Leaf Anatomy of the New Zealand Mangrove.
[Read before the Auckland Institute, August 9, 1939; received by Editor, March 20, 1940; issued separately, September, 1940.]
In New Zealand the mangrove formation comprises a single phanerogamic species referred in the present flora (Cheeseman, 1925) to Avicennia officinalis Linn., which is a widely ranging member of Schimper's eastern mangrove formation (1903). No anatomical study has hitherto been made of local material. The present investigation was carried out at Auckland University College under the direction of Professor T. L. Lancaster, to whom the author is indebted for encouragement and advice.
Leaves of the New Zealand mangrove are opposite, decussate and shortly petiolate. The lamina is elliptic-oblong, ovate-lanceolate or ovate (fig. 1), and coriaceous in texture. The upper surface is glabrous, rather glossy and yellowish-green in colour, the margin and midrib being yellow. The midrib is slightly raised and the
Text-fig. 1—A. Cross-section of lamina of mature leaf × 150. c, cuticle; e, epidermis; w, water tissue; p, palisade mesophyll; 1c, lower chlorenchyma; t, tomentum; s, stoma; tr, bundle-end tracheids.
B. Cross-section of lower epidermis and adjacent tissue × 250. cc, compact chlorenchyma; sc, spongy chlorenchyma; h, hypodermis; e, epidermis; s, stoma.
margin slightly reflexed. The lower surface is covered with short, dense, buff tomentum, and the midrib and main veins are prominent.
The petiole is semi-terete and, like the lamina, is glabrous above and tomentose below. A triangular hairy depression occurs in the upper surface of the broadened base of the petiole. It is shallow at its apex, which is directed towards the lamina, but deepens towards the base.
Leaves are frequently attacked by an Eriophyid mite which induces the formation of raised hair patches on the lower surface of the lamina. These are sometimes so numerous as to distort the leaf (fig. 1).
A cross section of the lamina of a mature leaf is shown in text-figure 1A, which is interpreted in the legend. Sections parallel to the epidermis (fig. 2) show that the lower chlorenchyma has the structure of ordinary spongy mesophyll in the interveinal areas. Adjacent
to the veins, however, it is compact and more nearly resembles palisade mesophyll. Where compact lower chlorenchyma occurs the epidermis is devoid of stomata, and there is a hypodermis comprising one or two layers of hyaline parenchyma (text-fig. 1B, figs. 2, 5, 17). Spongy chlorenchyma and stomata are thus confined to numerous small islands isolated in a network of veins and their accompanying compact chlorenchyma and hypodermis.
The veins ramify through the chlorenchyma. At first they project slightly into the water tissue. For some distance after they become completely submerged in the chlorenchyma contact with the water tissue is maintained through a flange-like projection of that tissue (fig. 5). The cross section of a primary vein is shown in fig. 4. Fibres composing the sheath are septate (fig. 3). The wood consists of spiral or pitted vessels embedded in elongated parenchyma, and the phloem of narrow sieve tubes, companion cells, relatively wide leptome parenchyma, and occasional bast fibres. The phloem embedded in the upper mass of septate fibres is found only in primary veins. It is frequently accompanied by a little xylem. The fibrous sheath tends to disappear as the veins grow smaller, persisting longest abaxially. The lower hypodermis increases to three or more cell layers beneath veins and thus comes directly into contact with the fibrous sheath except when the vein is small. Irregular groups of tracheids much wider than the conducting elements occur at bundle ends (fig. 6). Their walls bear spiral, reticulated or pitted thickenings.
The photosynthetic tissue thins out rather abruptly at the margin of the leaf (fig. 7). The water tissue is reflexed about the narrowed edge of the chlorenchyma and extended slightly below it, forming a narrow translucent border about the lamina.
Stomata are each accompanied by two subsidiary cells placed transversely to the pore (fig. 12).
The tomentum is composed of tricellular hairs, one of which surmounts practically every cell of the lower epidermis (fig. 10). The distal cell of each hair is thin walled and bladder-like, while the stalk cell has a characteristic cutinised thickening which makes the cell cavity dumb-bell shaped. In the basal cell a well-defined layer of the wall about the cell cavity stains more deeply with safranin than the rest. Cell contents are very meagre in hairs of this type. Hairs of leaves in the bud stage are peculiar in that each distal cell is drawn out into a long obtuse point directed towards the tip of the leaf (fig. 11). Such hairs cover both margin and lower surface of the young lamina.
