Published under the author's permission

AN ADAPTIVE FEATURE

OF SOME MANGROVES OF SUNDARBANS,

WEST BENGAL



SAUREN DAS
Agricultural Science Unit, Indian Statistical Institute,
203, B. T. Road, Calcutta-700 035, India.


  Mangrove taxa, apart from their morphological characters, have some unique leaf anatomical features which are very much related to their adaptation as the plants grow in unstable, variable and saline environments with regular tidal influence. Special stomatal structures with extended cuticies render the transpiration rate in many taxa. The presence of glandular and non-glandular hairs on the abaxial and/or adaxial leaf surfaces in some taxa are related to salt secretion of these plants. Comparatively large amounts of mater storage tissues occur in the hypodermal or mesophyll tissue of the leaves, reflecting the adaptive nature of mangroves in their stressful habitat. The occurrence of terminal tracheids helps with capillary water storage within the leaf. The coriaceous nature of the leaves in some taxa is due to the presence of sciereids within the mesophyll region. it is noted that Heritiera is unsuitable to the highly saline habitat of the Sundarbans forest region because of some anatomical peculiarities.

Key words: Sundarbans, leaf anatorny, mangroves, adaptation.

A typical mangrove formation embraces a peculiar assemblage of plant community, including shrubs and trees, dominating on low deltaic islands and sheltered estuaries where regular tidal influence of sea water prevails. These habitats are affected by humidity, precipitation, saline, substrats, and temperature. Plants are well adapted to the changing biological, chemical and physical traits of this environment through various xeromorphic properties, including morphology, anatomy and physiology (Mullan, 1931 a; Atkinson et al., 1967; Waisel, 1972; Zimmermann, 1983). Sundarbans, the largest block of mangrove forest in the world, is located between India and Bangladesh, and is formed by the two most important rivers of the subcontinent, namely the Ganga and the Brahmaputra. In the lndian part (western Sundarbans), the exact forest cover is merely 2300 km' and is traversed by a dense series of canals, creeks and rivers (Chanda and Dutta, 1986). Differential saline concentration prevails between the western and eastern zones of the Sundarbans as the sweet water influx in the west is much less and thus become more saline than that of the east (Chanda and Dutta, 1986). However, salinity of the water and soil has a direct influence on the leaf architecture of the plants (Chapman, 1976).

Certain aspects of leaf anatomical work have been investigated by several authors (Mullan, 1931a, 1931b; Wehe, 1964; Shah and Sunder Rai, 1965; Rao and Sharma, 1968; Rao, 1971; Chapman, 1976; Fahn and Shimony, 1977; Tomlinson, 1986;Seshavatharam and Srivalli, 1989; Das and Ghose, 1993, 1996). All those works provided mostly detailed descriptions of leaf anatomy but did not relate to the adaptive characteristics of the plants. This work was aimed at studying the adaptive significance of the plants in light of the leaf anatomy of 22 species of true mangroves from the Sundarbans delta of the Indian territory.

MATERIALS AND METHODS

Figure 1       Figure 2    Figure 3


  Fresh leaf samples of 22 typical well-identified mangrove taxa belonging to 10 families were collected from different islands of the western part of the Sundarbans forest. Among the collected specimens, 20 belonged to dicotyledons species and the remaining two were monocotyledons. Hand sections were made at a position approximately half-way between the base and apex of a sector from one side of the lamina, stained with Toluidine blue 0 and mounted in 50% glycerine. Transverse sections 10-1 6 microns in thickness were prepared by rotary microtome and stained with safranin and fast green Oohansen, 1940; Sass, 1958). Camera lucida drawings (Figs. 1 and 2) and photomicrographs of some representative taxa are provided (Fig. 3). Thickness of leaf, cuticle, epidermal layer, and colorless water storage tissue were also measured. The means and standard deviations of measurements were calculated based on an average of 15 transverse sections from each individual.


RESULTS


  Two types of leaf hairs occur in some species, glandular (salt-secreting glands) and non-glandular. The glandular hairs are present on both the abaxial and adaxial surfaces in Acanthus ilicifolius, Aegialitis rotundifolia, Aegiceras comiculatum and Avicennia (Fig. 1, L-0) but are totally absent in the rest of the species. The non-glandular hairs develop only on the abaxial surface in Avicennia sp., A. ilicifolius and Heritiera sp. (Fig. 1, P-S).

  The glandular hairs have one or two basal collecting cells, one or two stalk cells and a number of radiallyarranged secretory cells, which are covered with a thin cuticle layer. Non-glandular hairs have a multicellular sclerotic body which distally produces a shield-like expanse of thin-walled cells or branched star-like cells in Heritiera (Fig. 1, R and S) or unbranched filamentous body in Avicennia (Fig. 1 P and 3C).

