Springer-VerlagTokyo102650918-94401618-086030669031Journal of Plant Research J Plant Res18110.

1007/s10265-004-0181-3

J Plant Res (2004) 117:465–472 © The Botanical Society of Japan and Springer-Verlag Tokyo 2004
Digital Object Identifier (DOI) 10.1007/s10265-004-0181-3

ORIGINAL ARTICLE

Hery Purnobasuki • Mitsuo Suzuki

Aerenchyma formation and porosity in root of a mangrove plant,

Sonneratia alba (Lythraceae)

Received: June 28, 2004 / Accepted: September 28, 2004 / Published online: November 5, 2004

Abstract Aerenchyma gas spaces are important for plants either by rooting superficially in order to take advantage of
that grow in flooded and anaerobic sites or habitats, because the oxygen available in the upper soil or in water, or by
these gas spaces provide an internal pathway for oxygen developing aerenchyma, an extensive network of gas spaces
transport. The objective of this study is to characterize the throughout the root cortex (Armstrong 1979; Justin and
development of aerenchyma gas spaces and observe the Armstrong 1987; Laan et al. 1989; Jackson and Armstrong
porosity in roots of Sonneratia alba. Tissue at different 1999; Visser et al. 2000b). Aerenchyma is plant tissue that
developmental stages was collected from four root types, i.e. is permeated by gas spaces. Aerenchyma reduces flooding
cable root, pneumatophore, feeding root and anchor root, stress by allowing an internal pathway for oxygen to the
of S. alba. In S. alba, gas space is schizogenously produced root zone to aid in respiration and oxidation (Armstrong
in all root types, and increases in volume from the root et al. 1994; Schussler and Longstreth 2000).
meristem to mature root tissues. The aerenchyma formation Despite the importance of aerenchyma to the survival of
takes place immediately, or 3–5 mm behind the root apex. wetland species, little is known about the processes that lead
At first, cortical cells are relatively round in cross sections to its formation in mangrove plants. Most the research on
(near the root apex); they then become two kinds of cells, aerenchyma has taken place in other plants, i.e., the crops
rounded and armed, which combine together, forming Zea mays (Campbell and Drew 1983) and Oryza sativa
intercellular spaces behind the root apex. The average (Webb and Jackson 1986) and the grass Spartina alterniflora
dimensions of cortical cells increased more than 1.3 times (Maricle and Lee 2002); or is related to aerenchyma forma-
in the vertical direction and over 3.3 times in the horizontal tion in the shoots of Scirpus validus, petioles of Sagittaria
direction. At maturity, aerenchyma gas spaces are long lancifolia, and leaves of Sparganium eurycarpum, Sagittaria
tuberous structures without diaphragms and with numerous lancifolia and Typha latifolia (Kaul 1971, 1974; Schussler
small pores on the lateral walls. Within the aerenchyma, and Longstreth 1996). All of these investigations have been
many sclereids grow intrusively. Root porosity in all root of herbaceous plants and the lifespan of the anaerobic
types ranged from 0–60%. Pneumatophores and cable roots organs is rather short. In trees, the root system is more
had the highest aerenchyma area (50–60%). persistent. Therefore, it is expected that roots of trees grow-
ing in anaerobic conditions develop a more persistent aer-
Key words Aerenchyma · Cortical cells · Porosity · Roots · enchyma system than those of the herbaceous plants.
Sclereids · Sonneratia alba The importance of aerenchyma and the physiology of
root aeration to the survival of mangrove species has been
described (Scholander et al. 1955; Curran 1985; Curran et
al. 1986; Hovenden and Allaway 1994; Ashford and Allaway
Introduction 1995; Skelton and Allaway 1996; Allaway et al. 2001), but
very little is known about the development and organiza-
Prolonged seawater flooding leads to an anaerobic root tion of aerenchyma tissue in mangrove root systems.
environment for mangrove plants. Wetland species of Developmental study from the root apex to the mature
plants, however, have adapted to the anaerobic conditions parts would be required to understand this conclusively
(Allaway et al. 2001).
Sonneratia alba is a pioneering mangrove species of
H. Purnobasuki (*) · M. Suzuki Lythraceae and often grows in newly formed sand or mud
Botanical Garden, Graduate School of Science, Tohoku University,
flats in the outer fringe of the mangrove forest, and some-
Kawauchi, Aoba-ku, Sendai 980-0862, Japan
Tel. +81-22-2176789; Fax +81-22-2176761 times even constitutes a pure and sparse forest in the sea-
e-mail: hery33@mail.tains.tohoku.ac.jp ward zone. This species is fast-growing and can grow up to
466
4–5 m tall; at maturity, in Japan, it rarely exceeds 6 m. This
species develops a highly specialized root system of four
main types (cable root, feeding root, anchor root and pneu-
matophore) (Troll and Dragendorff 1931; Tomlinson 1986).
Anatomical knowledge of Sonneratia roots is scanty.
There have been some previous investigations dealing with
the structure of Sonneratia’s pneumatophores as aerating
