Download The Structure and Development of Eriocaulon septangulare With.

422
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
The Structure and Development of E r i o c a u l o n s e p t a n g u l a r e With. BY DR C.
LEIGHTON
HARE
(With Plate 22 and 40 Text-figures)
M.A., D.Sc., F.L.S.)
(Communicatedby Prof. J. MCLEANTHOMPSON,
[Read 7 June 19451
INTRODUCTION
Eriocaulon septangulare With., the subject of the present study, is a small, submerged
aquatic plant, the sole European representative of a large genus of well over two hundred
species, the great majority of which are plants of swampy soils, with a wide distribution
in the tropical and subtropical regions of both hemispheres. The present species occupies
a n extensive tract in the north-eastern United States and the adjacent parts of southern
Canada, but elsewhere is found only along the western seaboard of Ireland and in a few
isolated localities in the Hebrides. Thus it belongs to the small group of less than a dozen
plants, of diverse afhities, that together constitute the North-American element in the
British flora. The whole region within which E. septangubre is found in our islands forms
but a very small outlier, separated from the main area of the species in North America
by two thousand miles of open ocean. This striking discontinuity in the geographical
range of the plant, its occurrence far to the north of the bulk of the genus, its presence
on both sides of the Atlantic but its absence from the mainland of Europe, together with
its restricted distribution within the British Isles-collectively these facts present a
complex of problems of peculiar interest.
A good deal of discussion has centred around the North-American species in our flora,
and the problems involved have given rise to much speculation and not a little controversy, but progress in solving them may well have been hindered by the tendency to
regard the group as a homogeneous one. The questions a t issue are admittedly difficult,
and, if a further advance is to be made, a fresh approach seems necessary. A full list of
the plants comprising the North-American element, together with a summary of their
distribution, will be given in a later paper and it need only be stated here that they
differ from one another not only in their natural affinities and their life forms, but also
in their means of dispersal, their habitat requirements, and their respective ranges. Nor
can we assume that the manner of their introduction to Britain and the time of their
arrival here are necessarily the same for each of them. It would, in fact, be true to say
that every member of the group really presents a distinct and separate set of problems.
The most promising approach would therefore seem to be to confine attention to a single
species. The present study is concerned solely with E. septangubre. Its primary aim has
been t o examine afresh the questions raised by its peculiar geographical distribution and
to shed some further light on these, but more especially to arrive a t a clearer understanding of the restricted range of the species within the British Isles.
From the outset it became clear that little progress could be looked for until the
biological equipment and autecology of the species had first of all been investigated; for
these, together with certain historical factors, must have determined its present distribution. With this end in view, field studies have been carried on over a number of
years, a t first in Ireland, and later in the Hebrides. At the same time the plant has been
grown in culture under various conditions on a considerable scale, while further information has been gleaned from transplant experiments carried out a t several localities
in Scotland. I n this way the life history of the plant has been worked out and a general
picture of its climatic and edaphic preferences and tolerances gradually built up, though
many details of this picture still remain to be filled in.
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
423
Special attention has also been devoted to the structure and development of the
species, for although the relationship between structure and function may not always
be entirely clear, there can be no doubt that the morphology and anatomy of a plant will
often illuminate its particular mode of life and the nature of its adjustment to its environment. This is perhaps especially true when, as in the present instance, the species is a
fully submerged aquatic while the genus as a whole is predominantly terrestrial.
For convenience, the results obtained in the course of the investigation will be described
in two papers. The first of these, presented here, deals with the morphology and anatomy
of E. septangulare and their relation t o its environment. The second paper, to follow later,
will give an account of its biology and ecology, and will include a full discussion in
which the geographical distribution of the species will be re-examined in the light of the
facts which have emerged as the work proceeded.
ERIOCAULON
Apart from taxonomic studies, which do not concern us here, the literature relating to
the genus Eriocaulon is not extensive, while the present species has hitherto received but
little attention.
I n 1888 Poulsen published a paper on the anatomy of the family Eriocaulaceae. He
selected a series of types, representing each of the genera included a t that time in the
family, and one species of Eriocaulon ( E . helicrysoides) was described. I n 1903 there
appeared W. Ruhland’s comprehensive monograph on the family Eriocaulaceae. I n this
work, the detailed systematic descriptions are preceded by an introductory chapter giving
a general account of the range of structure met with in the family, and there are some
isolated references t o the present species. A paper by Holm (1904) dealt with some
features of interest in the histology of a single American species of Eriocaulon ( E . decangulare): further reference will be made t o this paper in describing the anatomy of
E. septangutare.
The French systematist Lecomte, in addition t o describing a number of Chinese,
Indo-Chinese, and Madagascan species of Eriocaulun, published three papers in 1908
dealing with some points of interest in the biology and anatomy of some of them. I n
one of these he gives an account of the remarkable method of dispersal of the fruits and
seeds of two species from swampy ground in Indo-China. I n these, the sepals have undergone a peculiar modification t o form a float, closely resembling in shape the shell of a
nautilus, whereby the fruits are prevented from sinking and are wafted on the surface of
the water t o emergent land, where germination can take place under conditions favourable to the establishment of the seedling. I n another paper Lecomte discusses the
nature of the curious glands, found near the tips of the petals in species of Eriocuulon,
and provides some evidence for his belief that these structures am really nectaries. I n his
third contribution Lecomte shows how certain anatomical peculiarities of the scape can
be employed as an aid t o the identification of some species of Eriocuulon.
I n 1919 another French botanist, L. A. Malmanche, published a thesis dealing with the
comparative anatomy of the Eriocaulaceae and some adjacent families, mainly with
a view to establishing their real sanities. A short general review of the anatomy of the
Eriocaulaceae is given in Part IV of Solereder and Meyer’s Systematische Anatomie der
Monocotyledonen (1929), in the course of which there are occasional references to E .
septangulare. I n a comparative treatment of the structure of monocotyledonous seedlings,
Boyd (1932) described the mature seedling of a single unidentified species of Eriocaulon.
Her interpretation of this seedling, which differs from that of the present writer, will be
fully discussed in a forthcoming communication.
Finally, there are three papers dealing specifically with E. septangulare. A lucid account
of its embryology and floral development (referred t o again later) was given by Smith in
PREVIOUS LITERATURE RELATING TO
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LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULaRE WITH.
1910. A brief paper by Solomon (1931),on some features of the anatomy of the rhizome
and root, displayed some confusion of thought and was marred by inadequate and
misleading illustrations. Adam, in 1933, described the successful cultivation of E . septungulare a t the Royal Botanic Gardens, Edinburgh, but recorded the failure of all attempts
to obtain germination of its seeds.
No comprehensive account of either the anatomy, ecology, or geographical distribution
of E. septangulare has hitherto appeared.
(a) MORPHOLOGY
General habit of growth
E. septangulare is, in its normal state, a fully submerged aquatic species, growing rooted
in the substratum beneath still waters. It is a gregarious plant, and in favourable habitats
will often cover considerable areas with a close, continuous sward. Plate 22, fig. 1,
shows a small colony of flowering individuals, left stranded above water during a period
of drought; but the general habit of growth is best displayed by an isolated specimen
and will be gathered from Plate 22, fig. 2, which shows a plant in vegetative condition,
after two seasons' active growth in culture.
Although the structure of the flowers is usually very constant, in other respects the
species is a variable one, individuals differing much in size and vigow, as well as in the
dimensions and proportions of the several organs. The more extreme forms encountered
in the field will be dealt with later, and the following description is based on typical
average individuals growing under normal conditions.
The plant has a short, tapering rhizome up t o 5 cm. long and 5 mm. a t its widest part,
attached to the substratum by very numerous adventitious roots, and terminating in a
rosette of bright green, narrow, sharply pointed leaves. The rhizome is creeping and, if
allowed sufficient room, grows forward horizontally over the soil surface, but in closely
packed colonies may assume an oblique or almost vertical position. As growth proceeds
throughout the warmer months new leaves continuously unfold, while the older ones
progressively die away, so that once maturity is reached the terminal leaf rosette remains
practically constant in size, while the greater part of the rhizome is then devoid of leaves.
Each 8eit8on a fresh increment of some 2 4 cm. is added to the rhizome, while the portion
formed in the previous season shrivels up as its food reserves are depleted, leaving only
the vascular cylinder (which often persists as a tough, hard core for one or more years
longer). The appearance of the plant towards the end of the season, with its Iris-like
horizontal rhizome, terminal leaf rosette and abundant roots, can be clearly seen in
P1. 22, fig. 2, which shows also on the right the shrunken remnants of the previous
season's growth. During the winter months the plant enters on a period of rest and
active growth ceases, although the leaves of the rosette remain green and are not shed.