Multicellular glandular hairs are present on both surfaces of the lamina. On the upper surface they are few in number (4–10 per sq. mm.) and occur singly at the base of the tubular infoldings of the epidermis (fig. 8). The head is composed typically of eight short columnar cells and the stalk consists of a single discoidal cell. This abuts on four to eight small modified epidermal cells. On the lower surface glandular hairs are relatively numerous (72–96 per sq. mm.) and differ from those of the upper surface in not being sunken, possessing a four-celled head, and having a single enlarged epidermal
cell at the base (fig. 9). They are much shorter than the non-glandular hairs. Glands are not especially numerous on the lower surface of young leaves, so it is obvious that new ones must form continuously as the leaves expand. On the upper surface, however, they occur so abundantly that they almost touch (fig. 18). It is evident that all glands present on this surface of the mature leaf are formed early in its development. They are at first superficial, but with the expansion of the lamina they are carried apart, and become sunken since only five layers of water-tissue are developed beneath glands, while elsewhere there are seven or eight (fig. 16).
The petiole and midrib.
The epidermis of the petiole resembles that of the corresponding surface of the lamina except that there are no glands or stomata on the underside. The parenchymatous ground tissue (figs. 19, 20) contains scattered mechanical cells bearing a lignified thickening which is reticulately pitted, the pits being sometimes so large that the thickening is reduced to a network of narrow strands. Well-developed lacunae occur at the sides of the petiole.
The vascular system is traced from the stem in the series of diagrams given in text-fig. 2. At the node the bundles (a) lying adjacent to the base of the petiole pass en masse into the petiole. A small group of bundles (c) is derived from further round the stem on either side. The intervening vascular tissue (b) forms the axillary bud traces (b' and b”).* A relatively large bundle group (d) is derived from still further round the stem on either side. The vascular tissue, with the exception of a small part (d') of each of the larger subsidiary groups (d) assembles about the central ground tissue of the petiole. The groups remaining at the side of the petiole (d') give rise to small veins at the base of the lamina (fig. 21). In some nodes the smaller subsidiary groups (c) were not observed.
The central ground tissue of the petiole includes numerous small bundles of phloem, the larger of which have a small quantity of xylem associated with them. These first appear shortly above the base of the petiole, and so increase in size and number that at the base of the lamina they contain a large part of the phloem passing into the leaf (figs. 20–22). No direct connection has been observed between this phloem and that of the main bundles of the petiole, but xylem elements have been seen in longitudinal sections to pass from the outer to the inner series of bundles.
Xylem in the petiole is composed of annular, spiral, or pitted vessels with transverse or slightly oblique end walls bearing a single circular perforation. These are embedded in rows in shortly elongated parenchyma. Phloem consists of numerous small sieve tubes and companion cells, occasional heavily thickened fibres, and leptome parenchyma. Cambium is fascicular only. The main group of bundles is ensheathed in non-septate fibres, many of which do not become lignified until they enter the midrib. Fibres ensheathing the small group of bundles at either side of the petiole are septate.
[Footnote] * There are two buds in each axil, and frequently both are functional in the inflorescence.
The midrib is structurally very similar to the upper part of the petiole (fig. 23). Veins are cut off from the ends of the crescentic fibrovascular mass so that it is gradually reduced to a circular form. The inner bundles consisting mainly of phloem, resemble, and appear to be continuous with, the bundles embedded in the septate fibres overlying main veins.
The depression at the base of the petiole is fringed with simple filamentous hairs composed of three or four cells (fig. 14), and lined with shorter hairs of the same type intermingled with glandular hairs much larger than those on the lamina (figs. 13, 18). The stalk and foot of each gland is unicellular. The head consists typically of four tiers, each comprising sixteen cubical cells. However, many glands are distorted by mutual pressure, as they are closely packed before the leaf is fully expanded.
Ecological significance of structure.
The salient structural differences between the leaf of the New Zealand mangrove and that of a typical mesophyte are due to the presence of tissues to which the function of water storage is usually ascribed (e.g. Haberlandt, 1914). The largest of these is the water tissue which constitutes approximately the upper half of the lamina. One or more layers of similar cells occur beneath much of the lower epidermis. Both tissues are in close contact with the veins. In addition, there is a highly-developed system of tracheids associated with the bundle ends. Subepidermal water tissue appears to be a common feature of mangrove leaves. Mullan (1931b), for example, records them in seven out of eight Indian mangrove species examined.