organs (Troll and Dragendorff 1931) and as water-
conducting systems (Sun et al. 2004).
The objective of this study was to examine and compare
the characteristics of the structure and arrangement of cor-
tical cells in four root types of Sonneratia alba to better
understand how aerenchyma gas spaces are formed.
Materials and methods
Material
All root samples were taken from adult trees of Sonneratia
alba J. Smith, which grow naturally in Komi estuary
(24°19¢N, 123°54¢E), Iriomote Island, Okinawa Prefecture,
Japan. The sampled trees were sparsely distributed in the
outer fringes (seaward) of a mangrove forest where the
plants were flooded by all high tides and easily influenced
by strong winds and tidal forces. Around the sampled trees,
we excavated root systems during low tide, and collected
(1) cable-root tips, (2) pneumatophore tips, (3) feeding-root
tips and (4) anchor-root tips. For each root type, we col-
lected ten roots. The root samples were cut out along the
axis of each root from the tip at 1 cm intervals.
Histology
The samples were fixed in FAA (70% ethanol, 10%
formalin, 5% acetic acid, 90 : 5 : 5). The air in the tissue was
evacuated using an oil rotary vacuum pump. The samples
were dehydrated in an ethanol series and embedded in
Paraplast Plus (Oxford Labs, USA) in 59°C. Sections were
cut, 10–12 mm thick, by a rotary microtome (HM 350
Microm, Heidelberg Germany), stained in safranin/fast
green (Johansen 1940; O’Brian and McCully 1981; Sander-
son 1994), and permanently mounted using Bioleit. The
observation was done using a light microscope (B ¥ 50,
Olympus, Japan). Microscopic images were taken by micros-
copy camera (Olympus PM-C35, Japan) and recorded on
Fuji Film Neopan F ISO 32/16° for black and white prints.
For scanning electron microscopy, the tissue was dehy-
drated in graded ethanol/t-butyl alcohol and freeze-dried at
-10°C (HITACHI ES-2030 Freeze Dryer). The dried sam-
ples were glued to the specimen stubs coated with conduc-
tive carbon tape. The samples were coated with platinum-
palladium in a vacuum evaporator (HITACHI E-1030 Ion
Sputter), and viewed and photographed using a scanning
electron microscope (HITACHI S-4100).
A maceration study was also carried out for sclereid
observation. The samples were trimmed into slivers thinner
than a toothpick and then kept in a mixture (1 : 1) of glacial
acetic acid and 6% hydrogen peroxide at 60°C for 36 h.
After this treatment, the macerated materials were washed
in distilled water and stained in safranin O. Macerated
sclereids were mounted for observations.
Porosity measurements
Digital images of root cross sections were first taken by a
digital microscopy camera (Fujix digital camera HC-300,
Japan) and saved as image files using a software package of
Fujix Photograb-300. The saved image files were then ana-
lyzed with Scion Image 1.63 software (Scion Corporation,
Frederick, MD) to measure the percentage of root area
composed of aerenchyma. Digital images of root cross
sections (Fig. 1A) were adjusted to maximize contrast by
converting the image to black and white only (Fig. 1B). To
determine total cross-sectional area, aerenchyma spaces
were filled, resulting in a solid, black silhouette (Fig. 1C),
and the number of pixels was quantified. Aerenchyma area
was determined by returning to the original image (Fig. 1B),
then inverting it to form a negative image (Fig. 1D). Pixels
composed of lacunae were quantified.
The root porosity was determined according to the
method of Armstrong (1979), Maricle and Lee (2002), and
Visser and Bögemann (2003) using the equation: root
porosity (%) = 100 ¥ (area of air spaces/total cross-sectional
area)
Root sections were taken from 1–100 mm from the root
tip at 2-mm intervals from 0–10 mm and 10-mm intervals
from 10–100 mm. Ten roots were sectioned for each root
type, then measured and averaged. Root porosity results
at each position relative to the apex were analyzed using
one-way analysis of variance (ANOVA; Minitab version 13;
a = 0.05).
Results
Development and structure of the aerenchyma
In anchor roots, tissues close to the root apex (100–300 mm)
lacked intercellular spaces, and cortical cells filled up the
area between the endodermis and the epidermis in each
root type (Fig. 2A). All the cells in the cortex appeared
round in cross section without intercellular spaces. In lon-
gitudinal view, cortical cells were tightly packed and
appeared in files parallel to the root axis starting 100–
300 mm behind the apex (Fig. 3A). Surrounding the cortex
there were generally three layers of small and rectangular
cells that represent a multilayered epidermis (Fig. 2D).
Inside the epidermal layers there were several layers of
cortical cells (outer cortex) which were slightly larger than
the epidermal cells and compactly packed side by side with
radially elongated shapes (Fig. 2D). Inside the outer cortex,
larger polygonal cells of the inner cortex filled the cross
section (Fig. 2D). A distinct endodermis marked the inner
border of the cortex (Fig. 2A, B). All cells of the root were
arranged in longitudinal files near the root apices (Fig. 3A).

