974 The physical biology of plant cell walls. Chapman and Hall, London, UK.
Quirk, J. T. 1980 Wood anatomy of the Vochysiaceae. International Association of Wood Anatomists Bulletin, New Series 1: 172–179.
———, and R. B. Miller. 1985 Vestured pits in the tribe Cassieae Brown (Leguminosae). International Association of Wood Anatomists Bulletin, New Series 6: 200–212.
Rao, R. V., S. S. Bissen, B. Sharma, and R. Dayal. 1987 SEM observations of perforation plates in Sonneratia Linn. (Sonneratiaceae). International Association of Wood Anatomists Bulletin, New series 8: 331–336.
———, and R. Dayal. 1992 The secondary xylem of Aquilaria agallocha (Thymelaeaceae) and the formation of ‘agar.’ International Association of Wood Anatomists Bulletin, New Series 13: 163–172.
Rao, V. S. 1974 The nature of the perianth in Elaeagnus on the basis of floral anatomy, with some comments on the systematic position of Elaeagnaceae. Journal of the Indian Botanical Society 53: 156–161.
Savile, D. B. O. 1979 Fungi as aids in higher plant classification. Botanical Review 45: 377–503.
Schirarend, C. 1991 The systematic wood anatomy of the Rhamnaceae Juss. (Rhamnales). I. Tribe Zizipheae. International Association of Wood Anatomists Bulletin, New Series 12: 359–388.
Schmid, R. 1965 The fine structure of pits in hardwoods. In W. A. Côté [ed.], Cellular ultrastructure of woody plants, 291–304. Syracuse University Press, New York, New York, USA.
———, and R. D. Machado. 1964 Zur Entstehung und Feinstruktur skulpturierter Hoftüpfel bei Leguminosen. Planta 60: 612–626. [CrossRef][ISI]
Schweingruber, F. H. 1990 Anatomie europascher Hölzer. Anatomy of european woods. Verlag Paul Haupt, Bern, Switzerland.
Scurfield, G., and S. R. Silva. 1970 The vestured pits of Eucalyptus regnans F.Muell.: a study using scanning electron microscopy. Botanical Journal of the Linnean Society 63: 313–320.
———, ———, and H. D. Ingle. 1970 Vessel wall structure: an investigation using scanning electron microscopy. Australian Journal of Botany 18: 301–312. [CrossRef]
Takhtajan, A. 1969 Flowering plants—origin and dispersal. Oliver and Boyd, Edinburgh, UK.
———. 1997 Diversity and classification of flowering plants. Columbia University Press, New York, New York, USA.
Van der Graaf, N. A., and P. Baas. 1974 Wood anatomical variation in relation to latitude and altitude. Blumea 22: 101–121.
Van Vliet, G. J. C. M. 1975 Wood anatomy of Crypteroniaceae sensu lato. Journal of Microscopy 104: 65–82.
———, and P. Baas. 1984 Wood anatomy and classification of the Myrtales. Annals of the Missouri Botanical Garden 71: 783–800. [CrossRef][ISI]
ter Welle, B. J. H. 1976 Silica grains in woody plants of the Neotropics, especially Surinam. In P. Baas, A. J. Bolton, and D. M. Catling [eds.], Wood structure in biological and technological research, 107–142. Leiden Botanical Series Number 3, Leiden University Press, Leiden, The Netherlands.
Yamauchi, F. 1976 Anatomical studies of woods of Japanese Elaeagnus. Bulletin of the National Science Museum, Serie B (Botany) 2: 107–126.
Zhang, S.-Y. 1992 Systematic wood anatomy of Rosaceae. Blumea 37: 81–158.
———, and P. Baas. 1992 Wood anatomy of trees and shrubs from China. III. Rosaceae. International Association of Wood Anatomists Bulletin, New Series 13: 21–91.
Zhang, X.-Y., and W.-H. Cao. 1990 Studies on the secondary xylem anatomy of Hippophae rhamnoides under different habitats. Acta Botanica Sinica 32: 909–915.
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