Plant, Cell and Environment (1982) 5, 455-460.
OPINION SECTION
The adaptive significance of amphistomatic leaves
KEITH A. MOTT,* ARTHUR C. GIBSON f & JAMES W. O'LEARY* *Department of Cellular
and Developmental Biology, University of Arizona, Tucson, Arizona 85721, and fDepartment of
Biology, University of California, Los Angeles, California 90024, U.S.A.
Received 6 April 1982; accepted for publication 21 April 1982
Abstract. A clear correlation between the presence of
stomata on both surfaces and factors such as habitat,
growth form, and physiology has yet to emerge in the
literature. However, certain loose trends with these
factors are evident, and these are reviewed along with
evidence for hypostomaty as the primitive form. It is
proposed that the effect of developing stomata on
the upper surface as well as the lower is to increase
maximum leaf conductance to CO2. Plants with a
high photosynthetic capacity, living in full-sun
environments, and experiencing rapidly fluctuating or
continuously available soil water (as opposed to
seasonal or long-term soil water depletion), are
identified as deriving an adaptive advantage from a
high maximum leaf conductance. The correlation
between groups of plants fitting the above conditions
and those noted to be amphistomatic is remarkable.
Plants not fitting the conditions are found to be
largely hypostomatic.
Key-words: amphistomatic; stomata; conductance; transpiration;
photosynthesis.
Gas exchange of most vascular plants is controlled by
stomata, which can occur on any aerial portion of a
plant but are usually most dense on leaves. Early
surveys of stomatal distributions (Kohne, 1899;
Salisbury, 1927; Wood, 1934, Metcalfe & Chalk,
1950) demonstrated that a significant number of plant
species have amphistomatic leaves, i.e. they possess
stomata on the adaxial (upper) as well as the abaxial
surface.
The amount of stomatal opening is one of the
principal factors determining rates of CO2
assimilation and water and heat loss; therefore, the
distributional pattern of stomata and the amount of
stomatal area could strongly influence the ecological
and evolutionary success of a species in a particular
habitat. Unfortunately, although many investigators
have made remarks on stomatal distributions, sizes,
and densities or frequencies, few have discussed
Correspondence: Keith A. Mott, Department of Cellular and
Developmental Biology, University of Arizona, Tucson, Arizona
85721, U.S.A.
0140-7791/82/1200-0455 $02.00
D1982 Blackwell Scientific Publications
patterns of plants with amphistomatic versus
hypostomatic leaves in relation to their preferred or
natural habitats.
Occurrence of amphistomaty 6
Amphistomaty is not coupled directly to plant life
form, annual or perennial, tree or herb, because
adaxial stomata are present in representatives of each,
especially in dry habitats (Wood, 1934). Nor is there a
correlation between water availability and
amphistomaty (Parkhurst, 1978). In summarizing the
distribution of amphistomaty in over 130 families of
dicotyledons, Metcalfe & Chalk (1950) noted the
presence of adaxial stomata in plants with either
vertically oriented leaves or isolateral and centric
organization of palisade mesophyll or both. Many
moncotyledons are also amphistomatic, especially
those with vertically oriented leaves. On the other
hand, amphistomaty occurs in most emergent aquatic
plants, crop plants, and herbaceous weeds, which
have dorsiventral leaves with bifacial mesophyll.
Descriptions of succulent CAM plants show that
stomata occur on all surfaces, which is expected
because the leaves are extremely thick and the
carbon-assimilating tissues are similarly distributed
just under the epidermis. Amphistomaty is also the
rule for leaves with Kranz anatomy, i.e. plants having
C 4 photosynthesis; thus species with the highest
known photosynthetic rates (Longstreth, Hartsock &
Nobel, 1980) all have amphistomatic leaves.
Occurrence of amphistomaty relative to leaf thickness
Parkhust (1978) attempted to model the adaptive
significance of amphistomatic leaves and concluded
that in thick leaves the diffusion pathway through the
mesophyll may be too long, and hence inefficient, if
stomata occurred only on one surface. To test this
prediction, we have measured leaf thickness from
transections of 119 dominant or very common
dicotelydonous species in the floras of Arizona,
California, and Mexico (Fig. la). Included in the
sample are species from coastal lowland and
montane habitats, most of them having semi-arid
climate with less than 1000 mm of annual
455
456 K. A. MOTT, A. C. GIBSON & J. W. O'LEARY
IOOr(Q)
D
O
1a. 50
100- 201- 301-
200 300 400
Figure 1. Percentage of species with amphistomatic leaves as a function of leaf thickness for (a) various dominant or very
common dicotyledonous species in Arizona, California, and Mexico, and (b) the genus Bursera.
precipitation. The percentage of amphistomatic leaves
for each thickness size class is given, and a slight trend
towards amphistomaty with thick leaves is present.
