B0t.J. Lin.Sac., 62,pp. 379-411.
With 11 plates and 5figures
October 1969
Resin ducts of Pinus halepensis Mill.-Their structure,
development and pattern of arrangement
ELLA WERKER
AND
A. FAHN, F.L.S.
Department of Botany, The Hebrew University of Jerusalem, Israel
Accepted for publication M a y 1969
The primary resin ducts in the axis of plants of Pinus halepensis Mill. consist of two separate
systems the pattern of which is correlated with the vascular systems of the organs in which
they appear. These systems are: (1) ducts of the roots and the hypocotyl; (2) ducts of all the
branches and juvenile leaves or scales. Both systems are produced by the apical meristems. I n
the needles there is a third system of primary resin ducts situated in the mesophyll. These ducts
are produced only to a small extent by the apical meristem of the needle and mainly by its intercalarymeristem. In addition to these primary ducts of the needle, which form a separate system
for each needle, at the base of the needle there may be ducts of secondary origin which are
situated within the vein. These are continuous with secondary ducts of the brachyblast axis.
The secondary ducts constitute one system in the secondary xylem and phloem of the roots,
branches and needle bases. They are formed by the cambium. In the xylem there are vertical
and radial ducts which together form co-planar radial networks. Each radial duct starts from
a vertical duct. The first location of the stimulus for the formation of the two types of ducts is
discussed. In the phloem there are only radial ducts, continuous with the radial ducts of the
xylem. The cavities of the radial phloem and xylem ducts are not continuous, as there are no
intercellular spaces in the region of the cambium.
The innermost vertical ducts of the secondary xylem form a kind of transitional type, in
respect of their response to internal and external factors, between the primary resin ducts and
the bulk of the secondary resin ducts.
CONTENTS
.
.
Introduction
.
. . .
.
Material and methods
.
Observations .
Resin ducts of the primary body
.
The root-hypocotyl
.
The connection between the primary resin ducts of main and lateral roots
The connection between primary and secondary ducts
The shoot
The connection between the primary duct systems of the main and lateral shoots
Theneedles
Development of the primary ducts
.
,
Development of the secondary ducts .
Resin ducts of the secondary body .
The first ducts in the secondary xylem .
The pattern of the resin duct system in the secondary body
.
Development of ducts of the secondary body
Length of vertical ducts
Discussion
.
Manner of duct development
Sizeofducts .
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E. WERICER AND A. FAHN
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Viability of duct cells
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Methods of classification .
Origin of ducts and the influence of internal and external factors .
The connections between resin ducts formed by different meristems
The spatial structure of the system of secondary resin ducts
Location of the stimulus for production of secondary ducts
Acknowledgements
References
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INTRODUCTION
Resin ducts are a common feature in conifers. I n the primary body they seem to be
quite constant (Hanes, 1927); but in the secondary body they are more liable to be
influenced by external factors. In the Pinaceae it has usually been stated that in genera
such as Abies, Tsuga, Cedrus and Pseudolarix the resin ducts are produced only as a
result of injury, while in other genera such as Pinus, Picea, Larix and Pseudotsuga they
appear as a normal feature of the wood. The Pinaceae have been classified in accordance
with this feature by Jeffrey in 1905 (Bannan, 1936).
More recent works, however, show that even in the second group the ducts are much
more closely Correlated with injury than was thought earlier. I n the first group of
Pinaceae mentioned above, the ducts are generally cyst-like and confined to tangential
series at wounds. In the second group they are longer and often scattered in distribution,
becoming further dispersed at a distance from the centres of injury. The more general
occurrence of ducts in this second group as compared with the first one is correlated
with the lengthening and scattering of ducts produced subsequent to injury, rather than
to normal occurrence independent of wounding as has been commonly supposed. The
different genera may be arranged in a series in which there is an increase and dispersion
of the response to injury. The genus Pinus might be considered to have the ducts which
are least controlled by external factors (Thomson & Sifton, 1925; Bannan, 1933, 1936;
Fahn, 1967; Mirov, 1967).
Many investigators have dealt with the secondary resin ducts of conifers because of
their importance for wood technology and resin extraction. Less attention has been
paid to the ducts of the primary body, which were usually described along with other
tissues.
Mayr (1884) published an extensive description of both the primary and secondary
systems of ducts in Picea and Larix. One of the few important publications on the
primary resin system of conifers, which is mainly that of the root-hypocotyl axis, is that
of Hanes (1927). He and Van Tieghem (1872,Jide Hanes, 1927) divided the resin ducts
of the root of Pinaceae (or the Abietineae) according to their location into the following
groups: (1) root-pole canals, those ducts which are closely associated with protoxylem
poles; (2) central canals, those ducts which occur in the middle of metaxylem. Hanes
includes the genus Pinus among the plants that have ducts of the first group.
In the Pinaceae the root ducts are situated longitudinally along the root axis extending
into the hypocotyl. I n the Pinus root and hypocotyl the protoxylem poles appear
Y-shaped in cross section, with a resin duct in the angle of the two arms of each Y.
Hanes further divided those Pinaceae which have root-pole ducts into four groups,
according to the height of termination of the ducts in the seedling: (1) at more than
halfway up the cotyledons; (2) at the bases of the cotyledons; (3) in the upper region of
RESIN DUCTS OF PINUS HALEPENSIS MILL.
381
the hypocotyl; (4) in the lower region of the hypocotyl. He considers P . halepensis to
belong to the third group.
According to Hanes’ classification Pseudotsuga belongs to the fourth group, whose
root-pole ducts terminate in the lower region of the hypocotyl. Bogar & Smith (1969,
however, who examined roots of P . rnenxiesii, did not find the primary ducts to be a
permanent feature in this species. Mayr (1884) found resin ducts in all the roots of
Picea and Larix except the smallest ones.
In the primary body of the branches of conifers resin ducts are usually situated in the
cortex (De Bary, 1877). Sacher, while examining the ontogeny and anatomical structure
of branches (1954, 1955~)and their cataphylls (19556) in trees of Pinus Zarnbertiana
and P. ponderosa, described also their cortical ducts and the connection between these
and the ducts of the cataphylls. Mayr (1884) described the duct systems in stems,
scales and needles of Picea and Larix and Frampton (1960) described those of L.
decidua; Sterling (1947) described the ducts in the shoots of Pseudotsuga taxifolia,
There are cases, however, where ducts appear not only in the cortex of branches but
in other tissues too. In Cephalotaxus ducts were found in the pith (Rothert, 1899), and
Kirsch (1911) reports an occasional appearance of ducts in the pith of Pinus banksiana.
Some authors (De Bary, 1877; Franck, 1923; Chattaway, 1951) claim that a ring of
vertical resin ducts in the xylem of the primary bundles of branches is found in species
of Pinus, Larix and Pseudotsuga.
The resin ducts of needles have been dealt with by many authors. In his book on the
anatomy of gymnosperm leaves, Napp-Zinn (1966) summed up the information
accumulated on the resin ducts of these organs. There are different methods of classifying the types of ducts of leaves and a few problems concerning them still remain
unresolved (details are given below, in the chapter dealing with resin ducts of
needles).
The systems of resin ducts of the secondary body of many genera of the Pinaceae,
although influenced by many different factors, seem to have several features in common.
In the secondary xylem the resin duct system consists of vertical and radial ducts. The
radial ducts originate at vertical ducts (Mayr, 1884; Hart, 1919; Thomson & Sifton,
1925; Chattaway, 1951) and apparently continue indefinitely (Mayr, 1884; Bannan,
1965). According to Haldenby (1940) it is always so for L. laricina, except for a few very
small ones obviously caused by injury. According to Thomson & Sifton (1925) no
anastomoses other than at the origin of the radial duct between radial and vertical ducts
have been found in stems of Picea canadensis, but such anastomoses have been found
in the roots of this species. On the other hand, Mayr (1884) and Munch (1919) found
such connections in the wood of trees in every instance when a radial duct passed
beside a vertical duct.
Some investigators (Mayr, 1884; Jeffrey, 1905, jide Thomson & Sifton, 1925)
consider the whole system of ducts, radial and vertical, as a spatial network. Munch
(1919) claims that there are connections between tangentially adjacent vertical ducts
through radial ducts, but says that these connections are not numerous.
In the secondary phloem of a few species of Pinus (Munch, 1919; Alfieri & Evert,
1968) and in Picea canadensis (Thomson & Sifton, 1925) no vertical ducts have been
found. There are radial ducts in the phloem, which are continuous with the radial ducts
382
E. WERKER AND A. FAHN
of the secondary xylem. I n the cambium of stems of Picea and Larix these radial ducts
were found to have no cavity (Mayr, 1884; Thomson & Sifton, 1925).
The length of the vertical ducts in the wood was found to increase with the age of the
organ in which it appears (Munch, 1919; Bannan, 1933, 1936; Reid & Watson, 1966).
The lengths found for different species of Pinus, Lank and Picea were from less than
0.5 cm to more than 80 cm. A greater range was found within the same species when
different ages were compared than between plants of comparable age in different genera.
The manner of development of the duct cavity in gymnosperms has been a matter of
controversy. Kirsch (1911) and Hart (1916) mention a few authors who thought that
the resin ducts develop lysigenously. Most researchers, however, are of the opinion that
development of gymnosperm ducts is schizogenous (e.g. Mayr, 1884; Kirsch, 1911;
Hart, 1916; Hanes, 1927; Bannan, 1936; Sacher, 1954; Bosshard, 1964; Napp-Zinn,
1966); but they may be further enlarged by lysigeny (e.g. Tschirch, 1906; Kirsch, 1911;
Thomson & Sifton, 1925). On the other hand in some gymnospermous genera such as
Welwitschia (Rodin, 1958), ducts develop solely in a lysigenous manner.
I n addition to the resin duct system there is a second secretory system in conifers,
consisting of very long cells termed ‘secretory cells’, which contains substances other
than resin. This system will not be dealt with here.
The aim of this work was to get a complete picture of the resin duct systems and their
interrelationship and development in the various organs and tissues. The study was
carried out on plants ranging from the embryonic stage to adult trees. Pinus halepensis
was chosen for this purpose because it is widely grown in Israel, and very little anatomical work has been done as yet on this species,
MATERIAL AND hlETHODS
For the study of the ontogeny and structure of the resin duct system of P. halepensis,
different organs at different ages were taken from adult trees which grow in and around
Jerusalem and from seedlings.
