American Journal of Botany 92(7): 1077–1084. 2005.

INTER- AND INTRASPECIFIC STRUCTURAL VARIATIONS

AMONG INTERVASCULAR PIT MEMBRANES,
AS REVEALED BY FIELD-EMISSION
SCANNING ELECTRON MICROSCOPY1

YUZOU SANO2
Laboratory of Wood Biology, Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589 Japan

The structure of the intervascular pit membranes of four dicotyledonous species (Salix sachalinensis, Betula platyphylla var. japonica,
Acer mono, and Fraxinus mandshurica var. japonica) was examined by field-emission scanning electron microscopy. The intervascular
pit membranes of F. mandshurica var. japonica had thin surface layers and a dense middle layer, while no similar middle layer was
detectable in the other three species. In F. mandshurica var. japonica, the entire area of each pit membrane was densely covered with
microfibrils. In the other three species, by contrast, openings were found in the pit membranes. In some of the intervascular pit
membranes of S. sachalinensis, B. platyphylla var. japonica, and A. mono, microfibrils were sparsely interwoven in small areas of the
pit membranes and openings of up to several hundred nanometers in diameter were present in such regions. These porous regions
tended to be located in peripheral areas of pit membranes. In S. sachalinensis and B. platyphylla var. japonica, ethanol-soluble extracts,
whose chemical nature and function remain unknown, were heavily distributed over the intervascular pit membranes. Our observations
suggest that the structure of intervascular pit membranes is more complicated than has previously been acknowledged.

Key words: Acer mono; Betula platyphylla var. japonica; field-emission scanning electron microscopy; Fraxinus mandshurica
var. japonica; intervascular pit; pit membrane; Salix sachalinensis.

The xylem of most dicotyledons includes specialized water-
conducting tissues called vessels. Each vessel is composed of
a number of vessel elements that are connected, via perfora-
tion, with each other. The end of one vessel generally makes
contact with another vessel but the junction is not perforated.
Individual vessels are partitioned by the pit membranes of in-
tervascular pit pairs. The vessels do not consistently run in
parallel, and they frequently exchange positions tangentially.
When two vessels cross and touch during the exchange of
positions, intervascular pit pairs are also generally found in
the common walls of the adjacent vessels (Panshin and de
Zeeuw, 1980; Dickison, 2000; Tyree and Zimmermann, 2002).
The basic structure of intervascular pit membranes in di-
cotyledons is not yet fully understood. Early studies by trans-
mission electron microscopy suggested consistently that inter-
vascular pit membranes are uniform structures with a primary
wall texture, without any distinction between torus and margo,
consisting of several layers or lamellae and lacking visible
openings that can be detected by transmission electron mi-
croscopy (Côté, 1958; Harada et al., 1958; Schmid, 1965;
Schmid and Machado, 1968). By contrast, later studies indi-
cated that a torus is present in the intervascular pit membranes
of some taxonomic groups (e.g., Ohtani and Ishida, 1978;
Wheeler, 1983; Dute and Rushing, 1988; Dute et al., 1992;
Jansen et al., 2004b), and openings were visualized by electron
microscopy in the intervascular pit membranes of several spe-
cies (e.g., Bonner and Thomas, 1972; Wheeler, 1982; Sperry
and Tyree, 1988; Dute et al., 1992; Sano, 2004). However, to
date, information about structural variations remains limited
and fragmentary for a large number of species and types of
pit, and descriptions of the structures of intervascular pit mem-
1
Manuscript received 11 October 2004; revision accepted 24 March 2005.
This study was supported by Grants-in-Aid for Scientific Research from
the Ministry of Education, Culture, Sports, Science and Technology, Japan
(nos. 12760112 and 16580127).
2
E-mail: pirika@for.agr.hokudai.ac.jp
1077
branes in the literature are very brief (e.g., Panshin and de
Zeeuw, 1980; Tsoumis, 1990; Dickison, 2000; Butterfield,
2003).
