Morphological and Anatomical Adaptations of Halophytes: A Review

Grigore, Marius-Nicusor; Toma, Constantin

doi:10.1007/978-3-030-57635-6_37

Marius-Nicusor Grigore² &
Constantin Toma²

451 Accesses
9 Citations

Abstract

The nature of many morphological and anatomical adaptations of halophytes is xeromorphic, because of the physiological drought occurring in saline environments. Succulence may have a dilution effect on accumulated toxic salts within plant tissues and plays a water storage role during dry periods. Intense lignification linked to successive cambia activity in roots and stems of halophytic chenopods could be also related to salinity and aridity. Salt secretion is an important strategy of recretohalophytes (crynohalophytes); salt glands and salt bladders are involved in the secretion of salt excess from aerial organs toward the exterior of halophytes. Kranz anatomy pattern occurs in C₄ halophytes as a physical support for physiological and biochemical processes typical for C₄ pathway. Bulliform or motor cells act in “amphibious halophytes” for rolling up the leaf during extended drought periods. In respect with special or local environmental factors (tropical halophytes), halophytes have special adaptations, as is the case of mangroves (aerial prop roots, pneumatophores, viviparity, aerenchyma).

Constantin Toma is deceased.

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Morphological and Anatomical Adaptations of Halophytes: A Review

Integrative Anatomy of Halophytes from Mediterranean Climate

Keywords

1 Introduction: Halophytes as an Ecological Group of Plants

Most of morphological and anatomical adaptations of halophytes are xeromorphic by their nature. Dealing with halophytes as a special case of xerophytes is an old idea promoted by the subtle observations of plant ecologists from the end of the nineteenth century, especially Warming (1897, 1909) and Schimper (1891, 1903) who emphasized the hypothesis of “physiological dryness” (see extensive discussions in: Grigore 2008; Grigore and Toma 2010a, b, c, 2011a, 2017; Grigore et al. 2014 and the references therein).

Botanists have noticed long time ago that adaptations of halophytes are similar with those found in xerophytes, and these features are strictly correlated with physiological drought of saline habitats (Henslow 1895; Grigore’s chapter on “Definition and Classification of Halophytes as an Ecological Group of Plants,” this handbook). If xerophytes and halophytes would be considered as distinct ecological groups of plants, it would be striking to find out that they share the same adaptations, as they would have something in common. While for some authors the position of halophytes within other ecological groups of plants may be confusing, for others it seems logical and natural to deal with halophytes under the umbrella of xerophytes. Actually, the reason for the common origin of morphological and anatomical adaptations of halophytes and xerophytes is mainly the drought of soils in which both groups vegetate – a physical drought in the case of xerophytes and physiological drought in the case of halophytes, as described by Schimper (1903) and especially by Warming (1909).

According to Schimper (1903), the major natural regions and environments where physiological drought is prevalent and consequently only xerophytes can survive are grouped (according to their physical characteristics) as follows:

1.
Deserts, steppes, and other areas with a dry substratum and dry air, occasional or persistent great heat, and intense illumination (Fig. 1)
2.
The bark of trees and rocks where there is rapid drying of the substratum, owing to deficient depth (Fig. 2)
3.
Sandy soil, gravel, and the like, on account of the rapid drying of the substratum, owing to its great permeability (Fig. 3)
4.
Seashores and solfataras, which have an abundance of soluble salts in the soil (Fig. 4)
5.
Peat bogs, because of the humic acids in the soil (Fig. 5)
6.
Polar zones and vicinity of glaciers in high mountains, where the temperature of the soil is low (Fig. 6)
7.
Alpine highlands, which experience rarefied air and the strong insolation characteristics of the alpine climate (Fig. 7)

At a glance, it is rather surprising that such habitats – so diverse by their geography and ecological conditions – can induce similar adaptations in plants that belong to different ecological groups but that are, in fact, so closely related to the nature of their adaptations (Figs. 1, 2, 3, 4, 5, 6, and 7).

The idea of “physiological drought” has been adopted by many authors who have subscribed to Warming’s and Schimper’s hypothesis, approaching the adaptations of halophytes and xerophytes. They realized that there is a phenomenon of convergence: drought conditions (either physically or physiologically considered) induce in plants the need for conjoint features, despite they vegetate in very diverse and heterogeneous environments.

Moreover, even before the promoting of this idea by Schimper (1891, 1903) and Warming (1909), some botanists observed that species from different regions and habitats of the world – of course, included in different ecological groups – may display similar (convergent) morphological features and anatomical adaptations.

Henslow (1895) noticed that there are certain peculiarities of halophytes (maritime plants) common with desert plants as well as with some alpine and subalpine species. Hooker (1891) noticed a certain general correspondence between the climate of some countries at the sea level and that of the Himalaya, both in the absence of animal life and in lacking certain natural orders of plants. He thus compares New Zealand, Fuegia, and Tasmania with Scotland and Norway. He attributes the absence of life to the moist and cold atmosphere. Following Hooker’s observation, Henslow pointed that several maritime plants are also found in mountains or certain varieties of them; despite that not all the mountains are characterized by a high intense aridity, he mentioned several species that illustrate “this coincidence”: Draba incana, Cochlearia officinalis ssp. alpina, Silene maritima, Plantago maritima , and Hieracium species.

Henslow pointed that the resemblances which may be seen in plants from such widely different localities as our seashores, alpine regions, and desert countries are readily explicable that certain elements of the environment are in excess; these act upon the plants in question, and the latter respond accordingly, so that much the same results occur. Thus, if hairiness be due to a check in the development of cellular tissue, it may arise from too much heat, as in the deserts of Africa, or from too great a degree of cold, as in Alpine and Arctic regions; both conditions are causing great aridity. Succulence in the deserts, especially where the soil is saline, arises from identically the same cause as in plants on our own seashores (see the Figs. 1, 2, 3, 4, 5, 6, and 7). Since the moisture of the air and soil is more charged with saline matters in maritime regions and salt marshes, it was a reasonable inference that the presence of salts was in some degree responsible for the remarkable succulence of such plants as Crithmum maritimum , Salicornia herbacea, and many others.

Lots of experiments supported that some morphological and anatomical features of maritime plants can be lost or diminished, under different ecological conditions, as the salinity influence; these is a complicate discussion about different species, “forms” (inland and maritime) of the same species – with particular features on the shore and in inland areas – or ecotypes of the same species. Iconic experiments and observations of Lésage (1890) (see extended discussions in Grigore and Toma 2017) confirmed that salt addition or its removal from cultivation conditions may induce the presence or absence of a morphological character.

For this chapter, two ideas must be underlined in order to discuss morphological and anatomical features of halophytes:

1.
A halophytes is here regarded and approached as a special case of xerophytes, because of physiological drought of saline environments; other groups of plants are under the multiple influence of this ecological situation, a fact that explains the presence of similar morphological and anatomical adaptations in desert plants, alpine plants, peat bog plants, epiphytes, and arctic (polar) plants.
2.
The climatic (biogeographical) and ecological diversity of saline habitats would add something particular to halophytes. Halophytes vegetating on seashore, saline deserts, saline steppes, tropical shores (mangroves), and inland saltmarshes are – according to first sentence and our vision about halophytes – xerophytic by the nature of their adaptations. However, each mentioned saline habitat brings something new and particular, an ecological scenario that would induce particular adaptations. If to use a plastic definition, a halophyte should then considered a general xerophyte plus something in addition, originated from individual ecological conditions of a given ecosystem. Indeed, looking at the diversity of saline habitats, it is obvious that a halophyte from a saline steppe and another from a mangrove plant community would have different adaptations, added to a common xeromorphic profile (both of them must face physiological drought, however).

The position of halophytes within other ecological groups of plants is thus tricky; Coulter (1900) considered that the classification of plants into hydrophytes, xerophytes, and mesophyte would be artificial, if based on the criterion on water accessible for plants. However, halophytes seem to have a special position as, according to the amount of water supply, they could be classified within xerophytes or hydrophytes groups; in fact, the water contains certain salts, notably common salt, gypsum, and magnesia. The water may be abundant enough to represent hydrophyte conditions, or it may be scanty enough to represent xerophyte conditions, but if these salts are present in the soil in sufficient abundance to strongly affect the water, the plants are halophytes.

According to Coulter (1900), such areas occur in various positions:

1.
In the vicinity of the seashore, where there are salty beaches, and swamps and meadows
2.
The margins of salt lakes, such as the Great Salt Lake, the Dead Sea, or Caspian Sea, and a host of smaller lakes
3.
About saline springs, which are common among the numerous medicinal springs of watering places
4.
Certain interior arid wastes, which probably mark the position of old sea basins.

2 Review of General Morphological and Anatomical Adaptations of Halophytes

The main morphological and anatomical features in halophytes are listed below. In this subsection morpho-anatomical adaptations are approached as major, “general” to have an accurate picture on their xeromorphic nature. Differences between different groups of halophytes – or to be more precise – special features found in halophytes vegetating in different saline environments, will be discussed in the next subsections. For this purpose, contributions of Henslow (1895), Warming (1877, 1891, 1906, 1909), Chermezon (1910), Grigore (2008, 2011), Grigore and Toma (2005, 2006a, b, 2007a, b, c, 2008a, b, c, 2010a, b, c, 2011a, b, 2014, 2016), Grigore et al. (2011a, b, 2012a, b, 2012c, 2013), Safiallah et al. (2017), and Kherraze et al. (2018) were followed here.

2.1 Succulence

Succulence – first morphologically noticed by botanists – seems to be the early important adaptation observed and discussed within the halophyte group by botanists (Grigore and Toma 2017). Perhaps the most obvious feature among halophytes is that they are nearly all succulent plants: the leaves are thick, fleshy (containing water storage tissues), and more or less translucent (Grigore 2008). This is due partly to the great amount of cell sap and lack of chlorophyll but partly to the small size of the intercellular spaces. In many cases, it has been a long time indicated that species present two ecological forms: the maritime or halophytic form, which has succulent, thick leaves, and the inland form, which has thin leaves (Lésage 1890; Holtermann 1907, Chermezon 1910 – see Grigore and Toma 2017 for extensive discussions). Such examples are Lotus corniculatus, Geranium robertianum, Convolvulus arvensis, Matricaria inodora, Hieracium umbellatum, and Solanum dulcamara. Experiments with culture substratum have demonstrated that certain halophytes cultivated on ordinary soil with little or no salt achieve thinner leaves and lose other characteristics; such is the case with Cakile maritima , Cochlearia officinalis, Salicornia herbacea, Spergularia media , and Salsola soda .

Conversely, certain inland species acquire thicker leaves when cultivated in a substratum treated with common salt, as is the case with Lotus corniculatus and Plantago major. This thickness of leaf is induced by an increase in volume of mesophyll cells that become large and roundish; in the interior of the leaf, poor in chlorophyll, thus making the leaf hyaline, a genuine water storage tissue can form. In some species, a typical water storage tissue occurs and is surrounded by palisade tissue, for instance, in Salsola kali , Batis maritima , and Salicornia europaea.

Lésage (1890) projected a very interesting and well-designed experiment regarding the modifications of leaves in species having two ecoforms: maritime (halophytes, varieté maritime) and inland varieties (varieté terrestre); he tested his hypothesis dealing with individuals collected from nature and in experimental conditions. Finally, he compared several histological parameters in leaves of plants collected near to the sea (maritime plants) and their variants from inland nonsaline area. This study looks like a very modern and complex study of experimental plant anatomy (Grigore and Toma 2017).

The background idea of Lésage study is that every species able to vegetate in both considered environments (maritime and inland) would modify more or less following the influence of environments where they develop. He further divides this idea in several hypotheses:

1.
Living usually on seashore, a species will have succulent (fleshy) leaves.
2.
If the same species is moved toward interior (on inland, nonsaline areas), it will develop thin leaves.
3.
If the species that usually vegetates in interior (nonsaline) environments is moved on seashore, it will acquire thicker leaves than those it has in inland areas.

Lésage suggested that seashore has, among other effects, the capacity of increasing leaf thickness. He took into his study 90 species collected from nature and finally compared the leaves of 85 species having two mentioned varieties (maritime and inland) and concluded that 54 of species are thicker in maritime form, 27 are indifferent, and 4 species are thicker in inland variant. He clustered these findings in several groups.

First group – Species that displayed a thicker leaf on seashore may be further divided in:

1.
Plants that are often found in interior than on littoral: Osmunda regalis, Ruscus aculeatus, Polygonum aviculare, Atriplex hastata , Beta vulgaris, Ranunculus sceleratus, Nasturtium officinale, Spergularia rubra , Samolus valerandi, Linaria vulgaris, Senecio vulgaris, etc.
2.
Littoral plants: Salicornia herbacea, Atriplex portulacoides , Beta maritima, Cakile maritima , Eryngium maritimum, Crithmum maritimum , Glaux maritima, Armeria maritima, Plantago maritima , Inula crithmoides , etc.

Second group – Species that remained indifferent:

1.
Inland (interior) plants: Scolopendrium officinale, Festuca rubra, Alisma plantago, Triglochin palustre, Hypericum perforatum, Lamium purpureum, Betonica officinalis, and Plantago major.
2.
Littoral plants: Psamma arenaria, Spartina stricta , Glyceria maritima , Ruppia maritima, Triglochin maritimum, Suaeda maritima, Althaea officinalis, and Euphorbia peplis.

Third group – Species that have a thicker leaf for inland (interior) variant: Asplenium trichomanes, Medicago lupulina, Convolvulus arvensis, and Galeopsis ochroleuca.

From this classification, he concluded that, in case of first group, an interior (inland) plant growing on seashore achieves thick leaves; conversely, a plant from seashore when cultivated in interior (nonsaline) area acquires thinner leaves.