Woody tissues were sectioned without embedding, by hand or with the aid of a
sliding microtome. Soft tissues were fixed in F.A.A., embedded in paraffin and sectioned with the aid of a rotary microtome.
Serial cross and longitudinal sections, 10-15 p thick, were prepared from all organs,
with the aid of a microtome. The embedded material was stained with safranin and
fast green. For sections of fresh material, an aqueous solution of FeCI3 for detection of
tannins, Sudan IV for suberin and resin (cf. Messeri, 1959) and phloroglucinol for
lignin were sometimes used,
Pieces of cortex and outer strips of wood were examined under a dissecting microscope
in order to see the course and length of ducts. In order to make the ducts more distinguishable from the surrounding tissues, the material was immersed in a 0.5% solution
of 2: 3 :5-triphenyl-tetrazolium chloride (T.T.C.) (colourless) for 24 hours in the dark
(Fahn & Arnon, 1963). The living cells reduce the T.T.C. to a red formazan which is
strongly soluble in fats and resins, and these substances are, therefore, stained with
this reagent. When the material for examination was not living and therefore incapable
of reducing T.T.C., or when it was too big to be put into a closed jar, reduced T.T.C.
has been used. This was done by reducing T.T.C. with sodium dithionite before
endodermis
secondary xyle-
ortex
phloem
hypocotyl
duct
e m duct
primary xylem/’
loher end of
s’em duct
1
-‘cambium
A
FIGURE
1. Schematic drawings of cross-sections of a three-months-old pine seedling. A. A tetrarch
root showing four primary resin ducts. B.Upper part of the hypocotyl showing the root-hypocotyl ducts between the cotyledonary traces and two of the lower ends of the stem ducts adjacent
to the vascular strands. C.Upper part of the hypocotyl at a higher level than the section in B,
showing resin ducts of both the root-hypocotyl (R) and the stem (S). ct, Cotyledonary traces.
D. Section through the cotyledonary node. Some of the cotyledonary traces are accompanied
by a resin duct. Resin ducts of the stem are situated in the cortex. E. Section just above the
cotyledonary node, showing resin ducts of the stem and the lower portions of the cotyledons.
F.Section of a lower part of the stem showing the bases of the juvenile leaves.
Resin ducts are marked by circles, xylem cross-hatched and phloem stippled.
3 84
E. WERKER AND A. FAHN
applying it to the material, as suggested by Witztum & Zamski (1969). For measuring
the length of ducts in the wood the method of Reid & Watson (1966), of staining with
12KI, was also found useful when used in the right season, i.e. before the commencement of cambial activity, when there is still starch in the living cells. The formazan
method, however, was found to be more suitable, because it can be used when the
ducts are on the surface of the wood and can be most easily distinguished.
OBSERVATIONS
The resin duct is an elongated structure formed by a layer of cells surrounding a
cavity. I n the genus Pinus these cells, termed ‘epithelial cells,’ are thin walled and
unlignified (Franck, 1923 ; Bannan, 1936; Mirov, 1967). T o the outside there are one or
more layers of cells with relatively thick unlignified walls, termed ‘sheath cells,’ the
walls of which are apparently very rich in pectic substances (Zamski, personal communication). Among the sheath cells there may be some dead cells (Plate 1A, B), which
may form a cylinder around the epithelial cells. T h e inner lamella of the wall of these
cells stains red with Sudan IV, which suggests that it consists of suberin. These dead
cells become crushed by further expansion of the duct during its growth. There is a
gradual increase in the height of the duct cells from the duct cavity outwards (cf. Hart,
1916; Munch, 1919).
Resin ducts are observed throughout the whole plant, both in the primary and
secondary body. I n structure there is no basic difference between the two types of
duct except that those of the primary body are much larger thanthose of the secondary
body.
Resin ducts of the primary body
The root-hypocoty2
The number of resin ducts in the primary body of the root was found to correspond
with the number of xylem strands. Each duct is associated with a protoxylem strand
(Figs 1A and 2B; Plate 1C). These ducts extend from a region adjacent to the root
apex, along the axis, into the hypocotyl. At the upper region of the hypocotyl, close to
the base of the cotyledons, splitting of one or more of the ducts often occurs. T h e number of ducts is thus increased (Fig. 1B). Some of the hypocotyl ducts end at the upper
portion of the hypocotyl, others at the base of the cotyledons, and still others extend to
the lower portions of the cotyledons together with the cotyledonary vascular bundles
and there fade out. T h e number of ducts of each type varies in different seedlings. From
the vascular system of the hypocotyl one or two vascular bundles extend into each
cotyledon. Cotyledons into which resin ducts enter contain two vascular bundles, and
the resin duct appears between the two bundles. After the resin duct ends the two
cotyledonary bundles fuse. The cotyledons into which no duct enters have a single
vascular strand (Fig. 1C-E). The number of cotyledons in P. halepensis is usually
six to eight.
The endodermal cells appear suberized mainly in their radial walls, as seen in crosssection of the root and hypocotyl. Concomitant with the divergence of the cotyledonary
RESIN DUCTS OF PINUS HALEPENSIS MILL.
385
0x
RD-k
I
leaf traces
I;
I
7
FIGURE
2. A.A cross-section of the stem, at a higher level than in Fig. I F (a continuation of the
series of sections in Fig. l), showing that each trace of a juvenile leaf is Accompanied by two
resin ducts. Xylem cross-hatched and phloem stippled. B. Schematic reconstruction of the
connections between the resin ducts of a lateral root and a parent root. X, Xylem; RD, resin
ducts. C.Diagram of the vascular and resin duct systems of a stem of a young pine seedling
spread out. Vascular bundles black and resin ducts white. Leaf bases are outlined.
vascular bundles from the stele at the top of the hypocotyl, the endodermal wall
thickenings in the regions between these bundles begin to disappear (Fig. 1C). At the
base of the cotyledons only individual endodermal strands can be seen outside each
cotyledonary bundle or a pair of bundles (Fig. 1E).These endodermal strands form
an outer abaxial layer of the transfusion tissue, in the lower portion of the cotyledons.
386
E. WERKER AND A. FAHN
Hanes (1927) classified those Pinaceae (or the Abietineae) which have root-pole
canals according to the place of the termination of the hypocotyl ducts. He puts P.
halepensis into one group with P. excelsa, P. strobus, P. maritima, P. coulteri, P. pinea
and P. gerardiana, where all the root-pole canals end in the upper portion of the hypocotyl. The group in which the root-pole canals end at the base of the cotyledons includes
the species P. sylvestris only. From what has been said above it appears that, at least in
the case of P. halepensis, this classification cannot be accepted.
I n the cotyledons there are no other ducts except for the occasional continuations of
the hypocotyl ducts.
The ontogeny of the root-hypocotyl ducts was examined in mature embryos and
seedlings (the youngest being 8 mm in length). It has been found that the duct initials
can be recognized very early in the life of the plant, sometimes even in the seed, and in
the early stages of a developing tissue, i.e. close to the root apex, both in a seedling and
in a mature plant. Near the root apex the duct initials can be distinguished already in
the region where the procambium differentiates, or even earlier. The duct cell initials
are larger than the procambial cells adjacent to them and their cytoplasm stains
more deeply. Between these initials, higher up in the root, the duct cavity is formed.
When serial cross sections are examined from the region of the initials upwards, the
manner of differentiation of the duct can be followed. The initial cells of the duct
become larger and form a rosette (Plate 2A). A few cells undergo divisions in various
directions, the main direction being periclinal to the future duct cavity. In this manner
the rosette becomes more distinct from the neighbouring cells. A central cell of the
rosette may undergo division and an intercellular space begins to form between the two
daughter cells. In most cases, however, the duct cavity develops between two existing
cells which are situated more or less in the middle of the rosette. The intercellular space
thus formed is surrounded by the first two cells and usually two other neighbouring
cells (Plate 2B). These four cells and the cells surrounding them may undergo further
divisions periclinally to the developing cavity. I n this manner a sheath of two or three
layers of cells is formed around the epithelial cells. Farther up in the axis the intercellular space expands and penetrates between the radial walls of some epithelial cells and
even between cells of the sheath. Thus some of the sheath cells also become part of the
final epithelial layer (Plate 2C).
Prior to the separation that occurs during the formation of the duct cavity, the
walls swell and become lens-shaped. This swelling apparently takes place in the middle
lamella and precedes its disintegration, Sometimes the commencement of the development of the duct cavity could be observed already in cross-sections of mature embryos.
During the further development of the duct the epithelial cells become flattened
tangentially and their nuclei may become elongated, as seen in cross-section of the duct.
This is in accordance with Hanes’ (1927) description of duct development in Cedrus
deoduru. It is also similar in principle to the development of mucilage canals in Zumia
(as described by Johnson, 1943). Hart (1916), who described the resin duct system of
some species of Pinus and Larix, found an analogy between their cortical ducts and the
mucilage canals in Cycadales.
In very young seedlings, in which the stem above the cotyledons is not yet developed
and the seedling axis consists only of the root and the hypocotyl, the differentiation of the
RESIN DUCTS OF PINUS HALEPENSIS MILL.
387
ducts is acropetal, towards both the root and the shoot apices. The ducts are thus largest
and most developed in the oldest, middle part of the root-hypocotyl axis, and differentiation proceeds gradually towards both apices. Slight deviations from this trend of
development, along small portions of the axis, can, however, be observed.
Later in the life of the organ a few scattered cells of the sheath may die and become
crushed by the expanding epithelial cells. In the dead cells an inner lamella, apparently
of suberin, was seen.
The connection between the primary resin ducts of main and lateral roots. As has been
mentioned above the number of resin ducts in the primary body of the root corresponds
to the number of xylem strands. This number varies from two to five, the common
number for the main root of the seedling being four. The number of xylem strands in
lateral roots, and thus also the number of resin ducts, was found to be usually smaller
by one or two than that of the root from which they branch. The smallest number of
ducts, i.e. two, was found to be the common one in the lateral roots.
All the resin ducts of a lateral root, regardless of their number, are connected with
one resin duct of the root from which the lateral root diverges. This resin duct of the
parent root is the one nearest to the place of emergence of the lateral root (Fig. 2B).
The connection between primary and secondary ducts. In the root and hypocotyl the
cambium begins to appear in strips, which are situated on the inner side of the primary
phloem groups. These cambium strips produce groups of tracheids that fill the gaps
between the protoxylem poles, thus also between the resin ducts (Fig. 1A; Plate 3A).