The functions of intervascular pit membranes also remain
to be clarified (Zwieniecki et al., 2001; Choat et al., 2003;
Jansen et al., 2004a, b). Since the ‘‘air-seeding’’ model was
proposed by Zimmermann (1983), particular attention has
been paid to the porosity of intervascular pit membranes. Ac-
cording to Zimmermann’s model, the susceptibility to the pro-
gression of water stress-induced cavitation, from one cavitated
conduit to the adjacent water-filled conduit, depends upon the
difference in pressure and the maximum size of the micropores
in the pit membranes that are located between the two con-
duits. Attempts have been made to confirm the relationship
between the ‘‘air-seeding’’ pressure that is required to advance
the cavitation from a cavitated vessel to the adjacent water-
filled vessel and the size of the micropores that are present in
the intervascular pit membranes. However, the results of such
attempts are inconsistent (e.g., Sperry and Tyree, 1988; Jar-
beau et al., 1995; Choat et al., 2003). It is now necessary to
examine the fine structure of intervascular pit membranes in
greater detail if we are to understand the mechanisms of water
transport in living trees.
The purpose of the present study was to examine the fine
structure of the intervascular pit membranes of four dicotyle-
donous species, namely, Salix sachalinensis Fr. Schmidt, Bet-
ula platyphylla var. japonica Hara, Acer mono Maximowicz,
and Fraxinus mandshurica Rupr. var. japonica Maximowicz.
My colleagues and I used S. sachalinensis, B. platyphylla var.
japonica, and F. mandshurica var. japonica in previously pub-
lished studies of the seasonal progression of cavitation of ves-
sels (Utsumi et al., 1996, 1998, 1999). Acer is a commercially
important genus and is physiologically interesting because of
the bleeding phenomenon that occurs in early spring. There-
fore, for the present study, I selected A. mono and the other
three species to examine structural variations in intervascular
1078 AMERICAN JOURNAL
TABLE 1. Sources of wood samples.
Sample trees DBH (cm) Sitea Seasonb
Salix sachalinensis A 25 1 1
B 17 1 1
Betula platyphylla var. japonica A 18 2 2
B 20 2 2
Acer mono 25 2 1
Fraxinus mandshurica var. japonica A 45 3 1
B 15 3 1
a 1 5 Government Forest in Sapporo; 2 5 Tomakomai Experimental
Forest of Hokkaido University; 3 5 Sapporo Experimental Nursery of
Hokkaido University.
b Season of sample collection: 1 5 early autumn soon after the for-
mation of current-year xylem had ceased; 2 5 late spring when leaves
were expanding.
pit membranes by field-emission scanning electron micro-
scopy.
MATERIALS AND METHODS
Materials—Samples of outer sapwood (longitudinal, radial, and tangential
dimensions were 10, 2, and 5 cm, respectively) were excised at breast height
with a chisel from sample trees (Table 1). Two to four samples were collected
from each tree. Half of the samples were put into 30% ethanol and stored at
room temperature. The remaining samples were immersed in liquid nitrogen,
brought to the laboratory, and stored at 2808C.
Field-emission scanning electron microscopy—Samples were prepared as
described by Sano (2004). In brief, samples were cut into small cubes (5 3
5 3 5 mm3) that included the outermost annual ring. The blocks cut from
frozen samples were freeze-dried in a freeze-drying apparatus at approxi-
mately 08C and 10 Pa. The blocks cut from samples that had been stored in
30% ethanol were air-dried after dehydration in absolute ethanol. All the dried
blocks were split along a tangential plane in the inner, middle, or outer layer
of the outermost annual ring, and then the specimens were affixed to alumi-
num stubs with electron-conductive carbon paste. They were coated with plat-
inum by vacuum evaporation and examined with a field-emission scanning
electron microscope (FE-SEM; JSM-6301F, JEOL, Tokyo, Japan) at an ac-
celerating voltage of 2.5 kV. More than 500 undamaged pit membranes in
more than 20 intervessel faces were examined for each species.
