2001/08/01 by A. J. Davy, A. J. Davy, G. F. Bishop +3 · 9 citations
Agricultural and Biological Sciences · Biochemistry, Genetics and Molecular Biology · #Mediterranean and Iberian flora and fauna #Plant Pathogens and Fungal Diseases #Mycorrhizal Fungi and Plant Interactions
paper · pdf · doi:10.1046/j.0022-0477.2001.00607.x
Salicornia L. (Chenopodiaceae) is a genus of annual, apparently leafless halophytic herbs that have articulated, succulent stems. A combination of inbreeding, which allows the development of locally differentiated populations, and considerable phenotypic plasticity has created great taxonomic complexity. Taxonomic difficulties have been compounded by very reduced morphology and the inadequacy of dried material in representing a succulent growth form. Although numerous species aggregates, species and microspecies have been described over the last 250 years in attempts to represent the observed variation, there is still no satisfactory taxonomic treatment and it is frequently impossible to assign published information specifically to taxa within Salicornia. Recent commentaries, with different perspectives on the taxonomic problems, are provided by Dalby (1989), Ingrouille (1989) and Rose (1989). This account reviews material referable to all of the taxa recognized provisionally by Stace (1997): Salicornia pusilla J. Woods, S. europaea L. agg. (S. ramosissima J. Woods, S. europaea L. and S. obscura P.W. Ball & Tutin) and S. procumbens Smith agg. (S. nitens P.W. Ball & Tutin, S. fragilis P.W. Ball & Tutin and S. dolichostachya Moss). It is possible that only three species (S. pusilla, S. europaea agg. and S. procumbens agg.) should be recognized (Stace 1997), corresponding with the Sections Pusillae, Salicornia & Dolichostachyae of Scott (1977). We also include relevant information for closely related putative species within the same complex world-wide. In Salicornia, the main stem and its opposite branches are composed of short, cylindrical or clavate internodes, each with a succulent, photosynthetic covering, conferring the articulated appearance. The root system tends to be superficial, often penetrating less than 10–20 cm into the sediment; the main root axis produces few branches in small individuals but larger plants develop several highly branched, woody main roots that originate from near the base of the stem. A pair of opposite, connate, highly reduced leaves constitute no more than a rim at each stem node. At the lower internodes the succulent covering may atrophy, leaving the base of the stem and some branches narrow, wiry and with ridge-like nodes. The arrangement of lateral branches is regularly decussate and in large plants may be of the 4th order; the uppermost primary branches make an angle usually less than 45° with the main stem and may be straight or curved upwards. At maturity, every branch terminates in a fleshy spike of contiguous, fertile segments; segments have convex or more or less cylindrical sides and each bears an opposite pair of (1–) 3-flowered cymes. The spike, with its decussately arranged dichasial cymes, may be distinctly tapered; it may be tinged red at maturity. The number of fertile segments per spike is variable but shows discontinuities, sometimes associated with species, resulting in modes of 2–4 (–12) or 3–12 (–22) or (4–) 6–30 fertile segments per spike. Each cyme consists of a central flower and (usually) two lateral flowers, deeply embedded in fleshy tissue at the proximal end of a segment and subtended by a rim-like upgrowth (which may have a scarious edge) of the segment below. Within a cyme, the florets are usually arranged in a triangle with the central one distinctly distal; the laterals may be either smaller than the central floret or almost as large. The 3 (–4) minute lobes of the perianth are connate almost to their apex, usually forming a tri-radiate slit through which the stigmas and anthers or pollen may emerge; they become hard or spongy in fruit. Each flower has 1 (anterior) –2, rarely 0, stamens. The anther length may be 0.6–1 mm (with dehiscence after exsertion) or 0.2–0.5 mm (with dehiscence before exsertion or when not exserted). Styles 2 or style bifid bearing in all 3 plumose stigmatic lobes c. 0.5–0.7 mm in length, or exceeding 1 mm in some tetraploids. The deeply embedded ovary is unilocular with a solitary basal ovule. The ovoid, flattened seed has a horse-shoe shaped embryo enclosed by a thin, membranous testa bearing hooked hairs (few or numerous, long or short, sometimes mucilaginous) or is sometimes glabrous. Seed mass 0.2–0.8 mg (see VIII C). Putative British species have been characterized as follows: S. pusilla (one-flowered glasswort). Mostly erect to 25 cm, simple to much branched and bushy. Branches more or less