Fig. 1A–D. Representative
images used in digital
quantification of root porosity.
A Grayscale digital image of
feeding roots cross section. B
Same image as A, converted to
black and white. C Total root
cross-sectional area. D
Aerenchyma spaces. Total
aerenchyma area is calculated by
dividing the number of pixels in
D by the number of pixels in C.
Adopted from Maricle and Lee
(2002). Bar = 300 mm
The aerenchyma formation occured in the inner cortex
and started to develop at 3 mm behind the root apex. Cells
were slightly separated (schizogenously) from the neighbor-
ing cells in some areas of the inner cortex (Fig. 2B). The
intercellular spaces became larger as the distance from the
root apex increased. Cortical cells in cross sections were
nearly round near the root apex and then differentiated into
two different shapes: rounded cells and armed cells with
three to four protruding arms. These cells together created
intercellular spaces (Fig. 2C, E). In longitudinal view, inter-
cellular spaces appeared between longitudinal files of the
cortical cells (Fig. 3B). The number of files between the
endodermis and the outer cortex did not change during
the root development (Table 1). Lysigenous cell dissolution
was not observed in any cortical tissues of any roots.
As the distance to the apex increased to 3–5 mm, the
cortical cells appeared to be separated and produced
schizogenous intercellular spaces (Fig. 3B). At 4 cm distant,
intercellular spaces were well developed, forming long
tubes running parallel to the root axis (Fig. 3C, D). At its
maturity, the aerenchyma was round or radially elongated,
elliptical or polygonal in cross section, 35–50 mm in diame-
ter, and took the form of long tubes of indeterminate length
in longitudinal section. The tubes had numerous small pores
(about 7–10 mm in diameter) on the lateral wall, which is
467
formed by cortical cells between the neighboring aeren-
chyma tubes. The pores were schizogeneously formed by
three or four cortical cells (Fig. 4A, B). The number of outer
cortical cells surrounding the inner cortex did not increase
during the root maturation (Table 1), and individual cells
were tangentially enlarged and flattened (Fig. 2C, E). Root
diameters in mature parts were about 1.8 times larger than
those near the root apices. As a result of thickening growth,
the primary epidermal layers had split and peeled away
without secondary growth.
The aerenchyma formation process observed in the other
three root types was fundamentally the same as that of the
anchor roots except for size variation. In feeding roots,
cable roots and pneumatophores, the aerenchyma also
formed by schizogeny. The aerenchyma was well-developed
and was created by a spatially regulated distribution of dif-
ferent degrees of cell separation, expansion and division
between cortical cells.
The increase in root diameter from the root apices to the
mature parts was about 1.8 times in feeding roots, 3.1 times
in pneumatophores and 3.7 times in cable roots (Table 1).
The average horizontal dimensions of the inner cortical
cells increased 1.3–1.4 times in the vertical direction and
3.3–4.2 times in the horizontal direction (Table 2). Aeren-
chyma diameter in cross section was 35–40 mm in feeding
468
Fig. 2. Cross sections of anchor roots of Sonneratia alba, obtained at
300 mm (A), 3 mm (B), 4 cm (C), 500 mm (D), and 8 cm (E), respec-
tively, distant behind the root apex, showing development of aeren-
chyma gas spaces in cortex. A The gas spaces are not yet developed,
cortical cells are relatively rounded. Bar = 100 mm. B Some cortical
cells have separated and formed gas spaces. en Endodermis.
Bar = 100 mm. C A well-developed aerenchyma (asterisk) is formed as
roots, 80–100 mm in cable roots and 90–110 mm in
pneumatophores.
There were many sclereids developed in the aerenchyma
of cable roots and pneumatophores (Fig. 4), while sclereids
were not observed in anchor roots or feeding roots.
Sclereids of cable roots and pneumatophores began to ini-
tiate in the inner cortex close to the root apex (3–5 mm from
the root apex) and matured at 30–50 mm distant from the
root apex. The sclereids were longitudinal with several arms
that grew intrusively within the aerenchyma tube (Fig. 4A,
B). The sclereid form was quite similar in cable roots and
pneumatophores (Fig. 4C, D).
Root porosity
Root porosity in all root types rapidly increased between 0
and 10 mm from the root apex (Fig. 5). The porosity soon
large lacunate cortex. There are two kind of cortical cells, rounded cells
(rc) and arm cells (ac). Bar = 100 mm. D Multilayered epidermis (ep),
outer cortex (oc) and inner cortex (ic) are visible. Bar = 50 mm. E Well-
developed aerenchyma (asterisk) and the outer cortical layers that do
not develop air spaces have replaced the epidermal layers for protec-
tion. Bar = 25 mm
reached its maximum in feeding roots (39%) and anchor
roots (41%), while gradually increasing further in cable
roots to about 50% and in pneumatophores to about 60%
at 10 cm from the root apex, although further increases may
be expected in those roots.
Discussion
Development and structure of the aerenchyma
There was a marked change in the shape and size of cortical
cells in all root types of Sonneratia alba during develop-
ment. The distorted shapes of the inner cortical cells in root
sections (transversal and longitudinal) with well-developed
intercellular spaces clearly revealed that the intercellular
spaces were created by the separation of cortical cells
 469