For measurements of diameters of intervascular pit membranes, 50 pit
membranes were selected at random on scanning electron micrographs of
samples that had been split tangentially at the middle layer of the outermost
annual ring, at a magnification of 4000–80003. Longitudinal and tangential
diameters of pit membranes were measured on these micrographs. In the case
of Fraxinus mandshurica var. japonica (ring-porous wood), diameters were
also measured at the earlywood.
RESULTS
Diameters of intervascular pit membranes—The diameters
of intervascular pit membranes were largest in Salix sachali-
nensis (Table 2; Fig. 1) and smallest in Betula platyphylla var.
japonica (Table 2; Fig. 2). The diameters of intervascular pit
membranes in Acer mono were slightly smaller than those in
S. sachalinensis (Table 2). In Fraxinus mandshurica var. ja-
ponica, diameters differed between inter-earlywood vessel pits
and inter-latewood vessel pits, being larger in the earlywood
(Table 2).
Organization of intervascular pit membranes—The orga-
nization of pit membranes differed between F. mandshurica
var. japonica and the other three species examined. In F.
OF BOTANY [Vol. 92
TABLE 2. Diameters of intervascular pit membranes. Each value (mm)
is the mean of results from 50 pits. Standard deviations are in
parentheses.
Middle layer of annual ring Earlywood
Species Longitudinal Tangential Longitudinal Tangential
Salix sachalinensis 6.9 (0.64) 7.7 (1.09) —
Betula platyphylla
var. japonica 2.3 (0.24) 2.6 (0.30) —
Acer mono 6.9 (0.73) 7.6 (0.69) —
Fraxinus mandshurica
var. japonica 3.9 (0.17) 4.2 (0.21) 4.9 (0.43) 5.8 (0.44)
mandshurica var. japonica, three distinct layers were detect-
able. On surface views, pit membranes appeared to be densely
covered with randomly oriented microfibrils (Fig. 3). In a re-
gion from which the superficial layer had peeled off, there was
a dense layer of parallel fibrils (Fig. 3), indicating that the pit
membranes consisted, at least, of outer thin layers of randomly
oriented microfibrils with a dense middle layer between them.
In the other three species, by contrast, no distinct middle layer
was visible in areas from which the superficial layer of the pit
membranes had been partly or entirely lost, and another su-
perficial layer that was faced to the adjacent vessel lumen often
appeared (Fig. 4).
There were fine curly fibrils in the intervascular pit mem-
branes of large earlywood vessels of F. mandshurica var. ja-
ponica (Fig. 3, arrow). The curly fibrils were not only present
on the surface of the pit membranes but also penetrated the
middle layer of the pit membranes (Fig. 3, arrow). There were
no similar curly fibrils in the intervascular pit membranes be-
tween the small latewood vessels of F. mandshurica var. ja-
ponica or in the other three species.
Porosity of intervascular pit membranes—The porosity of
intervascular pit membranes differed among species. In F.
mandshurica var. japonica, the surface layer of each pit mem-
brane was densely and evenly covered with randomly oriented
microfibrils. Although narrow inter-microfibrilar spaces were
noted in the thin surface layers, no such spaces were apparent
in the middle layer (Fig. 3).
In the other three species, the porosity varied among indi-
vidual pit membranes. In B. platyphylla var. japonica, many
pit membranes were densely and evenly packed with randomly
oriented microfibrils (Fig. 5). However, there were easily vis-
ible openings of up to 300 nm in diameter in some of the pit
membranes (Figs. 2 and 5). Most of such openings were less
than 150 nm in diameter. Openings more than 150 nm in di-
ameter were found in a few pit membranes of a few intervessel
faces. The openings tended to be located near the periphery
of the respective pit membranes (Figs. 2 and 5). The frequency
of occurrence of such porous pit membranes was approxi-
mately 5%.