Ramijhtion of the rhizome and vegetative reproduction
Branching of the rhizome can take place in two quite distinct ways : (i) by sympodial
branching, which is always associated with flowering; and (ii)by monopodial branching
which is of rarer occurrence, and usually found in sterile individuals only.
(i) Xympodial branching
The inflorescence is invariably terminal in position and the growing point is used up
in its formation. At the onset of flowering in early summer two buds arise in the a d s
of the uppermost leaves immediately surrounding the base of the young scape, one bud
on each side. As the scape elongates these buds develop into axillary branches, both
growing a t the same rate, so that by the end of the season two fresh increments of rhizome
have been formed, diverging a t an angle of about 20".This sympodial method of branching
is illustrated in Text-figs. 1-3, where the plants have been sketched after removal of all
LEIGHTON HAFLE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
425
the leaves except those of the axillary shoots, while in Text-fig. 2 the scape also has
been cut off so as t o display more clearly the forking of the rhizome. Text-fig. 1 shows
the condition a t the beginning, Text-figs. 2 and 3 that a t the end of the summer. As a rule,
axillary branches do not produce inflorescences in the season in which they are formed,
but in specially vigorous individuals they sometimes do so. When this happens, ramification of the rhizome is carried a stage further, for rudimentary branches of the second
order are always laid down a t the base of the secondary inflorescences, and in consequence, the rhizome may fork twice or thrice in a single season. This condition is
illustrated in Text-fig. 4, where I is the main inflorescence, and s, and s, the new axillary
shoots at its base (all other leaves having been removed). It will be seen that s, terminates
in a young secondary inflorescence i, while s2 has remained sterile.
(ii) Monopodial branching
Not all specimens of Eriocaulon flower in a given season, and those which do not,
frequently remain unbranched, but sometimes they resort to monopodial branching ;
buds arising in the axils of leaves some way from the growing point of the rhizome.
Monopodial branching of flowering specimens is a rare occurrence, but it has been noted on
one or two occasions : it seems to be associated with arrested development of the terminal
inflorescence. I n Text-fig. 5, which illustrates this condition, a and b are the normal
sympodial branches a t the base ofthe inflorescence I , while c and d are additional axillary
branches of approximately the same age, arising from the upper surface of the rhizome.
Branching of the rhizome of Eriocaulon, whether sympodial or monopodial, endows
the species with an effective means of vegetative increase; for as the older parts of the
rhizome progressively decay, the branches become isolated, each of them henceforth
leading an independent life. Once established in a suitable habitat, the plant can in
consequence spread rapidly.
The root and root-system
On fertile soils E. septangulure produces a vigorous and well-developed root system
(see P1. 22, fig. 2 ) ; on sterile or sandy substrata it is much reduced. The individual roots
are all adventitious and arise mainly from the lower surface of the rhizome, often breaking
through the bases ofthe leaves. They are pure white and translucent, soft in texture, very
flexible and have a curious and characteristic vermiform appearance, owing to the
presence of regularly spaced internal diaphragms. I n well-grown specimens they have
an average diameter of about 1 mm. and taper but little, except near the extreme tip.
The great majority do not branch a t all, but occasionally the more vigorous ones produce
a few very slender, secondary or tertiary branches. Root-hairs are entirely lacking. I n
contrast to the leaves, all the roots formed during the growing season persist until the
following spring.
The leaf
The leaf arrangement is two-ranked in the seedling but changes gradually to a rather
complex spiral as the plant matures. The phyllotaxy is then difficult to determine exactly,
because the horizontal or oblique position of the rhizome in relation to the incident light
results in a displacement of the leaves. The individual leaves, which are linear-lanceolate
in shape with a concave upper surface, are broadest just above the base and then taper
gradually to a very fine point. Their maximum length is about 7 cm. and their width
about 5 mm., but they are often smaller than this. Soft and rather brittle in texture and
bright green in colour, they are markedly translucent, and show a characteristic internal
fenestration, due to certain anatomical peculiarities which are described later.
The spathe and scape
The onset of the reproductive phase in the early summer is marked by the emergence
of the spathe in the centre of the leaf rosette; it takes the form of a narrow cylindrical
sheath, open only a t the extreme tip (Text-figs. 4,5). Growing a t first more rapidly than
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LEIGHTON HARE: THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
~sc.
Fig. 1
Fig. 5
Text-figs. 1-5. For legends see p. 427.
LEIGHTON HARE: THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
427
the scape, it forms a protective sheath within which the inflorescence slowly develops,
but after reaching a length of some 3-5 cm. it ceases to elongate, and shortly afterwards
the young capitulum breaks through the tip. This sequence of events is illustrated in
P1.22, figs. 3-5, which show how effectively the young inflorescence is protected throughout the early stages of its development within the spathe. The latter serves also as an
accessory organ of assimilation ; in colour, texture and internal structure i t resembles
a leaf in all respects except for its cylindrical form.
The scapes of E. septangulure are very variable in length, but in this respect show
a close correlation with the depth of water in which the plant is growing. I n very shallow
water they may not exceed a few inches, while in deeply submerged specimens they
reach several feet. I n North America they are stated t o reach 3 m. (Moldenke, 1937),
while Praeger (1934) reports scapes up to 3 ft. long in Ireland, but in Skye the writer
finds that they rarely exceed 2 ft. I n proportion t o their length they are remarkably
narrow, with a diameter (in an average specimen) of about 3 mm. just above the base,
and tapering gradually t o about half of this a t the apex. These dimensions are, moreover,
independent of the length of the scape, which is so buoyant that it needs but little
mechanical support. The cross-section is polygonal with projecting angles, but in spite
of the specific name of the plant, the number of angles is by no means always seven.
For example, out of ten scapes, all of approximately the same length, four showed six,
four others seven, while one had eight, and one nine sides. As it develops, the inflorescence axis frequently becomes spirally twisted.
The injlorescence
The inflorescence is a capitulum closely recalling that of some Compositae and Dipsacaceae and in the present species is almost spherical when young, though it becomes
broadly elipsoidal and vertically flattened as it matures (compare Text-figs. 1, 4).
At the same time the colour changes from nearly black t o pale grey as the flowers unfold.
The involucral bracts are usually five, though sometimes six in number, and the receptacle
is strongly convex and rounded on its upper surface. The flowers, each of which is subtended by a bract, are arranged in successive concentric whorls, which develop in centripetal order ; the members of any one whorl open simultaneously, although those near the
centre of the capitulum seldom reach maturity.
The total number of flowers in a given capitulum bears little relation to its size, although
in large heads of about 8 mm. in diameter the average number approximates one hundred.
The flowers are always unisexual, but the distribution of the two sexes within the capitulum is very variable and shows a number of features of interest. Although often
described as monoecious, this condition is in fact far from universal, unisexual heads also
occur, and these may be either male or female; again in monoecious heads although the
flowers of any one whorl are always of one sex, the distribution of sexes within the heads
shows great variability. Flowers of different sexes do not occur in alternate whorls nor
are they always grouped together near the centre or a t the periphery of a head, as stated
in some Floras; the arrangement is, in fact, irregular and unpredictable and varies from
head to head. These and other features relating t o the capitula are illustrated in Table 1,
Text-figs. 1-5. General morphology of the plant and mode of branching of the rhizome. Text-fig. 1.
A plant a t the beginning of the growing season, showing the young axillary shoots s1 and se at
the base of the developing inflorescence I . sp., base of spathe (the rest has been removed). ( x 1.)
Text-fig. 2. A plant at the end of the growing season, showing the fully developed axillary shoots
s1 and s, diverging from the base of the scape sc. ( x 1.) Text-fig. 3. Base of same plant as in Textfig. 2, after removal of scape, showing sympodial branching of the rhizome. ( x 2.) Text-fig. 4.
Plant in which one axillary shoot s1 has produced a secondary inflorescence i. cp., capitulum;
I, base of inflorescence. ( x 1.) Text-fig. 5. Plant showing sympodial branches a and b at the
base of the inflorescence I,and additional branches c and d arising farther back along the rhizome.
The young capitulum is still enclosed in the spathe. ( x 1.) [Note. I n all the plants figured
above, leaves (other than those of the branches) have been removed.]
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which shows the results of flower counts in a series of capitula of different kinds and
sizes. It will be seen that in five of the capitula, all of about 8 mm. diameter, the total
number of flowers ranged from 96 t o 137, while in two others, both about 6mm. in
diameter, the numbers were 30 and 72 respectively. Again, in the monoecious heads the
ratio of female to male flowers vaned from less than 1 t o over 14, though, on the average,
female flowers considerably exceed the male in any one capitulum. It should be added
that among the unisexual heads the female greatly predominate ; only one entirely male
head has in fact been noted among the large number examined (see no. 7 in Table 1).