Lésage included then in his study the following histological features in relation to leaf anatomy: epidermis, the external cell wall of epidermal cells (here including the thickness of cuticle), mesophyll (to check which tissue of it is involved in conferring thickness), nervures, vessels (their diameter), secretions, chlorophyll, and its distribution within cells. In respect with compared anatomical observations, he concluded that:

1.
Epidermal cells (as well as stomata and trichomes) have no clear relevance in relation to the influence of sea. The single exception is the vezicular hairs (nominated by Lésage as papilles, but they represent without doubt the well-known vezicular hairs of halophytic chenopods).
2.
The external cell wall of epidermal cells shown no clear differences in maritime and inlands forms.
3.
Mesophyll (and palisade tissue) can increase its thickness by enlargement of volume of all cells or by formation of a large number of cell layers; these variations may affect all mesophyll or a part of it (palisade tissue). Within the 54 species found to have thicker leaves, 11 species presented an equal development of all elements; 7 species indicated a development in volume and length of palisade tissue, without increasing the number of leaf layers; 5 species recorded an increase in number of palisade layers; and 31 species shown an increase in volume and length of palisade tissue as well as a higher number of palisade layers. He concluded that the thickness of leaves of maritime variants is based on the large development of palisade tissue.
4.
Nervures show nothing but a discrete increase in dimensions in the case of thicker leaves.
5.
Vessels diameter revealed very subtle or no differences between maritime and inland individuals.
6.
Secretions (calcium oxalate, tannin) do not shown significant differences between the two variants.
7.
Amount of chlorophyll generally recorded no important differences between maritime and inland individuals; in the rare situations were differences were significant, the maritime variants have the tendency of having less chlorophyll.

Lésage (1890) shown that in Eryngium maritimum, Aster tripolium , Thesium humifusum (Fig. 8), and Linum grandiflorum, the leaves are more succulent in individuals collected from littoral than from inland (nonsaline areas) cells.

Lésage concludes his study as follows:

1.
Plants that vegetate on seashore acquire thicker leaves than would in inland (nonsaline) areas. Nevertheless, he concludes that this rule does not apply to all species.
2.
In plants that manage to deal with salinity of sea, palisade cells are very developed. The thickness of leaf increases, following the extension of palisade cells; accordingly, the number of mesophyll layers may increase or can remain unchanged. If the leaf maintains more or less the same thickness in different situations, the palisade develops in such manner in which the ratio between palisade tissue and mesophyll is greater on seashore.
3.
Intercellular spaces greatly reduce in leaves of littoral plants.
4.
Chlorophyll tends to be less abundant in cells of plants vegetating on seashore. However, this finding is less rigorous than previous conclusions, as it applies to plants that subjected often to the influence of sea tide.
5.
Leaf modifications, such as succulence, development of palisade tissue, and reduction of meatuses and chlorophyll, can be replicated under experimental conditions, using cultures with different salt concentrations.

Warming (1897) evidenced succulence in various species of halophytes; many of investigated species have succulent or narrow-reduced leaves (Fig. 140), a xeromorphic adaptation (Grigore et al. 2014). Warming (1897) found water storage tissue in the leaf structure of many halophytes: Tournefortia gnaphalodes , Scaevola plumieri , Borrichia arborescens , Philoxerus vermiculatus , Remirea maritima , Euphorbia buxifolia , and Haloxylon ammodendron .

He described several types of water storage tissue, based on his anatomical observations on investigated species:

(a)
The epidermis is, after Westermaier (1881), commonly perceived as a water tissue. However, it is weakly chlorophyll-containing in many of the investigated species, as far as can be seen on the analyzed cross sections, for example, Heliotropium curassavicum . In some few cases, epidermis becomes particularly tall with large cell, so it can be assumed that it works especially as a water tissue, e.g., Juncus gerardi, Ionidium buxifolium (Fig. 9), Dolichos axillaris (Fig. 10), Ruellia monanthos, Canavalia obtusifolia, and Diodia radicans. However, following Westermaier’s opinion, Warming has not observed such epidermis, and only in two species he found mucous membranes. These building conditions appear more significant to xerophytes. Water-storing hairs (salt hairs, vezicular hairs) are found in Atriplex species (Figs. 90, 91, 92, 93, 94, 95, 99, 100, 101, 174, and 175).
(b)
Hypodermic water tissue occurs in certain species, usually only on one side, rare on both. On the upper side, water tissue is present in slight extent in Lippia nodiflora (Fig. 177) and Erithalis fruticosa and well-developed in Remirea maritima (Fig. 176). On lower side of epidermis, hypodermic water tissues occur in Euphorbia buxifolia (Fig. 172) and Philoxerus vermiculatus (Fig. 173). On both sides, hypodermic water tissue is found in Eryngium maritimum (Fig. 161) and Atriplex halimus .
(c)
The water tissue extends between the two epidermises, surrounding the nervure network. This building condition is found in Poaceae, Chenopodiaceae, and other plants that have Kranz anatomy type in the leaf.
(d)
The water tissue is in the middle of the leaf surrounded by all sides by chlorenchyma Acicarpha spathulata (Fig. 148), Atriplex hastata, Alisne (Halianthus) peploides, Silene nicaeensis, Conocarpus erecta (Fig. 149), Inula crithmoides (Fig. 27), Aster tripolium (Figs. 150 and 152 – where the isolateral character of the leaf may vary depending on the level of cross section through the leaf), Suriana maritima (Fig. 153), Beta vulgaris, Cakile aequalis (Fig. 154), Cakile maritima (Fig. 155), Crambe maritima, Heliotropium currasavicum, Polygonum maritimum, Bupleurum tenuissimum, Silene otites, Crucianella maritima, Statice limonium, Statice rariflora, Medicago marina (Fig. 156), Malcolmia littorea, Polygala cyparissias, Convolvulus soldanella, Sedum anglicum, Halocnemum strobilaceum , Sesuvium portulacastrum (Fig. 164), Borrichia arborescens (Fig. 165), Zygophyllum album, Batis maritima (Fig. 166), Echinophora spinosa, Triglochin maritimum, Salicornia, Salsola, and Haloxylon.
(e)
Tracheids without contact with the conducting tissue located in the palisade tissue: Salicornia.
(f)
Shorter, more isodiametric, thickened, and swollen tracheids associated with the nerves either with their sides or more frequently with their ends: together with genuine water tissues, in Batis; much more common is the mangrove plants (see the subsection with mangroves).

Succulence has been observed in many halophytes vegetating in Romanian saline environments (Grigore 2008; Grigore and Toma 2008a, c, 2010a, b; Grigore et al. 2012a, b; Ivan et al., 2013; Grigore et al. 2014) and in Mediterranean salt marshes (Grigore et al. 2011a, b, 2012b, 2013, 2014).

Grigore et al. (2014) underlined that succulence is a distinctive adaptation found in halophytes; it is built as a water storage tissue; and sometimes a well-developed palisade tissue may contribute to the succulent appearance of halophytes. Succulence is well noticed particularly in Chenopodiaceae species.

Grigore et al. (2014) and Grigore and Toma (2017) proposed several groups of succulent halophytes, based on the position of water storage tissue in respect with chlorenchymatic tissues (C₃ and C₄ photosynthetic pathways) and with epidermis.

(a)
C₃ halophytes with articulated segments: Salicornia europaea (Figs. 11 and 12), S. ramosissima (Fig. 13), Halocnemum strobilaceum , Sarcocornia fruticosa (Fig. 14), and Arthrocnemum macrostachyum (Fig. 15). These species are apparently leafless, and the developed water tissues contribute to succulent (fleshy) aspect of their habitus.
(b)
C₃ species with small, cylindrical, or flattened leaves, where water storage tissue dominates an important volume of leaves: Suaeda maritima (Fig. 16), S. spicata (Figs. 17 and 18), Bassia hirsuta (Fig. 19), B. sedoides (Figs. 20 and 21), and Halimione portulacoides (Fig. 22). Succulence was also evidenced in Plantago crassifolia (Fig. 23) and P. tenuiflora (Figs. 24 and 25), Plantago maritima (see Fig. 26), in Inula crithmoides (Fig. 27), Spergularia media (Figs. 28 and 29), Crithmum maritimum (Fig. 30).
(c)
C₄ succulent chenopods halophytes: the water storage tissue is confined to the center of the leaf; it is clearly and functionally delimited toward exterior by two typical chlorenchymatic tissues found in C₄ species: Petrosimonia oppositifolia (Fig. 31), P. triandra (Figs. 32 and 33), Camphorosma annua (Figs. 34 and 35), Salsola oppositifolia (Figs. 36 and 37), S. kali (Fig. 38), Suaeda splendens (Fig. 39) and Iranian species of Bassia turkestanica (Fig. 40), B. pilosa (Fig. 41), and B. stellaris (Fig. 42).
(d)
C₃ species with massive water storage cells located within mesophyll cells (Nitraria retusa ) (Fig. 43).

It has been suggested that succulence plays a role in the dilution of accumulated salts in plant organs and may therefore alleviate the toxic effect of ions in cells, thereby allowing plants to cope with large amounts of salts (Waisel 1972; Grigore 2008; Grigore et al. 2014; Grigore and Toma 2017).

2.2 Mucilage

In some halophytes, mucilage is present within plant cells, as in some xerophytes (Bari et al. 2007). Mucilage is thought to play a role in salinity tolerance in certain halophytic species by regulating water ascent and ion transport (Ghanem et al. 2010). Under salinity exposure, several halophytes increase their mucilage content, such as in Salicornia brachiata and Suaeda maritima (Jaiswar and Kazi 2016), or mucilage is present in halophytes from natural conditions, such as Nitraria retusa (Elhalim et al. 2016). Mucilage cells in many species can increase osmotic pressure, which improve capacity for water retention and water uptake, also providing a relatively wet microenvironment for surrounding photosynthetic cells (Su et al. 2005). In some mangrove species, mucilage cells can occur in leaf hypodermal region of Bruguiera and Rhizophora (Fig. 199) and beneath the epidermis of Sonneratia apetala (Das, 1999) .

2.3 Cell Sap

Cell sap of halophytes has to be more concentrated than soil solution, and this can be achieved by accumulation of large quantities of salt (ions) (Grigore et al. 2011c).

2.4 The Palisade Tissue

Palisade tissue in halophytes is often well-developed, as in Hydrophylax madagascariensis (leaf of isolateral diplophyll type), Scaevola plumieri (leaf isolateral of staurophyll-diplophyll type), Ipomoea pes-caprae , Crambe maritima, Honckenya peploides, Plantago crassifolia , P. coronopus, and Beta maritima, plants that are more or less succulent. In isolateral (cylindrical) leaves, palisade tissue is confined to the leaf periphery, where it forms a variable number of layers; it is clearly delineated from the rest of the leaf, as in Matricaria maritima, Artemisia crithmifolia, A. maritima, Salsola, Traganum nudatum, Anabasis, and Haloxylon. In other species, there is subtle transition between palisade tissue and the other tissues within mesophyll, as in Spergularia, Zygophyllum, Tetradiclis, Atriplex portulacoides, Salicornia, Arthrocnemum, and Suaeda. According to Schimper (1891), the leaves of plants vegetating in the proximity of the sea in the Barringtonia formation are thicker than those of plants growing in inland areas, because their palisade tissue is more developed.

2.5 The Intercellular Spaces

There are relatively few halophytic species with large intercellular spaces; this is mainly the case of species living in salt marshes (Triglochin maritima, Aster tripolium , Glaux maritima), where the cortex is more or less spongy in the stem. In the case of leaf, Armeria maritima has in the lower part of mesophyll small-round cells less compact. Chermezon (1910) found that halophyte species with a very compact structure, with very small intercellular spaces, usually vegetate in salt marshes, sea rocks, seashores, and saline deserts. He further pointed that inland species have littoral forms with a very compact leaf structure, while littoral plants when cultivated in interior often acquire leaves with less compact internal configuration. It is thought that the reduction of intercellular spaces is a xeromorphous feature and a halophytic adaptation in relation to leaf succulence. In halophytic species from Madagascar, intercellular spaces lack in palisade tissue; sometimes they are absent from lower area of mesophyll (Tribulus terrestris, Hydrophylax madagascariensis), fairly visible (Microrhynchus bellidifolius), or well noticeable (Ionidium buxifolium , Canavalia obtusifolia, Dolichos axillaris, Vigna lutea, Ruellia monanthos) (Denis 1919).

2.6 Wax

Wax is traditionally considered as an obstacle for limiting the high transpiration by causing a glaucous aspect of leaf surface (Grigore et al. 2014). Wax is found in a rather small number of halophytes, vegetating on maritime rocks (Crambe maritima, Silene maritima, Lathyrus maritimus), seashores (Eryngium maritimum, Polygonum maritimum, Euphorbia paralias ), and maritime dunes (Dianthus gallicus, Linaria thymifolia, Ephedra distachya) .

2.7 Tomentum

Generally, most of halophytes are glabrous; some salt-marsh species have a prominent tomentum (Artemisia gallica, A. maritima), and some Frankenia species have short trichomes. In saline deserts there are glabrous species, but also plants enabled with trichomes (Nitraria tridentata , Cressa cretica , Salsola tetragona ), but these species are always not as hairy as plants of proper deserts. Halophytic plants from seashores are usually glabrous, but some of them may have short trichomes (Salsola kali ) or may have a tomentum if they vegetate on sands distant from seashore (Medicago marina , Diotis candidissima). Developed tomentum is considered to be a xeromorphous adaptation; for this reason is natural that it is found more expressed in plants of dunes.