The intervascular pit membranes of S. sachalinensis were
generally porous, with openings of up to 100 nm in diameter
over the entire area of most pit membranes (Figs. 1 and 6). In
some of the pit membranes, microfibrils were sparsely inter-
woven in small areas of the pit membranes and openings of
up to 700 nm in diameter were present in such regions (Fig.
1, arrow). Most of such openings were less than 300 nm in
July 2005] SANO—STRUCTURAL VARIATIONS AMONG PIT MEMBRANES 1079

Figs. 1–4. Intervascular pit membranes. 1. Salix sachalinensis. The arrows indicate areas in which microfibrils are sparse and larger openings of up to
several hundred nanometers in diameter are present. 2. Betula platyphylla var. japonica. The arrows indicate the same features as in Fig. 1. 3. Part of a pit
membrane between large earlywood vessel elements of Fraxinus mandshurica var. japonica. Arrows indicate fine curly fibrils. The asterisk indicates a region
from which the surface layer of the pit membrane has been lost. 4. Part of a pit membrane of Salix sachalinensis. The asterisk indicates the same type of region
as in Fig. 3.
1080 AMERICAN JOURNAL OF BOTANY [Vol. 92

Figs. 5–8. Intervascular pit membranes. 5. Betula platyphylla var. japonica. 6. Salix sachalinensis. An example of a pit membrane in which microfibrils are
sparser in the central region than at the periphery. 7. Acer mono. The arrows indicate areas in which microfibrils are sparse and there are openings of up to
several hundred nanometers in diameter. 8. Part of a pit membrane of Acer mono.
July 2005] SANO—STRUCTURAL VARIATIONS AMONG PIT MEMBRANES
diameter. Openings more than 300 nm in diameter were found
in a few pit membranes of a few intervessel faces. These po-
rous regions tended to be located near the periphery of the
respective pit membranes (Fig. 1, arrow) although the central
region was occasionally more porous than the periphery (Fig.
6). It was difficult to define such localized porous areas clearly
since there was a continuous gradient with respect to changes
in the density of distribution of microfibrils (Fig. 6). The fre-
quency of pit membranes with typical localized porous areas,
which could be detected easily at a magnification of 40003,
was approximately 10%.
The porosity of intervascular pit membranes in A. mono was
intermediate between that in S. sachalinensis and that in B.
platyphylla var. japonica. In approximately 20% of the pit
membranes in A. mono, microfibrils were sparsely interwoven
in small areas and there were openings of up to 500 nm in
diameter in such regions (Figs. 7 and 8). Most of such open-
ings were less than 200 nm in diameter. Openings more than
200 nm in diameter were found in a few pit membranes of a
few intervessel faces. The microfibrils were more densely
packed in the remaining regions of intervascular pit mem-
branes that had such localized porous areas (Fig. 8) than those
in S. sachalinensis.
Presence of ethanol-extractable material—In freeze-dried
specimens of S. sachalinensis and B. platyphylla var. japonica,
intervascular pit membranes were covered by a conspicuous
coating (Figs. 9 and 10). The extent of the coating varied
among individual pits. The texture of microfibrils was detect-
able in cases of limited deposition (Fig. 10) but not in cases
of heavy deposition (Fig. 9). This type of coating was not
apparent in air-dried specimens that had been dehydrated in
ethanol prior to drying (Figs. 1, 2, 4–6). Indeed, the above-
described observations of the appearance of the pit membranes
of these two species (Figs. 1, 2, 4–6) were based on exami-
nations of air-dried specimens after dehydration in ethanol.
The ethanol-soluble material was also present in the lumina
of vessel elements and ray parenchyma (Figs. 11 and 12). The
material not only covered the intrinsic surfaces of cell walls,
but also partly or completely covered the fractured plane of
secondary walls, which appeared upon splitting of samples
(Figs. 9–11, arrows).
No similar differences were detected between freeze-dried
and air-dried specimens of A. mono and F. mandshurica var.
japonica, indicating that a similar ethanol-soluble coating was
absent in both of these species.