  In most cases, stomata are sunken in Aegiceras, Bruguiera, Ceriops, and Sonneratia with sub-stomatal chamber (Fig. 1, B-D, and H). Guard cells have cuticular beak-like outgrowths (ledges) on either the outer side or both outer and inner side of the stomatal pore in many species of A. ilicifolius, A. corniculatum (Fig. 3B), Ceriops sp., Rhizophora sp., Sonneratia apetala and Nypa fruticans (Fig. 1, A, D, G, H, K, and 3H). Stomata are usually restricted to the abaxial surface of dorsiventral leaves and are scattered throughout the lamina. In isolateral leaves, the stomata are equally distributed on both surfaces, and are arranged in longitudinal file along with the epidermal cells in Kandeiia candel, and S. apetala. Though the leaf is isolateral, stomata are restricted to the abaxial surface in Phoenix paludosa.

  Succulent leaves are a common feature of most mangroves. The highest leaf thicknesses occur in K. candel (1.6 mm), Xylocarpus mekongensis (0.94 mm) and S. apetala (0.9 mm) and lowest in N. fruticans (0.28 mm), A. rotundifolia (0.3 mm) and Heritiera fomes (0.37 mm). In most cases, lamina of mangrove plants are usuallv dorsiventral, but are isolateral in K. candel, P paludo sa, and S. apetala (Fig. 2, A-0).
  The cuticle is considerably thick in Bruguiera gyrnnorrhiza (0.01 4 mm), Avicennia officinales (0.009 mm), Ceriops decandra (0.009 mm), K. candel (0.009 mm) and S. apetala (0.009 mm) and thin in A. comiculatum (0.001 mm), Heritiera littoratis, N. fruticans (0.003 mm) and P paludosa (0.003 mm). The cuticular surface is usually smooth except in A. rotundifolia and S. apetala, where it is uneven (Fig. 2, C and K). The cuticle layer is interrupted due to the presence of stellate hairs in Heritiera sp. and uniseriate capitate hairs on the abaxial epidermis of Avicennia sp. (Figs. 2, H, A, and 3C). The epidermis is always cutinized, either wholly in A. comiculatum, Ceriops sp. and Rhizophora sp. or only the outer tangentiel walls in Avicennia sp., Bruguiera sp. and S. apetala. The adaxial epidermal cells are often larger than those of the abaxial cells in Avicennia sp., Bruguiera sp., and Heritiera sp..

  The hypodermis is composed of one or more layers of colorless cells below the adaxial epidermis. These colorless cells often function as water storage tissue. Four types of hypodermes have been distinguished based upon the number of hypodermal layers:

  (I) Hypodermis is totally absent: K. candel, S. apetala, and P paludosa (Figs. 2, J, K, N, and 3, F, 1).

  (II) Hypodermis is one-layered, below the adaxial epidermis; cells are polygonal, cubical or narrow and sometimes extensively vertically elongated: A. ilicifolius, Bruguiera sp., N. fruticans and X. mekongensis (Figs. 2, D, F, M, 0, and 3, A, G, D, L).

  (III) Hypodermis is two-layered, cells are polygonal and larger than the epidermal cels: Ceriops sp., Heritiera sp. (Figs. 2, F, H, and 3E).

  (IV) Hypodermis is more than two-layered, cells are cubical or polygonal in transverse section, larger than epidermal cells: Avicennia sp., A. corniculatum, A. rotundifolia, Excoecaria agatiocha, Rhizophora sp. and Xylocarpus granatum (Figs. 2, A - C, G, 1, L, and 3, C, J, K).

  The mesophyll is composed of thin-walled chlorenchymatous cells and is well differentiated in the dorsiventral leaf into one or more layers of adaxial anticlinally-extended palisade cells and oval- or round-shaped compact or loose abaxial isodiametric celis in A. ilicifolius, A. corniculatum, Avicennia sp., Bruguiera sp., Ceriops sp., E. agatiocha, N. fruticans, Rhizophora sp. and Xylocarpus sp.. One, two, or even three layers of columnar palisade cells occur beneath each surface, and the middle cells are polygonal and colorless as in K. candel and S. apetala. The adaxial palisade cells in Heritiera sp. are very loosely arranged and their intercellular spaces are well developed. These colorless cells seem to function as water storage tissue. Mesophyll tissue often contains dark brown-colored tanniniferous cells in the lower hypodermal region in Ceriops sp., and in both upper and lower regions in K. candel. Large mucilage cells occur in the adaxial hypodermal region in Bruguiera sp. and Rhizophora sp., and beneath the epidermis in S. apetala. Laticiferous cells are common in the hypodermal region of E. agallocha. Crystalliferous cells are common in many species of Bruguiera sp., Ceriops sp., E. agallocha, K. candel, Rhizophora sp. and Xylocarpus sp.. Branched fibre-sciereids occur in a few species and are scattered in the mesophyll ceils of A. rotundifolia and R. mucronata (Fig. 2, C and 1). Fibre bundles are frequent in the hypodermal tissue of P paludosa (Fig. 2N). Enlarged terminal tracheids are common in the mesophyli tissue of many species investigated, includi ng Avicennia sp., A. corniculatum, Bruguiera sp., Ceriops sp. and E. agallocha (Fig. 2, A-B, and E-C).