It is clear that in E . septangutare there is an effective mechanism for securing crosspollination, for in monoecious individuals the sexes are separated in time of development,
while in dioecious ones there is spatial segregation. I n a mixed colony, however, many
flowers of both sexes will mature simultaneously.
Table 1
No.
1
j
Diameter of
capitulum
(=.)
Total no.
of flowers
Male
flowers
Female
flowers
97
96
137
72
100
122
30
36
52
9
30
0
0
30
61
44
128
42
100
122
Total 654
157
497
0
In capitulum no. 3 in the table the nine male flowers were confined to the outermost whorl.
The jlowers
The morphology of the flower of Eriocaulon presents certain difficulties, and contradictory statements are still t o be found in the literature regarding it. This uncertainty
can be attributed in part t o the minute size of the flowers, which do not exceed 2 mm. in
length, and partly to the fact that in the course of development, the form and arrangement of the parts become much modified by intercalary growth. Hence, it is only by
following its ontogeny that the morphology of the flower can be interpreted with confidence. The structure of both male and female flowers is, on the whole, uniform and
constant, but a considerable number have been found which depart in various ways
from the normal type: these will be described in a separate paper, and the account which
follows refers to normal flowers only. It should, however, be mentioned that these
exceptional flowers provide evidence for the belief that the unisexual and dimerous flowers
of E . septangulare have been derived by reduction from an ancestral type which had
perfect ones constructed on a completely trimerous plan.
(i) The femalejlower
This is shown in bud, just before opening in Text-fig. 9 and fully developed in Textfig. 10 (after removal of the bract and the anterior petal, so as to display the gynaecium
t o better advantage). The two sepals, strongly concave and bearing a terminal tuft of
glistening white hairs, completely enclose the flower when in bud, but partially separate
and become reflexed a t the tip during anthesis. The two petals are free and strap-shaped,
tipped with white hairs and provided on the upper surface with an ovoid, subterminal,
glandular structure, whose real nature and function have long been in doubt. Usually
referred t o in taxonomic descriptions simply as a gland, Lecompte, in 1908, suggested
that it might be a nectary and (working apparently with herbarium material) he obtained
Fig. 6
b.
t.
Fig. 8b
ovu.
Fig. 11
Fig. 9
Fig 10
Text-figs. 6-11. Morphology of the flower. Text-fig. 6. Fully developed male flower, after anthesis.
( x 20.) Text-fig. 7. Immature male flower with subtending bract. ( x 20.) Text-fig. 8a. Very
young male flower, after removal of sepals. ( x 25.) Text-fig. 8 b . The same flower, after removal
of petals and two of the stamens. ( x 25.) Text-fig. 9. Nearly mature female flower, before
anthesis. ( x 20.) Text-fig. 10. Fully developed female flower, after anthesis; one petal removed.
( x 20.) Text-fig. 11. Gymecium of female flower, with ovary wall dissected away. ( x 20.)
[b., bract; s., sepals; p.$ petals; g1 and g,, petal glands; g3, gynaecial glands; st., staminodes;
ow., ovary; om.,ovule.]
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LEIGHTON HARE : THE STUDY O F ERIOCAULON SEPTANGULARE WITH.
some evidence that in two Indo-Chinese species of Eriocaulon these petal glands secrete
a reducing sugar. I n the present species it was found possible to collect and test the
actual secretion from the glands of living flowers and the results of these tests, coupled
with observations on the behaviour of visiting insects (to be described later), make it
clear that a t least in E. septangulure these petal glands do in fact function as nectaries.
The bilobed, bilocular ovary is shortly stipitate, and terminates in a style of variable
length with two divergent, hairy stigmas. Each loculus contains a single orthotropous
ovule, pendulous from its upper and inner extremity. Occasionally, one of the ovules
fails to develop, but as a rule each gives rise to an ellipsoidal or subspherical seed, which,
when mature, completely fills its loculus. I n Text-fig. 11 a mature gynaecium is shown,
with the ovary wall dissected away so as to reveal the ovules and their mode of attachment to better advantage. Immediately beneath the heart-shaped ovary and attached to
the short stalk which supports it are four minute emergences, arranged in two pairs lying
respectively in the anterior-posterior and lateral planes, one pair inserted slightly above
the other (see Text-fig. 10). Though extremely small, these structures are always
present in the living flower, yet they have been generally overlooked, and in taxonomic
descriptions are very rarely referred to. They were noted, however, by Saunders (1939)
who (presumably on comparative grounds) regarded them as staminodes. Some of the
abnormal flowers found by the present writer provide conclusive evidence that this
assumption is correct.
(ii) The male flower
This is also dimerous in arrangement, as seen in Text-fig. 7, which is a sketch of a
young male flower, together with its subtending bract. Text-fig. 6 shows, on the same
scale, a male flower just as it reaches maturity, but before dehiscence of the anthers
(the bract and one sepal have been removed). The two sepals are free, but the corolla
gives a t first the impression of having a trumpet-shaped tube with two divergent lobes,
and this is how it has usually been interpreted. Thus Hooker (1930) describes the inner
perianth of Eriocaulon as ‘a two- to three-lobed tube’ and speaks of the stamens as
‘inserted on the tube’. A very similar statement is made by Le Maout & Decaisne (1873),
while more recently Rendle (1930) says ‘the petals form in the male a two- to three-lobed
tube, on the upper part of which stand the stamens’. I n contrast to these authors,
Ruhland (1903) and Hutchinson (1934) describe the petals as ‘free’ but do not refer to
the mode of insertion of the stamens. It is evident, therefore, that the morphology of the
male flower presents some difficulty and that it has been interpreted in different ways by
different workers. The difficulty arises because of the extensive intercalary growth of the
axis in the development of the flower of Eriocaulon (a fact fist emphasized by Smith in
1910). This makes it necessary to study the early phases of development if the structure
of the mature flower is to be rightly understood.
Text-figs. 8a, b show a very young male flower: in (a)the sepals have been removed,
and in (b)the petals and two of the stamens in addition. At this stage it is easy to remove
the petals, leaving all four stamens in situ, when it becomes clear (1) that the latter are
inserted directly on the floral axis, and ( 2 )that the part of the flower below the level of
insertion of the stamens is solid, not hollow. Evidently, therefore, this portion of the
flower should be regarded as a torus, on the rim of which both petals and stamens are
inserted; during the later stages of development the torus grows rapidly, and eventually
simulates a corolla tube very closely;but the appearance is deceptive and careful examination a t sufficient magnification reveals its true nature.
Each of the petals is provided on its upper surface with a subterminal gland, larger
than those of the female flower, while the nectar-secreting mechanism of the male flower
is further augmented by two additional glands a t its centre. The latter are U-shaped and
occupy the upper surface of a shortly stalked organ, which terminates the floral axis and
rises slightly above the level of insertion of the stamens (Text-fig. 6). This organ is formed
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
43 1
a t an early stage in the development of the flower, just as the stamens are, and in the very
young flower represented in Text-fig. 8 b it can be clearly seen. There can be little doubt
that it should be regarded as gynoecial in origin; hence it provides additional evidence
of the derivation of the unisexual flower of Eriocaulon from a n ancestral type having
perfect flowers.
The seed
The seed, which is ellipsoidal in shape, is about 0.8 mm. long by 0.5 mm. wide and has
a light brown, smooth, tough and elastic testa (Text-figs. 12, 14). It is almost filled
with the white, starchy endosperm, while the minute UndifferFntiated embryo (whose
greatest dimension scarcely exceeds 0.2 mm.) is situated a t the extreme micropylar end.
I n taxonomic works, the embryo is usually referred to as ‘lenticular’, though Smith
(1910) is more precise and speaks of it as ‘bell-shaped, with flaring edges’; neither
description, however, quite conveys its true shape. When isolated from the seed and
carefully examined it is seen to have the form of a bi-convex lens, with a hemispherical
process a t the centre of one of its faces. It lies within the seed with this process immediately
opposite t o and directed towards the micropyle, so that when viewed from either end of
the seed, the embryo appears circular, while in longitudinal sections it has the shape
shown on the right of Text-fig. 13.