While these groups of secondary xylem increase in thickness in a radial direction, the
resin ducts also expand radially (cf. Mayr, 1884). This expansion is achieved by two
methods: (1) enlargement and stretching of the existing epithelial and sheath cells;
(2) separation of the epithelial cells from one another along their radial walls and also
the separation of the epithelial cells from the sheath cells so that the sheath cells join
the epithelial layer, In this manner the number of epithelial cells increases approximately from five to seven. This way of enlargement of the duct cavity is thus similar to
that described previously for the developing ducts in the apical region of the roothypocotyl axis, Here, however, the separation occurs between mature cells.
In the above-mentioned groups of secondary xylem, there are often secondary resin
ducts, both vertical and radial. The first-produced secondary ducts may sometimes
abut on the primary ones. The vertical secondary ducts, as observed in cross-section,
are much smaller than the primary ducts, a difference that is characteristic of primary
and secondary ducts in general. Because of this fact and due to the stellate structure in
cross-section of the secondary xylem at this stage of development, the secondary ducts
seem to be situated at the same depth as, or even nearer the centre of the axis than, the
primary ducts.
After the secondary xylem groups reach a thickness of about 9-15 tracheids, new
strips of cambium are formed outside the protoxylem poles and the primary resin
ducts. These cambial strips join the first-produced ones, so that a complete cylinder
of cambium is formed. The appearance of the newly formed cambial strips can be
distinguished in cross-sections by the formation of tangential walls in sheath cells
situated on the outer side of the primary resin ducts (Plate 3 A).
The secondary xylem produced by the new strips of cambium covers the primary
388
E. WERKER AND A. FAHN
resin ducts, which become included in it. Occasionally wide rays with radial ducts in
them appear in these xylem portions. The lumina of these ducts are continuous with
those of the primary vertical ducts. This is the only instance throughout the plant body
where a connection between the primary and secondary duct systems has been found.
Hanes (1927) described such radial ducts, which are connected with the ‘root-pole
canals’ in their upper portions, close to their endings. He found such connections in
those species whose root-pole canals end in the upper portion of the hypocotyl, and
according to his classification this would include P. halepensis. We have found that in
P. hdepemk such radial ducts are formed, at irregular distances, along the whole length
of the primary vertical ducts (cf. Bannan, 1941, for Larix and Picea; Bogar & Smith,’
1965, for Pseudotsuga). Connections between radial and vertical ducts seem to be a
regular feature in the secondary xylem, as will be shown later. Thomson & Sifton
(1925) claim that in Picea canademis no connections are found between primary and
secondary ducts in any part of the plant. Mayr (1884) on the other hand found in the
roots of Picea and Lank many radial ducts which originate from vertical ducts of the
vascular bundles. Mayr, however, did not consider the origin of the duct in this case
in terms of primary or secondary tissues.
The shoot
I n the region of the cotyledonary node new resin ducts develop. These ducts, which
continue upwards into the stem, have no connections with the root-hypocotyl ducts
(Fig. lB, C).
At the cotyledonary node there are usually four resin ducts, corresponding to the
usual number of vascular strands in the hypocotyl. At first they are formed in close
contact with the strands so that their lower end is attached to the outer side of the primary phloem (Fig. 1B, C). Higher up these ducts diverge gradually, but at a broad angle,
into the cortex and continue upwards in the cortical tissue. Usually soon after its
formation each of the four ducts split in two, so that eight ducts are formed. This is the
common number of primary ducts in stems. Sometimes the final number of ducts
increases to ten by a further splitting of the already existing ducts (Fig. lD, E) or,
in the young seedling, by the formation of new ducts in contact with vascular strands.
I n the seedling, only juvenile leaves are present. When the seedling grows these
leaves become more and more scale-like and, in the second year of the sapling, brachyblasts bearing needles appear in the axils of these leaves.
I n the stem, each vascular bundle that diverges into a juvenile leaf passes between
two cortical resin ducts (Figs 1F and 2A). Each of the stem ducts splits periclinally
into two ducts. One branch continues along the stern in the cortex and the second one
enters a juvenile leaf (Fig. 2A). Such splitting of the stem ducts of the seedling was also
described by Hanes (1927) for Pinus excelsa. Thus each leaf has two longitudinal resin
ducts (Crafts, 1943), which pass along its abaxial side, some distance from the corners.
The epithelial cells on the outer side of the duct are usually in direct connection with
the hypodermis.
A reconstruction of the vascular and resin ducts systems of the stem of a seedling is
shown diagrammaticallyin Fig. 2C. It can be seen that a close correlation exists between
the two systems, and that they are both correlated with the phyllotaxis. The same pattern
RESIN DUCTS OF PINUS HALEPENSIS MILL.
389
prevails in the primary body of the shoot throughout the plant from seedling to mature
tree. While the juvenile leaves change to scales, no change occurs in the shoot duct
system. The system only becomes more complicated by the emergence of lateral shoots,
as will be described later.
The differentiation of the stem ducts is acropetal. In the shoot apex, initials of the
resin ducts can be seen on both sides of the outer part of each provascular leaf bundle.
At this level the initials of both vascular and resin duct systems are in close contact,
but lower down in the stem and in the juvenile leaves they separate very quickly. It is
difficult to decide whether these systems have common initials or whether they have
different origins. The close correlation between the two systems, however, indicates
that common factors control their pattern.
The manner of resin duct differentiation from its initials is similar in the shoot to
that described for the root, except for the fact that in the shoot the initials are smaller
than the surrounding cells, especially as compared with the parenchymatous cells of
the pith.
The connection between the primary duct systems of the main and lateral shoots. As the
seedling grows, lateral branches develop from the axils of the juvenile leaves. With the
growth of the shoot the juvenile leaves, which in the lower part of the stem are needlelike, become more and more scale-like. The first branches to appear are usually dolichoblasts and the brachyblasts appear later. Two branch traces are seen to emerge from the
stele of the parent stem above the scale trace, between two resin ducts (Fig. 2A). The
resin ducts of the scales and all the resin ducts of the lateral branch are connected with
these two resin ducts of the parent stem. This differs from the case of P. lambertiana
(Sacher, 1954, 1955a), where inner cortical ducts are connected with the resin ducts of
the scales while outer cortical ducts are connected with those of the brachyblasts.
In the brachyblast, which is a very short shoot, there are usually three to five cortical
resin ducts, and from them branches enter the brachyblast scales. A pattern of five
resin ducts in the brachyblast was found in branches of mature trees of P. lambertiana
(Sacher, 1955b). No resin ducts end freely in the shoot apex, as all of them enter the
scales or the scale bases. The uppermost scales usually have no ducts.
A common example of the connection of resin ducts of the parent stem with a scale
and a short lateral shoot is seen in Fig. 3. All the ducts of the scale and brachyblast
derive directly from the two cortical resin ducts of the parent stem or secondarily from
branches of these ducts between which the scale trace and brachyblast trace pass. There
are variations, however, in the position and number of the resin duct branchings in
different lateral shoots and their substantive scales, even in shoots emerging from the
same parent stem. Because of these variations it is apparent that a different number of
ducts can be observed in cross sections made at different levels of a single brachyblast
and at the same level in different brachyblasts.
In most brachyblasts the ducts are highly differentiated, similarly to the ducts in the
cortex of the elongated branches, though smaller in diameter. There are, however,
brachyblasts in which it is very difficultto distinguish the ducts. In these cases, as seen
in cross-section, they have no cavity, the sheath cells are barely noticeable, if at all, and
the few epithelial cells can be distinguished from the other parenchymatous cells only
by their smaller size and their arrangement in a rosette.
390
E. WERKER AND A. FAHN
The pattern of branching of the resin ducts of the dolichoblasts from the ducts of the
parent stem is similar in its general features to that described for the brachyblasts. I n the
dolichoblasts, however, there are as many as eight cortical ducts. The greater number of
ducts is correlated with the departure of more branches from the two cortical ducts of
the parent stem and with further branching of the ducts, both at the place of branch
FIGURE
3. Schematic reconstruction of a portion of a stem (ST) showing the branching of resin
ducts into a brachyblast (BR) and a scale (SC).
insertion and in the dolichoblast itself. From the ducts of the dolichoblast axis, duct
branches enter the scales. The resin ducts of the dolichoblast axis extend to the apex
and their development keeps pace with the extension growth of the dolichoblast.
This pattern of the primary system of resin ducts in branches is fairly constant
throughout the plant, but there are some small variations. As has already been mentioned, the common number of cortical ducts is eight; but changes may occur along
small portions of a branch, generally leading to a reduction in number of the ducts.
These changes can occur in one of two ways : by merging of two neighbouring ducts or
by the extension of a resin duct of the stem into a brachyblast without dividing, so
that no branch continues upwards in the parent stem. The subsequent increase in
number of the ducts is obtained by splitting.
Changes may occur also in the diameter of the lumen of the duct, and portions of it
may become relatively narrow. The width of the lumen is correlated with the number of
epithelial cells and/or with their stretching, as seen in cross-section. The number of
RESIN DUCTS OF PINUS HALEPENSIS MILL.
391
epithelial cells has been observed to vary from 11to 44, along the same duct. Thegreatest diameter of a given duct, as seen in cross-section, may vary from 35-120 p or more.
With the increase in diameter of the stem, as a result of secondary growth, further
enlargement of the cortical ducts takes place.
Hanes (1927), in his description of the resin duct system of the shoot of seedlings of
P. excelsa, states that the cortical canals of each year’s extension growth form separate
systems which do not connect with the canals in the cortex above or below. Thomson
& Sifton (1925) claim that in Picea canadensis the cortical ducts of each year’s growth
become cut off later by periderm formation.
In order to see whether this is the case also in Pinus halepensis, we have made two
types of observation. (1) Serial cross sections of branches were made in those regions
which included the transition from one year’s extension growth to that of another.
A reconstruction of the cortical duct system was made, but no free endings of ducts
were found in these portions. The ducts pass along the cortex uninterrupted. (2) The
cortex was peeled off stems, mainly in those regions that included the transition from
one annual growth to the next. These portions of the cortex were immersed in 2: 3 :5triphenyl-tetrazolium chloride (T.T.C.). The formazan which is produced by the
cells is soluble in fats and resin (Witztum & Zamski, 1969). After 24 hours the phloem
was removed and the cortex portions examined under a dissecting microscope by
reflected light. By this method the red-stained ducts could be followed. It should
be mentioned that this examination cannot be carried out on very young branches, for
then all the cortical cells are living and capable of reducing the tetrazolium. With
aging, some of the parenchymatous cells of the cortex die and in the others the amount of
cytoplasm decreases and, therefore, the stained ducts become much more distinguishable from their surroundings. With this T.T.C. method fairly long portions of branches
can be examined, although it is crude compared with serial sections.
