1 Defining Halophytes: a Conceptual and Historical Approach in an Ecological Frame

Marius-Nicuşor Grigore* Alexandru Ioan Cuza University, Iaşi, Romania

Abstract Halophytes have certainly been recognized since the beginning of the 18th century, but subtle earlier allusions to salt-tolerant plants can be found back to 1500. By the time of the French Encyclopédie (1751–1765), and Goethe (1786), consistent data about halophytes had already been accumulated. Halophytes were brought to scientific attention through the classic and iconic papers of the German botanist Schimper, and especially those of the Danish plant ecologist Warming. However, their definitions remain controversial; the lack of a unique definition is related mainly to the complex features of this ecological group of plants. There are many definitions of halophytes, and some reflect the scientific background of the researchers who defined them. The ‘historical’ evolution of a definition can be delineated, and it especially reflects the progress of accumulating knowledge about halophyte biology. The definition of halophytes is thus manifold. The criteria and the historical context in which their definitions occurred and developed are discussed in detail in this chapter. Special attention is given to textual analysis that reveals the convergent approaches of researchers who used different languages. Ecological perspec- tives in defining halophytes suggest that, although they in fact represent a large ecological group of plants, their common xeromorphic nature must be universally recognized. Keywords: Ecology; Halophytes; Saline environments; Xerophytes

1.1 Historical and Semantic frame, with emphasis on the historical and lin- Evolution of Terms guistic evolution of basic terms. It is well known that the history of botany Many definitions of halophytes now exist. Halo- is a part of the history of science and reflects the phytes are so diverse from taxonomical and eco- cultural evolution of humanity (Von Sachs, logical points of view that there is no consensus 1890; Green, 1914; Arber, 1953; Isley, 1994; on a unique definition of the concept of ‘halo- Stevens, 1994; Grigore, 2016; Hardy and Tote- phyte’ (Grigore, 2008, 2012; Grigore et al., lin, 2016). Table 1.2 shows a list of terms, ex- 2010; Grigore and Toma, 2017). Several studies tracted from the languages most used in relation deal with this issue (Grigore et al., 2010, 2014; to halophyte semantics, with special attention Grigore, 2012) and in Table 1.1 new definitions to Latin, which was a rooting language for are mentioned and discussed in a conceptual French and Romanian. Latin was the universal

* Corresponding author e-mail: [email protected]

Table 1.1. A review of halophyte definitions (adapted from Grigore et al., 2010, 2014; Grigore, 2012).

Definition or descriptions related to halophytes References Comments

Plants of the seashore Willdenow First observations of halophytes were made (1805) of plants from seashore – regarded as the ‘absolute’ case of plants growing in saline environments. Later, plants from inland saline habitats were also recognized as halophytes; some botanists referred sometimes to ‘maritime’ and ‘terrestrial’ forms of the same species Plants that vegetate in saline soils Bischoff An ecological definition (1833) Saline plants are those found in maritime Balfour The ‘obligatory’ character of halophytes is situations, or near salt lakes, and which (1862) suggested seem to require much soda in their composition, and which have been called Halophytes Plants which inhabit salt marshes, and by Fowler An ecological definition burning yield barilla (1875) A plant containing a large quantity of Crozier Despite its earlier character, this definition is common salt in its composition, and (1892) interesting because it suggests the which thrives best in salty places capacity of halophytes to accumulate salt in large amounts. We now know that this is a group of halophytes accumulating salts, in contrast to those secreting it Salt-loving plants (are in the most of their Barnes Many plant ecologists consider halophytes characters, strikingly similar to the (1898) a particular case of xerophytes (see xerophytes) further comments in this table) Species of saline and alkaline soils Clements Saline and/or alkaline soils are terms more (salt plants) (1907) precise than other words designating saline environments A certain amount of soluble salts must be Warming How precise is the term ‘certain’? present before halophytic vegetation is called (1909) into existence Plants which grow where the water contains Bower In fact, the soil solution always contains salt; the effect upon them is seen in their (1911) ‘salt’; the issue is concentration. Not all fleshy habit halophytes display a fleshy tissue Strand plants, or Halophytes, living along Ganong We must discriminate that not all halophytes the margin of salt water, and therefore (1913) are strand plants; they can also appear in condensed and otherwise adapted to inland salt marshes/areas the difficult absorption thereof Halo-philous/phytes, plants of sea-coasts Willis Here we can notice the introduction of and salt-steppes, where the presence of (1919) ‘physiological drought’ hypothesis salt, by checking absorption, compels a characterizing saline soils. This is reduction of transpiration ‘famous’ for a certain period of plant ecology (see Grigore and Toma, 2010) Plants which at any stage of their life are Stocker The salt concept is an ambiguous one (see subjected to a concentration of salt, which (1928) the discussions above). It is difficult to is more than ‘normal’ glycophytic plants establish if the plants are exposed all the can bear without dying time to salt, at any stage of their life cycle Continued Defining halophytes – A conceptual approach 5