Fig. 3A–D. Longitudinal sections of anchor roots of Sonneratia alba,
obtained at 100 mm (A), 3 mm (B), 4 cm (C), 8 cm (D), respectively,
distant behind the root apex, showing development of aerenchyma gas
spaces (asterisks) in cortex. A The gas space is not yet developed and
cortical cells (co) are tightly packed. en Endodermis, ep epidermis, rc
root cap. B Some cortical cells are separated and form gas spaces. C
Gas spaces are elongated parallel to the root axis, and cortical cells
become enlarged. D Well-developed aerenchyma is formed as a wide
and long lacunae. Bar = 50 mm

Table 1. Root diameter and cortical cell numbers at difference distances from the root tip in four root types of Sonneratia alba
Distance from tip in different Diameter Cells in outer cortex Radial files of cells in the inner cortex
root types (mm) (mm) (cross-sectional view) (n) (longitudinal view) (n)

Feeding roots
2 0.95 ± 0.02 368 ± 8.57 22 ± 6.01
6 1.25 ± 0.02 366 ± 7.03 17 ± 5.23
10 1.68 ± 0.03 365 ± 8.24 16 ± 3.63
20 1.72 ± 0.02 370 ± 7.98 14 ± 4.03
Anchor roots
2 1.25 ± 0.02 269 ± 4.71 15 ± 2.54
6 1.50 ± 0.02 270 ± 4.73 15 ± 3.07
10 1.68 ± 0.01 270 ± 3.91 13 ± 1.89
20 2.25 ± 0.02 280 ± 4.80 13 ± 1.04
Pneumatophores
2 2.25 ± 0.02 430 ± 12.26 38 ± 7.44
6 3.50 ± 0.03 428 ± 15.04 37 ± 4.62
10 4.25 ± 0.03 445 ± 10.98 36 ± 5.41
20 6.88 ± 0.02 451 ± 20.43 36 ± 3.22
Cable roots
2 1.90 ± 0.02 465 ± 11.43 35 ± 4.21
6 2.60 ± 0.03 468 ± 12.56 32 ± 5.35
10 3.50 ± 0.03 473 ± 10.11 30 ± 4.76
20 6.95 ± 0.04 520 ± 23.65 30 ± 4.56
470