With this method the same results as withthe serial cross-sectionshave been obtained,
except for an occasional elimination or addition of a single duct along an extension
growth of a single year, which is a result of merging and splitting of ducts, as was
described above.
From the above results it may be concluded that the system of the primary resin
ducts of the shoot, excluding the needles of the brachyblasts, is continuous throughout
the plant. Only when inner scaly phelloderms are formed, as a result of further growth
of the plant, do portions of the cortex peel off together with the lower portions of the
primary cortical ducts.
The needles
There are different opinions among those who have worked on conifer needles as to
whether the resin ducts are connected with those of the brachyblast axis or form a
separate system. I n different species of Pinus Hanes (1927) and Sacher (1955 a), among
others, did not find any connection between the ducts of the two organs, while
Diaparidze (1937), for example, reports the existence of such connections. Summaries
of this subject are given by Diaparidze (1937) for Pinus, PlavZi6 (1934) for Picea and
Napp-Zinn (1966) for conifers in general.
Mirov (1967) and Zavarin (1968), who worked on the chemical composition of resin
392
E. WERKER AND A. FAHN
and mainly on its turpentine constituent, found that the chemical composition of the
resin of needles differs from that of other organs and tissues.
In his book on the anatomy of gymnosperm leaves Napp-Zinn (1966) presents a
summary of literature dealing with resin ducts in leaves. He gives the following classifications of the types of ducts of the genus Pinus according to their location in the leaf:
(1) ducts in contact with the hypodermis; (2) ducts surrounded by chlorenchyma;
(3) ducts in contact with the bundle sheath in the chlorenchyma; (4)ducts inside the
bundle sheath. Ducts of the last type are rare. They extend from the needle into the
brachyblast axis and are narrower than those of the other three types. In the brachyblast
axis they appear in the xylem and when they enter into the needle they shift into the
transfusion tissue. P. halepensis is mentioned by DSaparidze (1937) as one of the
examples of the last type.
For some species of Pinus examined it was found that, in the same species, both
ducts bordering the hypodermis and ducts embedded in the chlorenchyma may be
present (Masters. 1890; Steven & Carlisle, 1959; Schutt & Hattemer, 1959, Jide
Napp-Zinn, 1966).
The ducts of the first three types are further divided into two main ducts and a
varying number of accessory ducts (Thomas, 1863). The main ducts are broader and
longer than the accessory ducts and, unlike them, constant in number. According to
Hempel & Wilhelm (1889,Fde Napp-Zinn, 1966))in P. halepensis there are two ducts
on the adaxial side of the leaf and up to five on the abaxial side.
Zollikofer (1917) studied the endings of ducts of the leaves of different species of
Pinus and of Cedrus atlantica. She classified them into two types according to the cells
appearing at their ending. (1) Epithelial cells close the duct cavity without undergoing
any structural changes. Above them the sheath cells change into a mechanical tissue.
(2) After closure of the duct cavity the epithelial cells undergo gradual changes and
form transitional cells. Their walls, which are undulate in the duct, straighten and
thicken, and they change into typical mechanical cells. These produce, together with
the sheath cells, a fibre strand continuous with the duct.
In P. halepensis the needles grow in pairs at the apex of the brachyblast. Their length
when mature is 8-12 cm. Scale leaves envelope the dwarf axis.
I n order to study the resin duct system of the needles, serial cross-sections were
made. This technique is necessary because the ducts are shorter than the leaf and the
lower end of one duct may be close to the upper end of another duct. The examination
of single cross-sections may, therefore, give a partial or even a misleading picture.
From the examination of the ducts in P. halepensis it is apparent that in needles, as in
all other organs that have secondary thickening, primary and secondary ducts are
present. The primary ducts, which appear in the mesophyll parallel to the longitudinal
axis of the leaf, may be in contact with the hypodermis on their outer side (type 1 of
Napp-Zinn) or surrounded on all sides by mesophyll (type 2 of Napp-Zinn). The same
duct can pass from one type of location to another in different portions of the needle.
In a cross-section the needle is in the form of a semicircle. The flattened side is
adaxial and the curved side abaxial (Plate 3B). As no significant differences between
the various mesophyll ducts of the needles could be observed in P. halepensis, we do not
use the terms ‘main’ and ‘accessory)ducts mentioned by Napp-Zinn. For convenience
RESIN DUCTS OF PINUS HALEPENSIS MILL.
393
the ducts which appear nearest to the edges of the needle will be termed ‘lateral ducts’
(Esau, 1965).These appear usually at the adaxial side close to the edges, but sometimes
both ducts or one of them, along their entire length or along a part of it, are found on the
abaxial side, close to the edge (Plate 3B).
I n the lower portion of the leaf one can usually distinguish two lateral and two to
seven abaxial ducts, which terminate proximally at the very base of the leaf or somewhat
above it. There are slight differences in the level of these ends between the different
ducts of the same leaf. In some cases the lower ends of lateral ducts may even enter the
upper portion of the brachyblastsand terminate in the meristem of the brachyblast apex
(cf. Cross, 1940,for Tuxodium). Occasionally the lower ends of a pair of such ducts,
one from each needle, fuse together and then terminate at the shoot apex. But even in
these rare occasions there is no connection between the needle ducts and the cortical
ducts of the brachyblast axis.
The ducts reach various lengths and their upper ends can be found at different levels
in the needle. Some end in the lower quarter of the needle, others extend up into upper
quarter. Quite often near the end of one duct can be seen the beginning of another one,
which appears as a continuation of the first. Very often in the terminal portion of the
needle, above the upper ends of the lateral ducts and usually in continuation with them,
two very short ducts are present. Their length is about 1mm and they terminate about
0.5 mm below the tip of the needle (Plate 3 C). An example of such a pattern of the primary system of the ducts in a pair of needles is given in Fig. 4A.There are variations
within this pattern, however, even in needles belonging to the same brachyblast.
The primary ducts here, as in the primary body in general, are relatively large. The
sheath cells have thick, dignified walls and are oblong and rectangular in longitudinal
section (Plate 4A). They are filled with substances which are insoluble in alcohol,
stain strongly with safranin and do not darken with FeC1,. The sheath cells resemble
the hypodermal cells in form. No fibres are found around the epithelial cells, though
these occur in a few other species of Pinus (Thomas, 1863) and in Picea and Larix
(Mayr, 1884).
The ducts which appear in the xylem of the vein of the needle belong to a different
type, which is not produced before the cambium is formed (cf. type 4 of Napp-Zinn)
(Fig. 4B,C;Plate 5B).When the cambium commences its activity it may produce a
resin duct together with the first tracheids. Ducts of this type, therefore, are situated
between the primary and secondary xylem. They are very narrow even in comparison
with the usually narrow secondary ducts of other tissues. Such ducts situated between
the primary and secondary xylem are present in all the branches of the plant (see below).
The secondary ducts of the needles are continuous with the inner ducts of the secondary
xylem of the brachyblast axis, but not every duct of this type in the axis extends into
the needle. These secondary needle ducts terminate a short distance above the base of
the needle and are capped by a few layers of parenchymatous cells. The end of the duct
may be in the primary xylem or even in the parenchyma which borders on it on the
adaxial side.
Development of theprimary ducts. In Pinus, as in most Spermatophyta, leaf growth in
length is apical and subapical at first and later intercalary (Sacher, 1955a,b ;Napp-Zinn,
1966). The greater part of the leaf growth in Pinus is achieved by the activity of the
3 94
E. WERKER AND A. FAHN
duct
D
FIGURE
4.A. Pattern of arrangement of the resin ducts situated in the mesophyll of a pair of
needles. The length and width of the needles have not been increased to the same degree.
Lateral ducts in thick lines ;abaxial ducts in interrupted lines. B-E. Schematic drawings of cross
sections of a needle and a brachyblast : B, near the base of a needle, showing a duct embedded in
the secondary xylem ( x 40) ; C, the vein of the needle ( x 180) ; D, a brachyblast showing a duct
in the secondary xylem which is a continuation of the duct seen in B and C (x40) ; E, vascular
cylinder of the brachyblast ( x 180). Dotted areas-phloem; densely cross-hatched areasprimary xylem; sparsely cross-hatched areas-secondary xylem.
RESIN DUCTS OF PINUS HmE PE N SI S MILL.
395
intercalary meristem situated at the leaf base. The first ducts to be formed are, therefore,
the short lateral ones at the tip of the needle (Plate 3 C). I n young leaves (about 8 mm
long) these ducts were found to be already fully differentiated, while most of the other
ducts had not yet been formed. With further growth in length from the intercalary
meristem, all the other ducts are formed, both lateral and abaxial, starting with their
distal tips. Development and differentiationof the ducts is thus basipetal.
The duct complex, including sheath and epithelial cells, develops from the mesophyll
tissue (cf. Heimerdinger, 1951, for P. nigricans). A few mesophyll cells, while not yet
fully differentiated, undergo divisions in different directions, mainly radial and tangential, until a rosette of cells is formed (Plate 4B-D). I n the middle of this group of
cells the duct cavity is formed.
One or two tiers of epithelial cells can be seen at both ends of the duct, above the
closure of the cavity. Above these epithelial cells there are two or three tiers of sheath
cells, which are similar to the ordinary sheath cells of these ducts, but slightly shorter
(Plate 4A). This type of duct ending may correspond in general to the first type of
Zollikofer (1917), but in contrast to her description no mechanical tissue appears
beyond the cells that close the duct.
A comparison was made between the needles of young saplings and those of mature
trees. No difference in structure, appearance or location of the ducts has been found in
the different ages of the plant. In the needles of h i e s (Roller, 1966), different locations
of ducts were found in needles growing on plants of different ages.
Flotynsky (1967) found a correlation between the number of ducts in the needles of
P. sylvestris and the location of the needles in the tree crown. This phenomenon was
not examined by us in P. halepensis.