Chermezon (1910) made an interesting observation and stated that tomentum and succulence are excluding features: succulent species are almost always glabrous, and hairy species have thin external epidermal walls. Sometimes halophytes have soft or gray hairs, as in Kochia hirsuta, Senecio candicans, and Tournefortia gnaphalodes (Fig. 162). Water-storing hairs (vezicular hairs) are present on leaf surface of several halophytes, such as Atriplex, Halimione (Obione), and Mesembryanthemum; they have large, spherical, thin-walled terminal cells (bladders) filled with saline sap. They could be also considered as water reservoirs on leaf surface, apart from their role in removal of salt excess (Grigore and Toma 2017).

2.8 Coriaceous and Glossy Leaves

Coriaceous and glossy leaves can be observed in mangrove trees and shrubs, for instance, in Rhizophora, Bruguiera, and Nipa fruticans, and also in sandy littoral forests. Limonium gmelini and Lepidium crassifolium also have coriaceous leaves, which can contribute to an increased resistance to harsh environmental conditions such as aridity and salinity (Grigore 2012).

2.9 Stomata

Sunken stomata are generally regarded as a xerophytic mechanism for reducing the transpiration; however, to be effective, this stomatal disposition should be clearly delineated within halophytes leaves.

Chermezon (1910) found sunken stomata in several species of maritime rocks and shingle such as Crambe maritima, Silene maritime, and Crithmum maritimum ; from seashore, sunken stomata can be found in Eryngium maritimum, Polygonum maritimum, and Euphorbia paralias . According to Chermezon (1910), sinking of stomata is rather rare in littoral species; this xeromorphic feature is consistent in Mediterranean and desert species. Usually, succulent halophytic species have no sunken stomata. From succulent species, only Arthrocnemum macrostachyum (Fig. 44) has stomata clearly sunken; in addition, sinking of stomata seems to be in inverse relation with trichomes development.

Denis (1919) found that halophytes from Madagascar have no completely sunken stomata; several species can be protected by half sunken stomata: Scaevola plumieri , Microrhynchus bellidifolius, and Desmodium triflorum, while others (Tribulus cistoides, Ionidium buxifolium ) have no sunken stomata.

2.10 Tracheoidioblasts (Spiral Cells, Tracheids) and Mangrove Tracheids

In relation to succulence, in several species, tracheids were described: storage tracheids are located in the vicinity of the nervures ends (in mangrove species, Sonneratia acida – Fig. 200); in articulated halophytic chenopods (Salicornia species), they are isolated in the parenchyma (water storage and palisade tissues) and apparently do not come in contact with nervures (Grigore and Toma 2007a, b; Grigore and Toma 2008a; Grigore et al. 2014; Grigore and Toma 2017).

Their confusing terminology – that sometimes mixed tracheoidioblasts with stereids (see the next section) – has been reviewed and clarified previously (Grigore and Toma 2017), starting from the valuable work of de Fraine (1912). French botanists Duval-Jouve (1868), Mangin (1882), and Dangeard (1888) early observed and described tracheoidioblasts; each of them attributed a specific role to these curious structures. Other botanists tried to add new histological observations and to explain the physiological role of spiral cells (Monteil 1906; Warming 1909; Chermezon 1910; Cooke 1911; Ganong 1903; de Fraine 1912; Grigore et al. 2013, 2014). The spiral-like appearance of spiral cells (see Figs. 45, 46, 47, 48, 49, 50, and 51) convinced many of botanists to use a related ethymological nomenclature: (les grandes) cellules spiralées (French botanists, Duval-Jouve 1868; Mangin 1882; Dangeard 1888), spiral cells (English, de Fraine 1912), spiral tracheids, spicular cells (translated in English from German, Solereder 1908), spiraltracheiden, spikularzellen (German, Holterman 1907), stereïden (German), and spiralceller (Danish, Warming 1891).

Tracheoidioblasts (spiral cells, tracheids) are found especially in halophytic articulated species from Chenopodiaceae: Salicornia europaea (Figs. 45, 46, and 47), Salicornia patula (Fig. 48), Salicornia australis (Fig. 49), Salicornia ramosissima (Figs. 50 and 51), and Sarcocornia fruticosa (Fig. 157) (Grigore et al. 2014; Grigore and Toma 2017).

Different functions have been attributed to tracheoidioblasts (spiral cells, tracheids) in halophytes. Duval-Jouve (1868) suggested an air-storing function (les cellules aérifères); Mangin (1882) and van Tieghem (1884) proposed a mechanical role of spiral and underlined that they are not in contact with the stomata. Van Tieghem deals with them as elements of the cortical stereome. De Bary (1884) includes the tracheoidioblasts of Salicornia in the category of the scattered tracheids, located outside the vascular bundles; he does not explicitly grant them a particular function, but the simple fact that they are mentioned in this chapter (arrangement of the tracheae and sieve tubes – outside of the vascular bundles) could suggest that their assumed function is in relation to conducting system. Dangéard (1888), who noticed spiral cells in foliar sheaths of Salicornia peruviana, S. virginica, and Arthrocnemum ambiguum , speculated that they would belong to the cortical stereome.

Ganong (1903) referring on air storage system of Salicornia herbacea attributed to tracheoidioblasts an air-storing role, as Cooke (1911) in Salicornia australis (Fig. 49).

Holterman (1907) found spiral cells (spiraltracheiden) in Arthrocnemum indicum , inside the water storage tissue surrounding central cylinder; he ascribed them a role in conducting water toward peripheral regions of the plant.

Monteil (1906) believed that they have an air-storing function (cellules aérifères) in Salicornia patula (Fig. 48), S. sarmentosa, and S. fruticosa.

Warming (1909) nominated them water-storing tracheids, as they are filled with water; he considered that they play the same role as the xylem vessels from the vascular bundles. Chermezon (1910) evidenced spiral cells in the succulent articulated segments of Salicornia fruticosa; he speculated that these structures have a water storage function.

Several mangrove species (Fig. 201) have terminal tracheids at vein endings: Sonneratia apetala, Sesuvium portulacastrum , Avicennia rotundifolia, A. corniculatum, Bruguiera, Ceriops decandra, and Excoecaria agallocha (Das, 1999). They could be regarded as adaptive xerophytic features of the mangroves since tracheids provide mechanical support to the leaves and capillary water storage function.

2.11 Stereids (Spicular Cells, Sclereids, Idioblasts)

They are found in several chenopods succulent halophytes (Salicornia glauca, Fig. 52; Arthrocnemum macrostachyum , Figs. 53 and 54; Sarcocornia fruticosa , Fig. 55; Halocnemum strobilaceum , Fig. 56) and in mangrove species (Aegialitis rotundifolia, Sonneratia, Rhizophora; Fig. 199), which are located in the palisade in water storage tissue. Such elements can be also found in Limonium species, in leaf petiole (Fig. 57), leaf sheath (Fig. 58), and lamina (Fig. 59).

They play a mechanical role and might confer the coriaceous aspect of leaves of mangroves and Limonium species.

2.12 Lignification: The Special Case of Successive (Additional, Supernumerary) Cambia

A general tendency to lignification has been observed earlier especially in xerophytic (desert plants) and halophytic species, and it was correlated with severe climatic conditions in which these species grow (Grigore 2008). This tendency is sometimes correlated to an absence of medullary rays, or, if they exist, they are rare and have thick walls. In some species (Salsola kali , Eryngium maritimum, Echinophora spinosa), there are thorns, especially on leaves, but probably the sand where they vegetate would be involved in the production of the thorns. However, in many halophytes (especially in Plumbaginaceae, Chenopodiaceae, monocots) there is a significant production of sclerenchyma, at root and stem level (Grigore et al. 2014).

Within these species, halophytic chenopods represent a special case of lignification, as the vegetative organs display successive cambia products. This histological phenomenon that arises in the tertiary structure of these organs produces a huge amount of lignin included in the so-called conjunctive tissue (Grigore and Toma 2005, 2006b, 2007a, b, 2008b, 2017; Grigore et al. 2014).

The phenomenon of successive cambia is primarily known due to successive concentric rings from Beta vulgaris. It occurs in many halophytes genera, such as Atriplex, Bassia, Chenopodium, Petrosimonia, Halimione, Camphorosma, Suaeda, Salsola, Sarcocornia, Salicornia, (Grigore 2008, 2012; Grigore and Toma 2007a, b, c, 2008a, 2010a, 2017; Grigore et al. 2012a, b, 2014), and Sesuvium verrucosum (Abd Elbar 2015).

In short, supernumerary cambia acts as follows: the typical, structure is generated by a normal cambium that produces a few secondary phloemic and xylemic vessels. Afterward an additional (supernumerary) cambium derives from pericycle and generates a ring of fundamental parenchyma, where the vascular bundles are placed usually on a ring, with the phloem outside and the xylem inside. Each cambium is born after that from the phloemic parenchyma produced by the former cambium (Grigore and Toma 2017).

Grigore et al. (2013, 2014) found out that successive (additional) cambia were present in almost all of investigated species from Chenopodiaceae in their vegetative organs: Atriplex littoralis (Fig. 60), A. prostrata, A. tatarica, A. glauca (Fig. 61), Bassia sedoides (Fig. 62), Camphorosma annua , Chenopodium album (Fig. 63), Halimione verrucifera (Fig. 64), Petrosimonia oppositifolia , P. triandra, Salicornia europaea, S. ramosissima, Suaeda maritima , S. spicata (Fig. 65), S. splendens (Fig. 66), Salsola kali (Fig. 67), and Sarcocornia fruticosa .

Despite that there is no consensus on ecological and functional role of successive cambia in halophytes, there is some evidence that lignin deposits are likely to be involved in plant salt tolerance (Liu et al. 2018). Grigore and Toma (2017) suggested that lignin could increase the resistance of the cell walls to the high osmotic pressure found in saline soils.

Grigore and Toma (2006b, 2017) advanced a hypothesis about a possible ecological significance of successive cambia in halophytes. They speculated that the obtained structural configuration could be related to an increased internal surface of the root, considering the increased capacity of retention and “storage” of the saltwater within plant organs. In addition, the cork from periphery of the root could also diminute saltwater uptake. Consequently, salts penetrate slowly in roots, but once arrived there, they would be dispersed in this increased surface, and thus the transport of salts toward upper parts of plant organs (more sensitive to salt) would be delayed. Likely, increasing this surface would inevitably imply a dispersion area for salts, which would be diluted, thus alleviating their harmful effect to the plant. Therefore, successive cambia phenomenon can be considered – based on its effects (numerous vessels, high “internal” surface) as a beneficial “compromise” for the plant between the growth limitation necessity (controlled by the abscisic acid ABA) and the necessity of imposing dilution strategies of salts in the plant’s organ, except perhaps the higher regions of stem (Grigore and Toma 2017).

2.13 Salt-Secreting Structures

Salt-secreting structures (salt hairs and salt glands) are heterogeneously distributed in halophytes (Grigore 2008; Grigore and Toma 2010b), and the halophytes that possess such devices are called crynohalophytes (recretohalophytes). Salt secretion is a complex mechanism in halophytes, involving specialized and often elaborated structures created during evolution to remove the excess of salts from plants shoots (Grigore and Toma 2010b; Grigore et al. 2012a).

Recretohalophytes can secrete salt from the plant body to the outside through salt glands (as in Plumbaginaceae, Tamaricaceae, Primulaceae, Frankeniaceae halophytes) or into salt bladders for temporary storage, and then the salt will scatter from salt bladders when it encounters strong winds or other external stimuli (Chen et al. 2018).

Salt-secreting structures, namely, salt bladders and salt glands, are functional devices that directly secrete ions out of the plant, and they are also notable for their presence in recretohalophytes and absence from other halophytes and all non-halophytes (Shabala et al. 2014; Yuan et al. 2016).

According to Chen et al. (2018), there are 65 halophyte species grouped in 11 families that have salt glands (Table 1). Other halophytes have salt hairs (vezicular, bladders, salt bladders) and belong to Chenopodiaceae (Amaranthaceae) and single bladder epidermal cells (occurring in Aizoaceae).

Table 1 Distribution of salt-secreting structures in halophytes

Full size table

Grigore and Toma (2010b) have adapted, modified, and completed a previous definition of Fahn (1988) regarding secretory tissues in vascular plants, using an integrated anatomical vision in the salt-secreting structures of halophytes.

Salt-secreting structures of halophytes can be divided as follows (Grigore and Toma 2010b, 2017):

1.
Structures (salt hairs) that eliminate (secrete) salts into the vacuole, as in Atriplex and Chenopodium species. Salt is secreted into a central vacuole of the bladder cell of the leaf hair. Bladders are located on top of a narrow stalk, consisting of one to three cells. Increasing of bladder cell volume is based on formation and expansion of a central vacuole;
2.
Structures (glands) that eliminate salts outside of the cells. Here, two types of glands may be included:
1. (a)
  Glands of monocots – they are bicellular and monocellular glands and found mainly on Poaceae species.
2. (b)
  Glands of dicotyledons – they are multicellular glands, such as those of Limonium, Tamarix, Avicennia, Frankenia, Cressa cretica , and Lavatera arborea .
3.
Epidermal bladder cells from Aizoaceae (Mesembryanthemum species), which seems to occupy an intermediary position within salt secretory structures. Some authors have included these bladder cells in the group of secretory trichomes, but they look morpho-anatomically as lacking the stalk cell, thus maintaining only the terminal cell (the bladder of salt hairs).

2.13.1 Salt Glands of Plumbaginaceae

A typical trait of Plumbaginaceae is the presence of glands: chalk glands (Mettenius or Licopoli glands – salt glands) and mucilage glands located on leaves and stems (Grigore and Toma 2010b). The structure of these glands was frequently differently interpreted by some authors, although these controversies are related rather to details than their basic structure. The different reported numbers consisting cells of glands could be rather related to the inconsistent terminology of types of cells than to a real high diversity within recretohalophytes from Plumbaginaceae. Grigore and Toma (2016) reviewed the structure of glands in Plumbaginaceae, with an emphasis on contribution of Mettenius Licopoli, the two botanists who gave the parallel names of salt glands.