The same was done for 38 species within a single
genus, Bursera (Fig. lb), which has both stomatal
patterns, and the correlation between leaf thickness
and amphistomaty is clear in this figure. However, it
is also clear that ranges of thicknesses for
hypostomatic and amphistomatic leaves are broadly
overlapping. There are many herbaceous plants with
leaves only 100-500 um thick that are amphistomatic,
whereas many woody plants with leaves of the same
thickness do not possess upper stomata. In Bursera,
the species with amphistomatic leaves have neither the
thickest nor the thinnest leaves. The amount of
variation in the trend suggests a secondary correlation
between leaf thickness and amphistomaty rather than
a primary one, i.e. both may be positively correlated
with some other independently varying parameter.
Occurrence of amphistomaty relative to light levels
The distributional patterns of amphistomaty have not
been reviewed relative to light levels. Taking the same
surveys cited earlier, however, one prominent trend is
obvious—amphistomatic species are successful in
full-sun, high-light habitats. This is certainly the case
for coastal marsh and strand and also desert plants;
for example, in North American deserts over 90% of
the species have amphistomatic leaves, including
woody dicotyledons, rosette monocotyledons, C 3 and
C 4 herbs, and succulents (Gibson, unpublished data).
In contrast, plants of the tropical lowland rain forests
and montane forests are mostly devoid of upper
stomata except on epiphytes in the canopy, such as
orchids, which are CAM plants. It is well known that
all C 4 plants are adapted to high-light environments
(Ehleringer, 1978), and, as noted earlier, they are
amphistomatic.
In temperate latitudes the same condition prevails.
Amphistomaty characterizes plants of meadows,
disturbed habitats, and open aquatic habitats. Even
the woody plants with adaxial stomata (Kohne,
lOOr- ( b )
50
401- 501- 75- 126- 176-
500 125 175 225
Leaf thickness ( p )
1899), such as arborescent phreatophytic species of
cottonwood {Populus deltoides Marsh, and P.
fremontii Wats.) and willows (Salix spp.), are pioneers
of high-light environments. Other pioneer species of
open habitats are, of course, the many temperate
herbaceous weeds, nearly all of which are
amphistomatic (Salisbury, 1927), as are crop plants
and the many common herbaceous greenhouse plants
that thrive in full sunlight (Eckerson, 1908).
Salisbury's observations on British woodlands may
seem to falsify the hypothesis; however, the forest
floor herbs with amphistomatic leaves are those
whose principal photosynthetic activity occurs in the
spring before the trees produce leaves. Those plants in
which the majority of leaves are in partial or full
shade most of the time have hypostomatic leaves.
Much confusion surrounds certain species that are
reported as either hypostomatic or amphistomatic.
For example, Eckerson (1908) cites a greenhouse-
grown specimen of Tropaeolum majus L. as having
hypostomatic leaves, whereas Kramer & Kozlowski
(1979) indicate amphistomatic leaves for that same
species, with twice as many stomata on the abaxial
surface. This situation is vividly illustrated in certain
plant species we have examined growing both in full
sun and in full shade. Scrophularia californica C. and
S. var. floribunda Greene growing in full sunlight in
West Los Angeles, California, has stomata on both
surfaces, whereas they are absent from the adaxial
surface in full shade. We have found a similar pattern
in Ambrosia cordifolia (Gray) Payne growing in the
desert foothills above Tucson, Arizona. Plants
growing in open, sunlit areas had average stomatal
densities of 133 and 390 mm" 2 for upper and lower
surfaces, respectively. Those growing in densely
shaded environments had no upper stomata, and an
average stomatal density for the lower surface of
305 mm" 2 . In addition, other discrepancies in the
literature concerning the presence of adaxial stomata
in a given species suggest that this phenomenon may
not be all that uncommon. Clearly, not all plants
respond to full sunlight and full shade environments
in the same way, because Arnica cordifolia Hook.
 ADAPTIVE SIGNIFICANCE OF AMPHISTOMATIC LEAVES
showed no statistically significant differences between
plants in the two extreme conditions (Young & Smith,
1980).
Is amphistomaty a primitive or derived feature?