Development of the secondary ducts. In cross-section the xylem is arranged in a fan-like
manner (Plates 3B and 5A) with up to six tracheids of the primary xylem in a radial
row. The cambium differentiates when the leaf is still elongating, i.e. in the region where
the cambium is formed the cells have not yet reached their final length and in the leaf
base the intercalary meristem is still active. The cambium can already be distinguished
in leaves which are 3 cm long, and it nearly reaches the tip of the needle. Because the
leaves are still elongating after the primary xylem has undergone differentiation and
the cambium has started to produce secondary xylem, the primary xylem is crushed
and torn in many places. Sometimes holes are formed where the primary xylem had
been present (Plate 5 A) and then only secondary xylem remains. Therefore, where the
primary xylem is still present the secondary duct is found on its outer border, between
the primary and secondary xylem, while in those portions where the primary xylem is
crushed and torn, the secondary ducts are found within the secondary xylem, i.e.
bordering the adaxial side of the vascular bundle. There are cases, however, in which
the duct has its upper end in the primary xylem of the needle and continues into the
secondary xylem of the needle and then into the secondary xylem of the brachyblast.
The cambium in the needle is formed basipetally while in the brachyblast axis it is
formed acropetally. Therefore, the cambium is formed last in the region where the
leaf is inserted and the amount of secondary xylem, up to a certain age, is the smallest.
I n this region, at the time that the cambium is beginning its activity, the secondary
ducts appear in the outer part of the xylem. The cambium, however, continues to
28
3 96
E. WERKER AND A. FAHN
produce vascular tissue until the needles and the axis of the brachyblast are fully mature,
and it produces much more secondary xylem in the needle than it does in the axis
(Fig. 4B-E;Plate 5B,C). At maturity, therefore, the secondary ducts of the leaf base
seem to be more deeply embedded than do those of the brachyblast.
These facts may perhaps explain the shift position in of the ducts along the needle,
as observed by Diaparidze (1937), and also his observation that in the leaf base the duct
may be external to the xylem while lower down in the brachyblast axis it is within the
xylem.
The secondary ducts in our material, taken from saplings and mature trees growing
in the hills around Jerusalem, did not extend much above the bases of the needles. This
differs from what was described by Diaparidze (1937) for this species grown in the
U.S.S.R.
Resin ducts of the secondary body
In the primary body the location of ducts is constant and there are only small variations in their number. I n the secondary body the pattern of the ducts is much more
variable, though it is not haphazard (cf. Franck, 1923).
For the examination of the system of ducts in thc secondary xylem and the secondary
phloem, serial cross and longitudinal sections were made of stems and roots of saplings,
of branches and of blocks of wood and phloem obtained from trunks of adult trees.
It was found that there is a transition type of duct between the constant pattern of
arrangement in the primary body and the more flexible one of the secondary body, This
transition type of duct pattern will now be described.
Thejrst ducts in the secondary xylem
The vertical resin ducts of each growth ring in pines usually appear in the outer part
of the early wood and in the first-formed part of the late wood (Oppenheimer, 1945,
for P. halepensis;Munch, 1919, for species of Pinus; Ito, 1963, for L. kaempferi). In the
first growth ring of branches in adult trees, however, vertical resin ducts usually develop
from the cambium before the secondary xylem layer is more than four tracheids thick.
When studying cross-sections of branches in which a fair amount of secondary xylem
has developed, it is difficult to decide the origin of these ducts (Plate 7A). They may
be thought to belong to the primary body, situated on the outside of the primary xylem,
or to the secondary body and to represent the first elements formed by the cambium.
I n order to clarify this problem cross-sections of young branches in which secondary
thickening was just starting were studied. These sections revealed that resin ducts are
formed by the young cambium at the beginning of its activity. T h e initials of the resin
ducts can already be distinguished shortly after the first tangential divisions of the
newly formed cambium take place. The duct initials, usually four in number, begin to
enlarge (Plate 6A) while the tracheid initials are still flattcned tangentially. At this stage
the duct initials are still arranged in radial rows. An intercellular space then appears
between the enlarged duct cells (Plate 6B). Later on the number of enlarged cells
increases up to six or more and the intercellular space extends so that it is in contact with
all of them. Thus the radial arrangement of the parenchymatous cambial derivatives is
RESIN DUCTS OF PINUS HALEPENSIS MILL.
397
distributed where resin ducts are formed. Other cambial derivatives, which differentiate
into tracheids, retain their radial arrangement.
I n a cross-section the vertical inner resin ducts of the first growth ring, usually five to
ten in number, are arranged in a circle. At various levels they are tangentially split and
their number increases. Some (one to three) of these ducts, however, extend from the
stem into each of its lateral branches. The number of the internal secondary ducts as
seen in cross-sections of the stem, therefore, does not change much when it is compared
at various levels (Fig. 5 ) .
FIGURE
5. Schematic reconstruction of part of the resin ducts of a one-year-old branch. Ducts
extending into the lateral branches are stippled.
In addition to this internal circle of resin ducts other vertical resin ducts are often
present in this same first growth ring. These ducts, however, are not restricted to the
transition region between early and late wood but may be scattered throughout the
ring. This arrangement differs from those of the ducts of later growth rings except, in
most cases, the second one.
In roots such an inner circle of ducts of early secondary origin is formed only occasionally, and at the most only one or two ducts are found. I n the hypocotyl they are more
E. WERICER AND A. FAHN
398
common, but here too there are not more than two. In the root and hypocotyl the early
ducts are not situated close to the primary xylem, i.e. they are produced at a later stage
of cambial activity than in the stem.
In branches of young plants these inner ducts of the first growth ring are absent or
relatively scarce. This feature is not dependent on the amount of branching of the stem.
An attempt was made to find a correlation between the number of cortical resin ducts
of the primary body, which varies but slightly, and the number of inner resin ducts of
the first stem growth ring (Plate 7 4 . For this purpose cross-sections of branches of
adult trees were made. The results of the counts of the number of resin ducts, which are
given in Table 1, confirm the above-mentioned conclusions that the common number of
Table 1. Comparison between the number of resin ducts in the cortex
and the inner part of the first growth ring in branches
No. of tree
1
No. of cortical
ducts
No. of resin ducts in
the inner circle
of secondary xylem
4
8
8
5
8
3-5"
8
2 4
6
5-6'
No. of branch
1
2
3
2
5
7
6
8
8
1
2
8
5
6
6
8
10
3
1
2
8
8
8
8
5
4-5"
4
1
8
8
2
3
8
8
8-9'
4
1
8
3
4
5
5
2
3
4
5
10
8
8
5
5
7
7
5
1 3 in two very close circles
8
8
* Counted at different levels of the same branch.
vertical resin ducts in the cortex is eight and that it is usually constant along the branch,
while the number of internal resin ducts of the first growth ring is more variable along
the branch. Nevertheless, a fairly close correlation can be observed between the numbers of the two types of ducts. When the number is higher than usual in the cortex, it is
also higher in the inner ducts of the secondary xylem and vice versa.
This regularity in the number of ducts in the primary body and the oldest part of the
secondary body is in contrast to the variability in number of resin ducts in the bulk of the
secondary xylem. This difference indicates that the inner portion of the secondary
xylem forms a kind of transition from one type of duct determination, found in the
primary body and apparently dependent only on internal factors, to another type of
duct determination, found in the secondary body and readily influenced by external
factors as well as internal factors.
RESIN DUCTS OF PINUS HALEPENSIS MILL.
399
It can also be seen that there are differences in the number of each type of duct even
in different branches of the same tree.
The pattern of the resin duct system in the secondary body
In order to understand the pattern of arrangement of the ducts of the secondary body
serial cross-sections of one- to three-year-old branches from adult trees were prepared.
From these sections the system of secondary resin ducts was reconstructed, as in Fig. 5.
The reconstruction was then checked on portions of wood and bark of various ages.
From this scheme it can be seen that in P . halepensisthe inner end of each radial resin
duct is connected to a vertical duct of the secondary xylem and that the lumina of the
two types of duct are continuous. Each radial xylem duct extends to the cambium and
from the cambium outwards it continues as a radial phloem duct. The outer end of
each radial phloem duct is enlarged into a cyst-like vesicle (Plates 6 C and 7B), which is
sometimes slightly elongated downwards, upwards or in both directions. There are no
vertical ducts in the phloem (cf. Mayr, 1884; Hart, 1916; Thomson & Sifton, 1925;
Chattaway, 1951; Alfieri & Evert, 1968).
In the cambial region the lumen of the radial duct is closed (Plate 7C) (cf. Mayr,
1884, for Picea and Larix; Thomson & Sifton, 1925, for Picea canadensis). In Pinus
hazepensis there is not more than one radial duct in a ray (cf. Mayr, 1884; Bannan, 1965).
Radial resin ducts, on continuing outwards, come in contact with vertical resin ducts
situated on the same radial plane. In most cases the radial ducts pass through the
parenchyma of these vertical ducts. The vertical ducts may, in this region, shift slightly
to the side, so that no connection is formed between the lumina of the two types of
ducts (Plates 7D and 8B), but connections between the lumina are occasionallyformed
(Plate 10A, B). These observations differ from those made by Munch (1919) for the
Pinus species which he examined. Munch found numerous connections between radial
and vertical ducts whenever they came close together, and he even observed that a
vertical duct may bend toward a radial duct when the two are not exactly on the same
radial plane, and then a connection between the lumina of the two is formed,
The radial ducts are found within rays which have a special fusiform shape. With the
exception of the rays which include radial ducts connected to the first-formed secondary
vertical ducts, the fusiform rays are continuous with simple rays both into the earlier
(inner) xylem and the earlier (outer) phloem (Plate 8A). A simple ray in the xylem
changes into a fusiform ray at the point where a vertical duct appears (cf. Hart, 1916;
Thomson & Sifton, 1925;Chattaway, 1951).Not every simple ray that comes in contact
with a vertical duct changes into a fusiform ray. Simple xylem rays are often seen to
start from vertical resin ducts (cf. Hart, 1916).
Some vertical resin ducts were found to divide tangentially and then fuse again, a
feature observed in other species of Pinus by Strasburger (1891, jide Munch, 1919)
and Munch (1919). As a result they form a narrow loop, surrounding a small number
of cells which are generally parenchymatous. Both simple and fusiform rays were
often seen to pass through such a loop (Plate 8B,C).The cells of the ray may even
serve as epithelial cells of the vertical ducts where they come in contact with it. It may
be that the presence of the ray was the cause of the splitting of the ducts. Occasionally a
400
E. WERKER AND A. FAHN
branch trace passes through the loop between the two parts of the duct, and in such cases
the distance between the two parts of the duct increases and the fusion between them
takes place at a much higher level. Except for these splittings, which fuse again on the
tangential plane, no connections were found between vertical resin ducts situated in
different radial planes. Connections between different ducts are present only on the
same radial plane and these occur through the radial resin ducts. This means that the
resin duct system cannot be considered as a spatial network. The lack of tangential
connections was found to be true for all the secondary resin ducts except for those
formed in the innermost portion of the first growth ring, which branch and unite in
a tangential direction (Fig. 5).