There are two types of glands in halophytic Plumbaginaceae (Metcalfe and Chalk 1972).

1.
Chalk (chalk-secreting) glands , also known as Mettenius glands or Licopoli glands (“organs”) (for their nomenclature, see Grigore and Toma 2016), they are located on or in the cavities on the inner side of the leaves and stem and are sometimes surrounded by groups of elongated epidermal cells or by simple trichomes. A typical gland consists of four or eight epidermal cells arranged in palisade surrounded by one or two layers, each made up of four “accessory” cells. These glands have been generally described as chalk glands because they exude calcium salt and water; calcium salts are sometimes scattered on the leaf or stem surface by rain drops.
2.
Mucilage glands occur in some species of the Plumbaginaceae; they usually comprise a head resting on a head borne on a base consisting of few cells with very thick cuticle-lined walls.

Chalk glands (Licopoli organs) have been evidenced in Limonium furfuraceum (Fig. 68), Limonium narbonense (Fig. 69), Limonium girardianum (Fig. 70), Limonium gmelinii (Figs. 71 and 72), and Aegialitis annulata (mangrove species, Fig. 73).

2.13.2 Salt Glands of Tamaricaceae

Usually, Tamarix species have salt glands with six secretory cells and two collecting cells in a symmetrical structure (Figs. 74 and 75) (Yuan et al. 2016). In Tamarix aphylla , salt gland consists of six secreting cells (with dense cytoplasm) and of two extraglandular, collecting cells, intensely vacuolated. Secreting cells have a cuticular “sheath” except for some portions of cellular walls, which are involved in assuring the communication with collecting cells.

Other halophytic species with salt glands include Reaumuria oxiana (Fig. 76) (Paulsen 1912), Reaumuria kermanensis (Fig. 77) (Brunner 1908), Reaumuria squarrosa (Fig. 78) (Brunswik 1920), and Myricaria germanica (Fig. 79) (Brunner 1908).

2.13.3 Salt Glands of Frankeniaceae

They are glands completely surrounded by cuticular layer, as is the case of Tamarix and Limonium. They are found in Frankenia floribunda, F. pulverulenta (Fig. 80), F. grandiflora, F. revoluta, and F. laevis (Fig. 81 and 82).

These glands consist of eight cells; six of them are secretory cells and have dense cytoplasm, a high number of small vacuoles, and a large nucleus; the other two cells are collecting cells and have a large central vacuole. The entire complex of cells is covered by a cuticular layer, except for small areas of the walls between secretory and collecting cells (Grigore and Toma 2010b).

2.13.4 Salt Glands of Mangroves

Salt extrusion is a very important adaptive strategy of mangroves; it occurs through salt glands in the leaves of Avicennia officinalis (Fig. 83), A. nitida (Fig. 84), Acanthus ilicifolius, Aegiceras corniculatum (Fig. 85), Aegialitis (see Fig. 73), Clerodendrum inerme, and probably Laguncularia racemosa (Saenger 2002; Grigore and Toma 2010b) (see Table 1). Salt glands of mangrove species have different numbers of secretory cells: 6–9 cells in Avicennia officinalis , 8–12 cells in A. marina, 8 in A. germinans, and 20–24 in Aegiceras (Saenger 2002; Yuan et al. 2016).

2.13.5 Salt Glands of Halophytes from Primulaceae Family

Salt glands are found in Glaux maritima (Figs. 86, 87, and 88), Samolus littoralis, S. repens, and likely in Jacquinia armillaris (Kuster et al. 2018); they play an ecological role within adaptation of these species to maritime habitats (Grigore and Toma 2017).

Glands of Glaux maritima appear to be sunk in depressions of the epidermis (Fig. 86). Seen in front view of epidermis, glands appear to be surrounded by six epidermal cells arranged regularly. From the interior to the exterior of the gland, three types of cells can be observed: a large basal cell that corresponds to collecting cell of the gland. Close to it, there is a stalk cell, with a large nucleus. The external part of the gland consists of four to eight gland secretory cells, whose base is in continuation of the upper part of the stalk cell.

2.13.6 Salt Glands of Halophytes from Poaceae (Gramineae)

Salt glands of Poaceae secrete salt outside of the cells and display the simplest anatomy (bicellular or even monocellular-based structure) (Grigore and Toma 2010b). They usually consist of two cells, a basal and a cap cell; their shape, size, and position are highly variable among secreting halophytes.

Bicellular epidermal glands are the most characteristic and occur in more than 30 species of tribes Chlorideae, Eragrosteae, Aeluropodeae, and Pappophoreae, the well-studied glands being those from Aeluropus littoralis, Spartina (Fig. 89), and Sporobolus.

2.13.7 Salt Hairs (Vezicular Hairs, Salt Bladders, Bladders) from Chenopodiaceae

These salt hairs (also called in the literature vesicular/vezicular hairs, vesiculated hairs, salt bladders, bladder hairs, or simply bladders) are present in many halophytic species of Chenopodiaceae , especially in Atriplex, Halimione, and Chenopodium species (Grigore and Toma 2010b, 2017, Grigore et al. 2014).

These hairs consist of two cells: a stalk formed of one to three cells and one large cell, intensely vacuolated bladder cell (Fig. 90). Stalk cell contains a dense cytoplasm rich in mitochondria, endoplasmic reticulum, and numerous small vesicles. Inside bladder cells, sodium and chloride concentration is higher than in mesophyll cells and higher than that of the external environment. Salt flow direction is from internal media, through mesophyll, toward these secretory structures.

Salt hairs were observed in Atriplex leucoclada (Fig. 90), A. farinosa (Fig. 91), Halimione verrucifera (Fig. 92), H. portulacoides (Fig. 93), Atriplex tatarica (Fig. 94), and A. halimus (Fig. 95).

2.13.8 Epidermal Bladder Cells from Aizoaceae (Mesembryanthemaceae)

These cells occur in Mesembryanthemum and Aizoon species, but the well-known example is M. crystallinum, intensely studied also for its special capacity to switch from C₃ to CAM photosynthetic pathway (Grigore and Toma 2017). From structural point of view, these epidermal bladder cells would correspond to bladders of vezicular hairs found in Chenopodiaceae , since they lack stalk cell.

The epidermal bladder cells from M. crystallinum can accumulate large amount of water inside them, thus conferring the typical appearance of “ice plant,” the vernacular name of Mesembryanthemum (Grigore and Toma 2010b). Thus, they represent a xerophytic adaptation; in parallel, these bladder cells can be regarded as isolated water storage cells, forming a peripheral water storage tissue (Schimper 1903). In fact, some epidermal cells project above epidermis, forming large water vesicles (Figs. 96 and 97). According to Schimper (1903), when plant transpiration is weak, these vesicles are filled with water during the night or when the sky is cloudy; when transpiration is intense, these vesicles supply assimilating cells with water and then collapse. Under salt treatments, these cells become larger covering extended parts of aerial organs in Mesembryanthemum (Grigore and Toma 2010b).

Haberlandt (1914) attributed to bladder cells of M. crystallinum an adaptation typical of xerophytes, whose epidermal cells can sometimes increase their volume, thus acquiring a water storage role.

2.13.9 Other Salt Glands (Cressa cretica, Ipomoea pes-caprae, and Lavatera arborea)

Ipomoea pes-caprae , Cressa cretica (Convolvulaceae), and Lavatera arborea (Malvaceae) have salt glands, which are less studied than those previously discussed (Grigore and Toma 2010b).

Warming described the anatomical structure of Ipomoea pes-caprae, designating these glands as either “glandular hairs” or “hydathodes” (Fig. 98). Lavatera arborea has a gland consisting of a large basal cell, two intermediary cells, and five apical cells.

2.14 Kranz Anatomy Structures

Despite C₄ photosynthesis is found in many nonhalophytic species, in C₄ halophytes, Kranz anatomy is a good example of connection between structure and specific processes in C₄ photosynthesis. In C₄ plants metabolic processes of C₄ pathway need the cooperation of two distinct chlorenchyma tissues: an external one (or photosynthetic carbon assimilative – PCA) and an inner bundle sheath (or photosynthetic carbon reductive – PCR) tissue. These chlorenchyma tissues are usually arranged concentrically with respect to vascular tissues, forming a structural pattern known as Kranz anatomy (Muhaidat et al. 2007).

This internal structure physically partitions the biochemical events of the C₄ pathway into two major phases. In the first step, atmospheric CO₂ is initially assimilated into C₄ acids by PCA tissue-specific phosphoenolpyruvate carboxylase. In the second phase, these acids diffuse into the PCR compartment, where they are decarboxylated, and the released CO₂ is refixed by PCR tissue-specific Rubisco. This biphasic C₄ system enhances CO₂ levels around Rubisco, suppressing photorespiration and improving plant carbon balance (Kanai and Edwards 1999).

Kranz anatomy has been found in several Romanian halophyte species (Grigore and Toma 2007a, b, c, 2008a, 2017; Grigore et al. 2012a, c, 2014), Spanish (Grigore et al. 2011a, b, 2014; Grigore and Toma, 2017), and Iranian halophytes (Safiallah et al. 2017) revealed by Kranz anatomy in many Chenopodiaceae species: Atriplex tatarica (Fig. 99), A. glauca (Fig. 100), A. halimus (Figs. 95 and 101), Petrosimonia oppositifolia (Figs. 31 and 102), P. triandra (Figs. 32 and 103), Camphorosma annua (Figs. 34 and 104), C. monspeliaca (Fig. 105), Suaeda splendens (Figs. 39 and 106), Salsola kali (Figs. 38 and 107), S. oppositifolia (Figs. 36 and 108), and Bassia hyssopifolia (Fig. 109). Kranz anatomy has been also evidenced in several halophytic Iranian species of Bassia: B. prostrata (Fig. 110), B. pilosa (Fig. 111), and B. turkestanica (Fig. 112) (photo courtesy of Somayeh Safiallah).

2.15 Bulliform Cells

Bulliform cells (motor cells, “hinge cells”) have been evidenced in several Romanian salt-tolerant plants, nominated as “amphibious halophytes”: Juncus gerardii, Bolboschoenus maritimus, Carex distans, C. vulpina, Agrostis stolonifera, Alopecurus arundinaceus , and Puccinellia distans (Grigore et al. 2014; Grigore and Toma 2017). These cells ensure the rolling up of leaves under drought conditions and reopening again under favorable conditions of rehydration. Thus, they could be regarded as a xeromorphic adaptation in this group of halophytes; the abovementioned species are usually hygrophilous, vegetating in salt marshes that sometimes can be flooded but often are exposed to prolonged droughts. The temporary characters of soil moisture and atmosphere humidity induce anyway the necessity of some xeromorphic adaptations, as a response to both water stress and salt stress (Grigore 2012; Grigore and Toma 2014; Grigore et al. 2014).

Grigore and Toma (2010c) included halophytes with bulliform cells that vegetate in wet, salinized environments but also subjected to seasonal droughts in the category of amphibious halophytes: Bolboschoenus maritimus, Carex distans (Fig. 113), Carex vulpina (Fig. 114), Juncus gerardii (Fig. 115), Agrostis stolonifera (Fig. 116), Alopecurus arundinaceus (Fig. 117), and Puccinellia distans (Fig. 118).

3 Morphological and Anatomical Adaptations of Halophytes from (Nontropical) Salt-Marsh Formations

A typical example of adaptations of halophytes belonging to maritime formations (salt-marsh formation): Spartina stricta , Juncus roemerianus , Typha, Spartina patens, and Baccharis-Hibiscus associations will be provided (Kearney 1900, 1901).

These are the conditions of the physical environment that most probably affect the structure and habit of salt-marsh plants vegetating in various salt-marsh (“creek-marsh”) formations, often subjected to tidal influence (Kearney 1901):

1.
Liability to partial submersion at high tide
2.
A soft, more or less mobile substratum
3.
The presence of a relatively high percentage of common salt (sodium chloride) in soil and water

In respect to abovementioned and discussed ecological conditions that induce general and particular adaptations in halophytes, it is easily noticeable that it is important to take into account the substratum, the tidal influence, and the mechanical action of the wind.

The modifications of structure that can be attributed to the influence of these three factors may be included in several principal categories:

(A)
Structures preventing free access of water to submerged parts. The most obvious adaptation of this class is the persistence of the basal sheaths in grasses and grass-like plants. This is well exemplified in Spartina stricta maritima, where the bases of culms are tightly enveloped by the closely imbricated, large papery sheaths (Fig. 119).
(B)
Structures serving to hold the plant fast in the watery, incoherent soil. These take the form in most cases of long rootstocks, creeping through the mud and sending up erect leafy and flowering branches at frequent intervals (Fig. 120). This feature is found in the underground parts of the great majority of salt-marsh plants. Often, as in Typha, Spartina polystachya, Phragmites, and other large plants with a considerable weight to be supported, the rhizomes are very long and large. Annual plants, which are few in the salt marshes (Aster subulatus and Salicornia herbacea being the only common species), have less need of firm anchorage in the soil.
(C)
Structures serving to reduce the loss of water from the leaves, which would otherwise be excessive, as the chiefly herbaceous salt-marsh vegetation, unsheltered by large, woody plants, are directly exposed to the drying effect of the wind and to the strong light and heat of the sun. The necessity for such protection is greater because, as is well-known, roots absorb water with difficulty when it contains any considerable percentage of salts in solution, owing to the decreasing force of endosmosis when the degree of concentration of the external water approaches that of the cell sap. In order to compensate the reduced absorbing activity of the roots, it is obvious that the escape of water from the upper part of the plant, especially from the leaves, where it is normally greatest, must be correspondingly checked. To the plants of the salt marshes, growing in a soil that is impregnated with salt (in solution) and subject to partial or total inundation twice a day by brackish water, it is very important that the supply of water so scarce provided to their substratum should be carefully kept. However, even it is not easy for salt-marsh plants to absorb water, it would not be to their benefit to take it up in great quantities, because it would lead in an increased accumulation in the cells of sodium chloride, which would turn into a harmful effect (Grigore et al. 2014; Grigore and Toma 2017 and reference therein).