Aspirated pit membranes—Aspirated pit membranes were
often found in S. sachalinensis and A. mono (Fig. 13), but not
in the other two species. These aspirated pit membranes were
often torn (Fig. 13, arrow).
DISCUSSION
The present study revealed not only interspecific differences
in the porosity of intervascular pit membranes, but also intra-
specific differences in the porosity of the pit membranes. In
some of the pit membranes of Salix sachalinensis, Betula pla-
typhylla var. japonica, and Acer mono, microfibrils formed a
sparse network in a small area of the entire pit membrane, and
larger openings of up to several hundred nanometers in di-
ameter were present in such regions. There are no previous
reports, to our knowledge, of the existence and frequency of
1081
such pit membranes with small areas of sparse, interwoven
microfibrils. However, some electron-microscopic studies have
revealed porous intervascular pit membranes in Liriodendron
(Bonner and Thomas, 1972), Acer (Wheeler, 1982; Sperry and
Tyree, 1988), and Daphne (Dute et al., 1992).
Scanning electron microscopy is a useful method for ex-
amining and characterizing such structural variations. The po-
rosity of intervascular pit membranes has been estimated by
perfusion tests with minute particles of known size (e.g., Jar-
beau et al., 1995; Shane et al., 2000; Choat et al., 2003). This
indirect method allows the quantitative demonstration of the
sizes of micropores. However, it is difficult to demonstrate
variations in the pore sizes and in their uneven distribution
within an individual intervascular pit membrane using this
technique. Thus, visualization by electron microscopy seems
to be the method of choice for studies of the porosity of in-
tervascular pit membranes and for efforts to better understand
their true nature.
Intraspecific variations in the porosity of intervascular pit
membranes are important when we discuss the validity of the
‘‘air-seeding’’ model (Zimmermann, 1983; Tyree and Zim-
merman, 2002). As stated in the introduction of the present
paper, attempts have been made to examine the relationship
between the air-seeding pressure and the sizes of micropores
in intervascular pit membranes. In some studies, the diameter
of pores in intervascular pit membranes that was calculated
from the air-seeding pressure, which was estimated from a
determination of the loss of hydraulic conductivity, corre-
sponded to the measured diameter (e.g., Sperry and Tyree,
1988; Jarbeau et al., 1995). By contrast, Choat et al. (2003)
reported that, in two drought-deciduous and two evergreen
species in a seasonally dry rainforest, the diameters of pores
in intervascular pit membranes, as measured by scanning elec-
tron microscopy, were much smaller than the diameters esti-
mated from the air-seeding pressure. Choat et al. (2003) men-
tioned, as one possible explanation for this discrepancy, that
larger pores were indeed present in the intervascular pit mem-
branes that they examined but that these pores were too rare
to be detected by electron microscopy. After a subsequent
analysis, Choat et al. (2004) confirmed that this explanation
was more plausible than other possible explanations. In the
present study, the large openings found in some of the inter-
vascular pit membranes were more frequent than predicted by
Choat et al. (2003, 2004). It is likely that the frequency of pit
membranes with small loose zones differs among species. Al-
though Choat et al. (2003) did not find any such pit mem-
branes among 30–50 pit membranes, such porous pit mem-
branes might be found in the four species that they studied if
more pit membranes had been examined. The studies by Choat
et al. (2003, 2004) and the present study suggest that much
higher numbers of pit membranes need to be examined in the
future for an accurate characterization of the porosity of in-
tervascular pit membranes.