Fig. 4. Longitudinal scanning electron micrographs (SEM) showing (D). aer Aerenchymabar tube, co cortical cell, sc sclereid. Arrows indi-
aerenchyma and sclereids in the inner cortex of pneumatophores (A) cate small pores of aerenchyma walls. Bars = 120 mm in A, 200 mm in
and cable roots (B). Sclereids of pneumatophores (C) and cable roots B, 100 mm in C, 200 mm in D, respectively

Table 2. Size of cortical cells measured from longitudinal sections taken at 0–250 mm (no gas spaces present) and 2–4 cm (with well-developed
gas spaces) behind the root tip
Root types Size of cortical cells (mm) Size increase

0–250 mm 2–4 cm

Horizontal Vertical Horizontal Vertical Horizontal Vertical

Feeding roots 13.1 ± 1.9 9.6 ± 0.9 16.7 ± 4.2 40.6 ± 10.4 1.3 4.2
Anchor roots 11.3 ± 1.6 9.2 ± 1.3 15.7 ± 3.9 38.1 ± 7.6 1.4 4.1
Pneumatophores 16.7 ± 3.2 14.8 ± 2.7 24.2 ± 6.1 48.8 ± 6.8 1.4 3.3
Cable roots 16.3 ± 2.9 13.4 ± 3.3 23.9 ± 5.7 48.3 ± 10.2 1.4 3.6
Average 14.3 ± 2.5 11.7 ± 2.7 20.1 ± 4.5 43.9 ± 5.4 1.4 3.8