Typical spongy mesophyll is restricted to the immediate vicinity of stomata. This is in accordance with the general tendency for palisade mesophyll to predominate in leaves exposed to strong light (Maximov, 1929). It is possible that water tissue and tomentum are of value in reducing the intensity of light reaching the photosynthetic tissue.
The petioles of the two terminal leaves are opposed so that their basal depressions form a cavity enclosing the apical bud (fig. 18). Similar protection between petiole and stem is afforded for axillary buds. When a pair of leaves emerges from this cover their marginal tomentum is felted together and their upper surfaces remain in close contact until the glands thereon have sunken into the pits which protect them subsequently. Tomentum covers all other glands and also the stomata. Air which it imprisons when the leaf is submerged would have to be replaced before water could reach the stomata and enter the leaf. The work of Sen and Blackman (1933) on the injection of submerged leaves suggests that this would take a time far in excess of that for which mangrove leaves are ever submerged.
Leaf-bearing stems of mangrove are covered with thick cuticle and devoid of stomata and lenticels. The stem must thus be aerated through the foliage. The lacunar tissue in the petiole is apparently an adaptation for this purpose.
Fig. 1.—Upper row—Leaf types collected within a small area of dwarfed mangroves. Lower row—Leaves bearing raised hair patches caused by Eriophyid mites × ⅕. Fig. 2.—Section parallel to the lower epidermis × 44. c, compact chlorenchyma; s, spongy chlorenchyma; h, hypodermis. Fig. 3.—Septate fibres of a leaf vein in longitudinal section × 100.
Fig. 4.—Cross section of a main vein × 170. p1, phloem; p2, subsidiary phloem; x, xylem; f, sheathing fibres. Fig. 5.—Cross section of small vein × 270. w, flange of water tissue; c, compact chlorenchyma; h, hypodermis. Fig. 6.—Section through the chlorenchyma parallel to the epidermis showing a bundle-end × 170. t, tracheid. Fig. 7.—Cross section of the leaf margin × 110. w, water tissue; c, chlorenchyma.
Fig. 8.—Glandular hair on the upper surface of a mature leaf. a. Longitudinal section. b. Cross section through the head. × 530. Fig. 9.—Glandular hair on the lower surface of a mature leaf. a. Longitudinal section. b. Cross section through the head. × 530. Fig. 10.—Non-glandular hair on the lower surface of a mature leaf. a. Longitudinal section. b. End view of distal cell. × 250. Fig. 11.—Non-glandular hair on the lower surface of a young leaf. a. Longitudinal section. b. End view of distal cell. × 250. Fig. 12.—Stomata in the lower epidermis of the lamina. a. Cross section. b. Surface view. × 640. g, guard cell; s. subsidiary cell. Fig. 13.—Glandular hair in the depression at the base of the petiole. a. Longitudinal section b. Cross section of the head. × 530. Fig. 14.—Non-glandular hair from the depression at the base of the petiole. × 150.
Fig. 15.—Glandular haus on the upper surface of a very young leaf. × 880. c, cuticle. Fig. 16.—Glandular hairs becoming sunken into the upper surface of the lamina. × 180. Fig. 17.—Slightly oblique section along the lower epidermis of the lamina. × 260. s, stoma; e, ordinary epidermal cell; g, basal cell of gland; h, hypodermis. Fig. 18.—Longitudinal section through the stem apex. × 23. g1, glands on upper surface of young leaf; g2, glands at base of petiole.
Fig. 19.—Longitudinal section through the lacunar tissue at the side of the petiole. × 33 1, lacuna. Fig. 20.—Cross section of the petiole midway along its length. × 24. 1, lacuna. Fig. 21.—Cross section of the petiole at the base of the lamina. × 20. b, lateral group of bundles splitting up into veins. Fig. 22.—Cross section of the vascular tissue of the petiole at the base of the lamina. × 140. b1, main outer series of bundles; b2, inner bundles. Fig. 23.—Cross section of the midrib. × 48.
Large quantities of secretion are often present beneath the cuticle investing glands, particularly on young leaves. Its nature has not been investigated. Mullan (1931a) presents evidence indicating that similar glands on Indian halophytes secrete salt.