Embryology
A full account of the early stages in embryology is given in the paper by Smith (1910),
already referred to, and here it need only be said that he found that the development is
unusual, the embryo a t first passing through regular quadrant and octant stages, while
a suspensor is entirely absent. His account ends by emphasizing the striking lack of
differentiation of the resting embryo as it is found within the mature seed ; ‘at this stage ’,
he says, ‘there is no differentiation of the embryonic organs, nor any indication where
these shall have their origin’. This statement forms a fitting startingpoint for the
description given below of the post-seminal maturation of the embryo and the development of the seedling proper. The account should be regarded as a preliminary one, for it
is based on external morphological features only, and for this reason is couched in somewhat general terms. A fuller and more critical account and a comparison with other
monocotyledonous seedlings are in c o m e of preparation and will be presented as soon
as the histology of the embryo and seedling has been fully worked out.
Germination
On account of the lack of differentiation of the resting embryo the germination of
E. septangukcre necessarily takes place in two stages, though the transition between them
is a gradual one. The first stage covers the maturation of the embryo outside the seed
and the second the development of the seedling proper until it becomes established as
a self-nourishing plantlet.
Stage 1. The maturation of the embryo
The seed tends to settle on the substratum beneath the water with its long axis horizontal or nearly so, as shown in Text-figs. 12 and 14. I n this position the lenticular
portion p . of the resting embryo (Text-fig. 13, right) lies in the vertical plane, with the
process on its outer face immediately opposite the micropyle. When germination begins
in late spring or early summer the embryo first enlarges slightly, the inner face becoming
nearly hemispherical. The process (p., Text-fig. 13) then elongates and soon breaks through
the micropyle, appearing as a short, colourless, cylindrical body with a rounded end,
which grows forward horizontally till it reaches a length of about 1 mm. (Text-fig. 12).
If a t this stage the complete embryo is dissected out ofthe seed, it is seen to be mushroomshaped, as shown on the left of Text-fig. 13 (its parts are lettered t o correspond with
those of the resting embryo, so that the relation between the two will be apparent).
JOURN. LINN. S0C.-BOTANY,
VOL. LIII
2a
Fig. 13
Fig. 12
/c*
Fig. 16
Fig. 15
Fig. 20
Fig. 14
Fig. 17
Fig. 18
Fig. 19
Text-figs. 12-20. Morphology of the seed, embryo and seedling. Text-fig. 12. First stage in germhation, the embryo emerging from the micropyle. ( x 16.) Text-fig. 13. On the right the resting
embryo in longitudinal section; on the left the young embryo dissected from the seed. (Both
x 26.) Text-fig. 14. Second stage in germination. ( x 16.) Text-fig. 16. Another embryo at
same stage as Text-fig. 14, t o show lack of differentiation. ( x 32.) Text-fig. 16. Third stage in
germination showing the first leaf and rudiment of the second. ( x 12.) Text-fig. 17. Fourth
stage in germination, emergence of the radicle followed by the first adventitious root. ( x 12.)
Text-fig. 18. Another seedling at the same stage as Text-fig. 17, but showing the epicotyl, the
first node, and the strongly curved anchoring organ. ( x 12.) Text-fig. 19. A further seedling
of the same age, but possessing a definite hypocotyl. The seed has been dissected away to reveal
the ‘cotyledonary sucker’. ( x 12.) Text-fig. 20. A seedling 3 months old, showing the mature
habit, the seed still attached at the base, and one of the coiled roots. (8 natural size.) [n.,first
node; I,, Grst leaf; lz, second leaf; Tad., radicle; a.o., anchoring organ; cot., cotyledon; s., seed.
For other reference l0tbrS see text.]
LEIQHTON RARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
433
The distal end of p . now becomes clothed with a crown of rather stiff hairs, many of which
are backwardly directed, and a few days later a conical process c. arises on the upper side
of p . and half way along it. This grows vertically upwards until its length is about equal
to that of the horizontal portion from which it arises, so that the embryo as a whole is
now shaped like an inverted letter T (see Text-figs. 14, 15). Up to this stage, the
embryo is still colourless and undifferentiated, but the apex of c. now turns green and
a growing-point is organized here which gives rise to the plumule. With this event the
first stage in germination may be considered to end, for it is immediately followed by the
appearance of the first rudimentary leaf.
Stage 2. The development of the seedling
The embryo a t this time is still extremely small (its greatest dimension hardly yet
exceeds 1 mm.), but the first leaf grows rapidly and, after it has reached a length of a few
millimetres, the rudiments of a second one can just be discerned. The young seedling
now presents the curious appearance shown in Text-fig. I6 and it will be seen that there
is as yet no sign of a radicle. The latter organ, which in most plants is the fist t o emerge
on germination, is in the present species the last to appear. About this time, however,
it breaks through the base of the seedling a t a point vertically beneath the plumule: it
appears to be endogenous in origin. The axis of the seedling proper is now defined and it
will be seen that it is approximately a t right angles to the embryonic axis (Text-fig. 17).
The hairs, a t first confined to the tip of the axis, meanwhile gradually increase, and when
the radicle has reached a length of a few millimetres, they usually cover the whole under
surface of the seedling.
The hemispherical structure embedded in the seed is clearly the absorbing tip of the
greatly reduced cotyledon (the so-called ‘cotyledonary sucker ’) which is united to the
body of the seedling by a very short cylindrical limb passing through the micropyle.
This is made clear in Text-fig. 19 which shows a seedling a t a slightly later stage, where
the seed coat has been torn open and removed so as to reveal the structure within. That
part of the seedling which lies below the level of insertion of the cotyledon is usually
very much abbreviated, so that a hypocotyl can hardly be said to exist. Often, however,
there is a slight downward extension of the axis here, and occasionally a short but quite
definite hypocotyl is laid down (compare Text-figs. 17, 19). The epicotyl is better
developed, but it rarely exceeds a few millimetres in length ; occasionally, however, it
grows somewhat larger, so that a t this stage the seedling may have quite a slender appearance, as in the example sketched in Text-fig. 18. Subsequent internodes are always very
short so that the seedling soon assumes the squat appearance and rosette habit of the
mature individual (Text-fig. 20). The first adventitious roots arise in the epicotyledonary
internode (Text-fig. 17), the later ones in successively higher internodes, but the time of
their appearance varies considerably in different individuals.
Throughout the whole period of germination the seed remains firmly attached in a
lateral position a t the base of the epicotyl, where it is held in place by the pressure of the
testa around the cylindrical limb of the cotyledon, which is always of smaller diameter
than the absorbent tip embedded in the seed (Text-fig. 19). The seed is, in fact, held in
this way so effectively that it continues in position long after germination is complete.
It can be seen, for example, a t the base of the leaf rosette in Text-fig. 20, which is a sketch
of a seedling known t o be 4 months old, since it had been grown from seed.
Anchorage of the seedling
As noted above, the radicle is the last of the organs to appear, and long before it does SO
the seedling has become lighter than water, for even the &st leaves are provided with
the abundant aerenchyma which is so characteristic of every part of the mature plant.
In the absence of a radicle, some alternative mechanism must therefore be present for
securing the young seedling to the substratum, otherwise it would inevitably rise to the
2a2
434
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
surface and all hope of its establishment would then vanish. I n the initial stages of
germination, anchorage is effected by the distal end of the embryonic axis with its crown
of hairs. This may remain horizontal or, more frequently, bend more or less strongly
upwards (compare Text-figs. 16-18); i t becomes entangled in the particles of the substratum, holding the seedling in place, until fixation is later on secured in the normal way
by the roots. The mechanism recalls a grappling hook and does, in fact, function in the
same way. I n the mature seedling this curious anchoring organ appears as a lateral outgrowth at the base of the epicotyl, on a level with and opposite t o the cotyledon (Textfig. 19), but as explained above, it is actually a product of the still undifferentiated
embryo and is the f i s t part to emerge from the micropyle when germination begins.
Clearly this specialized anchoring mechanism is needed most urgently throughout the
Grst phase of germination (i.e. while the embryo is undergoing maturation outside the
seed) and also during the second phase, up to the time when the radicle and later the
adventitious roots appear. Towards the end of this period anchorage is rendered more
secure by the growth of hairs from the lower surface of the maturing embryo : the special
mechanism, however, remains functional until germination is well advanced. The need
for secure anchorage of the seedling even a t a relatively late stage is emphasized by the
frequent occurrence of twisted or coiled roots. A n example of the latter condition is
shown in Text-fig. 20, where one of the roots has coiled through 360" (presumably around
some object embedded in the substratum). Coiling of the roots, though uncommon, has
been reported in several other aquatic species (see Arber, 1920, pp. 205-6).