straight. Yellowish-green, becoming brownish or pinkish-yellow, often with pink tips to the branches. Terminal spike short, up to c. 6 mm, with only 2–4 fertile segments. Lower fertile segments 1–1.5 mm long and 1–1.5 mm wide at the narrowest point. Cymes one-flowered. Flowers almost circular with a single stamen. Fertile segments disarticulating shortly before the seeds are ripe. S. europaea (common glasswort). Erect to 35 cm, fairly richly branched. Lowest branches may be nearly as long as the main stem. Dark green becoming yellow-green and ultimately flushed pink or red. Terminal spike 10–50 (–60) mm. Fertile segments with distinctly convex sides, the lower ones 2.5–4 mm long and 3–4.5 mm wide at the narrowest point. Central flower distinctly larger than the two laterals. S. obscura (glaucous glasswort). (Perhaps a variant of S. europaea). Usually erect to 40 cm, typically with primary branches only; branches curving upward distally; lowest branches not more than half as long as the main stem. Dull glaucous green with a matt surface becoming dull yellow. Segments with an inconspicuous scarious border up to 0.1 mm wide. Terminal spike 10–40 (–45) mm, and lower fertile segments 2.5–4.5 mm long and 2.8–4 (–5) mm wide at the narrowest point, similar to S. europaea. S. ramosissima (purple glasswort). (Perhaps a variant of S. europaea). Erect or prostrate, to 40 cm, simple to much branched. Segments with a conspicuous, broad, scarious border c. 0.2 mm wide. Dark green becoming deep purplish-red. Branches more or less straight. Terminal spike (5–) 10–30 (–40) mm and lower fertile segments 1.9–3.5 mm long and 2–4 mm wide at the narrowest point. Central flower rounded-rhombic to almost circular. S. nitens (shining glasswort). Typically erect to 25 cm with primary branches only. Plant smooth, shining, somewhat translucent, green or yellowish green becoming light brownish purple/orange. Sterile segments conspicuously swollen near the top. Terminal spike 12–40 mm with lower fertile segments (1.8–) 2–3 (–3.5) mm long and 1.8–3.5 mm wide at the narrowest point. S. fragilis (yellow glasswort). Erect to 40 cm, usually primary branches only, the lowest normally less than one quarter the length of the main stem. Dull green becoming dull yellowish-green. Terminal spike (15–) 25–80 (–100) mm, distinctly tapering. Lower fertile segments more or less cylindrical, 3–5 mm long and 3–6 mm wide. S. dolichostachya (long-spiked glasswort). Erect to procumbent, 10–45 cm. Much branched and bushy, the lowest branches about as long as the main stem. Dark green becoming paler or dull yellow/brownish. Terminal spike (25–) 50–100 (–200) mm, distinctly tapering. Lower fertile segments more or less cylindrical, 3–6 mm long and 3–6 mm wide. Patterns of variation suggest that individuals exist as members of local, perhaps unique, inbreeding populations and characterization of the populations is more tractable than that of individuals. World-wide there are c. 13 species (Scott 1977) with innumerable variants. Variation within and between taxa is expressed in morphology, chromosome number, life-history characteristics, enzyme electrotypes and DNA polymorphisms. Numerical analysis of morphological variation in the field failed to support a distinction between the diploid species S. europaea and S. ramosissima (Ingrouille & Pearson 1987), although Jefferies & Gottlieb (1982) had found consistent differences at loci coding for six enzymes. Morphological variation in tetraploids of the S. dolichostachya group provided evidence for at least two taxa, one of which correlated with S. fragilis (Ingrouille et al. 1990). Wolff & Jefferies (1987a) used a combination of cytological, electrophoretic and morphometric characters to distinguish three groups of populations from Hudson Bay, the Atlantic coast and James Bay of North America. Transplant experiments between upper and lower levels of a salt marsh in north Norfolk, England, indicated genetically fixed differences in growth phenology between local populations (Jefferies et al. 1981). Subsequently, a detailed demographic analysis of reciprocal transplant experiments has shown clear losses of fitness in populations transplanted away from their local, indigenous microhabitats on the marsh and clear selection against alien populations at transplant sites (Davy & Smith 1985, 1988; Smith 1985). Analysis of ribosomal DNA polymorphism (RFLP) has confirmed the existence of genetically distinct forms but their distribution was correlated with elevation in the marsh tidal frame rather than with morphological characteristics (Davy et al. 1990; Noble 1990; Noble et al. 1992). Luque et al. (1995) have detected DNA polymorphism between three Spanish populations of Salicornia using a RAPD technique. Succulent plants of mainly