Many types of information indicate that
amphistomaty is the derived state for stomatal
distribution for land plants in general and for
angiosperms in particular. Vascular cryptogams are
almost exclusively hypostomatic (Ogura, 1972), and
so are many gymnosperms. Of the living
gymnosperms, adaxial stomata are known for a small
number of cycads, most notably those living in high-
light environments (e.g. Bowenia), and in numerous
highly specialized Coniferales (central palisade
mesophyll) and Gnetales (Napp-Zinn, 1966),
including many highly specialized forms like the
deserticolous Welwitschia. Some of the Cupressaceae
are even hyperstomatic. A review of amphistomaty in
fossil gymnosperms is needed.
Those dicotyledenous taxa regarded as having the
primitive features, such as the vesselless dicotyledons
and other members of the Annonales and
Hamamelidales, among other orders, have very few
reports of amphistomaty (Metcalfe and Chalk, 1950).
Moreover, in these families, species that have
amphistomatic leaves are highly derived forms of
open habitats, especially herbs, small shrubs, and
vines. Throughout the dicotyledons, adaxial stomata
appear in nearly every group living in open, high-light
habitats, either terrestrial or aquatic, being especially
common in the most successful and largest plant
families. Amphistomaty is very widespread in
monocotyledons, but because many of the species
with the primitive features also occur in full sunlight,
it is difficult to make a statement about the
evolutionary trends of amphistomaty in the group.
Although most families show a clear evolutionary
trend from hypostomaty to amphistomaty, there is no
reason to rule out reversals in this trend wherever
species evolve from one habitat preference to another.
We have not attempted to document such
evolutionary reversals, but they obviously have
occurred in grasses, legumes, and composites.
Effect of having stomata on both surfaces
One possible explanation for the occurrence of
amphistomaty is that adaxial stomata may be the best
way to achieve extremely high leaf conductance for
CO2 diffusion into the leaf. Let us assume, for the
moment, that a high maximum conductance for CO2
diffusion would be advantageous to a particular
plant, and hypostomaty is the primitive and existing
form. Then, in an evolutionary context, the plant has
essentially two options to produce a high leaf
conductance: (1) it can increase the size or the density,
or both, of the stomata on the abaxial surface; or (2)
it can add stomata to the adaxial surface. There are,
457
however, several considerations which may influence
which of the two options is the most advantageous.
At first glance it seems obvious that eventually the
lower surface may become 'filled up' as stomata are
made larger or added. However, there are a large
number of amphistomatic leaves which, based on
visual examination, do not appear to have this
problem (i.e. the ratio of groundmass epidermal cells
to guard cells is high). Hence this argument may apply
only in selected cases.
As stomata become denser, there may be
diminishing returns for diffusion capability if there is
interaction among the diffusion shells. The density of
stomata required for significant mutual interference
has been debated (e.g. Browne & Escombe, 1900;
Ting & Loomis, 1963, 1965; Parlange & Waggoner,
1970). The evidence indicates that interaction among
diffusional shells may be possible under certain
conditions. However, the complexity of the problem
has created controversy over the mathematics of the
situation, and a consensus on the effect does not
appear to exist in the literature.
Another possible advantage to forming upper
stomata is that as stomatal conductance becomes very
high, other conductances in series with the stomatal
conductance may become significant to the overall
pathway. The most important of these is the
boundary layer conductance of the leaf. The effect of
adding stomata to the upper surface of the leaf is to
add another boundary layer conductance to the
overall pathway, in parallel with that of the lower
surface.
Assuming stomatal conductance to be linear with
stomatal number (or density) at maximum aperture,
and that boundary layer conductance is identical for
the two surfaces, the effect of distributing a number of
stomata over two surfaces rather than one is to
double the boundary layer conductance for the leaf,
leaving stomatal conductance unaffected. For large
leaves, low windspeeds, and high stomatal
conductances the advantage can be well over 25%.
The same argument could be applied to the gas phase
intercellular conductance to CO2 for thick leaves,
leading to conclusions similar to those of Parkhurst
(1978). However, for intermediate thickness leaves
(100-500 urn), both amphistomatic and hypostomatic
leaves are abundant, suggesting the influence of some
other parameter.
Thus, it appears that amphistomaty may be an
adaptation designed to raise maximum leaf
conductance to CO 2 . However, a high conductance is
advantageous only if intercellular CO 2 concentration,
rather than some other factor, is significantly limiting
carbon assimilation. When this is not the case, an
increase in conductance would serve to increase water
loss with only a small increase in photosynthetic rate.
Under shaded conditions, photosynthesis will be
limited by light intensity; therefore, for a plant to
benefit from a high conductance, it must grow in an
environment such that its leaves are exposed to full
458 K. A. MOTT, A. C. GIBSON & J. W. O'LEARY
sunlight, for the majority of a day. Obviously, plants
of open fields, grasslands, and deserts fall into this
category, regardless of growth form. For deciduous
trees growing in dense forest, leaf area index is
sufficiently high so that most leaves spend a major
portion of the day partially or completely shaded
(Walter, 1979). Deciduous trees that are early
colonizers of open fields probably have a greater
proportion of their leaves sunlit at any one time, but
certainly not to the extent of small herbs and grasses.