(6)
ANATOMY
The leaf
When examined in surface view the leaf reveals beneath its epidermis, even to the
unaided eye, a regular and highly characteristic reticulation, and under a magnification
of 15 diameters a short segment of it presents the appearance shown in Text-fig. 22. The
structures responsible for this elaborate pattern are made clear by transverse sections,
such as that shown diagrammatically in Text-fig. 24 which was taken across the lower
third of the leaf. The sinuous outline, most pronounced on the abaxial face, is due to the
presence of a series of longitudinal ridges alternating with shallow furrows, which extend
from the base t o the apex of the leaf. Internally, the leaf is traversed longitudinally by
a series of air canals (a.c.), each of which lies opposite one of the ridges and is crossed a t
regular intervals by a succession of transverse diaphragms, dividing the space within
into compartments about 0.5 mm. long. The canals are separated from one another by
strips of parenchymatous tissue through the centre of each of which runs a single vascular
bundle (v.6.) ; hence the bundles are situated opposite t o the surface furrows. It is these
internal structures, seen through the translucent epidermis of the leaf, which produce the
characteristic reticulation referred to above. Owing to the gradual narrowing of the leaf
the number of air canals seen in any transverse section steadily decreases as the section
approeches the apex. For example, a well-grown leaf about 3 in. long showed thirteen
canals a t its base; 2 in. higher they were reduced to six in number, while a t the apex o d y
the central one remained. There is a corresponding reduction in the number of vascular
bundles, each of which pursues an independent course and remains unbranched in its
passage through the leaf.
The structure and disposition of the assimilatory tissue show marked specialization.
There is first a single hypodermal layer of chlorenchyma (shown cross-hatched in Textfig. 24), whose component cells have their long axes parallel to the leaf surface. This tissue
is shown in surface view in Text-fig. 25, and it will be seen that it forms a loose meshwork
with abundant intercellular spaces. The assimilatory tissue of the leaf is further augmented
by the diaphragms, whose thin plate-like cells are richly provided with chloroplasts, giving
them a vivid green colour, in striking contrast with the adjacent colourless parenchyma.
Fig. 23
Fig. 22
Fig. 24
Fig. 25
Fig. 26
Text-figs. 21-26. Anatomy of the leaf. Text-fig. 21. A portion of the epidermis, showing the small
conical hairs. ( x 150.) Text-fig. 22. A segment of the leaf under low magnScation, showin@(
the characteristic fenestration. ( x 16.) Text-fig. 23a, b. A stoma in section and surfam
view. ( x 340.) Text-fig. 24. A diagrammatic trsnsverse section of the leaf. ( x 20.) a . ~ .a,ir
canal; v.b., vascular bundle; chE., subepidermal chlorenchyma; diaphragms shown dotted.
Text-fig. 26. The subepidermal chlorenchyma in surfme view. ( x 360.) Text-fig. 26. Shorn
under high magnification the area enclosed by broken lines in Text-fig. 24. ( x 160.) a1 and a,, the
inner and outer sheaths of the vascular bundle; A., hair in transverse section. The chlorophsts,
which are shown in black, are omitted on the right of the diaphragm.
203
436
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
The area enclosed by dotted lines in Text-fig. 24 is drawn under high magnification in
Text-fig. 26. It shows the large radially elongated epidermal cells, the single layered
hypodermal chlorenchyma, a portion of one of the partition walls which separate the
air canals, with its central vascular bundle, and finally to the right a part of one of the
diaphragms. The cells of the latter exhibit the elaborate stellate outline and numerous
small intercellular spaces so characteristic of these structures in hydrophytic species
(the abundant chloroplasts are shown in black).
The vascular tissue of the leaf is a good deal reduced, though less so than in many
submerged aquatic plants. Each of the larger bundles has several vessels, always spirally
thickened, but otherwise thin-walled and scarcely lignified : in the smaller bundles there
may be only a single vessel. The phloem is poorly differentiated and consists mainly of
parenchyma. Surrounding each bundle is a well-marked sheath of small cells, yellowish in
colour, with slightly thickened walls and elongated in the direction of the veins. Considerable discussion has centred around the so-called double bundle sheaths of the leaves
of Eriocaulaceae. Poulsen (1888) described them as occurring in the leaves of all the
genera he studied, including Eriocaulon, and they were referred to also by Ruhland (1903)
and Boyd (1932). Holm (1904), in his study of E. demngulare, concluded that the outer
sheath had little real validity, since its cell structure was indistinguishable from that
of the adjacent collenchyma of the mesophyll: moreover, the sheaths were lacking in
other parts of the plant. I n E. septangulare there is also an apparent double sheath
surrounding the vascular bundles of the leaf only, but the outer layer is ill-defined, and
examination shows that it is composed of cells which differ only in size from those of the
parenchymatous tissue within which the bundle is embedded (Text-fig. 26).
The epidermal cells of the upper and lower faces of the leaf are similar; narrowly
rectangular in shape, they have smooth, thin, non-sinuous walls and contain no chloroplasts. Although the leaves appear a t first sight to be quite glabrous, examination shows
that both surfaces bear regular longitudinal rows of small, bluntly pointed hairs; the
latter are arranged in narrow parallel bands, lying within the furrows of the leaf, but
absent, or nearly so, from the ridges. A small portion of the epidermis bearing three of
the hairs is shown in surface view in Text-fig. 21, while one of them is seen in vertical
section in Text-fig. 26. Each of the hairs comprises a small rectangular basal cell (cut off
from the underlying epidermal cell) and a conical terminal cell, bent over so as to lie
parallel to the leaf surface, with its tip directed towards the leaf apex.
Although in ordinary circumstances the leaves of the present species are continuously
submerged, they are, nevertheless, provided with stomata of quite normal appearance.
The latter are, however, confined to the abaxial surface and are present only in very small
numbers, with a frequency of the order of 10 per cm.2. One of them is shown in surface
view and in section in Text-fig. 23a, b. The guard cells are in the plane of the epidermis;
they are thickened in the usual manner and each is in contact with a subsidiary cell of
about the same size lying parallel to it. A further feature of the leaf, unexpected in a submerged aquatic species, is the presence of a hydathode at its distal end. Near the apex
the converging veins (here reduced to about three in number) unite to form a single large
one which extends almost to the extreme tip where there is a single terminal aperture
through which contact is made with the surrounding water. The significance of the
presence of stomata and hydathodes on the submerged leaves of E . septangulare is considered in the final discussion.
The spathe
I n discussing the morphology of the spathe its resemblance to a leaf was emphasized,
and this impression is reinforced when it is studied anatomically. Internally the two
organs are indeed almost identical, as will be apparent when Text-fig. 27, (a diagrammatic
transverse section of the spathe surrounding the scape), is compared with Text-fig. 24,
a corresponding section of the leaf. The air canals, diaphragms, and vascular tissue are
closely similar in both organs, and the same is true of their surface features and the
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULaE WITH.
437
Text-figs. 27-30. Anatomy of the spathe and scctpe. Text-fig. 27. Diagrammatic transverse section
of the base of the scape and the surrounding spathe. (The tissues are shaded to correspond to
those of the leaf.) ( x 26.) Text-fig. 28. Diagrammatic transverse section of apex of scape. ( x 26.)
Text-fig. 29. One of the large vascular bundles of the scape. ( x 490.) Text-fig. 30. Shows under
high magnification the area enclosed by broken lines in Text-fig. 27 ( x 114) (chloroplasts
omitted from cells of the diaphragm).
438
LEICHTON HARE : THE STUDY O F ERIOCAULON SEPTANGULARE WITH.
distribution of the stomata. In the spathe, however, assimilatory tissue is not found
beneath the inner epidermis, and the parallel vascular bundles show occasional anastomoses, especially as they approach the tip; but these minor differences only emphasize
the essential similarity in structure of the two organs, which should clearly be regarded
homologous. It is of interest t o note that in E. decangzclare studied by Holm (1904),the
anatomical resemblance between the leaf and spathe is also very close.
Stomata1 frequency per mm.a
Scape no.
1
2
3
At base
At apex
9.20
7.26
7.96
16.50
8.33
14.70
Total
2442
Average 8 4 4
39.53
13.18
I n surface features there is again a close parallel with the leaf; lines of hairs occupying
the furrows, while stomata are found in longitudinal rows overlying the intervening
ridges. The stornatal frequency is of considerable interest, for whereas on the leaf it is
LEIOHTON HARE : THE STUDY OB ERIOCAULON SEPTANGULARE WITH.
439
of the order of about 10 per
on the scape it has an average value of approximately
10-7 per mm.2, i.e. over one hundred times as great. A number of counts were made in
order to determine if the frequency was constant or not throughout the length of the
scape, and the results are embodied in Table 2.