Table 1.1. Continued.

Definition or descriptions related to halophytes References Comments

Salt plants; Typical halophytes; true Braun- A good definition of obligate halophytes halophytes; absolute halophytes*; the Blanquet obligate halophytes are plants which for (1932) their normal development need certain ions of the alkali metals and halogens, and which, therefore, can exist and bear seed only in soils containing salt Plants that grow in saline soil or in salty McDougall An interesting definition stating that water are called halophytes and they (1941) halophytes are a peculiar case of are strikingly xeric xerophytes (for extensive comments, see Grigore and Toma, 2010) All plants that are capable of growing in Chapman Chapman’s comments: ‘its use [i.e. the an environment where there is more (1942) definition of ‘halophytes’] will not imply that than 0.5 per cent sodium chloride the species is either common or rare in such habitats nor will the term involve the assumption that a plant cannot grow under any other conditions’. Salinity is a very changeable ecological factor: choosing a number for drawing a line between two different plant groups could be hazardous Plants that can tolerate the concentrations Oosting of salts found in saline soils are termed (1948) halophytes Plants tolerant of various mineral salt in Lawrence the soil solution, usually sodium chloride (1951) Plants growing on salinized media Bucur et al. (1957) Plant that grow exclusively on salt soil Dansereau ‘Exclusively’ could also suggest that (1957) Dansereau was thinking only of euhalophytes Plants growing in saline soils Fernald (1950) Salt-tolerant plants Chapman Neither salt nor tolerant are well defined (1960) [..] the extremely saline soils which are Polunin A good definition of euhalophytes; however, inhabited only by specially adapted plants (1960) growing does not necessarily imply plant (halophytes); plants which habitually grow reproducing in very salty soils – halophytes, or at least can grow in such soils (facultative halophytes); Halophytes are plants which can tolerate a considerable degree of salinity Plants of salty or alkaline soils Correl and Johnston (1970) 1. Plants which grow and complete their life Waisel Very difficult to say precisely what ‘high salt cycle in habitats with a high salt content (1972) content’ represents. This remark of Waisel 2. Usually, the term is reserved only for suggests that the term be applied only to plants which appear in salty habitats euhalophytes (‘true halophytes’) constantly and specifically Continued 6 M.-N. Grigore

Table 1.1. Continued.

Definition or descriptions related to halophytes References Comments

Plants that can tolerate sea water, pure Duncan The sea water concentration is not a or diluted (1974) universal standard, so ‘pure’ or ‘diluted’ could be regarded as relative terms Plants of salty environments; plants adapted Flowers This is perhaps among the first to live in a saline environment, be it et al. physiological definition of halophytes seawater, a salt-water marsh, or a salt- (1986) desert. Plants found growing under naturally saline conditions; for terrestrial plants, this means a minimum salt concentration of about 100 mM in the soil solution. Plants adapted to complete their life cycles in salinities about that of seawater The term halophyte literally means salt Sharma and Perhaps referring also to the character of plants, but is used specifically for plants Gupta euhalophytes that can grow in the presence of high (1986) concentrations of Na salts Those species for which salt marsh is a Adam A good ecological definition major and, in many cases, only habitat. (1990) Plants that grow in saline conditions Ingrouille (1992) Plant species with a set of ecological and Gorham Some authors are aware of this physiological characteristics allowing growth (1995) arbitrariness and reproduction in a saline environment. [cited by Arbitrarily a salinity of 0.5% NaCl in soil Rozema, water should be tolerated by halophytic plants 1996] Halophytes are defined as those plants Breckle ‘Entire’ means inclusively producing seeds which grow and complete their entire life- (1995) to assur plant survival, colonization and cycle in saline habitats. Coping with salinity stabilization in any habitat needs adaptations on all levels from the A holistic definition autecological, the tissue and cellular level to subcellular and biochemical adaptations Plants that occur naturally on soils or in Dagar water too salty for the average plants are (1995) usually designated as halophytes [The growth] of halophytes is optimal at Marschner This is an example of an indirect definition relatively high levels of NaCl, a response (1995) of euhalophytes which can be explained only in part by the role of sodium as a mineral nutrient in these species Halophytes are adapted to survive in a Weber range of saline environments (1995) Halophyte species are those occurring Aronson and Also suggesting the ‘obligate’ character of in naturally saline conditions only Le Floc’h (some) halophytes (1996) The vegetation of saline habitats is Poljakkoff- Saline habitats are defined by these authors designated ‘halophytic’ Mayber as those whose soils contain a high and Lerner percentage of soluble salts, and one or (1999) more of these salt components is usually in excess Continued Defining halophytes – A conceptual approach 7