Literature on leaf anatomy of Avicennia.
Published accounts of leaf anatomy in the genus Avicennia are rather fragmentary. The earliest is that given by Wille (1883) of the leaf of A. nitida L. The petiole of this species resembles that of the New Zealand mangrove in possessing bundles of phloem in the pith which have no apparent connection with the extra-cambial phloem. There is a three-layered hypodermis beneath the upper epidermis of the lamina. The leaf is tomentose on both surfaces, the hairs being bicellular. Stomata are similar in type to those of the New Zealand mangrove, as are the glandular and non-glandular hairs at the base of the petiole.
Van Tieghem (1898) gives a general account of leaf structure in Avicennia which in most respects applies well to local material. The author states, however, that the petiole receives three meristeles from the stem, whereas in the New Zealand mangrove the number is usually five. A. officinalis is said to differ from the other two species of the genus in having three layers of water tissue instead of four or five. The New Zealand mangrove, though at present referred to that species, possesses a very well developed water tissue consisting of seven or eight cell layers.
Similar discrepancies in detail are evident when comparison is made with the work of Mullan (1931a, 1931b) in India. His measurements and illustrations show that in A. officinalis the water tissue consists of four cell layers and constitutes only one quarter of the thickness of the lamina. The tomentum, which is incompletely shown in his figures, appears to be composed of bicellular hairs, and some of the glandular hairs recessed in the upper surface of the lamina are unicellular. Glands very similar to those occurring in corresponding positions on the New Zealand mangrove do, however, occur on both leaf surface and at the base of the petiole. Practically identical glandular hairs are described also from A. alba Blume.
The difference in detail between the writer's descriptions and those of Van Tieghem and of Mullan suggest that the New Zealand mangrove may be distinct from A. officinalis. In his revision of the genus Bakhuizen van der Brink (1921) has transferred it to A. marina (Forsk) Vierh. var. resinifera. A comparative anatomical study of the genus would doubtless be of considerable assistance in delimiting species.
The leaf of the New Zealand mangrove varies considerably in form.
A water tissue beneath the upper epidermis occupies nearly half the thickness of the lamina.
There are three layers of palisade and approximately five of less elongated or isodiametric chlorenchyma. The latter is compact and resembles palisade in the vicinity of the veins, while in the interveinal areas it is spongy.
Stomata are confined to interveinal areas on the lower epidermis. They are accompanied by subsidiary cells.
The lower surface of the leaf bears a tomentum composed of hairs with bladder-like distal cells.
Water-storing tracheids occur at bundle ends.
Main veins contain subsidiary bundles consisting chiefly of phloem.
The petiole usually receives five groups of bundles from the stem. Bundles composed principally of phloem of unknown origin appear within the main ring of bundles in the petiole.
The cortex of the petiole contains lacunae and idioblasts.
Glandular hairs occur on both surfaces of the lamina and at the base of the petiole.
The probable significance of structural peculiarities of the plant is discussed.
Comparison with anatomical observations of overseas workers suggests that the New Zealand mangrove may not be referable to Avicennia officinalis Linn.
Bakiiuizen van der brink, R. C., 1921. Revisio generis Avicenniae, Bull. Jard. Bot. Btzg., Série 3, vol. 3, pp. 199–223.
Cheeseman, T. F., 1925. Manual of the New Zealand Flora, Wellington.
Haberlandt, G., 1914. Physiological Plant Anatomy, London.
Maximov, N. A., 1929. The Plant in Relation to Water, London.
Mullan, D. P., 1931a. On the occurrence of glandular hairs (salt glands) on the leaves of some Indian halophytes, Jour. Ind. Bot. Soc., 10, pp. 184–189.
— 1931b. Observations on the water-storing devices of some Indian halophytes, Ibid., 10, pp. 126–133.
Schimper, A. F. W., 1903. Plant Geography upon a Physiological Basis, Oxford.
Sen, P. K., and Blackman, V. H., 1933. On the conditions leading to the injection of leaves submerged in water, Ann. Bot., 47, pp. 663–671.
Van tiegiiem, M. Ph., 1898. Avicenniacées et Symphorémacées, Journ. de Bot., 12, pp. 345–365.
Wille, N., 1883. Om stammens og bladets bygning hos Avicennia nitida L., Bot. Tidsskr., 13, pp. 33–44 (French summary).