The figures are in each instance the average of twenty separate counts, made from strips
of epidermis removed from the lower third and upper third of the scapes respectively.
The final average figures are thus based on sixty separate counts and show that
the frequency a t the top of the scape is over 60% greater than a t its base; a result
whose significance is dealt with later when the structure of the plant in relation to its
environment comes under review.
The rhizome
Text-fig. 31 is a diagrammatic transverse section across the middle region ofthe rhizome,
drawn to the same scale as that of the scape, while Text-fig. 33 shows on a large scale
a small portion of the inner cortex and the vascular cylinder. The latter is very narrow,
with a diameter less than a quarter of that of the whole rhizome, and comprises an outer
ring of small almost contiguous bundles, enclosing a group of larger ones, scattered
irregularly, the whole series inter-connected by numerous anastomoses (Text-fig. 33).
I n each bundle phloem predominates, the xylem being considerably reduced, with the
vessels feebly lignified and only spirally thickened. The stele is bounded externally by
a narrow band of sclerenchyma but possesses no true endodermis. The parenchymatous
cells of the stelar region contain abundant starch which is not found elsewhere in the
plant save in the endosperm of the seeds. The very wide cortex, traversed radially by
numerous leaf traces, and in its lower half by the large adventitious roots, shows two
distinct tissue zones (see Text-fig. 31); a narrow outer one of compact parenchyma
beneath the radially elongated epidermis, and a wide inner one composed of narrow,
thin-walled, cylindrical cells, longitudinally elongated and provided with numerous,
radially arranged, spine-like processes by which alone the cells make contact with one
another (shown in detail in Text-fig. 32). Thus the whole of this zone is permeated
by innumerable, narrow, interstitial spaces, providing the rhizome with a continuous
internal atmosphere; a further example of the elaborate provision for aeration which is
so characteristic of the species.
I n the apical portion of the rhizome, where the imbricated leaf bases protect the internodal surface, the latter is clothed with fine, white, silky hairs. These are multicellular
and uniseriate, tapering gradually t o a very fine point: though variable in length, they
may reach 5 or 6 mm. The longer ones are remarkable for the extreme tenuity of the
narrow, cylindrical cells of which they are composed, for these may reach a length of
1400p, although their average diameter is but 20p, i.e. the cells may be as much as
seventy times as long as they are broad. On the older parts of the rhizome devoid of
leaves the hairs break away, leaving the surface almost glabrous.
The root
I n certain respects the root of E. septangulare is the most highly specialized of all its
organs. There is very elaborate provision for the effective aeration of all its parts, its
most striking feature being the occurrence of numerous, evenly spaced, cortical
diaphragms; structures which, as already noted, give the roots the curious vermiform
appearance so characteristic of the species. While diaphragms are present in various forms
in many other parts of the plant, in the root they attain a degree of complexity unapproached elsewhere. Moreover, in the root they exhibit a striking radial symmetry,
and the relationship of their component cells both to one another and t o the intervening
cortical cells is remarkably precise and regular. I n the description which follows, it
should be understood that the root is assumed t o be in a vertical position and hence with
all its transverse planes horizontal.
440
LEIGHTON HARE : THE STUDY 03 ERIOCAULON SEPTANGULARE WITH.
Fig. 31
Fig. 32
Fig. 33
Text-figs. 31-33. Anatomy of the rhizome. Text-fig. 31. Diagrammatic transverse section across the
rhizome showing the central stele, the many small leaf traces Lt., the adventitious roots r. The
dotted line marks the boundary between the two zones of the cortex. ( x 19.) Text-fig. 32. Two
cells from the inner zone of the cortex drawn at high magnification, showing the spinous processes
by which they make contact. ( x 290.) Text-fig. 33. Small portion of the stele and adjacent
inner cortex. ( x 290.) [s.g., starch grains; v.b., vascular bundles; scl., sclerenchyma; aer., aerenchyma of cortex.]
LEIGHTON HARE : T H E STUDY O F ERIOCAULON SEPTANGULARE WITH.
441
There is a normal growing point and root cap, but root-hairs are entirely lacking.
Immediately behind the apical meristem the cortex is homogeneous, but at a distance of
approximately 1 mm. from it the diaphragms begin to appear. At first they are crowded
closely together, so that in the second millimetre of length about ten occur, but the
interval between them rapidly increases and soon attains its maximum and nearly
constant value of approximately 0.5 mm. Longitudinal and transverse sections of the
root tip and of the mature parts of the root not only display successive stages in the
ontogeny of its stelar and cortical tissues, but also show how the regular spacing of the
diaphragms is brought about. The cortical cells are a t first all alike; they are thin-walled,
isodiametric and arranged symmetrically in very regular radial files. Later, as growth
and differentiation proceed, alternate transverse layers of cells behave in a different
way. The cells of one such layer elongate rapidly in the direction of the axis of the
root, but apart from a slight increase in diameter remain unchanged, so that when
mature they give rise to a short cylinder of elongated, thin-walled parenchyma about
0.5 mm. long. The cells of the next layer do not elongate, but undergo elaborate change of
shape and slight thickening, to form one of the thin, rigid, disk-like diaphragms described
in detail below. This sequence of events is repeated with perfect regularity in all succeeding layers, so that in longitudinal section the cortex of the root shows a regular
alternation of long and short cells, as seen in diagrammatic form in Text-fig. 34. The
portion of this figure enclosed within dotted lines is drawn t o a larger scale in Text-fig. 35.
The stele (8.) is surrounded by a cylindrical sheath of two layers (sh,) and (sh2),whose
component cells exhibit in less extreme form the structure already noted in the cortical
cells of the rhizome (cf. Text-fig. 32) : the sheath is in consequence permeated by intercellular spaces. I n the radial longitudinal plane of Text-fig. 35 the cells of the diaphragm d.
have a relatively simple outline, for their horizontal faces are smooth and lie in contact
with the rounded ends of the long parenchymatous cells above and below them, but as
seen in transverse sections of the root they have an extremely complex shape. This will
be apparent from Text-fig. 38, which shows two of them in accurate outline drawn from
a projected image. I n the right centre of the figure they are seen in plan, above and below a t
(a)and (b) are sections along the planes A A and BB respectively, while to the left at ( c )
is a section along CC, the radial longitudinal plane of the root. The central part of
these cells is approximately cylindrical, but each has a thin marginal flange in the transverse plane broken up into a highly complex series of narrow, almost linear lobes,
which appear to be due to radial and tangential strains, accompanied by local lesions of
the middle lamella. Each of the cells has four main lobes, projecting diagonally one
from each corner ; and if these alone are retained and all minor lobing is omitted, the cell
outline can be reduced to the simplified diagrammatic form shown a t ( d ) in Text-fig. 38.
Text-fig. 39 shows a sector of a complete diaphragm. Although semi-diagrammatic, it
is drawn t o scale, with the cells in their true relative positions, but in order to avoid
confusion these have been given the simplified outline just referred to: in this way the
structure of the diaphragm as a whole can be more clearly displayed. The stele in the
centre (shown shaded) is surrounded first by two rings of sheath cells and then by five
concentric rings of diaphragm cells. It will be seen that, in the inner rings, strictlyradial
alinement of the cells is maintained, and adjustment to the increasing circumference of
successive rings is effected merely by a steady increase in the size of their component
cells. When the latter become unduly large (this happens first in ring 3 in the figure)
one or more of them in each ring is attached in the next outer ring to two smaller ones.
I n the figure this is seen in each of the cells lettered a to e , the outer ends of which have
in each instance bifurcated, so as to provide the surfaces of contact for the two smaller
cells joined to them in the following ring. The effect of this adjustment is that in the
outer rings the number of cells per ring steadily increases, so that the strict radial symmetry of the diaphragm breaks down. It will be clear, however, that besides preserving
a highly characteristic shape the cells are linked together throughout the diaphragm in
442
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
d.
c.p.
Fig. 35
Fig. 34
C
A
Fig. 36
1-:I
Simplified
'
Fig. 37
outline
0
Fig. 39
Figs. 3 4 4 0 . For legends see p. 443.
Fig. 38
Fig. 40
LEIGHTON HARE : THE STUDY O F ERIOCAULON SEPTANGULARE WITH.
443
a remarkably precise and regular manner. This is further emphasized by the constant
spatial relationship between the diaphragm cells and those of the cylinders of parenchyma
immediately above and below them; as indicated in Text-fig. 37, where a few cells of a
diaphragm are drawn with the overlying parenchymatous cells (shown by dotted lines)
superimposed upon them. If this figure is compared with those showing the radial and
tangential sections of the root (Text-figs. 35, 36) it will be clear that while each complete ring of diaphragm cells corresponds in position with a ring of parenchymatous cells
immediately above it, the individual cells of the two systems regularly alternate.