Table 1.1. Continued.

Definition or descriptions related to halophytes References Comments

Salt tolerant plants (halophytes, including Khan and A good holistic definition salt marsh and mangrove plants) are highly Duke evolved and specialized organisms with (2001) well-adapted morphological and physiological characteristics allowing them to proliferate in the soils possessing high salt concentrations Plants that can grow on soils with a high salt Fitter and content are termed halophytes Hay (2002) Plants that can survive in or benefit from Mooney and an environment with a high level of salt Canadell (i.e. sodium chloride), as in saline soils (2002) and seawater Halophytes are salt-resistant or salt-tolerant Ness (2003) plants that thrive and complete their life cycles in soils or waters containing high salt concentration Halophytes are able to adapt faster and to Schulze A deeper physiological definition tolerate extreme salinity et al. (2005) Plants that are able to grow on mildly to Ingrouille ‘Mildly’, ‘strongly’, ‘high levels’ are not strongly saline soils (halobiomes). and Eddie well-defined terms. However, these Halophytes which tolerate or endure high (2006) authors are among the only ones levels of salt are known as euhalophytes distinguishing between ‘halophytes and salt-tolerant plants’, a very subtle but pertinent remark in the context of our previous discussions on semantics Plants that survive to reproduce in Flowers and environments where the salt concentration Colmer is around 200 mM NaCl or more (2008) Halophytes grow naturally in very salty soils; Koyro et al. they still have not lost their resistance (2008) mechanisms to salt-stress conditions Plants of saline habitats Holzapfel (2009) Plants able to complete their life cycle on Koyro et al. saline substrates (2009) Plants that are tolerant of excess salt Quinn (2009)

*The term absolute halophytes was solely found in Braun-Blanquet (1932).

language for natural sciences from the time of 1.2 Halophytes: Starting ancient history, during the Middle Ages and to- to Define Them as an Ecological wards the beginning of the 19th century. In par- Group of Plants allel, however, some people started to use their national languages in scientific works from the Table 1.2 shows the earlier references to halo- 17th century. phytes in Latin language, which may be further 8 M.-N. Grigore

Table 1.2. Terms used in different languages in relation to halophytes – an historical overview.

