Root System of the New Zealand Mangrove By G. T. S. Baylis, Botany Department, University of Otago [Read before the Otago Branch, November 8, 1949; received by the Editor, November 11, 1949.]

tetrarch, with the metaxylem reaching the centre of the stele. The small pith of penultimate rootlets is composed of lignified cells, isodiametric in transverse sections, but in larger roots only the peripheral pith cells are of this nature, the inner zones grading rapidly into delicate lacunar tissue similar to the primary cortex, which is described below. This is not, however, the case in the upper subaerial parts of pneumatophores—in these these is relatively little enlargement of the intercellular spaces in the inner pith, and reticulately pitted lignified cells are scattered among the thin-walled ones.

A normal vascular cambium appears in all but the finest roots, though in penultimate branches its activity is very limited. The anomalous development of a succession of pericyclic cambiums which has been often recorded in stems of Avicennia (e.g. Solereder, 1908) is also a feature of main roots (Fig. 18), but it has not been observed in any of their branches. In pneumatophores the original cambium may build up a wood zone exceeding 1 mm. in width, whereas in main roots it is superceded by the first pericyclic cambium after forming less than half this quantity.

Secondary wood in stems is characteristically denser than in roots (Eames and MacDaniels, 1947), and it is noteworthy that pneumatophore wood has fibre and vessels with approximately half the diameter of those in underground roots. To this, and to lack of interxylary phloem, can no doubt be ascribed the flexibility of pneumatophores in comparison with which main roots are decidedly brittle.

Cortical Tissues

In all but the finest roots the primary cortex shows the extensive development of air spaces characteristic of marsh plants. The cortex of exposed parts of pneumatophores and of main roots that have not yet entered the mud, or have emerged from it owing to obstruction by rock, is com posed of cells in the form of a squat X, Y or T united by the ends of their arms into a network (Fig. 11). In longitudinal sections the meshes of this network prove to be lacunae of limited vertical extent, but the sheets of cells separating them are freely perforated by small intercellular pores (Figs. 1, 10). Scattered cells develop cutinised bars on their walls. These first appear in swollen bladder-like cells (idioblasts) which are present in young cortices, and the thickening runs along lines of contact with neighbouring cells. As the tissue ages these thickenings appear in an increasing number of ordinary cortical cells.

The cortex of exposed pneumatophores is firm, whereas that of all underground parts including pneumatophore bases is soft and spongy, with considerably larger air spaces. This different texture is due in part to greater extension of the arms of cortical cells and in part to actual collapse of numerous cells, their walls folding together so completely that what was originally a cell or plate of cells appears as a simple membrane (Figs. 12, 13). In the outer cortex about half the cells collapse, but in the deeper layers the proportion is less. In penultimate rootlets the cortical cells do not become drawn out into arms, but the tissue develops lacunae through collapse of cells (Fig. 16). Cell collapse is not a regular feature in the ultimate rootlets,

the cortex of which may remain fairly compact (Fig. 17). Thickening bars occasionally occur near the stele in large roots—apart from this they are absent from the original cells of underground cortices.

At the junction of branch and main roots there is an abrupt constriction of the branch and a diaphragm of small rounded cells passes obliquely across the cortex at this point. The cortical lacunae of the two roots intercommunicate only via the many small intercellular spaces of this layer which is, however, less than 10 cells through.

The phellogen is initially shallow-seated in mangrove roots and the primary cortex is thus persistent. It is sufficiently elastic to accommodate the limited expansion of the stele which occurs in branch roots, but not the continued secondary thickening of main roots. The tangential strain which this causes must be greatest where the circumference of the cortex is Ieast, that is to say nearest the stele, and it is here that subdivision of the cortical cells begins. Some of their stretched arms become divided into short chains of cells, and in addition a loose rubble-like tissue fills the old lacunae, its cells frequently reinforced with thickening bars (Figs. 4, 12, 13). This proliferation both expands and strengthens the cortex. It extends slowly outward, but does not appear to reach the outer layers before they are shed by an inward movement of the phellogen.

Formation by the phellogen of significant quantities of secondary cortex is restricted to main roots. This tissue is relatively compact and presents much the same appearance both in transverse and longitudinal sections (Figs. 5, 15). The cells are in radial rows and are united to cells of adjacent rows by slight prominences between which are a multiplicity of air spaces much smaller than those of primary cortices and not subject to any lysigenous enlargement. Thickening bars develop in many of the cells, often co-ordinated in irregular series. The phellogen forms initially at the periphery of the cortex, but later sheets of it extend inward and ultimately reach the stele, thereafter replacing the entire primary cortex by secondary cortex. As Fig. 6 illustrates, this replacement is effected piecemeal, and during the process the cortex is a mosaic of primary and secondary tissue.

Apical and Dermal Structures

The structure of the root apex is most readily interpreted in the finest roots. In some of these the median section clearly shows a tier of plerome initials surmounting one of periblem initials (Fig. 3), but this is not invariably discernible (Fig. 8). However, the dermatogen always appears as a well-marked layer of larger and clearer cells which crosses the tip and passes down the sides of the periblem and by its division forms the root cap. This cap is not large, but it does not slough off entirely behind the apex—part of it remains as a persistent investment about the cortex. Rootlets sectioned transversely where the stele is mature (Figs. 16, 17) show differentiation of their peripheral layers. The two or three outermost are of polygonal or somewhat collapsed cells, and the next is of small cells with a cellulose thickening on their outer and radial walls. This is underlain by layer of stout cells, beneath which occasional cross walls indicate the

beginnings of phellogen formation. It is not easy to determine which of these layers passes into the dermatogen when traced to the apex, as the sequence is never entirely unambiguous, but the interpretation given in Fig. 8 fits best all the material examined, i.e. the layer of small thickened cells appears to be the true epidermis with cap cells external to it and an exodermal layer beneath. Root hairs are never developed, but since they are often lacking in marsh plants (Haberlandt, 1928), one cannot assume that the persistent cap layers are fundamentally responsible for lack of hairs in mangrove roots.