Text-figure 40 is a transverse section of the central part of a root and shows the stelar
tissues in detail. The endodermis has its cell walls uniformly but only slightly thickened.
The phloem is a good deal reduced, but the xylem is fairly well-developed and usually
takes the form of a single, large, central vessel (though two are not infrequent) surrounded
by a varying number (three to five) of smaller ones, which almost always abut directly
on to the endodermis, so that the pericycle is interrupted a t these points. Long ago
van Tieghem (1891) drew attention to this peculiarity in the roots of Eriocaulon, and the
matter was further investigated by Holm (1904) in E. decangulure. The latter found that
in this species the interruption, though often observed, was by no means constant and he
pointed out that this is true also of other families in which it had previously been reported:
for this reason he regarded this character as having little phylogenetic significance. There
are no purely mechanical tissues in the root, but the diaphragms themselves are relatively
rigid, while the intervening parenchyma is so soft and delicate that the epidermis sags
inwards in these regions, emphasizing the vermiform appearance of the roots. Clearly
this method of construction, while preventing collapse, imparts to the roots great flexibility. I n the older parts of the root there are signs of disorganization and partial breakdown of the parenchymatous tissue between the diaphragms.
Chromosome number
The chromosome number of the present species has not yet been determined exactly,
but preliminary counts made from metaphases in the cortical cells of root tips make it
clear that the number is in the neighbourhood of 60. Very few other species of Eriocaulon
have been hvestigatedcytologically ,but the chromosome numbers of three species are given
by Darlington & Janaki Ammal(l945) on the authority of Erlandsson. They are as follows
( X = 8 or 9): E . cinereum, 32; E. trumtum, 32; E . sexangulare, 36. Evidently, therefore,
the present species is a higher polyploid. The significance of this fact will be referred to
when the geographical distribution of the present species comes under review.
THESTRUCTURE OF ERIOCAULON
SEPXANGULARE IN RELATION TO ITS ENVIRONMENT
In concluding this account of the morphology and anatomy of E . septangulure it will be
of interest t o consider the structure of the plant in relation t o its aquatic environment.
Clearly the species is markedly specialized; indeed, it is not possible to examine it in
Text-figs. 34-40. Anatomy of the root. Text-%. 34. Diagrammatic radial longitudinal section of
the mature root, showing the disk-like diaphragms alternating with cylinders of parenchyma.
( x 44.) Text-fig. 35. Shows at higher magni6cation the portion of Text-fig. 34 enclosed by
broken lines, ( x 125.) [s., stele; 3h, and sh,, inner and outer sheaths; d., diaphragm; c.P., cortical
parenchyma.] Text-fig. 36. Diagrammatic tangential longitudinal section through cortex of
root. ( x 140.) Lettering as in Text-fig. 35. Text-fig. 37. A few cells of the diaphragm seen
from above; the simplified outline of d, Text-fig. 38, has been used. Overlying cortical cells shown
dotted. ( x 170.) Text-fig.38. I n right centretwocellsof thediaphragminaccurateoutline. ( x 400.)
a,section along A A ; b, section along BB; c, section along CC; d, simplified diagrammatic outline,
as used in Text-figs. 37 and 39. Text-fig. 39. A section of a diaphragm in surface view shown
diagrammatically, with the adjoining stele and its sheaths. 1 t o 5, the concentric rings of
diaphragm cells; a to e, diaphragm cells whose outer ends have bifurcated. ( x 125.) Text-fig.40.
Transverse section of the stele of a root showing pentarch structure and the protoxylem in contact
with the endodermis. ( x 490.)
444
LEIGHTON HARE: THE STUDY OB ERIOCAULON SEPTANGULARE WITH.
detail, or study its performance in the field, without recognizing how closely it is attuned
to the conditions which govern its life beneath the water. I n endeavouring to interpret
its structural peculiarities there is, nevertheless, an initial difficulty, for without resort to
carefully controlled experiment it would not be possible to distinguish precisely between
those features that are inherent in the genotype and those which may be due to the
direct, phenotypic response of the individual to its environment. Long familiarity with
the plant in the field, coupled with observation of its performance under diverse conditions
in culture, has, however, revealkd the fact that the present species is a n unusually plastic
one; both the external form and the internal structure of the individual plant can be
modified to some extent by corresponding changes in the milieu. Some account of these
observations will be given in a subsequent paper and in the following discussion the
salient stmctural features of E . septangulare, in its typical normal form, will be passed
briefly in review without considering how they have arisen, and an attempt will be made
t o relate them t o the conditions under which the species grows in its natural habitat.
With its narrow, subulate leaves, grouped in a compact rosette, Eriocuulon has a habit
of growth especially prevalent in those aquatic plants that grow rooted in the substratum beneath still water. Littorella uni$ora and Lobelia dortmannu, frequent associates
of Eriocuulon in the lochs of Ireland and the Hebrides, both resemble it in this respect,
while Isoetes lacustris, though taxonomically so remote from it, provides a still more
striking parallel. Leaves of the type referred t o are well adapted t o withstand the
fluctuating stresses set up by wave action, and it is perhaps significant that all the species
named inhabit the shallow margins of lochs and pools, where in stormy weather surface
movements can be quite severe. Plants with this habit of growth are not, however,
confined t o such situations.
A much clearer correlation with environmental conditions is shown by the seeding,
which, it will be recalled, possesses a peculiar anchoring device which secures it to the
substratum before the radicle appears, so counteracting its natural buoyancy and preventing it from rising t o the surface of the water beneath which it germinates.
It is, however, in its internal structure that Eriocaulon septangulare provides the
clearest evidence of accommodation t o sub-aqueous conditions. This is seen perhaps most
clearly in certain peculiarities in the structure and disposition of its tissues, particularly
those which are concerned: (a) with support, (b) with photosynthesis, and (c) with
aeration. These three aspects of its organization will be considered briefly in that order.
(a) Tissues concerned with support
It may be well to emphasize here that the problem of support in submerged aquatic
plants differs in certain fundamental respects from that of terrestrial species. I n the
first place, the former are protected from the bending and torsional stresses occasioned by
the wind, to which the great majority of land plants are exposed and t o withstand which
they must be adequately equipped. I n the present species this is reflected not only in the
absence of specialized mechanical tissues throughout the plant body but also in the
unusual disposition of its vascular bundles. I n all the organs of the plant, even those of
axial nature, the vascular strands are grouped near the centre; in none of them does the
usual peripheral series occur.
Although protected from the wind the plant is, as already noted, exposed to wave
action and it is of interest t o note that the parenchymatous tissues of the stem and leaf
and scape are so arranged that they provide in themselves the requisite degree of strength.
Thus, from the mechanical point of view, the leaf with its crescent-shaped cross-section,
its external corrugations and internal girder-like partitions is adequately stiffened, while
the scape with its alternating ridges and furrows, and its internal radial ribs, separated
by circular canals, has a typical columnar structure. I n this way both organs acquire
sufficient strength, yet do so without sacrificing either lightness or flexibility. There can
be no doubt that a nice adjustment of these three complementary qualities makes for the
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANGULARE WITH.
445
success of the species in its life beneath the water; a fact which may be overlooked when
it is grown in culture but which becomes clear enough when it is observed in its natural
habitat. The behaviour of the inflorescence axis provides a rather striking illustration.
This organ varies in length from a few inches when the plant is growing in shallow water
t o several feet when it is deeply submerged, and is so constructed that it achieves rigidity
when short yet becomes perfectly flexible when long. The reactions of the two kinds to
stormy weather are instructive. Whereas the short scapes withstand the shock of the
wavelets on shallow shores and remain upright and unbending, the long ones in deeper
water meet the menace of the larger waves not by resisting but by yielding to them,
bending and straightening again as the waves approach and pass, yet all the while
bearing aloft the capitula clear above the troubled water. Under the same conditions the
flowers of Lobelia Dortmanna, borne on rigid stems, often become waterlogged.
A further consequence of submergence is the upward reaction of the water, which acts
in opposition to the force of gravity. For Eriocaulon septangulare this upthrust exceeds
the weight of the plant itself, which is in consequence subject to a resultant force acting
upwards, not downwards as in all terrestrial species. With these conditions in mind the
absence of mechanical tissues throughout the plant is natural enough, for no part of it
has any weight t o carry; yet a t the same time the upthrust of the water may become
a positive danger, since it tends to drag the plant from its moorings. We have already
seen how this danger is met in the seedling by means of a special anchoring mechanism,
but the mature individual is exposed to the same risk and in a later paper, dealing with
the ecology of the species, it will be shown that the tendency to uprooting sets a limit
to the successful establishment of E . septangukre in certain habitats, which in all other
respects are highly favourable to it.