Language Time period Terms and references Remarks

Latin 1700–1799 Plantae salsae (Leonhard, 1753; An interesting classification is given by Georgi, 1777) Oeder (1764): under salt (marine) water Herbae salsae (Henckel, 1722, ecosystem, he includes ‘marinae 1755) plantae’, which ‘nourish without roots, Marinae plantae (Oeder, 1764; being subjected to wave’s fluctuations’; Nemnich, 1798) he may be referring to algae or perhaps Plantae marinae Zostera species. Under ‘sea shore’, he (Boerhaave, 1724; includes ‘maritime (littoral) plants Brückmann, 1749; Khell, 1755) [littoraceae maritimae], which often taste salty, are succulent and they are found even in continental saline environments’. Note that Latin has two different terms related to plant succulence: ‘succulentae’ and ‘carnosae’ 1800–1899 Halophyta (Pallas, 1803) Latin was used almost exclusively as the Plantae salsae; plantae botanical language until the first decades salsuginosae (Bischoff, 1833) of the 19th century when it started to be abandoned, to be replaced by national languages French 1700–1799 Plantes marines (Prevost d’Exile, Sometimes, there is a substantial difference 1777); between plante marine and plante maritime Plantes maritimes (du Monceau, in the French language: for instance, Roux 1755; Macquer, 1756, 1778; (1765) refers to the first as organisms Roux, 1765; Rozier, 1781; that belong today to animals, while Miller, 1788) plantes maritimes are ‘plants that grow Plantes salines (de Haller, 1776; on seashore like the soude’ (a species de la Peyronie, 1793) that corresponds to Salsola species) 1800–1899 Halophytes (Meyen, 1840; Bortschof, 1859; Grisebach, 1875); Plantes salicoles (Gadaceau, 1881) 1900–Present Halophytes English 1700–1799 Marine plants (Short, 1746) Plants as love the sea-side (Tournefort, 1741) 1800–1899 Maritime plants (Willdenow, 1805) Halophytes (Balfour, 1862; Sullivan and O’Reilly, 1863; Grisebach, 1864; Hoblyn, 1865; Brown, 1874; von Hellwald, 1874) 1900–Present Halophytes; salt tolerant plants; salt plants; high salinity tolerant plants; salt loving plants; halophylous plants; halophytic plants; maritime plants (Grigore, 2012) Continued Defining halophytes – A conceptual approach 9

Table 1.2. Continued.

Language Time period Terms and references Remarks

German 1700–1799 Meere pflanzen (Willdenow, 1792) Salzpflanzen (von Lehman, 1791; Hochheimer, 1793) 1800–1899 Halophyten (Göbel,1838) 1900–Present Romanian 1800–1899 Plante halofile, Halofite (Grecescu, 1898) Specii litorale (Brândza, 1880) 1900–Present Halofite; plante de sărătură; plante halofile; plante iubitoare de săruri; plante de locuri sărate (Grigore, 2012) found in the specific etymology of several mod- The monumental French work, L’Ency- ern languages. Thus, plantae (herbae) salsae liter- clopédie (17 volumes, 1751–1765) contains many ally means salt(y) plants, and the ecological references about or related to halophytes as a affinity of this group is clearly correlated with salt resource. Thus, the contributor Jaucourt saline environments. This is because the refer- dealt with the terms Salicornia, Statice, Kali and ences to halophytes were to plants that grow in soude (sel de soude) (1765); and Venel with sel locis salsuginosis (salty habitats), a description marin (sea salt) (1765). Soude is defined as ‘the of habitats largely widespread in the 18–19th ash of many plants that contain marine salt and centuries. Many salt plants (plantae salsae, as which grow mostly on seashores – despite some they are called) also taste salty, and this purely of them are also found in the interior (salt- sensorial observation is of great importance in marshes)’ (Jaucourt, 1765). This is a good impli- the 18th century, since it is also related to succu- cit definition of halophytes. The French language lence and maritime habitats. This simple but uses the term soude for the ash of halophytes and striking finding most likely led to major research for species of the actual genus Salsola. The fact in the chemistry of salt – typical in the context that halophytes can also grow in inland saline of the increasing modernity of chemical and environments is also a good observation from an mineral sciences from the Age of Enlightenment ecological point of view and for the French lan- (Hutchings, 1969; Conlon, 1991). Halophytes guage, which also used the term plantes mari- were recognized from that time as natural re- times for halophytes. Detailed information about sources of salt – soda (English), sel de soude (soude) the tradition of extracting this soude is also (French). An extensive literature is dedicated to given, particularly in two iconic works from that this issue, and especially to the tradition and period: de Jussieu (1717) and Henckel (1760). practice of obtaining salts to be used in manu- The French author de Jussieu gave an account of facturing, especially that of glass. However, most a halophyte species, Kali d’Alicante, which is likely, saline environments were recognized much most likely a species of Salsola (kali). He offers earlier than the plants living on them. This is a much accurate information about this species simple but important aspect, because it can ex- (having ‘cylindrical and succulent leaves’) in re- plain how a particular type of habitat was delin- spect of the extraction of salt and its use; and, eated in relation to a dominant (ecological) finally, he concludes that ‘the history of other factor such as the salt. For instance, early foreign species that provide these types of salt, the par- travellers in the Romanian Principalities men- ticular and physical observation of each species tioned salty environments within their observa- of Salsola [soude, in the original French] … are so tions: Paul de Alep (1637–1667) referred to extended, that they would offer material for an- sară tură (salty area) and noticed that all the surface other work’ (de Jussieu, 1717: p. 78). area of this land (‘this land’ refers to Ocnele Mari) Henckel (1760) elaborated a massive treatise is salty (Alexandrescu-Dersca Bulgaru, 1976). on mineralogy (Pyritologia, 1725; 1755, German 10 M.-N. Grigore

