Polar Biol (2000) 23: 531538

Springer-Verlag 2000

ORIGINAL PAPER

Andre Mantovani Ricardo Cardoso Vieira

Leaf micromorphology of Antarctic pearlwort

Colobanthus quitensis (Kunth) Bartl.

Accepted: 14 January 2000

Abstract The leaf micromorphology of Antarctic

pearlwort, Colobanthus quitensis (Kunth) Bartl. was
analyzed. Plants were collected at King George Island
(625S, 5823W). Leaves were analyzed by optical and
scanning electron microscopy, and quantitative analyses
performed on leaf tissues and their internal geometry.
C. quitensis leaves are ca. 588 lm thick, and composed
of palisade and spongy parenchyma, respectively ca. 171
and 312 lm thick. Cuticles are thin and cover short
epidermal cells. The central vein is surrounded by two
bundles of achlorophyllous cells. Sclerenchymatic tissues
are poorly developed. SEM analysis reveals faint striations over leaf surfaces. Stomata are present on both
surfaces, but restricted to the leaf margins on the abaxial
side. The ratio of mesophyll cell surface area per unit
leaf area (Ames/A) is 34.2. The number of cells per
cross-sectional area occupied was 24% higher for the
palisade than for the spongy tissue, which determines a
higher cell surface area per cross-sectional area for the
former tissue. The authors correlate these results to
plant ecological distribution in Antarctica and to water
and carbon economy.

Introduction
The Antarctic biome is a hostile environment for plant
growth (Smith 1984). Although growing conditions are
more favourable along the Antarctic peninsula and
islands to the north (e.g. South Orkney and South
Shetland Islands), plant diversity is low in comparison to

A. Mantovani R. C. Vieira (&)

Universidade Federal do Rio de Janeiro,
Departamento de Botanica, CCS, Bloco A,
Cidade Universitaria, 21949-900, Ilha do Fundao,
Rio de Janeiro, RJ, Brazil
e-mail: vieirarc@biologia.ufrj.br

Arctic regions, even 20 of latitude farther north. Abiotic factors such as low temperature, low rainfall and
water availability (Smith 1993) and low nutrient status
(Smith 1985; Hall and Walton 1992) are limiting conditions for the majority of plants (Kennedy 1996). Only
two native phanerogams, Deschampsia antarctica Desv.
and Colobanthus quitensis (Kunth) Bartl., occur in
Antarctica to almost 69S (Smith 1994). The establishment of these plants is an important tool for research
on adaptations of terrestrial plants to the prevailing
Antarctic conditions.
Numerous studies have been made of the habitat
(Smith 1985, 1993), distribution (Moore 1970; Smith
and Poncet 1987), taxonomy (Parodi 1949; Greene
1970), physiology, growth and reproduction (Corner
1971; Greene and Holtom 1971; Smith and Stephenson
1975; Edwards and Smith 1988; Convey 1996) and
ecology (Kennedy 1996; Smith 1996) of these two vascular plants. However, anatomical aspects are lacking.
Vieira and Mantovani (1995) studied the leaf anatomy of D. antarctica, providing a brief review of structural studies in this genus. However, comparable data
for the genus Colobanthus are few. Metcalfe and Chalk
(1950) and Chalk (1985) provided a general account of
the family Caryophyllaceae. Pyykko (1966) studied one
unindentied species of Colobanthus in her study of the
Caryophyllaceae and other families from the Patagonian
ora. Betts (1918), studying the ora of D'Urville
Island, New Zealand (4007S, 174E), gave some
information on the anatomy of C. apetala.
The aim of this work is to provide information on the
leaf micromorphology of C. quitensis, contributing to
the knowledge of plant survival in Antarctica.

Materials and methods

Study site
Individuals of C. quitensis were collected at the northern end of
Admiralty Bay, South Shetland Islands (6205S, 5823W) (Fig. 1).