The present study also highlighted differences in the layered
structure of intervascular pit membranes among species. Var-
iations in the layered structure of intervascular pit membranes
have not previously been fully appreciated. Early reports of
the fine structure of the intervascular pit membranes of several
species stated consistently that pit membranes are uniform
structures with a primary wall texture, without a distinctive
torus and margo and that they consisted of several layers or
lamellae (Côté, 1958; Harada et al., 1958; Schmid, 1965;
Schmid and Machado, 1968). Interspecific differences in the
1082 AMERICAN JOURNAL OF BOTANY [Vol. 92

Figs. 9–12. Field-emission scanning electron micrographs of sapwood samples. Figs. 9, 10. Intervascular pit membranes of S. sachalinensis in freeze-dried
samples that had not been soaked in ethanol. Arrows indicate fractured plane in the secondary walls of vessel elements. 9. Example of a thick coating of
ethanol-soluble material on pit membranes. 10. Example of a thin coating of such material. The microfibrils are partially visible. Figs. 11, 12. Ray parenchyma
of Betula platyphylla var. japonica. 11. Freeze-dried sample that had not been soaked in ethanol. Arrows indicate ethanol-soluble material that might have
spread from the lumina of ray parenchyma after metal coating. 12. Air-dried sample that had been immersed in ethanol prior to drying.
July 2005] SANO—STRUCTURAL VARIATIONS AMONG PIT MEMBRANES
Fig. 13. Part of an aspirated intervascular pit membrane of Acer mono.
Arrows indicate areas from which the pit membrane is missing, and the pit-
chamber-side of pit border is visible.
layered structure have not been fully considered, and more
attention was focused on the occurrence and structure of torus-
bearing pit membranes (e.g., Ohtani and Ishida, 1978; Wheel-
er, 1983; Dute and Rushing, 1988; Dute et al., 1992; Jansen
et al., 2004b). Information on the layered structure of inter-
vascular pit membranes remains limited. The presence of a
middle layer probably influences both the porosity and the
rigidity of pit membranes. It is very likely that the properties
of pit membranes, such as the tendency toward pit aspiration,
differ between pit membranes with a dense middle layer and
those without a middle layer. Thus, further investigations are
necessary to characterize the layered structure if we are to
develop a better understanding of the structure and function
of intervascular pit membranes.
We also need to examine the nature and function of the
ethanol-soluble material on some of the intervascular pit mem-
branes. Such material is also present on the intervascular pit
membranes of B. platyphylla var. japonica (Sano, 2004). In
the present study, a similar material was also noted on those
of S. sachalinensis. The material might also be present in
many more species. It has been reported that intervascular pit
membranes are heavily covered by deposits in heartwood
(Bonner and Thomas, 1972; Kininmouth, 1972; Thomas,
1976; Wheeler, 1981, 1982, 1983; Wheeler and Thomas, 1982;
Sano and Fukazawa, 1994). However, the chemical compo-
nents of the ethanol-soluble material found in the outer sap-
1083
wood probably differ from those of the materials that are sec-
ondarily deposited during heartwood formation cannot be re-
moved by organic solvents.
Interesting hypotheses have recently been proposed with re-
spect to functions of the lipids in vessel lumina and the cell
wall matrix in intervascular pit membranes. Schneider et al.
(1999) found a lipid layer that covered the vessel side of ves-
sel-to-parenchyma pit pairs in the resurrection plant Myro-
thamnus flabellifolia. They suggested that such a lipid layer
might play a role in preventing loss of water from the proto-
plast of the parenchyma under severe drought. By contrast,
Zwieniecki et al. (2001) demonstrated that the flow rate
through stem segments was reversibly enhanced by switching
the perfusion medium from deionized water to dissociating
solutes, such as KCl, NaCl, and KNO3. They suggested that
such reversible enhancement of water flow might have been
caused by the reversible shrinkage of the pectin that covered
the cellulose microfibrils in the intervascular pit membranes.
The ethanol-soluble material might also serve some function
that is associated with water conduction, although the solubil-
ities of lipid and pectin in organic solvents are quite different
from that of the ethanol-soluble material found in the present
study (Wagner et al., 2000). The ethanol-soluble material
might also play an important role in the flow of water in B.
platyphylla var. japonica and S. sachalinensis. Further studies
are required to clarify the nature and function of such extra-
neous or matrix material in the flow of water in living trees.
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