editions) and a curious, interesting work – Flora taxonomic purposes, but also from an ecological Saturnizans (1722). The 1760 French edition of perspective. Since the use of terms derived from the latter includes an explanation of this title, halophyta had not been recorded in any modern ‘where the author shows the alliance between languages before his work, we may consider that plants and minerals’, and he added two long it was a starting point for creating halophyta- chapters to its supplement. These chapters are derived terms in French (halophytes), English (halo- very well documented: ‘Historical description phytes), German (halophyten), Romanian (halofite) and chemical analysis of Kali geniculatum and and Danish (halofyt). However, the Greek etymol- Chemical analysis of Kali geniculatum’. These ogy is clear and logical and we cannot exclude chapters may be regarded as genuine parts of a the possibility that it will have been foreseen by modern treatise on plant biochemistry, and par- botanists before 1800. Pallas’s contribution has ticularly on the ‘mineral nutrition’ of halophytes. been extensively discussed and commented on The French contributor Venel (1765), who (Schrader, 1810) and, in this context, some au- was responsible for the sel marin (marine salt) thors refined the definition of halophyta. Schrad- entry in the Encyclopédie, underlines the point er (1810) said in a footnote ‘better to nominate that plants from seashores represent a natural this family as Halophyta, where to include all the resource for salt: ‘some plants contain perfect (pure) plants that love the salt or soda’. marine salt, while others, potassium’. Finally, a sim- Before using actual names (derived from ple circuit of marine salt is recognized. Salt passes halophyta – as described by Pallas or elsewhere), through plants that are nourished by it and, with other relevant terms have been used in different their decomposition, salt moves through the soil. languages (Table 1.2); most suggest the influ- However, we found a much earlier record, ence of maritime (marine) salt on plants and, most likely in a relation to a salt plant, in a Latin consequently, on their origin. As already under- translation of the medical works of the famous lined, even from the time of the French Ency- Persian Muhammad al-Rāzı ̄ (Rhazes, Rasis – clopédie, botanists realized that halophytes also Latinized names, 854–925), from 1500 (Rhazis grow in inland saline environments. et al., 1500). In a section of this translated work, Therefore, the origin of the first references Synonima Rafis, there is an entry on cali cinis cri- to halophytes and their subsequent refinements bellatus (filtered ash of c(k)ali) withherba salsa and extensions are of an ecological nature. This within its short explanation. observation is very important because it can Pallas’s iconic work from 1803 is an im- explain the logical evolution of concepts and the portant moment in the evolution of concepts associated fields of research to be conducted by related to halophytes. His contribution, Illustra- future botanists. Actually, this explains why tiones plantarum imperfect vel nondum cognitarum, many studies from the 19th century – especially cum centuria iconum. De halophytis, seu plantis conducted in the frame of German, Danish and apetalis kalicis generatim, is perhaps the first that French botany schools – emphasized the xero- introduces the term Halophyta. Despite his work morphic nature of many halophytes and its being written in Latin, Pallas preferred the Greek- close correlation with the action of salt water or based term Halophyta. His choice could have salt spray upon these plants. been motivated by the fact that he included Goethe made an interesting observation under this concept a distinct botanical family, in during his stay in Italy, in 1786. He later wrote: order to deal with these problematic species. He says that ‘[I] understand under this family species On the sea-coast I found also several plants gathered based on natural affinity: Salicornia, whose characters similar to others I already Anabasis, Salsola, Suaeda, Polycnemum, Cam- knew, enabled me to recognize pretty well their phorosma which correspond today to Chenopo- properties. They are all alike, fat and strong-full diaceae (or Amaranthaceae)’. The indissoluble of sap and clammy,- and it is evident that the old relationship with the salinity factor is clearly de- salt of the sandy soil, but still more the saline atmosphere gives them these properties. Like lineated and underlined in the context of defin- aquatic plants they abound in sap and are fleshy ing halophytes: ‘plants that prefer salinity […], and tough like mountainous ones: those whose living in salty and maritime environments, which leaves shew a tendency to put forth prickles after are preferentially loved by these plants’. There- the manlier of thistles have them extremely fore, Pallas created the term Halophyta for these sharp and strong. striking halophytic chenopod species, mostly for (Goethe, 1885) Defining halophytes – A conceptual approach 11