The vertical ducts are often surrounded by parenchymatous cells in addition to their
epithelial and sheath cells. The radial ducts of the xylem have different numbers of
sheath cells above and below the epithelial cells. Laterally they may have one layer of
sheath cells on one or on both sides or they may have no sheath cells at all (Plate 9A, B).
The phloem ducts may have, in addition to the sheath cells, which always appear above
and below the epithelial cells, one or two layers of sheath cells on each side.
The radial ducts are much smaller in cross-section than the vertical ones (cf. Munch,
1919; Franck, 1923).
Sometimes a strand of parenchymatous cells with no duct in it appears in the vertical
system of the secondary xylem. It is not known whether resin ducts can develop at later
stages in these parenchyma cells. Other strands of parenchyma are found in continuation with the endings of vertical ducts (cf. Mayr, 1884; Hart, 1916). Occasionally more
than one vertical duct is found embedded in one tangentially extended parenchymatous
strand,
In the secondary body of the roots the same general structure of the resin duct system
prevails. Moreover, the ducts of the root and shoot constitute one continuous systemvertical ducts starting in the root are seen to continue into the shoot. The distribution
of ducts may of course vary in different roots, as it does in different branches, according
to external conditions (cf. Bannan, 1941).
I n reconstructions made from several branches (cf. Fig. 5), it can be seen that the
distance between radial ducts connected to a vertical duct varies considerably. Occasionally as many as four radial ducts are attached to one vertical duct along 2.5 mm, while
none are attached to neighbouring vertical ducts along the same length. The spacing
of ducts, both radial and vertical, needs special investigation.
Development of ducts of the secondary body
The vertical ducts are formed by fusiform initials of the cambium (cf. Rannan, 1936)
and the radial ducts from ray initials. The manner of development of the vertical ducts
is similar to that described by Hart (1916) for P. sylvestris and to that described in a
previous section for the internal ducts of the first growth ring. It should only be added
here that the first changes into duct cells which can be observed take place in the xylem
mother cells in the cambial zone. These changes are transverse divisions of the cells
as seen in radial and tangential longitudinal sections, divisionswhich form the epithelial,
sheath and parenchyma cells. The duct cavity usually begins to form very early, when
RESIN DUCTS OF PINUS HALEPENSIS MILL.
401
the duct cells are still close to the cambial initials. In this stage the adjacent walls of the
young duct cells swell and then separate to produce an intercellular space which
develops into a duct cavity. This process is similar to the development of the duct
cavities in the primary body.
Occasionally initials of simple rays are seen to change into initials of fusiform rays
(i.e. rays containing ducts). Cells at approximately the centre of an uniseriate ray undergo divisions in different directions to form the epithelial cells, and some divisions in
cells above and below them also occur. This new fusiform ray produces a radial phloem
duct on the outer side of the cambium and a xylem duct on the inner side.
This change from simple ray initials into fusiform ray initials always occurs in connection with the formation of a vertical duct by fusiform initials, and there is always a
connection between the two types of duct. The question then arises whether the production of both ducts is simultaneous, or whether one type of duct is formed before
the other.
There are indications that the radial duct is the first to be formed. Usually the amount
of secondary phloem produced is much smaller than that of the secondary xylem, but
the examination of cross-sections of stems with young ducts in the secondary body
reveals that the length of the radial phloem ducts is approximately the same as that of
the respective radial and vertical xylem duct complex. (Plate 7B). I n one case a young
radial duct of the phloem was observed outside the cambium with no corresponding
duct inside the cambium (Plate 9C).
In any case it seems certain that a group of cells in the cambial region, both fusiform
and ray cells, produces ducts after receiving some stimulus. T h e newly formed epithelial cells of the radial duct are not produced symmetrically at the place of connection
with the vertical ducts. They become drawn apart on the side where the differentiating
cavities of the two ducts fuse. T h e epithelial cells of the radial duct thus become
continuous with those of the vertical duct. With further development of the radial
duct, some distance from the vertical duct with which it is connected, one layer of
sheath cells is formed on one or both sides of the epithelial cells (Plate 9A, B).
When a radial duct in the course of its development comes in contact with a new vertical duct, one of three possibilities may occur. (1) The radial duct may pass between the
vertical duct cells without forming any connection with the lumen of the vertical duct
(Plates 7D and 8B) and usually without undergoing any noticeable change of its own
cells. It may pass between the epithelial and sheath cells of the vertical duct or between
any other parenchymatous cells surrounding the vertical duct (cf. Thomson & Sifton,
1925). (2) If the radial duct happens to pass through the middle of the vertical duct,
the vertical duct may split without forming any connection with the lumina of either
part (Plate 8 G ) . (3) A contact may be formed between the lumina of the vertical and
radial ducts. The epithelial cells on one side of the radial duct are then drawn apart
from one another (Plate 10A, B). At this point no epithelial cells of the vertical ducts
appear and the epithelial cells of the radial duct come into contact with the neighbouring
epithelial cells of the vertical duct. Thus a connection between the lumina of the two
ducts is formed (cf. Munch, 1919, fig.). Whenever such a corinection is formed, the
radial duct, before coming into contact with the vertical duct, lacks a sheath layer on
the side where the connection between the two ducts occurs. In later stages of develop-
402
E. WERKER AND A. FAHN
ment such a sheath layer is usually formed. The appearance and disappearance of
sheath cells on the sides of the radial ducts, however, was also seen without any connection with vertical ducts.
I n the earlier-formed parts of the secondary body the rays are much shorter in the
longitudinal direction than in older parts. When such short rays change into fusiform
rays they may consist of epithelial cells only with no ordinary ray or sheath cells. I n
these same rays sheath and ordinary ray cells later appear.
The change of the outer end of the radial phloem duct into a vesicle-like enlargement
does not occur during the formation of the duct by the cambium (Plate 6C), but somewhat later when the radial duct has reachedsome length (cf. Thomson & Sifton, 1925).
Radial ducts formed in the first two years of cambium activity are specially abundant in
connection with the medullary rays, The phloem part of many of the radial ducts is
thus formed between the groups of primary phloem. When the enlargement of their
vesicle-like endings takes place they extend deep into the cortex. The phloem parts of
radial ducts, including their vesicle-like enlargements, are completely embedded in the
secondary phloem in later years, and their vesicular enlargements are smaller than those
formed in the first years.
Growth in width does not change the radial arrangement of the secondary xylem.
I n the phloem, however, the arrangement of the tissue is soon blurred and therefore,
with increased distance of the outer portions of the phloem ducts from the cambium,
they curve or bend at their ends (cf. Srivastava, 1963). I n those portions of the phloem
which cease to function, collapse of certain phloem cells and enlargement of other
cells occurs (Plates 8A and 1OC) (Srivastava, 1963). In this case the cells of the phloem
ducts enlarge, mainly in the tangential direction. I n the radial direction they enlarge
very little or not at all. Sometimes there is even a shrinkage in the radial direction due to
shrinkage of the whole phloem in this direction, which is a result of the collapse of
certain cells, as mentioned above (Plate 1OC).
When successive scaly phellogens are formed in the secondary phloem, they develop
also in the epithelial and sheath cells of those phloem ducts which traverse the plane of
the phellogen. Prior to the formation of the phellogen the cells of the duct enlarge and
close the duct cavity, and deformation of the fusiform ray occurs (Plates 10D and 11A,
B). The phellogen produces a few layers of phelloderm inwards. Those phelloderm
cells produced by the phellogen formed in the duct cells are narrower than the rest of
the phelloderm cells, as are also the duct cells in comparison with the phloem parenchyma. Towards the outside the phellogen produces, in the duct region as in the rest
of the phloem, sctereids and cork cells which separate the outer part of the duct from
the inner living portion.
In the secondary xylem, even in the last-formed growth ring, crystals accumulate in
some sheath cells and the cells die (Plates 1B and 7D). The cells remain unlignified but
an inner lamella is formed in them which stains red with Sudan IV, suggesting that it is
composed of suberin. The dead sheath cells, which occur in both radial and vertical
ducts, form a partial cylinder around the epithelial cells. Bailey (1909), Munch (1923)
and Bannan (1936, 1965), among others, describe a complete or partial ring of dead,
slightly lignified cells in different species of Pinus.
Munch (1923) and Bannan (1936)found in a few species of Pinus which they examined
RESIN DUCTS OF PINUS HALEPENSIS MILL.
403
that ducts of the secondaryxylem are occluded by tylosoids when the xylem is converted
to heartwood. On examination of trees of P. halepensis 54 years old such tylosoid formation in the innermost rings was not observed by us, though the cells of the ducts were
already dead.
Length of vertical ducts
The most convenient time for examination of the length of the vertical ducts of the
secondary xylem is shortly after their formation by the cambium, when they are on the
outer surface of the wood, i.e. in June or July for P. halepensis. At this time of the year,
the ducts can be quite clearly distinguished with the aid of a dissecting microscope after
peeling off the bark. In order to be able to observe them more precisely, treatment with
2 : 3 :5-triphenyl tetrazolium chloride was used or, when living material was not
available, freshly prepared formazan was applied, as suggested by Witztum & Zamski
(1969).Both these methods stain the resin in the duct cells and cavity red. The iodine
method which Reid & Watson (1966)used for measuring the length of the ducts in P.
contorta was also found suitable when used at the right season, i.e. before the commencement of cambial activity. For these measurements branches 0-5-2 cm in thickness as well as much thicker ones (nine years of age) were used. Longitudinal strips
were also removed from the external part of the wood of trunks of 12-year-old trees.
The length of ducts obtained by all these methods was 4-10 cm. It seems to us that
in the young branches the proportion of short ducts was higher. According to the results of Munch (1919), Bannan (1936) and Reid & Watson (1966), the ducts in old
trees may be longer than those we observed.