DISCUSSION


  The anatomical observations showed four common features in mangrove plants:   Considerably thick cuticles are present on the epidermal rayer of mangrove taxa, which also restricts non-stomatal water loss. This adoptive feature in mangrove plants was aiso supported by Waisel (1 972). Due to the presence of colorless water storage tissue at different levels of mesophyll and hypodermai layers, mangrove leaves become thick and succulent, which can be correlated with the extra water storage capacity. Comparatively succulent leaves occur in those plants which usually grow in the slope region, where the tidal influence of sea water is maximal (twice a day), such as in B. gymnorrhiza, C. decandra, Kandelia and Sonneratia. Wehe (1964) has experimentallv proven that the leaf succulence of mangroves increases with the increase of substrate salinity.
  The glandular (salt-secreting) and non-oandular leaf hairs present in some taxa were investigated. In Avicennia, glandular hairs occur in both abaxial and adaxial surfaces of the leaf; on the adaxial side, the glandular hairs are sunken in densel%,-distributed crypts, whereas on the abaxial side the,, occur on the leaf surface and are distributed along with non-glandular hairs. Glandular hairs on both surfaces of the leaf occur in Aegialitis, but in Aegiceras it is restricted to the abaxial surface. The glandular hairs show some structural similarities in ail of the above cases, such as having a basal cell, one or two cutinized stalk cells and a capitate group of terminal-radiating cells. Fahn and Shimony (1977) commented that in Avicennia, ail glandular and non-glandular haires are formed similarly up to the three-celled primordium stage, but after this two types of hairs start to appear. Osmand et ai. (1969) experimentally showed that sait is secreted by the cytoplasm of the secretarv ceils into the large vacuole and that secretary celis d ry out with the aging of the leaf and sait remains on the leaf surface as a white, powdery layer. Atkinson et al. (1967) provided experimental evidence that glandular hairs are responsable for secretary function in Avicennia and Aegiatitis. Non-glandular hairs are only present on the abaxial surface of the leaf in Avicennia and Heritiera.










Thickness¹
 and
± sd² of
SI
Name of the
investigated taxa
Family
Leaf
symmetry
Leaf
Cuticle
Epidermidis
Colorless zone








1 Acanthus ilicifolius L. Acanthaceae Dorsiventral
0.61±0.22
0.004±0.01
0.026±0.05
0.065±0.03
2 Aegilitis rotundifolia
Roxb
Plumbaginaceae Dorsiventral
0.30±0.01
0.007±0.01
0.017±0.03
0.043±0.09
3 Aegiceras corniculatum
(L.) Blanco
Myrcenaceae Dorsiventral
0.37±0.13
0.001±0.04
0.072±0.03
0.082±0.07
4 Avicennia alba
Blume.
Avicenniaceae Dorsiventral 0.44±0.21
0.006±0.02
0.001±0.01
0.12±0.04
5 Avicennia marina
(frosk.)Vierh.
Avicenniaceae Dorsiventral
0.48±0.17
0.004±0.02
0.011±0.06
0.085±0.03
6 Avicennia officinalis L. Avicenniaceae Dorsiventral
0.41±0.11
0.009±0.05
0.019±0.08
0.10±0.03
7 Bruguiera cylindrica
(L.) Bl.
Rhizophoraceae Dorsiventral
0.39±0.23
0.006±0.05
0.015±0.05
0.12±0.04
8 Bruguiera gymnorrhiza
(L.) Lamak
Rhizophoraceae Dorsiventral
0.54±0.42
0.014±0.07
0.018±0.02
0.027±0.03
9 Bruguiera parviflora
W.&A.
Rhizophoraceae Dorsiventral
0.55±0.56
0.006±0.06
0.01±0.03
0.037±0.03
10 Ceriops decandra
(Griff) Ding Hou.
Rhizophoraceae Dorsiventral
0.70±0.63
0.009±0.03
0.017±0.02
0.097±0.02
11 Ceriops tagal
(Pierr.) Robins
Rhizophoraceae Dorsiventral
0.61±0.73
0.004±0.03
0.014±0.03
0.084±0.02
12 Excoecaria agallocha
L.
Euphorbiaceae Dorsiventral 0.50±0.49
0.006±0.07
0.014±0.04
0.045±0.04
13 Heritiera fomes
Buch. Ham.
Sterculiaceae Dorsiventral
0.37±0.62
0.005±0.05
0.019±0.03
0.037±0.02
14 Heritiera littoralis
Dry
Sterculiaceae Dorsiventral
0.41±0.71
0.003±0.06
0.016±0.03
0.036±0.03
15 Kandelia candel
(L.)
Rhizophoraceae Isolateral
1.60±0.84
0.009±0.04
0.016±0.03
1.35±0.03
16 *Nypa fructicans
(Thunb.)Wurmb.
Areceae Dorsiventral
0.28±0.42
0.003±0.03
0.006±0.02
0.14±0.05
17 *Phoenix pludosa Roxb. Areceae Isolateral
0.22±0.38
0.003±0.02
0.006±0.02
-
18 Rhizophora apiculata Bl. Rhizophoraceae Dorsiventral
0.48±0.59
0.004±0.04
0.013±0.02
0.068±0.02
19 Rhizophora mucronata
Lam
Rhizophoraceae Dorsiventral 0.54±0.47
0.006±0.03
0.015±0.05
0.074±0.02
20 Sonneratia apelata
Buch. Ham.
Sonneratiaceae Isolateral
0.90±0.68
0.009±0.03
0.015±0.04
0.54±0.02
21 Xylocarpus granatum
Koning
Meliaceae Dorsiventral
0.49±0.51
0.006±0.02
0.015±0.03
0.10±0.03
22 Xylocarpus mekongensis
Pierre
Meliaceae Dorsiventral
0.94±0.83
0.004±0.06
0.016±0.04
0.59±0.04