Goethe thus recognized the xeromorphic the second seek drought and, consequently, super- nature of halophyte adaptations and clearly in- ficial soils. He also subdivided hygrophytes into dicated that salinity is responsible for character- péliques (growing on a clay soil), psammiques (pre- istics like succulence. ferring sandy soils) and pélopsammiques (species Poiret (1820) described plantes maritimes or growing in both clay and sandy environments). salines as plants that – without growing immersed Nevertheless, with respect to this point, we in salt water and without floating on its surface – can consider that the halophytes have been need to live near to salt water so they can absorb clearly defined as an ecological group of plants, the necessary amount in their nutrition. They, and plant ecologists such as Schimper and like Salicornia species, grow in salt marshes and Warming have consequently refined this vision seem to absorb saline compounds through their in terms of the adopted physiological drought roots and leaves. Others, like Eryngium campestre, concept (see Grigore and Toma, 2011). do not require (need) salt water but live on sea- This is the moment when halophytes – shore like others because they are robust enough based on their anatomical and morphological to withstand the action of salt water. Poiret clearly features and characteristics of saline environ- suggested that some halophytic species are ‘ob- ments – started to be considered as a (special) ligatory’; he foresaw that these kinds of species type of xerophyte. uptake salt water and it is necessary for their Schimper (1898, 1903) emphasized that, growth, while others are ‘accidental’: they do not apart from the structural features of halophytes need salt, but simply resist its action. or xerophytes, environmental characteristics (especially of the water and soil) are also of great importance for establishing the nature of adaptations 1.3 Halophytes and Physiological in plants. A distinction should, therefore, be made Drought in Soil between physical and physiological dryness and between physical and physiological moistness. Halophytes have been perceived as a heteroge- He pointed out that only the physiological charac- neous ecological group of plants, and are recog- teristics need to be considered in plant life and in nized and discussed as such today (Grigore, geographical botany. Hygrophilous vegetation 2008, 2012; Grigore and Toma, 2010, 2011, corresponds to physiological moistness, and xero- 2017). The works of Battandier (1887) and phylous vegetation to physiological dryness. Contejean (1855, 1874), Brick (1888 and refer- Schimper (1903) concluded that physio- ences therein) demonstrate that this ecological logical drought is caused by external factors that vision of halophytes will have been delineating either reduce water uptake or favour transpir- within plants, especially those growing on the ation; frequently, there is a combination of these seashore. However, under the great influence of influences (Grigore and Toma, 2011, 2017; Thurmann’s work (1849) on the dispersion of Grigore et al., 2014). Among the factors that re- plants under the influence of adjacent rocks, duce water uptake, an abundance of soluble many botanists felt that – in relation to maritime salts in the soil must be mentioned for the halo- flora – an ecological approach is logically needed phytes. As Schimper shows, a small quantity of in order to consider also the chemical nature of salt favours absorption, while a large quantity the soil with respect to halophyte distribution. impedes it. The degree of concentration at which Thus, Contejean (1874) first distinguished be- the retardation commences varies with the spe- tween flore maritime (terrestrial species that grow cies of plant, but rarely exceeds 0.5%. Mixtures in free-air spaces and shores) and flore marine of salts impede absorption more than pure salts, (species that grow exclusively immersed under and certain types (for example NaCl) act more saline waters – mostly the case of algae). He then energetically than others. emphasized that all halophytes contain consist- The most important natural regions and ent amounts of sodic salts and their existence is habitats where physiological dryness prevails closely related to the presence of NaCl in the in- and only xerophytes therefore thrive are grouped terior of continents, next to the sea and around according to their physical characters: salty efflorescences and saline sources. Further, he realized that within halophytes (maritime flora) 1. Deserts, steppes, and other districts with a dry the hygrophytes and xerophytes must be recog- substratum and dry air, occasional or persistent nized. The first seek humidity and deep soils and great heat, and intense illumination [Fig. 1.1]; 12 M.-N. Grigore

Fig. 1.1. Zygophyllum cornutum; xerophilous structure; hot, dry, desert climate (Engler, 1896).