DISCUSSION
Manner of duct development
The resin ducts throughout the tissues of the plant were found to develop in a similar
manner. A group of a few initials is formed by the meristematic tissue. Between the
initials at the centre of the group an intercellular cavity is formed by the disintegration
of intercellular material. The initials usually undergo a few divisions in various directions, either prior to, during or after the formation of the duct cavity. In no part of the
plant was lysigenous development observed. Sometimes certain sheath cells become
relatively thick-walled and die and they are then sometimes crushed by the neighbouring duct cells. This might help in the expansion of the already developed lumen of the
duct, but it is not the mode of formation of its cavity. Resin ducts were found to develop
in a similar way in many other conifers (Hanes, 1927). Bannan (1936) also states
that very little evidence of lysigeny was found in any of the genera of Pinaceae
studied. Thomson & Sifton (1925) report both schizogeny and lysigeny in the development of Picea canadensis ducts. This may indicate that in conifers lysigeny may occur
in the more cystose-like ducts. Other types of ducts found in some gymnosperms,
e.g. mucilage canals of Cycadales (Johnson, 1943),are also formed schizogeneously in a
similar manner. There are, however, a few cases of pure lysigeny, as described for
Welwitschiaby Rodin (1958)and for Ginkgo by Sprecher (1909,fide Napp-Zinn, 1966).
404
E. WERKER AND A. FAHN
Size of ducts
The width of a duct, i.e. the diameter of its cavity and the number of the epithelial
cells surrounding it, varies considerably between the ducts of the primary body and
those of the secondary body. This might be determined to a great extent by wall-thickness and density of the cells of the surrounding tissue. I n the case of the primary ducts
the surrounding tissue is usualIy parenchymatous and the ducts themselves are relatively large. In the secondary xylem the vertical ducts develop between the tracheids. The
radial ducts of the secondary xylem, which are even smaller than the vertical ones, are
embedded within rays consisting of thick-walled cells on their upper and lower sides,
and the whole ray is enclosed by tracheids. The radial ducts of the phloem, which are
also embedded in rays, become larger than those of the wood with increased distance
from the cambium (cf. Alfieri & Evert, 1968, in three other species of Pinus). In the
phloem of P. halepensis the whole ray, the cells of which are thin-walled, is surrounded
by thin-walled cells which also eventually increase in size. The cyst-like outer ends of
the ducts grow larger when in contact with the cortical parenchyma and smaller when
they are wholly embedded in the phloem tissue. Thomson & Sifton (1925) mention that
growth occurs later in the life of the phloem duct, and that a reason for this might be
that there is more room for such expansion in the phloem than in the xylem. The
smallest ducts are the secondary ducts of the needles, which are situated in a dense
tissue of small tracheids.
Viability of duct cells
A partial cylinder of dead cells around the epithelial cells is found only in ducts of the
secondary xylem. In the primary body only occasional single dead cells may be found
among the sheath cells, while in the secondary phloem they are completely absent. This
layer was considered by Munch (1923) and Bannan (1936, 1965) to be an air mantle,
which prevents water from entering the osmotically active epithelial cells too rapidly.
It may be that this layer, which forms a more or less firm sheath around the epithelial
cells, plays an important role in resin secretion from the secondary xylem.
Franck (1923) denies the existence of a layer of dead cells in P. sylvestris, in contrast
to the results obtained by the above authors. Schubert (1964) claims that the death of
sheath cells occurs only after the tree is 12 years old. He explains it as a result of the
commencement of the transformation from sapwood to heartwood.
I n P. halepensisthe dead cells, unlike those described for other species, do not become
lignified. An inner lamella, apparently of suberin, is often formed in these cells.
Methods of class$cation
Our understanding of different features becomes easier when they are put in some
order. I n some classifications, however, the variations within a type exceed those
between different types. This has happened in a few methods of classification of ducts
or portions of ducts. When we tried to classify the ducts of P. halepensis according to
the existing classifications, they did not always fit.
Hanes' (1927) classification of the root-hypocotyl ducts according to the place of
termination of their upper end was not found to be useful for P. halepmis. (Fig. 1C,D).
RESIN DUCTS OF PINUS HALEPENSIS MILL.
405
Nor was any significance found in the manner of the termination of the ducts in the
needles, which was used by Zollikofer (1917) in her classification (Plate 4A). T h e same
is true of the distinction between main and accessory ducts in needles (Thomas, 1863;
Napp-Zinn, 1966) (Plate 3B).
Origin of ducts and the injluence of internal and externalfactors
I n the primary body of P. halepensis three entirely independent types of systems of
resin ducts are found : (1) the root-hypocotyl system, which includes the roots and the
hypocotyl; (2) the shoot system, which includes the stem and all its branches, both
long and short, and their juvenile leaves or scales; (3) the needle systems, separate for
each needle.
I n the first two systems the pattern and development of the vascular tissues and of the
resin ducts are closely related (Fig. 2B, C). I n the root and hypocotyl the number of
ducts corresponds to the number of protoxylem poles. I n the shoots the system of ducts
is correlated with the vascular system and both these systems are correlated with the
phyllotaxy. Moreover, the initials of the resin ducts in both root and shoot apices are in
close contact with the provascular tissue. These facts may suggest that both systems are
controlled by the same factors.
Hanes (1927) suggested that the resin ducts of conifers are an integral part of the
primary body and not a result of the influence of any external factors. T h e situation is
quite different in the secondary body, in which the duct system is much less constant.
Hanes thought that in the primary body an injury does not induce the formation of new
parenchymatous cells with accompanying resin ducts, while in the secondary body
wound parenchyma is produced and, therefore, new resin ducts as well. I n those
seedlings of P. halepensis examined by us which were found after sectioning to have
been injured previously by an unknown factor, tylosoids were formed in the mature
normal resin ducts (Plate l l C ) , but no new resin ducts were formed. Thomson &
Sifton (1925) however, remark that in Picea canadensis‘the primary tissues can be made
to produce more resin canals, but only by stimulating the tissues when active, i.e. in the
primary growing point.’ However, no details of this experiment are mentioned. I n
order to examine whether Hanes’ view is correct and the primary duct system, in contrast to the secondary system, is not determined by external factors, experiments
exposing the apical meristems of both root and shoot to different external factors should
be made. It might be that both vascular and duct systems are influenced by external
factors if applied at the right place.
T h e location of the primary duct system of each needle has no relation to that of the
vascular bundle. I n each needle there is one bifurcated vascular bundle, while the
ducts are situated in the mesophyll in a certain pattern, within which slight variations
occur. According to Flotynski (1967), however, resin tapping by incisions in the trunk
of Pinus sylvestris may induce an increase in duct formation in the needles.
At the beginning of the first growth ring in branches of adult trees there is usually a
ring of vertical resin ducts. The appearance of these ducts, although of secondary origin,
seems to be largely independent of those external factors which influence the bulk of
secondary ducts, as their location is constant and their number falls within a fixed
406
E. WERKER AND A. FAHN
range. T h e absence or scarcity of these internal secondary ducts in the root and hypocotyl suggests the possibility that their occurrence is somehow correlated with the
lateral appendages of the stem. Whether the appearance of this type of duct is determined
by phyllotaxis (i.e. the arrangement of the scales) or by the appearance of lateral branches
is difficult to decide, I n mature trees these internal ducts were found throughout the
branches, both in those regions which bear brachyblasts and in those which have scales
only. I n saplings these internal ducts are rare and do not seem to depend on the amount
of branching of the sapling. They begin to appear somewhat higher in the plant, where
the first brachyblasts are usually found. Whether the absence of both inner ducts and
brachyblasts is a juvenile characteristic of the plant and whether the appearance of the
brachyblasts influences the formation of the ducts is not known.
On the other hand, the absence or scarcity of the inner ducts in the root and hypocotyl
may be correlated with the existence of the big primary pole-ducts, which occupy in
these organs a position similar to that of the innermost secondary vertical ducts in the
stem.
Ducts sometimes appear in the first growth ring in species of genera which normally
lack resin ducts in the secondary xylem. This phenomenon may be of some value in
phylogenetic studies. I n Sequoiagigantea, for example, no resin ducts are present in the
wood except in the first growth ring, in which they are always present. On the other
hand in S. sempervirens even the resin ducts of the first growth ring appear only as a
result of wounding (Jeffrey, 1917). Jeffrey (1905,fide Bannan, 1936) also observed ducts
in the first annual ring of vigorous branches of one or two species of Abies, a genus which
generally has no ducts except when injured.
Resin ducts in the primary bundles of the branches have been described in a few
species of Pinus, Larix and Pseudotsuga (De Bary, 1877). Chattaway (1951) also describes an almost complete ring of vertical ducts within the primary wood ring of
Pinus radiata.
The exact delimitation of the boundary between primary and secondary body is a
difficult task, and therefore it is also difficult to decide about the origin of the internal
ducts of the xylem. However, when the origin of these inner ducts of P. halepensis was
examined, it could be seen that they are not produced by the apical meristem but by
the newly formed cambium. This appears to apply also to P. banksiana, as seen in Fig. 1
drawn by Kirsch (1911).
These inner ducts of the first growth ring are a sort of transition from one type of
duct, which is apparently influenced only by internal factors, to another which might
be influenced by both internal and external factors. This feature might be related to
Bannan’s (1936) conclusion that in individual species the resin-secreting tissue resulting
from injury increases from the seedling to the adult stage and from the inner to the
outer wood in both seedling and adult.
The connections between resin ducts formed by different meristems
The problem of the connection between the ducts of needles and those of the brachyblast axis seems now to be clear for P. halepensis. T h e primary ducts of the needle are
not connected with any of the ducts of the brachyblast axis, while the very short
RESIN DUCTS OF PINUS HALEPENSIS MILL.
407
secondary ducts are connected with the secondary ducts of the axis. I n some needles,
however, the upper end of the short ducts may be of primary origin. T h e secondary
ducts of the needles seen by us occupy a minute portion of the leaf, much smaller than
that described for this species by Diaparidze (1937).
Mirov (1967) and Zavarin’s (1968) results of the analysis of the resin of needles show
that its composition differs from that of the resin of other organs. A difference between
the resin of the primary needle ducts and the resin of the cortex of branches would be
difficult to explain if there were connections between the ducts of the two tissues. This
argument is valid if there is streaming of resin in the intact plant, at least if the streaming
were caused by gravity.
Connections between primary and secondary ducts have been found only in the root
and hypocotyl, between primary vertical ducts and secondary radial ducts and
occasionally in the vein ducts of the needles. This observation differs from the findings
of Thomson & Sifton (1925) for Picea canadensis, according to whom there are no connections between the primary and secondary ducts throughout the whole plant body.
It would be of interest to analyse the composition of the resin in both the primary
and secondary ducts of the root and hypocotyl and, if differences are found, to check
whether a mixture of the two types of resin occurs where the tissues join, From the
last type of examination it may be possible to learn whether some streaming of resin
occurs in the intact plant (cf. Wilson et al., 1963).