*monocot; 1-thickness measured in mm; 2-calculated on 15 random observations of each sample; 3-considering the colorless non-assimilatory zone.

In Avicennia, it the hair is a three-celled structure in which the basal cell is heavily cutinized like the adjacent epidermal cells and the terminal cell has a thin cuticle. Stellate, multicellular hairs densely occur in Heritiera. Metcalfe and Chalk (1950) suggested the adaptive significance of glandular and non-dandular hairs in Avicennia. The salt-secreting mechanism of the above taxa and the occurrence of epidermal hairs are very much important in relation to their adaptive nature.

In the dorsiventral leaf, stomata occur only on the abaxial surface, but in the isolateral leaf, stomata are on both surfaces in K. candel and S. apetala but not in P.paludosa. Most of the mangroves have sunken stomata, but not A. ilicifolius, A. rotudifolia, A comiculatum or Xylocarpus sp. (Das and Ghose, 1993). The depth to which stomata are sunken may depend on the leaf age (Chapman, 1976). Mullan (1931a) observed that the stomata are not depressed in young leaves of S. apetala.

Sclereids of different shape occur in Rhizophora sp. and A. rotundifolia and terminal tracheids are common in Avicennia sp., A. comicuiatum, Bruguiera sp., Ceriops sp. and E. agallocha. These features can be interpreted as adaptive characters of the mangroves since the terminal tracheids provide mechanical support to the leaves and capillary water storage function (Zimmermann,1983). Tomlinson (1986) has suggested that in addition to water storage, sclereids might also provide mechanical support to leaves with diminished turgor, or discourage herbivores. The coriaceous nature of many mangrove leaves is probably due to presence of these sclereids.

It is interesting to note that Heritiera sp. possesses some anatomical features which do not help with adaptation to its habitat, for example, the presence of the highest number of stomata per unit area (Das and Chose, 1993), a thin cuticle interrupted by stellate hairs, an almost absence of water storage tissue, loosely-arranged mesophyll tissue, extensive bundle sheath extension up to both hypodermal tissue layers, and poor presence of chlorenchyma cells. All these features indicate that Heritiera sp. is unsuitable to the highly saline habitat of the Sundarbans. A somewhat similar situation is also noticed in N. fruticans and P patudosa.

The saline conditions of water and soil have direct impact on the succession of vegetation as evident in mangrove swamps. Troup (1926) explained that edaphic forest formations are well represented in India with instances of mangroves and tidal forests of littoral regions in which water happens to be the controlling factor. The eastern part of Sundarbans receives comparatively huge amounts of fresh water from the Ganga-Brahmaputra system and its tributaries, but the western Sundarbans receives much less fresh water because of the river Hooghly (Ganga) which serves the purpose of local drainage, heavy silt deposition in the river bed and the southern extremities which act as arms of the sea. Consequently, the western part is more saline and does not accumulate silt to the same extent as the eastern Sundarbans. Chanda and Dutta (1986) have opined that the impact of the changed circumstances has proved disastrous for the two major species, N. fruticans and H. fomes, which have become very rare in the western part of the delta but are stili found growing well along the water c'ourse in Bangladesh. The leaf anatomical features can also explain why these two species are not in equilibrium with the present environment of the western Sundarbans .

LITERATURE CITED


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