Fig. 5. Root-porosity development in the four root types of Sonneratia
alba. Diamonds feeding roots, squares anchor roots, crosses cable roots,
triangles pneumatophores. Data points are averages ± 1SD of 10 roots
for each given length from the root apex, n = 10
(schizogenous origin). Close to the root apices where
there were no intercellular spaces, cortical cells appeared
rounded in cross section and were generally arranged in
longitudinal files with intimate contact between adjacent
files. Intercellular spaces developed because cortical cells
became wide in the radial dimension and long longitudi-
nally to the root axis. As the number of longitudinal files of
cortical cells did not increase (Table 1), the increase in root
diameter with distance from the root apices was mainly
caused by cell expansion and the formation of intercellular
spaces.
Aerenchyma formation only occured in the inner cortex.
The outer cortical layers that did not develop intercellular
spaces replaced the epidermal layers for protection, and
only resembled the exodermis of monocotyledon roots.
There were three to four outer layers (Fig. 2D, E) which
were darkly stained, presumably a deposition of suberin or
lignin. These layers may play a role in preventing or reduc-
ing the outward radial diffusion of oxygen (Smirnoff and
Crawford 1983; Justin and Armstrong 1987) and may also
be the necessary structural framework for aerenchyma for-
mation in mangrove plants.
The aerenchyma type found in the present study is of the
same general type in Rumex species (dicotyledonous
wetland plant) and has been termed “honeycomb” by Justin
and Armstrong (1987) and Laan et al. (1989). Honeycomb
aerenchyma has been classified as schizogenous by Justin
and Armstrong (1987) and Laan et al. (1989), but it is also
clear that this type of aerenchyma arises from “differential
expansion” (Seago et al. 2000).
In longitudinal sections, cortical cells were usually elon-
gated in the plane of the root axis and joined together
forming longitudinal files. Consequently, the longitudinal
471
intercellular spaces were essentially tubular and non-
tortuous in character (Justin and Armstrong 1987; Jackson
and Armstrong 1999).
Conard (1905) long ago noted that in Nymphaea the
expansion of the lateral cells caused an increase in the size
of lacunae and of the root itself. The mature aerenchyma of
Nymphaea contains wide lacunae interrupted by dia-
phragms with small intercellular spaces. Some of the dia-
phragms appear to be punctured by astrosclereids that
would presumably aid longitudinal air flow. As shown in this
paper, Sonneratia alba has long aerenchyma tubes without
diaphragms. Therefore, sclereids do not serve this function
(puncturing the diaphragms) in this species. Besides the
absence of diaphragms, this species has numerous small
pores on the lateral walls of aerenchyma tubes. The small
pores will support the orthographical transport of oxygen
against the root axis. We observed sclereids only in the
thicker roots (cable roots and pneumatophores) in S. alba.
The absence of sclereids in the narrower roots (anchor roots
and feeding roots) may mean that the sclereids serve only
as mechanical support in the thicker roots.
Root porosity as link to aerenchyma formation
Root porosity in all root types of Sonneratia alba showed
that these organs contain high percentages of gas spaces
(39–60%). This condition was also found in many emergent
wetland plant species: Nardus stricta (41.6%), Eriophorum
angustifolium (50.6%) (Smirnoff and Crawford 1983);
Carex nigra (31.6%), C. otrubae (36.7%), Juncus effesus
(36.1%), J. inflexus (53%) (Justin and Armstrong 1987); and
Halophila ovalis (37%) (Connel et al. 1999). Other man-
grove plants with data taken from seedlings also showed
various degrees of root porosity: Avicennia marina (45.7%),
Rhizophora stylosa (27.9%), Bruguiera gymnorrhiza
(30%), Aegiceras corniculatum (27.4%), Hisbiscus tiliaceus
(14.8%), and Excoecaria agallocha (17.8%) (Youssef and
Saenger 1996). High porosity is characteristic of plants
adapted to growth in anaerobic sediments or flooded con-
ditions, as it enhances the internal movements of gases
(Sifton 1945; Armstrong 1979; Justin and Armstrong 1987).
The high porosities in S. alba would facilitate the movement
of oxygen from the aerial to the underground part of the
roots. The porosity is higher in the pneumatophores
(60.7%) and cable roots (50.1%) than in anchor roots
(41.1%) and feeding roots (38.9%). Oxygen is taken in by
pneumatophores at their lenticels which are aerial above
the ground. The oxygen is supplied to feeding roots through
the pneumatophores and to anchor roots through the pneu-
matophores and cable roots. The feeding and anchor roots
are situated at the end of the oxygen pathway. Therefore,
the lower porosity in these two root types may be adequate
for oxygen requirements.
High porosity in wetland plants is attained at various
distances behind the root apex. S. alba attained high poros-
ity within 80–100 mm of the root apex (38–60%). Other
wetland plants with schizogenous aerenchyma, such as
Rumex palustris, attain high porosity within 5–10 mm (40–
472
45%), Carex acuta within 70–80 mm (40–45%) (Laan et al.
1989; Visser et al. 2000a), and Spartina alterniflora and S.
anglica within 80–100 mm (25–35%) (Maricle and Lee
2002).
The strategy of aerenchyma development in response to
anaerobic conditions may involve a tradeoff between main-
taining physiological function and reducing tissue respira-
tion. While the aerenchyma system can provide benefits to
the plant in terms of facilitating oxygen transport and
increasing metabolic efficiency, the formation of aeren-
chyma also presents certain costs. Loss of cortex tissue can
impede other root functions such as water and mineral
uptake and transport (Moog 1998). Nonetheless, the aeren-
chyma in Sonneratia alba develops well and maximally in
all root types. The present study revealed that this plant has
developed the structural adaptation in its roots as an adap-
tation to its anaerobic habitat.
Acknowledgements We thank Prof. Tokushiro Takaso, Research
Institute for Humanity and Nature, Kyoto, and the staff of Iriomote
Station, Tropical Biosphere Research Center, University of Ryukyus,
for their great support in our field research; Dr. Qiang Sun for helpful
comments and criticism on the manuscript. We also thank Kazutaka
Kobayashi, Takahisa Tanaka, Youichi Hasegawa, Masanori Seki, and
Hiroaki Terasawa for their field-sampling assistance.
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