2. The bark of trees, rocks where there is rapid as a distinct ecological group (in relation to xero- drying up of the substratum, owing to deficient phytes and hydrophytes) can be questioned (Kear- depth [Fig. 1.2]; ney, 1904). Kearney (1904) believed that even 3. Sandy soil, gravel, and the like, on account of halophytes should be regarded as a subdivision the rapid drying up of the substratum owing to of xerophytes (referring especially to succulence, its great permeability; Kearney considered that, in halophytes, this fea- 4. Sea-shores, solfataras, which have an abundance of soluble salts in the soil [Fig. 1.3]; ture is of a xerophytic nature). He stated that, 5. Peat-bogs, because of the humic acids in the soil; in using the term ‘halophyte’, it should not be 6. Polar zones, vicinity of glaciers in high forgotten that halophytes do not constitute an mountains, where the temperature of the soil ecological class coordinated with hydrophytes is low; and xerophytes, but are properly only a subdiv- 7. Alpine highlands, which are under rarefied ision of the xerophytes. Like other xerophytes, air and strong insolation characteristic of the they are generally characterized by having vari- alpine climate. ous adaptations for reducing transpiration, as (Schimper, 1903) promoters of physiological drought (Warming All these types of habitats have been mentioned 1895, 1897; Schimper, 1903) have pointed out. to better understand how one common factor Kearney (1904) underlined that halophytes are (physiological drought) found in various envir- xerophytes owing to their need for a reduction in onments can induce similar xeromorphic traits transpiration largely owing to the presence in in plants growing in habitats that seem to be so the soil of an excessive amount of readily soluble different (Grigore et al., 2014). Based on these salts. Despite Kearney believing that the charac- details, together with some experiments aimed ter of the soil is the final criterion governing to show plant behaviour in saline conditions, whether the vegetation should be called halo- Schimper concluded that the morphological phytic or non-halophytic, halophytes and xero- characteristics of halophytes are consistent with phytes may actually occupy similar habitats. those of xerophytes. According to Kearney (1904), no ecological char- Therefore, it would be correct to consider acters can be cited as exclusively halophytic, al- a halophyte to be a special form of xerophyte though halophytes seem to show a more marked (Wiesner, 1889; Warming, 1909; Grigore and tendency than other xerophytes towards develop- Toma, 2010, 2011). This statement is sup- ment of water-storage tissue. The well-marked ported both by analysis of habitat characteristics succulence in halophytes has been discussed in (physiological drought-affected), and especially detail in their ecological context (Grigore, 2008; by histo-anatomical features of halophytes. In Grigore et al., 2014; Grigore and Toma, 2017). In this context, it seems that considering halophytes halophytes, the xerophytic habit is often developed Defining halophytes – A conceptual approach 13

Fig. 1.2. Xerophilous structure – dry substratum of tree bark and rocks. Octomeria ssp. (left) and Cattleya bicolor (right) (Schimper, 1903). to an extreme; this may be explained by the fact that, in saline environments, a combination of stressing factors occur, and drought and high salinity in the soil are synergic factors that induce Fig. 1.3. Batis maritima; xerophilous structure; wet, the xeromorphic character of anatomical adapta- saline soil of tropical shores. Plant with succulent tions in halophytes. leaves (Dammer, 1893). Henslow (1895), in his important work on plant adaptations to living environments, also matter in maritime regions and salt marshes, the stressed the similarities between the anatomical presence of salts is to some extent responsible for characteristics of halophytes and xerophytes. succulence in many halophytes. Particularly taking into account plant succu- This concept of physiological dryness lence and pubescence, he concluded that there (drought) was further adopted by several re- are certain peculiarities in common between searchers who studied plant ecology. McDougall desert plants and alpine and sub-alpine species. (1941) described halophytes as ‘plants of habi- Henslow (1895) believed that resemblances in tats that are physiologically dry’. Plants that plants from widely different localities such as grow in saline soil or in salty water are called seashores, alpine regions and desert areas can halophytes, and they are strikingly xeric. Per- be explained by the fact that certain elements in haps the most characteristic feature of halo- the environments are found to excess. Through phytes as a group is their succulence, which is the simplest deduction, he stated that these accompanied by very high osmotic pressure. elements act upon the plants, and they respond Oosting (1948) defined halophytes as plants accordingly, so that much the same results occur. that can tolerate the concentrations of salts For instance, the succulence of desert plants, es- found in saline soils. If not actually dry, these sa- pecially where the soil is saline, arises from iden- line habitats may be termed ‘physiologically dry’ tically the same cause as that of plants from because of the high concentrations of salts, seashores. He concluded correctly that, since the which limit osmotic activity and, consequently, moisture of the air and soil is charged with saline absorption of water by ordinary plants. 14 M.-N. Grigore