The apical organisation of the larger underground roots is essentially the same as in rootlets. The region of convergence of periblem and plerome is broader (Figs. 2, 19) and the dermatogen, though still distinct at the apex, fails to develop a cellulose thickening when its meristematic function is completed. The exodermal layer is recognisable, however, in cross sections cut a few centimeters behind the tip, flanked by cap layers externally and cork cambium within (Fig. 7). As the pneumatophore emerges from the mud its apical structure rapidly changes. The small cap enlarges to a corky wart, and more than a dozen corky layers extend down the sides of the apex (Fig. 20). These increases are probably due in part at least to extension of the cork cambium into the apex, as has been described in Sonneratia (Troll and Dragendorff, 1931), but the situation is obscure, since the exodermis, which usually serves to delimit the cork from cap layers, is not distinguishable, and the cork cambium is a poorly defined layer in pneumatophores. The apices of aerial roots are structurally identical with those of pneumatophores.

The activity of the cork cambium is negligible in ultimate and penultimate rootlets, but in all larger roots it replaces the original surface layers by cork. This cork is interrupted by frequent lenticels on pneumatophores and aerial roots, and occasional ones may be found on other roots that have become exposed. Structurally the lenticels present no unusual features. They are of the type with loose complementary tissue and periodic closing layers of compact cork (Figs. 10, 11), and are identical with the stem lenticels of the plant.

Discussion

I have had access to only three papers in which the root system of Avicennia is treated in any detail, those of Brenner (1902) on A. tomentosa, which is doubtfully distinct from A. nitida (Bakhuizen van der Brink, 1921), of Libau (1914) on A. officinalis, and of Chapman (1944) on A. nitida. The two older papers are of limited scope with few figures, but material handled seems to have differed from the New Zealand Mangrove in some respects. Brenner refers to phelloderm replacing primary cortex on pneumatophores. However, he attributes this to injury. His figure of secondary bark of earth roots and his description suggests that he had seen a proliferated primary cortex. He also figures curious spirally thickened hairs which project into into intercellular spaces of aerial roots. Libau describes and figures a closely connected system of idioblasts in the subterranean parts of pneumatophoros which seems to accord better with A. nitida than with New Zealand material. Though he examined roots old enough

to show four successive stelar cambiums, he states that there is no replacement of primary cortex by phelloderm.

The Jamaican material of A. nitida more recently studied by Chapman shows various differences in detail compared with the New Zealand mangrove. A distinction is made between rough and smooth types of pneumatophore. In the main underground root, cells of the primary cortex are arranged in rather well-marked radial rows, and include rows of idioblasts, whereas in New Zealand material underground cortices have a similar netted appearance to the closer-textured pneumatophore cortex, and practically no thickened cells. The stem lenticels of A. nitida are said to differ from those on the roots in lacking closing layers. Replacement of primary cortex by phelloderm on old main roots is recorded, but no mention is made of the striking proliferation of the primary cortex which precedes this process in New Zealand, and it is specifically stated that production of a succession of stelar cambiums was not seen in roots. Interesting points of agreement are the occurrence of cell collapse in cortex of underground roots, some persistence of root cap layers at a distance behind the root apex, origin of phellogen beneath the exodermis, and absence of root hairs. While it appears that structural specialisation will prove to follow a similar course in all species of the genus, it is clear that, as with leaf anatomy, there are differences in detail which may be useful in delimiting species.

Troll and Dragendorff (1931) have recently made a detailed study of the root system in Sonneratia (Lythraceae), a polypetalous genus quite unrelated to the sympetalous Avicennia (Verbenaceae). Yet there are striking resemblances between them. The branching of the root system is identical; main roots are polyarch and medullated, and a bsorbing rootlets triarch without pith; root cap layers persist (except in the ultimate rootlets of Sonneratia which have no cap); cell plates separating cortical lacunae are perforated by pores; the phellogen is shallow seated and the persisting primary cortex accommodates itself to stretching by proliferation; the pneumatophore apex resembles other roots until it emerges from the mud, when increased cork formation occurs. These resemblances show that the habitat has powerful morphogenic effects, and the work of McPherson (1939) seems to be a step towards their elucidation. He has shown that in Zea roots lysigenous development of cortical lacunae is caused by scarcity of oxygen. It is likely that the same factor causes cortical cells to collapse when an aerial root of Avicennia enters the mud, a process which ceases in any branches which subsequently emerge as pneumatophores or in the main root itself if it is forced to the surface.

Summary

The root system of the New Zealand Mangrove is entirely adventitious, but has a well-defined mode of branching, most of the primary brunches being pneumatophores. Large roots are polyarch, absorbing rootlets triarch. No root hairs are present, all roots being invested by persistent root-cap layers. In all larger roots cortex and pith are lacunate and in subterranean roots the lacunae are extended lysigenously. In main roots the stele is augmented by a succession