Photosynthetic increases achieved by high
conductances will be greater for a leaf of high
photosynthetic capacity—i.e. one in which enzyme
and chlorophyll content are not limiting
photosynthesis significantly—than one of a lower
capacity. In addition, leaves with high photosynthetic
capacities will be more likely to develop steep CO 2
gradients within the leaf. This idea is similar to that of
Parkhurst (1978) for thick leaves and long diffusion
distances. However, even fairly thick leaves will
develop only shallow concentration profiles if
they have low photosynthetic rates, due either to low
light intensities or low photosynthetic capacities.
Thus, amphistomaty may be an advantage to thick
leaves, but only if plant and environmental conditions
favour high photosynthetic rates.
There is considerable evidence in the literature that
maximum photosynthetic rate varies according to
habitat and growth form. Korner, Scheel & Bauer
(1979) have recently reviewed the literature on
maximum stomatal conductance and photosynthetic
rates for plants of specific habitats and growth forms.
Low maximum photosynthetic rates are observed for
succulents, evergreen conifers, deciduous woody
plants, herbs from shady habitats, evergreen woody
plants, and desert and steppe shrubs. Higher
maximum values are obtained for deciduous fruit
trees, wild grasses, cultivated C 4 and C 3 grasses,
herbaceous crop plants, herbs from open habitats,
and plants from aquatic habitats and swamps. Bazzaz
(1979) cites evidence that the maximum
photosynthetic rate declines through successional
stages in a plant community, pointing to higher rates
for open field plants and grasses and lower rates for
canopy deciduous trees and shade habitat herbs.
Early successional trees appear to be intermediate in
photosynthetic rates.
Data from both Korner et al. (1979) and Bazzaz
(1979) show a decrease in stomatal conductance with
decreasing photosynthetic rates, raising the possibility
that stomatal inhibition of photosynthesis is
responsible for the lower rates observed in some
groups. However, since the data of both Korner et al.
(1979) and Bazzaz (1979) show lower residual
conductances with lower stomatal conductances, it
seems likely that the lower photosynthetic rates
characteristic of the plant groups discussed above are
chiefly a reflection of lower inherent photosynthetic
capacities.
In addition, recent data of S.C. Wong (in
Farquhar, 1979) suggest that leaf conductance
increases with photosynthetic capacity when
photosynthetic capacity is varied by limiting nitrogen.
The above considerations indicate that under
conditions of high light and high photosynthetic
capacity, a high conductance would be advantageous
to a plant because it allows a high rate of CO 2 uptake.
However, equally important is the fact that high
conductances lead to both higher transpiration rates
and higher transpiration ratios (Raschke, 1975,
1976); hence low efficiency of water use, especially for
a C 3 plant. At first glance this consideration seems to
rule out all plants except those living in permanently
wet conditions, for example, on the edges of lakes,
swamps, or marshes or those with deep roots tapping
underground reservoirs. Efficiency of water usage is
not an important consideration for these plants, and a
high conductance would be an advantage if it
improved photosynthetic rate even a small amount.
A high maximum conductance does not, however,
imply that leaf conductance must always remain high.
Plants living in environments in which water remains
in the soil around their roots for only short periods of
time would benefit from being able to create an
extremely high conductance to gas exchange under
certain conditions. Cohen (1970) has hypothesized
that plants with very shallow roots, or roots
overlapped considerably by those of other plants,
should use water quickly and inefficiently when it is
present. A plant in this situation is at a competitive
disadvantage if it adopts a slow, efficient usage of
water because the water will quickly be lost either to
other plants or by percolation and evaporation. This
strategy has also been recognized by Passioura (1976),
who states that the better strategy would be to use the
water faster, less efficiently, and grow quickly while it
is available. As the soil dries, the plant then must
lower leaf conductance to prevent damaging water
deficits. In considering succession in broad-leaved
deciduous forests, Bazzaz (1979) notes that early
successional plants experience a more rapidly
fluctuating environment than later successional
plants. Because of this they tend to use resources such
as soil water and nutrients quickly before they are
used by competitors.
It seems probable that a high maximum
conductance would be adaptive to plants in the
situation described above. A high conductance would
permit high photosynthetic rates under wet
conditions, allowing the plants to gain as much
carbon as possible while water was available. Plants
with lower conductances would assimilate less carbon
during the brief wet periods, and presumably would
be at a competitive disadvantage if all other things
were equal.