There are several morphological-anatomical modifications that may be involved in diminishing transpiration (Warming 1897, 1909; Henslow 1895; Kearney 1901; Schimper 1903; Coulter 1900; Børgesen and Paulsen 1900; Grigore and Toma 2017):

(a)
Thickening of the cuticle and epidermis walls, which is exhibited, often to a high degree, by nearly all plants of the salt marsh (Fig. 121). This thickening (sometimes forming papillae) is often evident when species of the salt marsh are compared with nearly related species from other localities or even when individuals of the same species, vegetating in salt marsh and some in inland habitat, are compared.
(b)
Hairy covering sufficiently dense to act as a protection against excessive transpiration occurs only in Borrichia frutescens , which has both leaf surfaces very densely covered with two- to four-celled hairs (each epidermis cell being thus extended by tangential division) (Fig. 122a, b). Hairs located on both leaf surfaces are also found in Kosteletzkya virginica, Lippia nodiflora (Fig. 123), Monniera monniera, Iva frutescens (Fig. 124), and Solidago sempervirens.
(c)
Waxy covering in Panicum amarum, Uniola paniculata, and Euphorbia polygonifolia .
(d)
Stomata , protected by being located in furrows of the leaf surface, where all or at least most of the stomata lie, especially in Spartina species and several sedges.
(e)
Leaf conduplicate or involute (Fig. 125), thus concealing the ventral surface, where all or most of the stomata are located, especially in the species of Spartina and in certain sedges.
(f)
Leaf vertical in Juncus roemerianus , Fimbristylis spadicea (Fig. 126), and Typha latifolia (Fig. 127), nearly vertical in species of Spartina and other grasses and in Baccharis, Aster spp., Iva frutescens, and other dicots with isolateral leaves.
(g)
Transfer of the normal functions of leaves in large part to the (erect) stems, in Juncus roemerianus , Scirpus species (Fig. 128), and Salicornia herbacea (Fig. 129). It refers mainly to photosynthetic function, transferred to stem by the important development of chlorenchyma.
(h)
Small size of the leaves, and thus of the transpiring surface, without transfer of function to the stems, in Aster subulatus (Fig. 130), Aster tenuifolius (Fig. 131), Sabbatia gracilis (Fig. 132), Lythrum lineare (Fig. 133), Lippia nodiflora (Fig. 134), Monniera (Herpestis) monniera (Fig. 135), and many other species.
(i)
Succulence : of stem (accompanied by reduction of the leaves to mere scales) in Salicornia herbacea (see Figs. 45 and 129) and other halophytic chenopods with articulated stems and of leaves (moderate) in Borrichia (Fig. 122), Solidago sempervirens, and Aster subulatus (Fig. 136) (where the stems are also somewhat succulent). Succulent plants lose their water much more slowly than do others, since the water storage tissue, the strong development of which causes the thickening of the succulent parts, gives up its supply reluctantly. This is in some cases due to the presence of mucilage in the cells of water storage tissue, which contribute to a better retaining of water (Volkens 1887; Grigore 2008; Grigore et al. 2014; Grigore and Toma 2017).
(j)
Presence of a considerable amount of mineral salts , especially sodium chloride, in solution in the cell sap. A plant organ which holds in its cells more than the ordinary quantity of dissolved mineral substances loses through transpiration less than the ordinary amount of vapor of water.
(k)
Development of compact palisade tissue (Fig. 122), usually on both surfaces of the (in such cases) isolateral leaf. Nearly all the species, of both sand strand and salt marsh, are characterized by the development of palisade, a compact chlorophyll tissue with cells more or less elongated at a right angle to the surface and occupying the exposed face or faces, i.e., the ventral face in bifacial leaves, both faces in such as are isolateral. Such tissue is believed to have, among other functions, that of protecting against excessive loss of water the remainder of the leaf (the interior or the lower face, as the case may be), which is usually occupied by less compact tissue (Kearney 1900).
(l)
Aromatic (volatile) oil – secreted by Myrica species, it has been suggested that volatile oils enable a protection against excessive loss of water by formation around the plant in an envelope (Henslow 1895; Kearney 1900;Volkens 1887).

(D)
Adaptations to exposure to the mechanical action of the wind A notable characteristic of the vegetation is the prevalence of low forms. Tall stems (more than 1 meter high) among herbaceous species which are not grass-like are almost lacking. Often the stems creep above or below the surface of the ground and root at intervals. Lippia nodiflora , Monniera monniera, Capriola dactylon, and Paspalum distichum have stems creeping upon the surface. These may be regarded as correspondent representatives of the Ipomoea pes-caprae form, which is also characteristic of tropical strands (Warming, 1897, 1906). Some salt-marsh species have creeping subterranean stems, from which arise subaerial leafy and flowering branches, such as Panicum amarum minus and Uniola paniculata; other species such as Juncus roemerianus , Typha latifolia, and Spartina stricta possess strong, creeping rhizomes that form a dense network in the marshy soil. In Uniola paniculata the rhizome is strong and descends obliquely or almost vertically deep into the sand. Physalis viscosa has a long, slender, branching root, which creeps horizontally often a distance of a meter or more near the surface and originates at intervals erect, leafy, and flowering branches. Teucrium nashii possesses thick stolons, which arise in the axils of the scale-like, lowest leaves (Kearney 1900).

Another adaptation against the coast winds, whose harmful effect upon plants is greatly increased by the quantity of carried sand, is the great development of mechanical tissue (Kearney 1900, 1901) in the leaves of many species: Uniola paniculata, Juncus roemerianus , Quercus virginiana – and the strong thickening of the outer cell walls of the epidermis, in grasses, and in the evergreen leaves of Quercus virginiana and Ilex.

A synthesis of leaf anatomical features of salt-marsh species is presented in Tables 2, 3, 4, and 5 (Kearney 1900).

Table 2 Leaf anatomy of salt-marsh species from Ocracoke Island, general characters (Kearney 1900) (+, character present; /, imperfect development of the character)

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Table 3 Leaf anatomy of salt-marsh species from Ocracoke Island, stomata in respect to epidermis (Kearney 1900) (+, character present; /, imperfect development of the character)

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Table 4 Leaf anatomy of salt-marsh species from Ocracoke Island, hairs in respect to epidermis and collenchyma (Kearney 1900) (+, character present; /, imperfect development of the character)

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Table 5 Leaf anatomy of salt-marsh species from Ocracoke Island, stereome, chlorenchyma, water storage tissue, and vascular bundles (Kearney 1900) (+, character present; /, imperfect development of the character)

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4 Morphological and Anatomical Adaptations of Littoral (Tropical, Nontropical) Halophytes (Seashore Plants, Sea-Coastal Plants, Strand Plants, Psammohalophytes)

As already underlined, diverse ecological conditions where halophytes vegetate delineate different contexts in which adaptations of halophytes can be discussed and approached. The terminology of halophytes may be difficult, tricky, and sometimes confusing – different terms that are not perfectly interchangeable describe slightly different halophytic plants – but it covers a large spectrum of salt-ecological realities (Grigore 2008, 2014; 2019; Grigore and Toma 2010a, b, 2017; Grigore et al. 2014).

While not all littoral (seashore) plants are true halophytes, stricto sensu (see Grigore and Toma 2017, and references therein), the halophytes from littoral areas must be particularly approached; moving forward, halophytes from tropical and nontropical seashores should be differently approached.

There is a large list with classic papers dealing with morphological and anatomical adaptations of halophytes from littoral, being nontropical (Harshberger 1909; Chermezon 1910) or tropical (Warming 1897; Børgesen and Paulsen 1900; Warming 1906; Børgesen 1909; Denis 1919).

Børgesen and Paulsen (1898) divided the halophytic vegetation of the Danish islands (former Danish West Indies) in:

(a)
The seagrass vegetation
(b)
The sand strand vegetation
(c)
The rocky coast vegetation
(d)
The mangrove vegetation
(e)
The marsh land vegetation near lagoons and salt ponds

In a later study on the halophytic vegetation from the Danish West Indies, Børgesen (1909) added new material and consequently divided the coastal halophytic vegetation in:

A. The Hydrophyte Vegetation

I. The muddy and sandy soil vegetation

1. The seagrass (and algae) formation

B. The Halophyte Vegetation

I. The muddy soil vegetation

1.
The mangrove formation
2.
The Salicornia formation
3.
The Conocarpus formation

II. The sand strand vegetation

1.
The Pes caprae formation
2.
The Tournefortia formation
3.
The Coccoloba-Manchineel formation

III. The rocky coast vegetation

This chapter does not intend to deal with halophytic flora and vegetation, but this unique example of complexity of classifying halophytes clearly illustrates the heterogeneous nature of morphological and anatomical adaptations in halophytes that vegetate in different ecological conditions.

The vast majority of the Caribbean plants of the West Indies are shrubs, either larger as Suriana maritima , Scaevola plumieri , Tournefortia gnaphalodes , Borrichia arborescens, Conocarpus erectus, Salicornia ambigua (Fig. 137), Batis maritima (Fig. 138), Heliotropium fruticosum or curassavicum, Ernodea littoralis , and Erithalis fruticosa or smaller shrubs as Cakile aequalis and Euphorbia buxifolia (Warming 1897).

This salt-bush vegetation, which has been mentioned in direct connection with the mangrove vegetation and included under the Salicornia formation (Børgesen (1909)), occurs partly and especially on the wide marsh-like flats, which lie in the interior of lagoons, partly it also encircles the lagoons and salt ponds, where the mangrove vegetation is absent (Børgesen and Paulsen 1898, 1900). The West Indian Salicornia formation closely corresponds to the Salicornia formation of the Danish shores, and the West Indian species and Salicornia herbacea are also nearly related even perhaps the same species (Raunkier 1907). Salicornia ambigua has almost evenly thick, cylindrical branches, and they are sometimes erect, sometimes lying, rooting, and from the latter numerous side branches merge in such great number that compact bush arise (Fig. 137); this is an adaptation to wet, coastal, saline conditions.

Batis maritima has long, prostrate, rooting main branches often almost straight as a line, from which at each internode two opposite branches, the one more vigorous than the other, emerge upward; and a similar number of roots descend toward the salt marshy soil (Fig. 138). The plant is commonly fresh green and has thick, fleshy, glossy, erect leaves. Sesuvium portulacastrum is also a typical halophyte with prostrate, rooting branch (Fig. 139).

Warming in his consistent study referring to structural characteristics of tropical halophytes from West Indies seashore (1897) described succulent or narrow-reduced leaves (Fig. 140), which is a xeromorphic adaptation (Grigore et al. 2014).

Based on his extensive results on anatomical adaptations of tropical halophytes, but also reported to those collected from Denmark, Norway, Greenland, Warming (1897) tried to cluster them in different groups. This consistent data are very important because they bring data about epidermis, chlorenchymatic tissues, water storage tissue, bundle sheaths, and hypodermis and relation between them in the context of saline conditions.

Thus, Warming described:

A.
Dorsiventral leaf – differs little or nothing from usual leaves. No water tissue, all leaf cells are green tissue cells. No real bundle (veins) sheaths. The leaves are distinctly dorsiventral, reminding of the common profile of mesophilic leaves. This foliar type also occurs in halophytic species from moderate and cold climates, but there are also Mediterranean and tropical plants among them. Vascular sheaths could be found, but they are weakly pronounced. In this group can be included Glaux maritima (Figs. 141 and 142), Erythraea vulgaris, Plantago major f. scopulorum, Cochlearia officinalis, C. anglica, Teucrium polium, Canavalia obtusifolia, Acanthospermum xanthioides, and Diodia radicans.
B.
Dorsiventral leaf of the ericoid type (Frankenia laevis ) (see Figs. 81 and 82).
C.
Intermediate forms between dorsiventral and isolateral leaves. In most, there are chlorophyll-containing bundle sheaths. After the aspect of the epidermis, it must be referred to the dorsiventral type, but after the succulence of the leaf, to the isolateral. The group is close to that described at the point “A” and contains, like this, species that vegetate in moderate climates: Mertensia maritima (Fig. 143), Silene maritima, Chenopodium ambrosioides, Euphorbia paralias , Armeria vulgaris, and Juncus gerardi.
D.
Isolateral leaves with chlorophyll-containing interlayer, clear sheaths around bundles. The leaves are isolateral. Mesophyll is a palisade tissue with a thinner or thicker intermediate layer, which has less chlorophyll content than the palisade tissue, but is not yet a genuine pure water tissue. The nervures lie in the middle layer and have clear sheaths (at least on the larger nerves). In the latter species, there is more than one layer of clear cells that connect to the nerves: Plantago maritima (Fig. 144), Plantago coronopus, Plantago crassifolia (Figs. 23 and 145), Silene inflata, Statice monopetala, Tetragonolobus siliquosus, Matricaria inodora, Glyceria maritima , Ipomoea pes-caprae (Fig. 146), I. acetosaefolia, Baccharis dioica, and Ernodea littoralis (Fig. 147).
E.
Isolateral leaves with more or less developed chlorophyll-containing interlayer, chlorophyll-containing bundle sheaths (but not starch sheaths) in some species, indistinct or no sheaths in others. The leaves are in this group isolateral. The leaf mesophyll is formed by palisade tissue and a thin intermediate layer, which may be more or less chlorenchymatic, but cannot yet be called water tissue and is not sharply distinct from palisade tissue. The nervures are confined to this middle layer: Acicarpha spathulata (Fig. 148), Atriplex hastata , Alisne (Halianthus) peploides, Silene nicaeensis, Conocarpus erecta (Fig. 149), Inula crithmoides (see Fig. 27), Aster tripolium (Figs. 150, 151, and 152 – where the isolateral character of the leaf may vary depending on the level of cross section through the leaf), Suriana maritima (Fig. 153), Beta vulgaris, Cakile aequalis (Fig. 154), Cakile maritima (Fig. 155), Crambe maritima, Heliotropium currasavicum, Polygonum maritimum, Bupleurum tenuissimum, Silene otites, Crucianella maritima, Statice limonium, Statice rariflora, Medicago marina (Fig. 156), Malcolmia littorea, Polygala cyparissias, Convolvulus soldanella, Sedum anglicum, and Halocnemum strobilaceum .
F.
Isolateral leaves, the intermediate layer is sharply delimited from the palisade tissue and is more related to a water tissue. No special sheaths around vascular bundles. The leaves are isolateral, and the leaf succulence is mainly due to palisade tissue: Suaeda maritima (Figs. 16 and 157), Suaeda (Sarcocornia) fruticosa (see Figs. 13, 14, and 158), Spergularia marina (Fig. 159), S. media (see Figs. 28 and 29), Obione (Halimione) portulacoides (Fig. 160), and Halimus sp.
G.
As group F but with hypodermic water tissue. In Eryngium maritimum (Fig. 161 – Toma 1979), its water tissue may still have a little chlorophyll, so it is not quite clear if it has a hypodermic genuine water tissue.
H.
Isolateral leaves with an intermediate layer that is genuine water tissue. The vascular bundles lie in one plane and have no contact with the chlorenchyma. No vascular sheaths: Tournefortia gnaphalodes (Fig. 162) and Scaevola plumieri (Fig. 163).
I.
Isolateral leaves with central water tissue in which the main nervures lie. A net of thin nervures start from them to all sides, but does not enter into contact with palisade tissue. There are no bundle sheaths. The leaves, which are very thick, have a large, colorless layer (water tissue), surrounded by chlorenchyma tissue for all sides: Sesuvium portulacastrum (Fig. 164), Borrichia arborescens (Fig. 165), Zygophyllum album, Batis maritima (Fig. 166), Echinophora spinosa, and Triglochin maritimum.
J.
Similar to the type I, but the morpho-anatomical conditions indicate the “leafless” stems (Salicornia type): Salicornia herbacea (Fig. 129; see Figs. 45 and 48, Salicornia patula ; 49, Salicornia australis ; 50 and 51, Salicornia ramosissima; 52, Salicornia glauca), Ephedra distachya, and Tamarix gallica.
K.
Isolateral leaves with large central water tissue, surrounded by a starch sheath (internal chlorenchyma), which is again surrounded by a palisade tissue (external chlorenchyma). There are fine nerves in contact with internal chlorenchyma (Salsola type): Salsola kali (Fig. 167; see Figs. 38 and 107). This corresponds to a C₄ photosynthetic type (Grigore 2008; Grigore et al. 2014; Grigore and Toma 2017).
L.
Like “L” type, but the morphological and anatomical features suggest a “leafless” stem (Haloxylon type): Haloxylon ammodendron (Fig. 168 and 169).
M.
More or less dorsiventral or isolateral leaves with complete starch bundle sheaths, wreath palisades in many species. Water storage tissue is present in smaller or larger extent: Heliotropium fruticosum (Fig. 170), Pectis humifusa (Fig. 171), Euphorbia bahiensis , E. buxifolia (Fig. 172), Portulaca oleracea, Philoxerus vermiculatus (Fig. 173), Sporobolus virginicus, Stenotaphrum americanum, and Cynodon dactylon.
N.
As previous type, but the starch bundle sheath is opened on the phloem side. Even around the smallest nerves, the sheath is interrupted: Atriplex farinosa (Fig. 174), Atriplex cristata , Atriplex halimus (Fig. 175), and Atriplex laciniata. It is also a C₄ photosynthetic type (Grigore and Toma 2017).
O.
As N type, but a mechanical sheath is inserted between the starch bundle sheath (internal chlorenchyma) and the external chlorenchyma tissue, which is more or less a typical Kranz palisade: Remirea maritima (Fig. 176) and Galilea mucronata.
P.
Dorsiventral leaf with hypodermic water storage tissue, which has different disposition: Lippia nodiflora (Fig. 177), Erithalis fruticosa , and Sophora littoralis.

5 Mangroves (Tropical Coastal Halophytes, Littoral Swamp Forest, Tidal Forest)

The term mangrove is manifold; in this subsection, the morphological and anatomical adaptations of mangrove species are discussed in general terms, without following the classification of halophytic coast vegetation above mentioned (Børgesen and Paulsen 1898, 1900; Børgesen 1909).

Davis (1940) refers to mangrove as a general term applied to plants, which live in muddy, loose, wet soils in tropical tide waters. According to Macnae (1968), mangroves are trees or shrubs that grow between the high water mark of spring tides and a level close to but above mean sea level. They are circumtropical on sheltered shores and often grow along the banks of rivers as far inland as the tide penetrates (Walsh 1974).

Børgesen (1909) dealt with mangroves from Danish West Indies as a formation of tree-like evergreen plants growing on the sheltered shores, partly in shallow, salt, or brackish water, partly on low-lying soil that is comparatively rarely, and sometimes perhaps never covered by salt or brackish water.

In very general terms, there seem to be five basic requirements for extensive mangal development: tropical temperatures, fine-grained alluvium, shores free of strong wave and tidal action, salt water, and large tidal range (Walsh 1974).

Warming (1877, 1883, 1909) described very well the environmental conditions where mangrove species vegetate. They occur by all tropical seas, especially on flat, muddy shores, where the water is relatively calm, as in lagoons, inlets, estuaries, but not where rocky soil and breakers prevail. The soil is flooded with water either permanently or at high tide. In many places mangrove vegetation extends far inland along the banks of large rivers. The water is usually more or less brackish, as far as the tide extends.

The soil, which in places is not covered with water at low tide, is soft, deep, black mud, and full of rotting, organic bodies in which bacteria abound. The water between the trees may be covered with dirty film and bubbles of gas rising from the bottom burst at the surface.

The morphological and anatomical adaptations of mangrove species are well-documented (Warming 1877, 1909; Liebau 1914; Bowman 1917; Schimper 1891, 1898, 1903; Børgesen and Paulsen 1898, 1900; Børgesen 1909).

Warming (1909) reveals the adaptations of mangroves.

a. Fixation in the Substratum with Aerial Prop Roots

The degree of softness of the soil and the variety in depth of water evoke differences and cause the species to assume a zonal distribution into associations. On the landward side, mangrove plants vanish and are replaced by other shrubs and trees. Furthest out toward the sea are those that are best capable of fixing themselves in deep water, namely, species of Rhizophora; within these, in shallower water or on drier ground, succeed those species that have smaller capabilities in this respect, species of Avicennia, Bruguiera, Aegiceras, Carapa, and others. The species of Rhizophora are fixed by prop roots that are aerial roots, which spring from the main trunk and form arched stilts which penetrate the ground. Sometimes, the aerial roots arise adventitiously from the lower branches of the tree; they curve down to the ground in an arching fashion. These bow-like roots upon which the tree depends are very numerous; the foundation of the tree is firmer, and its power of resistance to bending, which may be caused by wind or movements of the water, is greater than if the stem was the sole support (Figs. 178 and 179).

The anatomical construction of these roots agrees with the unusual nature of the demands to which they are exposed as supporting structures and deviates from that of most other roots in that the mechanical tissue is made to assume a tubular arrangement around large pith (Fig. 180). Similar prop roots are possessed by Ceriops and Acanthus ilicifolius. The lower parts of these prop roots are often beset with algae.
b. Respiratory Roots (Pneumatophores)

Respiration is a process under difficulty in the soil, which is water-logged, rich in organic bodies, and poor in oxygen. For this reason all the mangrove plants have a strongly developed system of aerenchyma; the submerged parts are very spongy and soft in structure; stomata and unusually large lenticels on parts projecting above water place the atmosphere in communication with the intercellular spaces. The prop roots of Rhizophora serve as respiratory roots. Other species possess quite peculiar respiratory roots (pneumatophores). Avicennia has erect, unbranched “asparagoid” roots a foot in height; these stand in very long rows, which radiate from the tree and indicate the position of the horizontal roots from which they emerge (Figs. 181, 182, and 183). Their respiratory role is revealed by anatomical structure (Fig. 184).

Similar respiratory roots are found in Sonneratia acida, Laguncularia racemosa (Figs. 185 and 186), Bruguiera caryophyllaeoides (Fig. 187a), B. gymnorrhiza (Fig. 187b), and Carapa obovata (Fig. 187c); bent knee-like roots, with the knee projecting above water, occur in Bruguiera and to a less extent in Lumnitzera, while comb-like prolongations connected with the root occur in Carapa. Anatomical configuration supports this function. In Laguncularia racemosa , the primary cortex develops initially as air-storing tissue, and the inner part of cortex is delimited by a distinct endodermis; in its growth, the primary cortex diminishes, and the large area of phloem acquires an air-storing function (Fig. 188). Idioblasts (trichoblasts) like those evidenced in Rhizophora are also found in Sonneratia (Fig. 189) and Bruguiera gymnorrhiza (Fig. 190).
c. Germination and Vivipary

Vivipary is defined as the process in which the seed remains attached in the fruit to the mother tree, germinates into a protruding embryo with a long hypocotyl, and finally falls from the tree (Robyns 1971). That means the embryo plant, while still attached and nourished by the parent tree, grows into a more or less developed plant without undergoing any resting period (Warming 1909). Several series of stages may be evidenced:
1. i.
  In Aegiceras the embryo emerges from the seed but remains inside the fruit; it has a large stem and is green.
2. ii.
  In Avicennia (Figs. 191 and 192) the endosperm and subsequently the embryo emerge from the seed and lie uncovered within the chamber of the ovary. The embryo is green and obtains food from the parent plant by means of a long, repeatedly branched, hypha-like haustorial cell, which traverses the placenta.
3. iii.
  In Rhizophora (Figs. 193 and 194) and allied genera (Bruguiera caryophylloides, Fig. 193; B. parviflora, Fig. 195; Kandelia rheedii , Fig. 196; and Ceriops), the embryo grows not only out of the seed but also out of the fruit and projects from the latter in the form of a green seedling displaying the hypocotyl and root, which in some species exceed one-third of a meter; then, the full-formed seedlings hang down from the branches. The cotyledons serve as a haustorium, sucking food from the parent plant. Finally, the seedling breaks loose from the cotyledons (Rhizophora has only one cotyledon), which remain behind inside the fruit and shrivel with it. Seedling falls into the water or mud; its club shape and pointed root end help it to penetrate the mud, into which it rapidly thrusts lateral roots that had previously been initiated. If the seedling does not succeed in fixing itself, it floats and may strike root on some distant shore; in this way the species is provided with means of dispersal by water.
d. Means of Migration

The mangrove includes approximately the same species along all the tropical shores from Australia to East Africa. This is due in part to the fact that the medium temperature remains uniform throughout and in part to the efficient means of dispersal. Due to air-containing spaces in the integument or in other parts and to the consequent decrease in specific gravity, fruits, seeds, and seedlings of mangrove plants can float for a very long time, without losing their germinative power (Warming 1909).
e. Xerophytic Structure

The great majority of mangrove species are shrubs and trees. Despite the circumstance that these plants grow in flooded muddy soil, their shoots display a number of structural features that occur in plants adapted to withstand drought. In other words, as already underlined in this chapter, their habitat is affected by physiological drought conditions (Warming 1909; Schimper 1891, 1903; Grigore 2008; Grigore and Toma 2010a; Grigore et al. 2014; Grigore and Toma 2017).

Xeromorphic adaptations of mangroves can be found in the following structural features:

(a)
The leaves are thick, coriaceous, or succulent in some extent: Sonneratia, Lumnitzera (Fig.197), Carapa (Fig. 198), Rhizophora, and Avicennia.
(b)
The epidermis is thick-walled and strongly cutinized; the leaves are often very glossy: Rhizophora mucronata (Fig. 199) (Schimper 1891, 1903).
(c)
Salt glands.
(d)
Stomata are often sunk beneath the general surface of epidermis.
(e)
Water storage tissue is always present (Fig. 198) and sometimes massive. In Rhizophora mucronata , the older leaves, which no longer assimilate, become thicker than younger leaves; this is caused by an enlargement of the water storage tissue, and thus the leaf changes its function.
(f)
The mesophyll has few intercellular spaces, but the palisade tissue is well-developed, as main or unique chlorenchyma: Sonneratia (Fig. 200) and Lumnitzera.
(g)
The ends of nervures dilate into water-storing tracheids: Sonneratia (Fig. 201), Bruguiera, Avicennia, and Ceriops.
(h)
Long stone cells or bast-like mechanical cells are lodged between the palisade cells in Rhizophora (Fig. 199), Sonneratia, and Carapa and in the pith of Rhizophora.
(i)
Mucilage cells occur in species of Sonneratia and Rhizophora (Fig. 199).
(j)
Some species are strongly and densely clothed with hairs: Avicennia .