532
Mean air temperature for the summer months (December to
February) ranges from )1 C to +1 C, with a mean annual air
temperature of )2.7 C (Smith 1993). Mean annual precipitation is
low, around 400 mm (Smith 1996). Soil is generally an oligotrophic
lithosol, with low nutrient availability to plants (Smith 1985; Hall
and Walton 1992).
Leaf anatomy
In the eld, leaf material was xed in FAA 70 (formalin: acetic acid:
alcohol 70GL, in 1:1:18 ratio) and brought to the laboratory in
Brazil. Sections of leaf sheath and proximal, median and distal parts
of the leaf lamina were dehydrated in a series of increasing-strength
alcohol, embedded in paran and sectioned with a Spencer rotary
microtome (Vieira 1995). Sections 10 lm thick and stained with
astrablue-acid fucsin (Roeser 1962) were examined microscopically
in order to quantify leaf trait dimensions. Whole leaf, cuticle, epidermis and chlorenchyma thickness were measured on an ocular
micrometer glass slide adapted for a light microscope. Five sections
from ve dierent leaves (one per leaf) from ve individuals were
examined. Leaf thickness was measured at ve dierent points
within each section. For cuticle, epidermis, palisade and spongy
parenchyma, 5 contiguous cells from each section were examined,
with a total of 25 measurements per tissue. For stomatal dimensions
(equatorial and polar axis length, and longitudinal length of pore)
and distribution, paradermal sections from the paran-embedded
leaves were used, following the same methods described above.
Scanning electron microscopy (SEM)
Sections from the middle region of xed leaves were dried
by critical-point drying, covered with gold-palladium and analyzed

in a Zeiss scanning electron microscope, model DSM960,

at 20 kV.
Leaf internal geometry
The leaf internal parameters measured were cell surface area per leaf
area (Ames/A, sensu Nobel 1980), cell transverse-sectional area and
percentage of aerenchyma. These three parameters were quantied
for palisade and spongy parenchyma, and for the whole leaf.
Transverse sections from leaves embedded in paran were used.
Sections 200 lm wide (on an adaxial basis) were treated as units,
and all cells below it were drawn with a camera lucida at 400
magnication (Nobel 1976). Cellular perimeter was measured with a
planimeter and the value divided by 200 lm, to obtain the ratio
Ames/A. Cell cross-sectional length was treated as 1 lm (Araus
et al. 1986). For cell transverse-sectional area, the same drawings
were used and the area of cells and air spaces quantied through the
weight of trimmed paper moulds calibrated against the weight of a
paper square of known area. Five 200-lm-wide sections from ve
dierent leaves (one per leaf ) were used for the measurements.
Regarding cell morphology, the cell occupation eciency was
here classied as the capacity of a tissue to present the highest cell
surface area per transverse-sectional area occupied.
Statistics
For comparisons between internal geometry of palisade and
spongy tissues, a Student's t-test was used (Zar 1996).

Results
C. quitensis is a low herbaceous cushion plant of
1.55 cm height, with sessile, linear to linear-triangular
leaves, with an acute apex and a base forming a colourless sheath (Fig. 2).

Fig. 1a, b Location of the study site. a Antarctic Peninsula and South
Shetland Islands in relation to South America. b South Shetland
Islands showing the site where individuals of Colobanthus quitensis
were collected on King George Island (arrow)

Fig. 2 Adult individual of Colobanthus quitensis (Kunth) Bartl.

collected on King George Island, South Shetland Islands

533
Table 1 Leaf anatomical data for Colobanthus quitensis. Data are
mean standard deviation (n 25, except for aerenchyma
n 5)

Fig. 3ad Leaf surface of Colobanthus quitensis. a Adaxial leaf

surface with short cells and paracytic stomata. b Abaxial surface
over leaf margins, showing the presence of stomata. c Abaxial surface
over the central vein without stomata. d Stomata from the adaxial
surface in transverse section

In surface view, both epidermises are composed of

polygonal cells with sinuous anticlinal walls, the abaxial
ones being larger (Fig. 3a, b). Veins on the abaxial
surface have long epidermal cells, with straight anticlinal
walls arranged parallel to the longitudinal axis of the
leaf (Fig. 3c).
Diacytic stomata are found on both leaf surfaces,
characterizing an amphistomatic leaf (Fig. 3a, b).
However, on the abaxial side, stomata are restricted to
leaf margins, accompanying palisade parenchyma distribution as shown in Fig. 5a,c. Stomata are small
(Table 1) with the polar axis parallel to the longitudinal
axis of the leaf (Fig. 3b). In transverse section, stomatal
cells are raised above the level of the epidermis (Fig. 3d).
SEM analysis shows the presence of faint parallel
striations over the abaxial epidermal cells beneath the
central vein (Fig. 4a). Over the leaf margins, however,
striations are more prominent but randomly distributed
(Fig. 4b). Over the adaxial surface, striations are also
faint and parallel (Fig. 4c), occurring among the
stomata (Fig. 4d).
Dimensions of leaf characters in transverse view are
summarized in Table 1. C. quitensis leaves comprise
a layer of epidermal cells ca. 21 lm thick, covered by
a thin cuticle of 23 lm thick (Table 1, Fig. 6b).