( b ) Tissues concerned with photosynthesis
The present species grows a t depths beneath the water ranging from a few inches to over
five feet, with the majority of individuals occurring within the range of one to three feet. The
water is usually clear ; nevertheless, some measurements made by the writer in the lochs
of Skye confirm Pearsall’s findings for the English lakes (1917), and show that the light
intensity under water falls off rapidly with increasing depth below the surface; a t a few
feet it is reduced to a fraction of its value in the air above. If, then, the plant is t o survive
and flourish under these conditions it is clear that it must utilize to the full its capacity
for photosynthesis, and certain peculiarities of its structure and organization are best
explained in the light of this necessity. Thus we find that not only the leaf but also the
spathe and scape are bright green and richly supplied with chloroplasts; each of these
organs plays its part in carbon assimilation. The role of the scape merits special consideration: appearing in late spring it persists throughout the summer and autumn,
when maximum demands are made on food resources, and is then discarded. Again,
although the leaf rosette a t soil level may be feebly illuminated beneath deep water,
the scape a t least reaches to the light; its upper, bright green portion, rising above the
surface, where it is always well illuminated. Moreover, the scape has a compensatory
action, for the more deeply submerged the plant, the larger the scape and the greater
the part this plays in photosynthesis; hence, it must have a balancing effect on the total
assimilation.
Passing to the internal structure of the leaf we find again signs of specialization. This is
seen perhaps most clearly in the unusual disposition of its assimilatory tissues, which are
arranged in two planes mutually a t right angles. There is first a subepidermal layer of
chlorenchyma beneath both faces of the leaf, forming a loose reticulum, with wide intercellular spaces. This renders the leaf markedly translucent and light penetrates it freely
to fall on the series of transverse diaphragms, which a t frequent intervals cross the air
canals traversing the leaf from base to apex. These diaphragms, which in most aquatic.
plants are colourless, or nearly so, are in the present species bright green and richly
446
LEIGHTON HARE : THE STUDY O F ERIOCAULON SEPTANGULARE WITH.
supplied with chloroplasts ;whatever other part they play their assimilatory role is patefit.
The structural peculiarities of the leaf of E . septangulare recall the ‘shade’ type of
organization and suggest equipment for e&cient assimilation in low light intensities.
(c) Tissues concerned with aeration
Turning now to the problem of respiration, it is evident that the manner of growth
of E. septangulare in dense colonies, rooted in finely divided silt beneath static water of
considerable depth, creates conditions which demand adequate supplies of oxygen and
effective provision for gaseous diffusion. The remarkable elaboration of its aerating
system-perhaps the most striking feature of the anatomy of the species-seems clearly
related t o this demand. All the submerged parts of the plant are provided with intercellular spaces, but the character of the air spaces in the several organs varies and
reflects their diverse functions and different environmental conditions. Thus for the root
and rhizome, buried in waterlogged soil or creeping over its surface, the need for oxygen
is most acute, and in these parts the aerenchyma exhibits small but very numerous
intercellular spaces, so that the internal atmosphere bathes almost every cell outside the
vascular tracts. For the leaf and spathe and scape, conditions are less severe and here we
find wide longitudinal canals which facilitate the downward diffusion of oxygen. Once
again the scape has a significant role, for it provides a channel of communication linking
the oxygen-starved organs below with the well-aerated upper layers of the water.
Eventually there is direct access to the air above, for the upper part of the scape, well
provided with stomata, rises at length above the surface of the water. The diurnal cycle
of gaseous exchange can be observed in a very direct way in the present species by a
change in colour. During the day, and especially in bright sunlight, oxygen accumulates
in the intercellular spaces, and the leaves and spathes then appear bright, glistening,
silver-grey beneath the water. With the onset of darkness assimilation ceases, and during
the night the oxygen is largely removed; partly perhaps by slow difhsion into the water,
but there can be little doubt that most of it is directly utilized in respiration. The result
is that with the returning light, the plant is seen to have lost its silver tinge and now
appears a bright grass green.
Finally, the occurrence of stomata and hydathodes on the leaves of E . septangulare
calls for comment. Both those structures might well be regarded as anomalous in a species
which is fully, and often deeply, submerged beneath the water; nevertheless, they have
been reported in several other plants of similar habitat. I n some of these the stomata
have been shown t o be permanently closed, roofed over by the cuticle, or otherwise
rendered non-functional and in all such instances they are doubtless vestigial; they
suggest that for the species in question the aquatic habit is derived rather than primitive.
In E . septangulare the stomata appear t o be quite normally constituted, but the frequency
of their occurrence on the leaves is so low that they can scarcely be of much significance,
nor is it likely that they would lead to flooding of the tissues unless a strong negative
pressure developed within the leaf.
On the scapes the stomatal frequency is much higher and steadily increases from the
base of the organ to its apex. I n terrestrial plants stomatal gradients of this kind ar0
well known (see, for example, Zalenski, 1904; Yapp, 1912)) and taken in conjunction
with other anatomical gradients of a similar kind they have been regarded as indicationa
of increasing xeromorphy; the distal portion of a leaf being farthest from the waterconducting tracts of the stem, while the upper leaves develop in an increasingly dry
atmosphere. I n a submerged aquatic plant such an explanation can hardly apply, since
all the stomata are laid down and develop in a uniform and constant humidity; but
however the gradient in stomatal frequency on the scapes of the present species may have
come about, it would appear to have real significance. It will be recalled that the upper
.part of the scape (where the stomata are relatively abundant) emerges at length above
the water, so that the stomata here have direct access to the air. Thus a diffusion
LEIGHTON HARE : THE STUDY OF ERIOCAULON SEPTANOULARE WITH.
447
gradient will be established in the wide longitudinal canals of the scape and the supply
of oxygen t o the submerged organs will be much facilitated. Throughout the reproductive
phase, therefore, the scape provides a channel of communication linking the roots and
rhizome of the plant, buried in waterlogged silt, with the open air above the water.
The hydathodes of E . septangulare closely resemble those reported by Sauvageau
(1891) in Potarnogeton densus and take the form of open pores a t the leaf apices. The
veins of the leaf converge towards this point, where the ultimate tracheids come into
open communication with the surrounding water. The writer has found that if the water
overlying growing specimens of the plant is lowered until the tips of the leaves just
protrude the surface, and if the plants are then covered with a bell-jar, the familiar
phenomenon of guttation 1s soon observed. Evidently there is a ‘transpiration stream’
throughout the plant, and since this must be maintained by the roots, the latter should
not be regarded merely as a means of anchorage, but as actively absorbing organs.
E . septangulare thus comes into line with other rooted aquatic plants in which a similar
movement of water has been demonstrated (Arber, 1920, pp. 260-6).
ACRNOWLEDOEMENTS
The greater part of the work involved in this investigation was carried out a t the University
of Aberdeen, and I desire particularly to thank Prof. J. R. Matthews for his kindly
criticism and advice :his interest in my work has been throughout a constant inspiration
and encouragement.
I am also indebted t o Sir Edward Salisbury and Dr C. R. Metcalfe, who kindly provided
facilities for continuing the work a t The Royal Botanic Gardens, Kew. Prof. J. McLean
Thompson has given me every encouragement to complete the work at the University
of Liverpool. I also acknowledge with gratitude a generous grant from the latter
University towards the cost of illustrathg the present paper.
Other friends and colleagues have helped me by supplying material and in various other
ways, for which full acknowledgement will be made in a forthcoming paper dealing with
the ecology and geographical distribution of E. septanguhre.
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EXPLANATION OF PLATE 22
Fig. 1. Shows a small colony of specimens of E. septangulare at Cregduff Lough, Connernara, Ireland.
(These are seen in the figure exposed above water after a period of drought.) This photograph,
taken by Mr Welch, is reproduced by kind permission of the author and publishers, from Dr R.
Lloyd Praeger’s The Botanist in Ireland (Hodges, Figgis and Co.), Dublin, 1934.
Fig. 2. An isolated specimen of E. septangulare which had been grown in culture at Aberdeen. (Actual
size.)
Figs. 3-5. Specimens selected to show stages in the growth of the spathe and scape. (Actual size.)
C. LEIGHTON HARE
Journ. Linn. SOC. Bot. Vol. LIII, PI. 22
Eriocaulon septangulare With.