The spatial structure of the system of secondary resin ducts
We have found that in Pinus halepensis there are connections between radial and
vertical ducts situated on the same radial plane, though they do not occur in every case
in which a vertical and radial duct come close together. Thomson & Sifton (1925) state
that connections of this type occur only in old roots but not in the branches of Picea
canadensis. Munch (1919), on the other hand, has found numerous such connections in
the species of pines which he had examined. Further study of conifers might perhaps
reveal some phylogenetic significance for this phenomenon. T h e inner end of the
radial ducts is always connected to a vertical duct.
We found no connections between vertical ducts situated on different radial planes,
except for the innermost ducts of the first growth ring and occasional splitting and fusion of the same duct. Thus it can be concluded that the ducts do not constitute a threedimensional anastomosing network, as recorded by some authors for other species
(Mayr, 1884; Jeffrey, 1905, jide Bannan, 1936; Munch, 1919), but form many twodimensional networks each situated in one radial plane. These networks are scattered in
the secondary body throughout the plant, i.e. in the roots, stems and needles.
Although each radial duct is continuous from the xylem into the phloem, no cavity of
the duct has been observed in cambial region. This fact was also stated by Mayr (1884)
and Thomson & Sifton (1925) for Picea and Larix. The lack of a cavity in the cambium
means that the resin in the secondary xylem is separated from that in the secondary
phloem.
Location of the stimulus for production of secondary ducts
I n the secondary xylem every radial duct is connected at its origin to a vertical duct
(Mayr, 1884; Hart, 1916; Thomson & Sifton, 1925; Chattaway, 1951), and from this
408
E. WERKER AND A. FAHN
fact arose various interpretations as to the location of the initial stimulus for duct formation. Hart (1916) thought that, after the stimulus affects the fusiform initials, the ordinary function of the cambium is interrupted for a time. It produces a vertical duct and
then, when the stimulus ceases to be effective, it resumes the production of tracheids.
Sometimes the stimulus continues and the tissue resulting from the transformation of
ray tracheids assists in forming the horizontal ducts. Kirsch (191l),on the other hand,
thought that the resin-secreting tissue in the wood results from the proliferation of the
xylem rays both vertically and tangentially. Thomson & Sifton (1925) thought that the
vertical ducts arose earlier than the radial ones. Chattaway (1951) rightly stated that the
vertical ducts are clearly a result of some stimulus that has permanently affected the
daughter cells of the fusiform initials and not the fusiform initials themselves, while the
radial ducts are a result of a permanent change which has occurred in the ray initials.
Chattaway’s conclusion was, therefore, that ‘a horizontal canal appears to be formed
when a ray initial occurs in the area of the cambium that is stimulated to form a vertical
canal.’
Before discussing this problem further, a few facts which we observed on Pinus
halepensis should be mentioned. Not every simple ray that comes in contact with a
vertical duct turns into a duct bearing a fusiform ray. I n young ducts of the secondary
body the distance of the outer ends of the radial phloem ducts from the cambial initials
was seen to be approximately the same as that from the cambium to the inner side of the
vertical duct, which is continuous with the radial xylem duct, although usually much
less phloem than xylem is produced by the cambium (Plate 7B). This might suggest that
the formation of ducts on the phloem side precedes the formation of ducts on the xylem
side. On one occasion the formation of a phloem duct before the formation of the vertical
and of radial ducts inside the cambium was observed. As seen in tangential and radial
longitudinal sections, at the place of fusion of the radial and vertical duct cavities, the
epithelial cells of the radial resin ducts are continuous with the epithelial cells of the
vertical duct.
From these facts the best working hypothesis appears to be that the stimulus for the
formation of ducts first affects the ray initials. Therefore, in branches the beginning of
phloem ray ducts may be seen before a vertical duct can be detected on the xylem side.
The observations made by us and by Chattaway (1951) that the origin of the ray ducts
occurs in the region of initials, whereas the origin of the vertical ducts occurs in the
xylem mother cells, gives further support to this view. Our hypothesis is that the stimulus which affects the ray initials is conducted horizontally by the ray inwards, spreads
vertically for a certain distance in the fusiform xylem mother cells and causes them to
change into duct cells. This hypothesis should, of course, be tested expcrimentally.
It should be mentioned that in young roots and in the hypocotyl early-formed radial
resin ducts of secondary origin may start from primary vertical ducts that are produced much earlier. However, these vertical ducts seem to enlarge radially with
the development of the radial ducts.
ACKNOWLEDGEMENTS
This investigation has been supported in part by grant No. FG-Is-209 madc by the
United States Department of Agriculture under P.L. 480 to A.F.
RESIN DUCTS OF P I N U S H A L E P E N S I S M I L L .
409
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EXPLANATION O F PLATES
PLATE1
A. Cross-section of a vertical resin duct of the secondary xylem ( x 480).
B. Longitudinal section of a vertical resin duct of the secondary xylem, showing epithelial cells (ep) and
dead sheath cells filled with crystals (cr). T h e sectioned material was embedded in Epon after fixation
with glutaraldehyde and osmic acid (x 990).
C. Cross-section of a young root showing a primary resin duct situated between the arms of a protoxylem
group (px). dc, duct cavity ( x 560).
PLATE2
Cross-sections of a young root showing different stages in duct (d) development ( x 320).
A. Duct initials form a rosette.
B, C . Duct cavity has been formed and sheath cells have undergone tangential divisions.
PLATE3
A. Four ducts of a tetrarch root. Secondary thickening is seen between the ducts. A cambium has been
formed in the outer sheath cells of some of the ducts ( x 47).
B. Cross-section of a needle showing two lateral and two abaxial ducts in the mesophyll ( x 145).
C. Longitudinal section of a young needle showing a short resin duct at the tip of the needle ( x 49).
dc, Duct cavity.
PLATE4
A. Part of Plate 3C showing the lower end of the duct ( x 495). dc, Duct cavity.
B-D. Portions of successive cross-sections of a young needle near its base, showing three stages in
development of a lateral duct ( x 505). di, Duct initials.
Hot.
r. Lim. SOC.,62 (1969)
E. WERKER
AND
A. FAHN
Plate 1
(Facing p . 410)
Rot. J
'. L i / i i z . Snc., 62 (1969)
E. WBRKER
AND
A . FAHN
Plate 2
Not.
7. L 7 m .
Soc.,
E WEKKEK
62 (1969)
AND
A. FAHlV
I’lwte 3
Hot. . .'7. U11n. Sot., 62 11Yti9)
E. WEHKER ,......._ll A. FAH~·
Plate 4
Rot. J. Linn.
SOC.,62 (1969)
E. WERKER
AND
A. FAHN
Plate 5
I?. WERKER
AND
A. FAHN
Hot. .?. I,in77.
E. WERKER
soc., 62 (1969)
~ N I J A.
FAHN
Plate 7
Rot. J.
hr71.
Soc., 62 (1969)
E. WEIIKER
ANr)
A. PAHN
I’lwte 8
/ j o t . .J’. Li7rn. Sor.., 62 (1969)
E. WERKER
AND
A. FAHN
Hot. J. Linn . Soc., 62 (1 969)
E. WEHKElt
AN n
A . FAHN
l'latf \()
Bot. J. f,i/?u.Soc., 62 (1969)
I<.WERICER
AND
A. FAHN
Plate 1 1
RESIN DUCTS OF PINUS HALEPENSIS MILL.
411
PLATE
5
A. Cross-section of the vascular tissue of the basal part of a needle showing crushed primary xylem (cx)
and a hole (h) left by torn primary xylem (x 590).
B,C . Cross-sections showing the position of secondary resin duct (d) in the xylem of a brachyblast and
of a needle ( X 600); B, in the brachyblast; C, in the basal part of a needle. c, Cambial zone.
PLATE6
Portions of cross-sections of a young branch at the beginning of the formation of the secondary vascular
tissue (x 600).
A,B. Two stages of duct (d) formation. c, Cambial zone.
C. An early stage of development of radial-vertical duct complex. vd, Vertical duct; pd, phloem duct;
c, cambial zone.
PLATE
7
A. Cross-section of a young branch showing the primary cortical ducts (cd) and the innermost ducts of
the secondary xylem (xd) ( x 40).
B. Portion of a cross-section of a young stem showing a radial duct (rd) connected to a vertical duct (vd)
(x 110). c, Cambial zone.
C , D. Successive sections of a radial duct (rd) adjacent to a vertical duct (vd) (x 520) : C, in the cambial
zone, the radial duct has no cavity; D, in the xylem, the cavity of the radial duct is open on the side of
the vertical duct, but no connection is formed between the two cavities.
PLATE
8
A. Cross-section of secondary phloem showing the outer portion of a radial duct. A simple ray is continuous with the duct ( x 148). cp, Crushed phloem cells.
B. Tangential longitudinal section of secondary xylem showing a simple ray (sr) locally splitting a vertical
duct (vd) into two ducts. Other simple rays pass between the cells of the vertical duct and not through
its cavity. A fusiform ray (fr) adjacent to the vertical duct is also visible; there is no connection between
the two (x 150).
C . Cross-section of secondary xylem showing two branches of a vertical duct (vd) between which a
fusiform ray (fr) is situated ( x 145).
PLATE
9
A,B. Tangential langitudinal sections of secondary xylem showing radial resin ducts ( x 600) : A, sheath
cells are present only on one side of the duct; B, sheath cells are present on both sides of the duct.
C. Portion of a cross-section of a young branch showing an early stage of development of a radial duct of
the phloem (pd) opposite a pith ray (pr). No xylem duct is visible to the inside ( X 590). c, Cambial zone;
x, secondary xylem.
PLATE10
A,B. Portions of tangential longitudinal sections of wood showing a connection between a vertical (vd)
and a radial (rd) duct: A x 150, B x 590.
C, D. Resin ducts of the secondary phloem: C , cross-section showing that the duct cells in the active
phloem (ap) are flat and elongated radially compared with the duct cells in the outer inactive phloem
(x 145) ; D, the epithelial cells of the duct in the region of the peridenn occlude the duct cavity ( X 550).
cp, Crushed phloem cells; dc, duct cavity.
PLATE11
A,B.Successive tangential longitudinal sections of the secondary phloem in the periderm region. The
epithelial cells occlude the duct cavity (x 150). d, Duct cells.
C. Portion of a cross-section of the cortex of a wounded branch showing the tylosoids in a cortical duct
(d) ( x 140). w, Wound.
29