Characters

Dimensions

Whole leaf thickness (lm)

Whole leaf aerenchyma (%)
Adaxial cuticle (lm)
Adaxial epidermis (lm)
Palisade mesophyll (lm)
Palisade aerenchyma (%)
Spongy mesophyll (lm)
Spongy aerenchyma (%)
Abaxial epidermis (lm)
Abaxial cuticle (lm)
Stomatal polar axis (lm)
Stomatal equatorial axis (lm)
Stomatal pore length (lm)

588.4 30
21.3 4
3.1 0.4
21.4 3.8
171 14.6
23.8 4.7
312.8 31.6
19.6 7.6
21.2 3.3
2.4 3.3
22.7 0.6
9.2 1.1
7.7 1.1

Chlorenchyma is composed of palisade and spongy cells

(Fig. 5a, b).
Palisade parenchyma occurs near the adaxial surface
and to some extent on the abaxial surface at the leaf
margins (Fig. 5c). The two to three layers of palisade
cells are arranged in medium to high density, creating air
spaces in ca. 24% of the total palisade area. Spongy
parenchyma is 46% thicker than palisade parenchyma,
composed of 911 layers of cells, with 20% of the area
occupied by air spaces (Table 1). Druse oxalate crystals
are found only in spongy cells, mainly near veins.
Leaf lamina vascularization is illustrated in Figs. 5a, b
and 6a. The vascular system is composed of ve colateral bundles in the middle leaf region. The central vein is
composed of a sheath formed by the achlorophyllous
parenchymatic cells of two vascular bundles, the external one comprising large cells and the inner ones formed
by smaller cells (Figs. 5b, 6a). The proto- and metaxylem do not show regular organization, while the phloem
occurs in dispersed groups (Figs. 5b, 6a). The thin
cuticle is shown in Fig. 6b.
The leaf sheath, generally larger than the lamina,
partially envelops the stem. Both epidermises are
unistratied and without stomata. In transverse view the
vascular system is represented by only one vascular
bundle of the colateral type, which is also surrounded by
a bundle sheath (Fig. 7a, b). Mesophyll is composed of
achlorophyllous parenchymatic cells in a single layer at
the leaf margins (Fig. 7c).
Internal geometry
The cell geometry of C. quitensis leaves is summarized in
Table 2. The ratio of mesophyll cell surface area to unit
leaf area (Ames/A) is 34.2 3.5. The mean cell surface
areas per leaf area of the palisade (Apal/A) and the
spongy (Aspo/A) parenchyma are not signicantly
dierent. Both parenchymatic tissues are composed of
2226 cells per section, which confer to palisade and
spongy cells an identical surface area of 140 lm2 per

534

Fig. 4ad SEM analysis of leaf surface of Colobanthus quitensis.

a Abaxial surface over central vein. Note ne and parallel striations
over long cells. b Detail of stomata on abaxial surface over leaf
margins. Note the prominent striations randomly distributed.
c Adaxial surface showing short cells. d Detail of the stomata,
showing polar axis positioned to the long axis of the leaf. Bar is 20 lm

cell. Considering the transverse-sectional area, the

spongy tissue occupied an area 38% higher than the
palisade. These data confer dierent occupation eciencies for palisade and spongy parenchyma (Table 2).
The ratio of number of cells/transverse-sectional area
occupied by palisade tissue is 24% higher than for
palisade parenchyma. It means that in a pre-determined
transverse area of leaf mesophyll (for example,
1000 lm2), the palisade parenchyma would be composed of 24% more cells than the spongy tissue
(Table 2). Considering that both types of parenchymatic
cells have an identical surface area of 140 lm2 per cell,
the higher number of palisade cells would produce a
higher Ames/A. Presenting a higher total surface area
per transverse-sectional area, the palisade parenchyma
has a higher cell occupation eciency.