6 Conclusions

This contribution reinforces the idea that halophytes are – from morphological and anatomical point of view – a special case of xerophytes. For practical purposes, their adaptations were here called “general” and approached consequently; in fact, these morphological and anatomical features are xeromorphic, and this is due to the so-called physiological drought that affects all saline environments. Different described situations (nontropical salt-marsh halophytes, sea-coast halophytes, mangroves) illustrate that, without losing their xeromorphic profile, halophytes’ adaptations can be regarded as the fine results of various environmental factors – not only restricted to elevated salinity – and the mangroves support perfectly this idea. They have coriaceous, thick often succulent leaves; some of them have salt glands, tracheids, mucilage cells, and well-developed palisade tissue. Because of the particular ecological conditions, mangroves are viviparous and have aerial, prop, and respiratory roots. None of the other types of halophytes have all of these last mentioned adaptations; however, halophytes free from the power of sea winds and sprays, vegetating in salt deserts or steppes, may be succulent or can possess salt glands. But all of them have in common the fact that must face the physiological drought of their environment.

References

Bari, E. M. M. A., Yassen, B., & Al-Thani, R. F. (2007). Halophytes in the state of Qatar. Doha-Qatar: University of Qatar.
Google Scholar
Børgesen, F. (1909). Notes on the shore vegetation of the Danish West Indian islands. Botanisk Tidsskrift, 29, 201–259.
Google Scholar
Børgesen, F., & Paulsen, O. (1898). Om vegetationen paa de Dansk-Vestindiske øer. Kjøbenhavn/Bogforlaget: Det Nordiske Forlag/Ernst Bojesen.
Book Google Scholar
Børgesen, F., & Paulsen, O. (1900). La végétation des Antilles danoises. Revue Generale de Botanique, 12(135), 99–107; 12(136), 138–153; 12(138), 224–245; 12(139), 289–297; 12(141), 344–354; 12(143), 434–446; 12(144), 480–510.
Google Scholar
Bowman, Η. Η. M. (1917). Ecology and physiology of the Red Mangrove. Proceedings of the American Philosophical Society Philadelphia, 56, 589–672.
Google Scholar
Breckle, S.-W. (1995). How do halophytes overcome salinity? In M. A. Khan & I. A. Ungar (Eds.), Biology of salt tolerant plants (pp. 199–213). Karachi: Department of Botany, University of Karachi.
Google Scholar
Breckle, S.-W. (2002). Salinity, halophytes and salt affected natural ecosystems. In A. Lauchli & U. Lüttge (Eds.), Salinity: Environment-plants-molecules (pp. 53–77). New York: Kluwer Academic.
Google Scholar
Britton, N. L., & Brown, H. A. (1896, 1897, 1898). An illustrated flora of the Northern United States, Canada and the British Possessions (Vols. 1, 2, 3). New York: Charles Scribner’s Sons.
Google Scholar
Brunner, C. (1908). Beiträge zur vergleichenden Anatomie der Tamaricaceen. Beih zum Jahrbuch der Hamburgischen Wissenschaftlichen Anstalten, 26, 89–162.
Google Scholar
Brunswik, H. (1920). Über das vorkommen von gipskrystallen bei den Tamaricaceae. Sitz der Kaiser Akad der Wissen. Matematisch-natur, 129, 115–136.
Google Scholar
Chen, M., Yang, Z., Liu, J., Zhu, T., Wei, X., Fan, H., & Wang, B. (2018). Adaptation mechanism of salt excluders under saline conditions and its applications. International Journal of Molecular Sciences, 19(3668), 1–13.
Google Scholar
Chermezon, H. (1910). Recherches anatomiques sur les plantes littorales. Annales des Sciences Naturelles; sér 9 Botanique, 12, 117–313.
Google Scholar
Cooke, F. W. (1911). Observations on Salicornia australis. Transactions and Proceedings of the New Zealand Institute, 44, 349–362.
Google Scholar
Coulter, J. M. (1900). Plant relations; a first book of botany. New York: D Appleton and Company.
Book Google Scholar
Dangeard, P. A. (1888). Note sur la gaine foliaire des Salicornieae. Bulletin de la Société Botanique de France, 35, 157–160.
Google Scholar
Das, S. (1999). An adaptive feature of some mangroves of Sundarbans, West Bengal. Journal of Plant Biology, 42(4), 109–116.
Article Google Scholar
Davis, J. H. (1940). The ecology and geologic role of mangroves in Florida. Pap. from the Tortugas Lab. Vol. 32. Carnegie Institution of Washington Pub. 517, 303–412.
Google Scholar
de Bary, A. (1884). Comparative anatomy of the vegetative organs of the Phanerogams and Ferns. Oxford: Clarendon.
Book Google Scholar
de Fraine, E. (1912). The anatomy of the genus Salicornia. Journal of the Linnean Society: Botany, 41, 317–348.
Google Scholar
de Fraine, E. (1916). The morphology and anatomy of the genus Statice as represented at Blakeney Point. I. Statice binervosa G.E. Smith and Statice bellidifolia D.C. (Ľ Statice reticulata). Annals of Botany (London), 30, 239–282.
Google Scholar
Denis, M. (1919). Recherches anatomiques sur quelques plantes littorales de Madagascar. Révue Générale de Botanique, 31, 33–140.
Google Scholar
Duval-Jouve, J. (1868). Des Salicornia de l’Hérault. Observations anatomiques et morphologiques. Bulletin de la Société Botanique de France, 15, 132–140.
Google Scholar
Duval-Jouve, J. (1870). Étude anatomique de quelques graminées et en particulier des Agropyrum de l’Hérault. Paris: J-B Ballière et Fils.
Google Scholar
Elbar Abd Ola, H. (2015). Development of the successive cambia in Sesuvium verrucosum Raf (Aizoaceae). Annals of Agricultural Sciences, 60(2), 203–208.
Article Google Scholar
Elhalim, M. E. A., Abo-Alatta, O. K., Habib, S. A., & Abd Elbar, O. H. (2016). The anatomical features of the desert halophytes Zygophyllum album L.F. and Nitraria retusa (Forssk.) Asch. Annals of Agricultural Sciences, 6(1), 97–104.
Article Google Scholar
Fahn, A. (1988). Secretory tissues in vascular plants. The New Phytologist, 108, 229–257.
Article PubMed Google Scholar
Fitch, W. H., & Smith, W. G. (1880). Illustrations of the British flora: a series of wood engravings, with dissections of British plants. London: L. Reeve & Co., 5, Henrietta street, Covent Garden.
Google Scholar
Ganong, W. F. (1903). The vegetation of the Bay of Fundy Salt and Diked marshes: An ecological study. Botanical Gazette, 36(3), 161–186, 280–302, 349–367, 429–455.
Article Google Scholar
Ghanem, M. E., Han, R.-M., Classen, B., Quetin-Leclerq, J., Mahy, G., Ruan, C.-J., Qin, P., Pérez-Alfocea, F., & Lutts, S. (2010). Mucilage and polysaccharides in the halophyte plant species Kosteletzkya virginica: Localization and composition in relation to salt stress. Journal of Plant Physiology, 167, 382–392.
Article CAS Google Scholar
Gorham, J. (1996). Mechanisms of salt tolerance of halophytes. In R. Choukr-Allah, C. V. Malcom, & A. Hamdy (Eds.), Halophytes and biosaline agriculture (pp. 31–54). New York: Marcel Dekker Inc.
Google Scholar
Grigore, M.-N. (2008). Introducere în Halofitologie. Elemente de Anatomie Integrativă. Iași: Ed. PIM.
Google Scholar
Grigore, M.-N. (2011). Secreţia sărurilor la halofite: o strategie adaptativă complexă şi eficientă. Natura (Biologie) ser. III, 53(1), 86–97.
Google Scholar
Grigore, M.-N. (2012). Romanian salt tolerant plants. Taxonomy and ecology. Iași: Edit. Tehnopress.
Google Scholar
Grigore, M.-N. (2019). Defining halophytes – A conceptual and historical approach in an ecological frame. In M. Hasanuzzaman, S. Shabala, & M. Fujita (Eds.), Halophytes and climate change: Adaptive mechanisms and potential uses (pp. 3–18). Wallingford: CABI.
Chapter Google Scholar
Grigore, M.-N., & Toma, C. (2005). Contributions to the knowledge of the anatomical structure of some halophytes (I). Studii și cercetări Științifice Universitatea din Bacău Seria Biologie, 10, 125–128.
Google Scholar
Grigore, M. N., & Toma, C. (2006a). Ecological anatomy elements related to Asteraceae halophytes species. Studii și Comunicări Complexul Muzeal de Ştiinţele Naturii „Ion Borcea” Bacău, 21, 94–98.
Google Scholar
Grigore, M. N., & Toma, C. (2006b). Evidencing the successive cambia phenomenon on some halophylous representatives among Chenopodiaceae and its possible ecological-adaptive implications. Studii și Comunicări. Complexul Muzeal de Ştiinţele Naturii „Ion Borcea” Bacău, 21, 87–93.
Google Scholar
Grigore, M. N., & Toma, C. (2007a). Histo-anatomical investigations in some halophyte species of Moldavia. In Proceedings of the 1st international conference environment – Natural sciences- food industry in European context, Baia Mare, November 16–17, 2007, pp. 239–244.
Google Scholar
Grigore, M. N., & Toma, C. (2007b). Aspects on the ecological and functional anatomy of some halophyte species from the Chenopodiaceae family. In Proceedings of the 1st international conference environment – Natural sciences- food industry in European context, Baia Mare, November 16–17th 2007, pp. 257–264.
Google Scholar
Grigore, M. N., & Toma, C. (2007c). Histo-anatomical strategies of Chenopodiaceae halophytes: Adaptive, ecological and evolutionary implications. WSEAS Transactions on Biology and Biomedicine, 12(4), 204–218.
Google Scholar
Grigore, M. N., & Toma, C. (2008a). Ecological anatomy of halophyte species from the Chenopodiaceae family. Advanced topics on mathematical biology and ecology. In Proceedings of the 4th WSEAS international conference on mathematical biology and ecology – MABE ’08, Acapulco, Mexico, January 25–27, pp. 62–67.
Google Scholar
Grigore, M. N., & Toma, C. (2008b). A histo-anatomical study on some halophylous species of the Lepidium genus. Studia Universitatis “Vasile Goldiş”, Seria Ştiinţele Vieţii (Life Scences Series), 18, 27–23.
Google Scholar
Grigore, M. N., & Toma, C. (2008c). Ecological anatomy investigation related to some halophyte species from Moldavia. Romanian Journal of Biology – Plant Biology, 53(1), 23–30.
Google Scholar
Grigore, M.-N., & Toma, C. (2010a). Halofitele. Aspecte de anatomie ecologică. Iași: Edit. Universității „Alexandru Ioan Cuza”.
Google Scholar
Grigore, M.-N., & Toma, C. (2010b). Structuri secretoare de săruri la halofite. O abordare integrativă. București: Edit. Academiei Române.
Google Scholar
Grigore, M.-N., & Toma, C. (2010c). A proposal for a new halophytes classification, based on integrative anatomy observations. Muz. Olteniei Craiova. Studii și Comunicări, Științele Naturii, 26(1), 45–50.
Google Scholar
Grigore, M.-N., & Toma, C. (2011a). Halofitele, o categorie ecologică polimorfă. Între seceta fiziologică a solului și stresul salin. Revista Botanică (Chișinău), 2(3), 38–46.
Google Scholar
Grigore, M.-N., & Toma, C. (2011b). Ecological implications of bulliform cells on halophytes, in salt and water stress natural conditions. Studia Universitatis “Vasile Goldiș”, Ser Șt. Vieții, 21(4), 785–792.
Google Scholar
Grigore, M.-N., & Toma, C. (2014). Integrative ecological notes on halophytes from “Valea Ilenei” (Iași) nature reserve. Memoirs of the Scientific Sections of the Romanian Academy, 37, 19–36.
Google Scholar
Grigore, M. N., & Toma, C. (2016). Structure of salt glands of Plumbaginaceae. Rediscovering old findings from 19th century. ‘Mettenius’ or ‘Licopoli’ organs? Journal of Plant Development, 23, 37–52.
Google Scholar
Grigore, M.-N., & Toma, C. (2017). Anatomical adaptations of halophytes. A review of classic literature and recent findings. Cham: Springer International Publishing.
Google Scholar
Grigore, M.-N., Toma, C., & Boscaiu, M. (2011a). Ecological notes on halophytes species from Mediterranean climate. Lucr Șt (Horticultură), USAMV “Ion Ionescu de la Brad” Iași, 54(1), 29–34.
Google Scholar
Grigore, M.-N., Toma, C., & Ivănescu, L. (2011b). Anatomical and ecological observations on Mediterranean halophytes: Suaeda Forssk. ex Scop. genus. Lucr Șt (Horticultură), USAMV “Ion Ionescu de la Brad” Iași, 54(1), 23–28.
Google Scholar
Grigore, M. N., Boscaiu, M., & Vicente, O. (2011c). Assessment of the relevance of osmolyte biosynthesis for salt tolerance of halophytes under natural conditions. The European Journal of Plant Science and Biotechnology, 5(Special Issue 2), 12–19.
Google Scholar
Grigore, M.-N., Toma, C., Zamfirache, M.-M., & Ivănescu, L. (2012a). A survey of anatomical adaptationsin Romanian halophytes. Towards an ecological interpretation. Fresenius Environmental Bulletin, 21(11b), 3370–3375.
CAS Google Scholar
Grigore, M.-N., Toma, C., Boscaiu, M., Zamfirache, M.-M., & Ivănescu, L. (2012b). Anatomical and ecological observations on psammo-halophytes species (Eastern part of Spain). Lucr Șt (Horticultură), USAMV “Ion Ionescu de la Brad” Iași, 55(2), 19–24.
Google Scholar
Grigore, M.-N., Toma, C., Zamfirache, M.-M., Boscaiu, M., Olteanu, Z., & Cojocaru, D. (2012c). Ecological anatomy in halophytes with C4 photosynthesis: discussing adaptative features in endangered ecosystems. Carpathian Journal of Earth and Environmental Sciences, 7(2), 13–21.
Google Scholar
Grigore, M.-N., Toma, C., Zamfirache, M.-M., Ivănescu, L., & Daraban, I. (2013). Anatomical and ecological observations in succulent (articulated) halophytes from Chenopodiaceae. Lucr Șt (Horticultură), USAMV “Ion Ionescu de la Brad” Iași, 56(2), 19–24.
Google Scholar
Grigore, M.-N., Ivănescu, L., & Toma, C. (2014). Halophytes. An integrative anatomical study. Cham/Heidelberg/New York/Dordrecht/London: Springer.
Book Google Scholar
Haberlandt, G. (1914). Physiological plant anatomy. London: MacMillan.
Google Scholar
Harshberger, J. W. (1909). The comparative leaf structure of the strand plants of New Jersey. Proceedings of the American Philosophical Society, 48, 72–89.
Google Scholar
Henslow, G. (1895). The origin of plant-structures by self-adaptation to the environment. London: Kegan Paul, Trench, Trübner, & Co Ltd.
Google Scholar
Holtermann, C. (1907). Der Einfluss des K1imas auf den Bau der Pflanzengewebe. Leipzig: Verlag Von Wilhelm Engelmann.
Google Scholar
Hooker, J. D. (1891). Himalayan journals. London: Minerva Library edition.
Google Scholar
Ivan, M. A., Grigore M.-N., Zamfirache, M. M., & Toma, C. (2013). Histo-anatomical aspects referring to the vegetative organs on some halophytes from Romania. Lucr Şt (Horticultură), USAMV “Ion Ionescu de la Brad” Iaşi, 56(1), 25–30.
Google Scholar
Jaiswar, S., & Kazi, M. A. (2016). Composition and localization of mucilage under short term NaCl stress in Salicornia brachiata Roxb. and Suaeda maritima (L.) Dumort. Indian Journal of Natural Products and Resources, 7(2), 162–168.
CAS Google Scholar
Kanai, R., & Edwards, G. E. (1999). The biochemistry of C4 photosynthesis. In R. F. Sage & R. K. Monson (Eds.), C₄ plant biology (pp. 59–87). San Diego: Academic.
Google Scholar
Kearney, T. H. (1900). The plant covering of Ocracoke Island: a study in the ecology of the North Carolina strand vegetation. Contrib from U.S. National Herbarium, 5(5), 261–319.
Google Scholar
Kearney, T. H. (1901). Report on a botanical survey of the Dismal swamp region. Contrib from U.S. National Herbarium, (6), 321–585.
Google Scholar
Kherraze, M. E., Belhamra, M., & Grigore, M.-N. (2018). Aspects of ecological anatomy of Traganum nudatum Del. (Amaranthaceae) from the Northeast of the Algerian Sahara. Acta Biologica Szegediensis, 62(1), 25–36.
Article Google Scholar
Kuster, V. C., da Silva, L. C., Possatti, L., & Schneider, S. Z. (2018). Leaf morphology and anatomy of Jacquinia armillaris Jacq. (Primulaceae) from two coastal Restinga environments. Iheringia (serie Botanica), 73(3), 240–249.
Article Google Scholar
Lesage, P. (1890). Recherches expérimentales sur les modifications des feuilles chez les plantes maritimes. Revue Générale de Botanique, 2, 55–65;106–121;163–173.
Google Scholar
Liebau, O. (1914). Beiträge zur Anatomie und Morphologie der Mangrove-Pflanzen, insbesondere ihres Wurzelsystems. Beiträge zur Biologie der Pflanzen, 12, 181–213.
Google Scholar
Liu, Q., Luo, L., & Zheng, L. (2018). Lignins: Biosynthesis and biological functions in plants. International Journal of Molecular Sciences, 19, 1–16.
Google Scholar
Macnae, W. (1968). A general account of the fauna and flora of mangrove swamps and forests in the Indo-West-Pacific region. Advances in Marine Biology, 6, 73–270.
Article Google Scholar
Mangin, L. (1882). Sur le development des cellules spiralées. Bulletin de la Société Botanique de France, 29, 14–17.
Google Scholar
Martius, C. F. P., & Eichler, A. G. (1844). Flora Brasiliensis, vol. 3, part 3. Lipsiae: Monachii, apud Frid. Fleischer in Comm.
Google Scholar
Metcalfe, C. R., & Chalk, L. (1972). Anatomy of the dicotyledons (Vol. 2). Oxford: Clarendon.
Google Scholar
Meyer, J. (1905). Meyers Großes Konversations-Lexikon. Bd 8: Glashütte bis Hautflüger. Neuer Adbruck. Bibliographisches Institut: Leipzig und Wien.
Google Scholar
Monteil, P. (1906). Anatomie comparée de la feuille des Chénopodiacées, Thèse. Ecole Supérieure de Pharmacie, no. 9, Université de Paris.
Google Scholar
Moțiu, T., Toma, C., Tiron, A., & Niță, M. (1987). Contribuții la cunoașterea structurii organelor vegetative de Limonium gmelini (Willd). O. Ktze. Analele Științifice ale Univ “Al I Cuza” Iași, s. II a. (Biologie), 33, 11–14.
Google Scholar
Muhaidat, R., Sage, R. F., & Dengler, N. G. (2007). Diversity of Kranz anatomy and biochemistry in C₄ eudicots. American Journal of Botany, 94(3), 362–381.
Google Scholar
Paulsen, O. (1912). Studies on the vegetation of the Transcaspian lowlands. In The second Danish Pamir expedition (conducted by Olufsen O). Copenhagen: Gyldendalske Boghandel, Nordisk Forlag.
Google Scholar
Raunkier, C. (1907). Vegetationsbilleder fra dansk Vestindien; Krauses Lagune. Bot Tidsskr, 28, III-V.
Google Scholar
Robyns, W. (1971). Over viviparie en biotecnose bij planten. Meded Kon Vlaamse Acad Wetensch Lett Schone Küsten Belgie, 33, 3–14.
Google Scholar
Saenger, P. (2002). Mangrove ecology, silviculture and conservation. Dordrecht: Springer Science+Business Media.
Book Google Scholar
Safiallah, S., Seyed, M. M. H., Grigore, M.-N., & Jalili, S. (2017). Micromorphology and leaf ecological anatomy of Bassia halophyte species (Amaranthaceae) from Iran. Acta Biologica Szegediensis, 61(1), 85–93.
Google Scholar
Schimper, A. F. W. (1891). Die indo-malaysche Strandflora. Bot Mit Trop, 3, 1–204.
Google Scholar
Schimper, A. F. W. (1898). Rhizophoraceae. In A. Engler & K. Prantl (Eds.), Die natürlichen Pflanzenfamilien. Leipzig: Verlag von Wilhelm Engelmann. III(7–8):42–56.
Google Scholar
Schimper, A. F. W. (1903). Plant geography upon a physiological basis. Oxford: Clarendon.
Book Google Scholar
Schmidt, J. (1905). Bidrag til kundskab om skuddene hos den gamle verdens mangrovetraeer. Botanisk Tidsskrift, 26, 1–113.
Google Scholar
Schtscherback, J. (1910). Über die Salzausscheidung durch die Blätter von Statice gmelini (Vorläufige Mitteilung). Berichte der Deutschen Botanischen Gesellschaft, 28, 30–34.
Google Scholar
Shabala, S., Bose, J., & Hedrich, R. (2014). Salt bladders: do they matter? Trends in Plant Science, 19, 687–691.
Article CAS PubMed Google Scholar
Solereder, H. (1908). Systematic anatomy of the Dicotyledons. A handbook for laboratories of pure and applied Botany, vol 2. Oxford: Clarendon.
Google Scholar
Su, P. X., An, L. Z., Ma, R. J., & Liu, X. M. (2005). Kranz anatomy and C₄ photosynthetic characteristics of two desert plants, Haloxylon ammodendron and Calligonum mongolicum. Acta Phytoecol Sinica, 29(1), 1–7.
CAS Google Scholar
Sutherland, G. H., & Eastwood, A. (1916). The physiological anatomy of Spartina townsendii. Annals of Botany, 30, 333–351.
Article Google Scholar
Toma, C., Flenchea-Teodorescu, G., Rășcanu, S., & Zaharia, M. (1979). Trăsăturile anatomo-ecologice ale unor plante litorale (Cakile maritima Scop. și Eryngium maritium L.). Culegere de Stud. și artic. de Biologie, Univ. “Al.I.Cuza” Iași (Grăd. Bot.) (Lucrările simpozionului “120 de ani de la înființarea la Iași a primei grădini botanice din România”), 1, 273–287.
Google Scholar
van Tieghem, P. (1884). Traité de botanique. Paris: Librairie F, Savy.
Google Scholar
Volkens, G. (1887). Die Flora der aegyptisch-arabischen Wueste auf Grundlage anatomischphysiologischer Forschungen. Berlin: Gebrüder, Borntraeger.
Google Scholar
von Minden, M. (1899). Über die Aussonderung wässeriger Lösungen bei den Nicotiana-Arten und Glaux maritima. Die Bedeutung des Epithems bei der Sekretion, part V – Beiträge zur anatomischen und physiologischen Kenntnis Wasser-secernierender Organe. Bibliotheca Botanica, 46, 56–76.
Google Scholar
Waisel, Y. (1972). Biology of halophytes. New York/London: Academic.
Google Scholar
Walsh, G. E. (1974). Mangroves: A review. In R. J. Reimold & W. H. Queen (Eds.), Ecology of halophytes (pp. 51–174). New York/London: Academic.
Chapter Google Scholar
Walter, H., & Steiner, M. (1936). Die ökologie der Ost-Afrikanischen mangroven. Zeit für Bot, 30(3/4), 65–193.
Google Scholar
Warming, E. (1877). Om Rhizophora mangle L. Botaniska Notiser, 13–21.
Google Scholar
Warming, E. (1883). Tropische fragmente. II. Rhizophora mangle L. Botanische Jahrbücher fur Systematik, Pflanzengeschichte und Pflanzengeographie, 4, 519–548.
Google Scholar
Warming, E. (1891). Botaniske Exkursioner. 1. Fra Vesterhavskystens Marskegne. Vidensk Meddel Fra D naturh Foren Kjøben, 52, 206–239.
Google Scholar
Warming, E. (1897). Halophyt-studier. D Kgl Danske Vidensk Selsk. Skr, 6, Raekke, naturvidenskabeling og mathematisk Afd. VIII. 4, 173–272.
Google Scholar
Warming, E. (1906). Dansk Plantevaekst. 1. Strandvegetation. København og Kristiania: Gyldendalske Boghandel Nordisk Forlag.
Google Scholar
Warming E. (1909). Ecology of plants. An introduction to the study of plant communities (English edition prepared by P. Groom, I.B. Balfour). Oxford: Clarendon Press.
Google Scholar
Westermaier, M. (1881). Beiträge zur Kenntniss des mechanischen Gewebesystems. Monatsberichte der König Preuss Akad der Wissen Berlin, 61–78.
Google Scholar
Wille, N. (1882–1883). On stamens og bladets bygning hos Avicennia nitida L. Botanisk Tidsskrift, 13, 33–44.
Google Scholar
Yuan, F., Leng, B., & Wang, B. (2016). Progress in studying salt secretion from the salt glands in recretohalophytes: How do plants secrete salt? Frontiers in Plant Science, 7, 1–12.
Google Scholar