The introduction and operational use of available to the plant only to a slight extent). physiological drought complicated the ecological This class is, therefore, composed of xerophilous classification of plants, and especially of halo- species. Next to the halophytes he placed oxylo- phytes, to some extent (Warming, 1895, 1909), phytes (formations on acid soil) and psychro- Schimper (1898, 1903) and Clements (1920). phytes (formations on cold soil). A typical example relates to the iconic works The soil can be also physically dry, and its of the Danish pioneer of plant ecology, Warming, slight power of retaining water determines the who in 1895 published a book on plant ecology vegetation, the climate being of secondary im- in Danish. This was subsequently translated into port; the formations are therefore likewise other languages: German (1896, 1902, 1914) xerophilous. and English (1909). These translations are also It can be seen, as emphasized in the para- revised editions of the original book. This is a graphs above, that in contrast to previous edi- very important point, because the evolution of tions of Warming’s work, halophytes are not still ecological classifications of plants can be ob- treated as a principal group of the plant in the served during the period. The ‘volatile’ position English translation (1909). This distinction in of halophytes is also noticeable within these edi- plant classification into ecological groups was tions. Thus, until the 1909 English edition, the motivated explicitly by Warming, in the fore- classification system in ecological classes (verein- word to the English edition (1909), having taken sklasse, formationklasse in German; (o)ecological into account the soil and climatic differences in- class or classes in English – terms used here to volved in shaping plant adaptations. mean an ecological group of plants – contained Clements (1907) included halophytes in the following plant communities: hydrophytes, the category of xerophytes growing in condi- xerophytes, halophytes and mesophytes. Schim- tions where the chresard is low, the soil is physic- per (1903) divided the plants into terrestrial and ally or physiologically dry, the climate is usually aquatic, with terrestrial plants including xero- dry or variable and transpiration is low. Halo- phytes, hygrophytes and tropophytes. phytes grow in environments where the chre- In the English (and comprehensively re- sard is low because of an excess of soil salts. vised) edition, Warming (1909) emphasized the role of physiological drought when choosing the place of halophytes within the xerophyte group. 1.4 Conclusion The soil is physiologically dry when it contains a considerable amount of water which, neverthe- Semantic analysis of the works consulted re- less, is available to the plant only to a slight vealed the natural etymology of terms related to extent or can be absorbed only with difficulty, halophytes. Many of the associated terms have either because the soil holds firmly to a large origins in Latin and Greek. Halophytes have been quantity of water or because the osmotic force correctly defined and described as an ecological of the root is inadequate to overcome that of the group of plants since the early years of their concentrated salt solution in the soil. This may formal study. The specific characteristic of saline be the case when: environments – those affected by physiological 1. The soil is rich in free humic acids, or in drought – was a fair criterion for considering chemical bodies that by their peculiar action on halophytes as a special set of xerophytes. Further the plant evoke xerophily; there result those for- investigation and critical analysis of literature mations that grow on acid soil; will contribute to identifying new criteria for the 2. The soil is rich in soluble salts, usually com- definition (and especially the classification) of mon salt, which brings into existence the form halophytes; biochemical and molecular investi- of xerophily we see in halophilous formations. gations should clarify if there is the possibility of Consequently, a halophyte is, in fact, a special clustering them according to their ability to syn- form of xerophyte. thesize and accumulate specific biochemical compounds in relation to soil salinity. In parallel, Based on these considerations, Warming literature surveys and textual analysis are ex- (1909) included halophytes in the class subor- pected to bring new and challenging data about dinated to formations where the soil is physiolo- cultural and historical implications of salt from gically dry (the soil contains water which is an ecological perspective. Defining halophytes – A conceptual approach 15

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