Discussion
In Antarctic fellelds, C. quitensis and D. antarctica
occur scattered amongst cryptogams (Smith 1994) and
occasionally develop small dense stands referred to as
Antarctic herb tundra formation (sensu Gimingham and
Smith 1970). This community must tolerate low temperatures, low water availability and short growing
seasons (Kennedy 1996; Smith 1996).
In the Antarctic environment, survival depends on
the ability of organisms to endure cold and desiccation
(Pickup and Rothery 1991). However, the microclimate
at plant level frequently exceeds 20 C within the densely
packed structure of plants (Edwards and Smith 1988;
Smith 1994). The low stature and cushion habit of
C. quitensis reduce water and heat loss, and wind abrasion (Larcher 1986; Salisbury and Ross 1992). In winter,
snow cover can maintain temperatures about 15 C
above ambient (Edwards and Smith 1988).
The optimum temperature for photosynthesis and
germination of both vascular plants is between 15 and
20 C, conditions achieved only in summer for a few

535

Fig. 5ac Leaf lamina of Colobanthus quitensis. a Vascular system

constituted by ve colateral bundles. Note the identical distribution of
palisade tissue and stomata. b Transverse sections of leaf lamina,
showing the palisade and spongy parenchyma. Note the central vein
surrounded by a sheath formed by achlorophyllous cells. c Leaf
margin composed of palisade tissue. Note the presence of stomata in
both adaxial and abaxial surfaces

hours on sunny days (Smith 1994). Under overcast sky

at night, leaf temperature often remains several degrees
above freezing, demonstrating the leaves' heat retention
capacity (Smith 1994).
Stomatal conductance to water vapour is limited by
wax structures partially covering the stomatal pores
(Rentschler 1974; Bolhar-Nordenkampf and Draxler
1993). Vieira and Mantovani (1995) reported the
presence of a dense layer of wax on the adaxial surface
of D. antarctica, extensive to stomata, almost blocking
the apertures. Since transpiration rates and leaf temperature are closely linked (Gates 1968), wax cover
could act as an adaptation for the retention of heat,
limiting transpiration in leaves of D. antarctica.
Although showing retention of heat (Smith 1994), SEM

analysis shows the absence of ornamented epicuticular

wax over both surfaces of C. quitensis leaf. This implies
that factors others than leaf epicuticular wax, such as
the cushion habit, are key determinants of temperature
in C. quitensis.
Experimental data on cuticular/epidermal resistances
to water vapour diusion in C. quitensis species were not
obtained. Anatomical studies revealed a thin cuticle in
C. quitensis (ca. 3 lm). Colobanthus sp. growing in the
semi-deserts of Patagonia has a leaf cuticle about 6 lm
thick (Pyykko 1966). The values for C. quitensis are low
in comparision with other genera (Chalk 1985; Vieira
1995; Mantovani 1999). However, as water loss is not
always a function of the thickness of the cuticle
(Schonherr 1982), a more detailed investigation is necessary to evaluate the eciency of cuticular resistance of
C. quitensis.
Mesophyll arrangement of C. quitensis leaves, represented by a compact palisade and spongy parenchyma,
was also found by Betts (1918) for C. apetala growing
in New Zealand. However, Pykko (1966) reported a
homogeneous mesophyll for Colobanthus sp. from Patagonia, a pattern also found for the only other Antarctic
grass, D. antarctica (Vieira and Mantovani 1995). The
arrangement of the mesophyll has an ecological role, by
the improvment of the water economy.
C. quitensis has a dorsiventral mesophyll with palisade cells following stomatal distribution. Leaf thickness
and mesophyll surface area values for C. quitensis are
typical of xeric plants (Nobel 1976, 1980). Leaf anatomy
inuences photosynthesis, improving light (Vogelmann
1993) and water use eciency (Nobel 1980). Although it
has a higher Ames/A ratio, spongy parenchyma is less
ecient in occupation (Table 2). The parallel occurrence
of palisade and stomata constitutes a higher cellular
surface area for CO2 exchange. For Arctic and subAntarctic plants, the rate of photosynthesis appears to
be limited by mesophyll resistance (Pammenter et al.
1986; Crawford 1988).
The presence of a bundle-sheath as found in
C. quitensis was also found in D. antarctica (Vieira and
Mantovani 1995), although in the latter species the
sheath was composed of two layers of cells with the inner one lignied. Some authors (Van Fleet 1942; Evert
et al. 1985; Fahn 1990) have suggested that this structure
functions as an endoderm, limiting apoplastic movement
of water to the mesophyll. However, neither Canny
(1986) nor Eastman et al. (1988) conrmed this hypothesis.
Sclerenchyma is the main source of leaf strength
(Turner 1994), acting as a mechanical barrier to wind
(Pyykko 1966) and herbivory (Turner et al. 1993). Chalk
(1985) stated that in cushion plants, the epidermis also
provides mechanical resistance, a phenomenon known in
the genus Pycnophyllum and in the family Caryophyllaceae. Although lignied structures are absent in
C. quitensis, this role of the epidermis probably does not
occur as its leaves have herbaceous or soft textures
(Betts 1918).