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Grigore, MN., Toma, C. (2021). Morphological and Anatomical Adaptations of Halophytes: A Review. In: Grigore, MN. (eds) Handbook of Halophytes. Springer, Cham. https://doi.org/10.1007/978-3-030-57635-6_37

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DOI: https://doi.org/10.1007/978-3-030-57635-6_37
Published: 19 May 2021
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Morphological and Anatomical Adaptations of Halophytes: A Review

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Morphological and Anatomical Adaptations of Halophytes: A Review

Integrative Anatomy of Halophytes from Mediterranean Climate

Integrative Anatomy of Halophytes from Mediterranean Climate

Keywords

1 Introduction: Halophytes as an Ecological Group of Plants

2 Review of General Morphological and Anatomical Adaptations of Halophytes

2.1 Succulence

2.2 Mucilage

2.3 Cell Sap

2.4 The Palisade Tissue

2.5 The Intercellular Spaces

2.6 Wax

2.7 Tomentum

2.8 Coriaceous and Glossy Leaves

2.9 Stomata

2.10 Tracheoidioblasts (Spiral Cells, Tracheids) and Mangrove Tracheids

2.11 Stereids (Spicular Cells, Sclereids, Idioblasts)

2.12 Lignification: The Special Case of Successive (Additional, Supernumerary) Cambia

2.13 Salt-Secreting Structures

2.13.1 Salt Glands of Plumbaginaceae

2.13.2 Salt Glands of Tamaricaceae

2.13.3 Salt Glands of Frankeniaceae

2.13.4 Salt Glands of Mangroves

2.13.5 Salt Glands of Halophytes from Primulaceae Family

2.13.6 Salt Glands of Halophytes from Poaceae (Gramineae)

2.13.7 Salt Hairs (Vezicular Hairs, Salt Bladders, Bladders) from Chenopodiaceae

2.13.8 Epidermal Bladder Cells from Aizoaceae (Mesembryanthemaceae)

2.13.9 Other Salt Glands (Cressa cretica, Ipomoea pes-caprae, and Lavatera arborea)

2.14 Kranz Anatomy Structures

2.15 Bulliform Cells

3 Morphological and Anatomical Adaptations of Halophytes from (Nontropical) Salt-Marsh Formations

4 Morphological and Anatomical Adaptations of Littoral (Tropical, Nontropical) Halophytes (Seashore Plants, Sea-Coastal Plants, Strand Plants, Psammohalophytes)

5 Mangroves (Tropical Coastal Halophytes, Littoral Swamp Forest, Tidal Forest)

6 Conclusions

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