Most open-field herbs, low shrubs, grasses, and
early successional trees would fall into this category.
Desert plants, while probably not competing for
water amongst themselves, are exposed to very rapid
fluctuations in soil water content due to rains and
 ADAPTIVE SIGNIFICANCE OF AMPHISTOMATIC LEAVES
subsequent percolation and evaporation. This
situation has forced many desert plants into the same
strategy of rapid inefficient use of water to maximize
carbon uptake. Maximov (1929) contributed the first
supporting evidence for this type of strategy in desert
plants when he reported that many so-called
xerophytes showed high transpiration rates when well
watered.
It does not seem likely that large, deeply rooted
plants such as canopy deciduous trees or woodland
trees would adopt this type of strategy. Although
these plants, in most cases, experience water stress,
the time scale for the development of stress is
considerably longer. Data for trees (e.g. Kozlowski,
1968) show that water stress develops over a period of
many weeks rather than days, as for shallow rooted
plants. It is unlikely that these plants would benefit
from a rapid inefficient usage of water. Since they do
not compete for the water to the extent of smaller
plants, slow efficient usage will result in more CO2
assimilated per unit of water lost, and allow for a
longer period without water stress. For these plants a
high maximum conductance is probably not an
adaptive advantage.
In most species wtith dorsiventral leaves, the
density and size of adaxial stomata are not the same
as on the abaxial surface. A sample of the ratios can
be obtained from any of the above cited surveys.
Generally, there are fewer stomata on the adaxial
surface; in some cases they are larger and in some
they are smaller (Eckerson, 1908). In addition, upper
and lower stomata often do not respond identically to
environmental stimuli. These differences in response
have recently been reviewed by Pospisilova &
Solarova (1980). However, for well-watered, sunlit
leaves both surfaces typically have a high
conductance, consistent with the proposed advantage
over hypostomaty. The large differences in
conductance commonly present under low light
intensities or low water availability seem more likely
to be significant as adaptations for controlling
stomata once they are present on both surfaces, rather
than an advantage over hypostomaty.
Conclusions
In summary, we suggest that amphistomaty is
correlated with high conductances to CO2 diffusion,
and as such should be advantageous to plants that
benefit from a high maximum leaf conductance. We
have examined the conditions under which high leaf
conductances would provide an adaptive advantage,
and the correlation of these conditions with the
observed distribution of plants with amphistomatic
leaves is remarkable. Both amphistomaty and
environmental conditions favouring high maximum
leaf conductances are characteristic of open area
plants; full-sun herbs, low shrubs, early successional
deciduous trees, desert plants, and marsh, swamp,
lakeside and phreatophytic plants. These are all
459
plants living in full sun, typically with high
photosynthetic capacities which, when water is
available, show high photosynthetic rates and grow
quickly.
Perhaps the most convincing piece of supporting
evidence for this hypothesis is the observation that the
presence of adaxial stomata in some plants is
dependent on the light intensity at which that leaf was
formed. The obvious conclusion is that under high
light intensities a higher photosynthetic capacity leaf
is formed which, combined with high light intensities,
allows for high maximum photosynthetic rates. The
resulting need for high leaf conductance is provided
by adding adaxial stomata.
Not ali species of full sunlight will be
amphistomatic. Less rapidly growing plants, implying
lower photosynthetic rates and lower conductances,
tend to be hypostomatic. This condition is typical of
the evergreen oaks (Quercus), which are almost totally
hypostomatic, typically grow in full sun, often have
very thick leaves, but show low photosynthetic rates
and slow growth rates.
This hypothesis explains the loose correlation of
amphistomaty with leaf thickness. Full-sun leaves are
usually thicker and have higher photosynthetic
capacities than do shade leaves (e.g Nobel, 1976) so
amphistomaty will be secondarily correlated with leaf
thickness. In addition, extremely thick leaves (> 500
um) will tend to be amphistomatic as discussed
earlier, adding to the correlation between
amphistomaty and leaf thickness.
The hypothesis does not, however, explain the
almost complete absence of hyperstomatic leaves in
plants with stomata on only one surface. If the
hypostomatic condition is the primitive one, as we
have suggested, it may be that there is no particular
selective advantage to a hyperstomatic leaf. This
possibility as well as others (see Parkhurst, 1978)
needs to be explored to understand whether there are
disadvantages to having adaxial stomata under
certain environmental or biological situations.
Acknowledgments
Some of the ideas expressed in this paper have
resulted from stimulating discussions and critical
comments by several people, especially Dr Anthony
Hall, Dr David Parkhurst, and Dr Park Nobel.
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