536

Fig. 6a, b SEM analysis of the Colobanthus quitensis leaf lamina.

Transverse sections. a The central vein surrounded by two parenchymatic bundles, the external one comprising large achlorophyllous cells
(thick arrow) and the inner one made of small cells (thin arrow).
b Transverse section of the epidermis, showing the thin cuticle plus
cuticle strata. Bars are 20 lm

Although often having to contend with low water and

nutrient availability (Smith 1993; Kennedy 1996),
C. quitensis does not develop distinct leaf xeromorphism.
The family Caryophyllaceae has other species with hairy
leaves, sti epidermis and hypodermis, water storage and
sclerenchymatic tissues, also living under xeric and oligotrophic conditions (Pyykko 1966; Chalk 1985). In
Arctic and sub-Antarctic regions, sclerophyllous and
non-sclerophyllous plants occur together (Warming
1909; Pammenter et al. 1986; Crawford 1988), representing dierent survival strategies in cold and desiccating environments. Hard leaves with sclerenchymatic
tissues are an advantage in exposed sites where wind
causes abrasion (Pyykko 1966; Vieira and Mantovani
1995). However, the lack of sclerenchyma allows more
carbon to be invested in photosynthetic tissues (Pammenter et al. 1986). Considering the preference of
C. quitensis for moist sheltered sites (Edwards and Smith
1988), this species invests more biomass in green tissue,
which explains the thick mesophyll without bers, a
pattern not found, for example, in Colobanthus
sp. growing in exposed conditions in semi-desert areas of
east Patagonia, with heavily lignied leaves up to 225 lm
thick (Pyykko 1966).

Fig. 7ac Leaf sheath of Colobanthus quitensis. a Vascular system

comprising only one bundle. b Transverse sections of sheath, showing
the homogeneous mesophyll. c Sheath margin composed of only one
layer of cells

Table 2 Leaf anatomical data for Colobanthus quitensis. Internal geometry for leaf sections 200 lm wide (on an adaxial basis). Data are
mean SD (n 5) (na not applicable). Dierent letters indicate signicant dierences (P < 0.05)
Character

Ames/A
(unitless)

Whole leaf
34.2 3.5
Palisade parenchyma 15.4 1.9a
Spongy parenchyma 18.5 2.5a

Number
of cells

Ames/cell
(lm2/cell)

49.4 7.2
22.6 5.6a
26.8 2.9a

na
na
141.3 21a 5.3 0.4a
a
140.2 6.4 8.2 1.5b

Cell transversesectional
area (103 lm2)

Number of cells/
transverse-sectional
area (cells/lm2)

No. of cells Ames in

in 1000 lm2 1000 lm2

na
0.0042 0.0008a
0.0032 0.0002b

na
4.2 0.8
3.2 0.2

na
577.3 42.6a
457.9 26.7b

537

A plant's survival under stressful conditions is based

on its anatomy and physiology (Levitt 1980). Thick
leaves and internal leaf architecture, associated with the
low stature, dense growth form, cushion habit and
photosynthetic metabolism, contribute to the successful
survival of C. quitensis in Antarctica.
Acknowledgements The authors are grateful to Dr. R.I. Lewis
Smith (British Antarctic Survey) for his improvements to this
paper. The authors thank Professor Ulysses Lins (Microbiologia/
UFRJ) for the critical-point drying, Ailton Lu s S. Souza
(CENPES) for the specimen metalization, and Professor Maria de
Fatima da Silva Lopes (DCMM-PUC/RJ) for the SEM photomicro- graphs. The authors are also indebted to Professor Antonio
Batista Pereira, for the collection of plant material during the
expedition to King George Island, and to Anael Jacob for help with
references. This work was funded by Fundacao Universitaria Jose
Bonifacio (FUJB) and Fundacao de Amparo a Pesquisa do Estado
do Rio de Janeiro (FAPERJ).

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