moist, saline habitats, particularly coastal salt marshes; they also grow in inland saline areas. The composite distribution of all taxa of Salicornia in Britain (Fig. 1) faithfully reflects the availability of salt-marsh habitats around the whole coastline. Salicornia is largely absent from British inland salt marshes, despite apparently suitable habitats (Lee 1977), but it occurs in at least one, at Northwich, Cheshire. Some records are not assigned to individual species, or even species aggregates, and so the constituent taxa are more or less under-recorded. The S. europaea agg. is the most widely distributed form (Fig. 2a); S. europaea and S. ramosissima both occupy most of its range, whereas records of S. obscura are confined to a few locations, mainly in East Anglia and on the Bristol Channel (Fig. 2b–d). The tetraploid S. procumbens agg. (Fig. 3a) is apparently less abundant than S. europaea agg., especially in Scotland, Ireland and south-west England, although it is undoubtedly under-recorded; the reasonably distinctive S. dolichostachya (Fig. 3b) is the most widely recorded of its constituent taxa and S. fragilis (Fig. 3c) also occurs around much of the English and Irish coasts, whereas S. nitens (Fig. 3d) appears to be very sparsely distributed on a latitudinal range from the Isle of Wight to Orkney. The highly distinctive S. pusilla, with its single-flowered cymes, is confined to coastal marshes in the south and east of Britain, from the Humber around to S. Wales and the southern coast of Ireland (Fig. 4). The composite distribution of all taxa of the genus Salicornia in the British Isles. (O) Pre-1950; (●) 1950 onwards. Each dot represents at least one record in a 10-km square of the National Grid. Mapped by Mrs J. M. Croft, Centre for Ecology and Hydrology, using Dr A. Morton’s DMAP programme, mainly from records collected by members of the Botanical Society of the British Isles. The distribution of Salicornia europaea agg. in the British Isles. (O) Pre-1950; (●) 1950 onwards. Each dot represents at least one record in a 10-km square of the National Grid. Mapped by Mrs J. M. Croft (see Fig. 1). (a) S. europaea agg., (b) S. europaea, (c) S. ramosissima, and (d) S. obscura. The distribution of Salicornia procumbens agg. in the British Isles. (O) Pre-1950; (●) 1950 onwards. Each dot represents at least one record in a 10-km square of the National Grid. Mapped by Mrs J. M. Croft (see Fig. 1). (a) S. procumbens agg., (b) S. dolichostachya, (c) S. fragilis, and (d) S. nitens. The distribution of Salicornia pusilla. in the British Isles. (O) Pre-1950; (●) 1950 onwards. Each dot represents at least one record in a 10-km square of the National Grid. Mapped by Mrs J. M. Croft (see Fig. 1). Salicornia is found around much of the coastline of Europe from the Arctic to the Mediterranean, as well as on the shores of both the Black Sea and Caspian Sea; it is also present sporadically where inland salines occur across Europe (Atl. Fl. Eur.; Fig. 5). Much of this distribution can be tentatively attributed to the S. europaea agg. (Fig. 6). Members of the S. procumbens group are recorded from the coasts of the Beloye More inlet of the Barents Sea, the North Sea, the English Channel, the Atlantic coasts of France and Portugal, and the Mediterranean coast of France (Fig. 7). Outside Britain, S. pusilla occurs only on the northern and western coasts of France (Fig. 8). The distribution of the genus Salicornia in Europe. Each dot (●) represents at least one record in a 50-km square. (+) extinct; ( × ) probably extinct. Reproduced from Atl. Fl. Eur., vol. 5 by permission of the Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo. The distribution of Salicornia europaea agg. in Europe. Each dot (●) represents at least one record in a 50-km square. (+) extinct; ( × ) probably extinct. Reproduced from Atl. Fl. Eur., vol. 5 by permission of the Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo. The distribution of Salicornia procumbens agg. in Europe. Each dot represents at least one record in a 50-km square. (●) S. dolichostachya, S. fragilis and S. nitens; (▴) S. veneta. Reproduced from Atl. Fl. Eur., vol. 5 by permission of the Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo. The distribution of Salicornia pusilla in Europe. Each dot (●) represents at least one record in a 50-km square. Reproduced from Atl. Fl. Eur., vol. 5 by permission of the Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo. From Europe and the North African coast, the distribution of Salicornia extends through the near East and Caucasus and central Asia, including much of The Russian Federation, where it forms enormous thickets on solonchaks in steppes and deserts (Fl. URSS 6); it is found again at the coast near Vladivostok, around Sakhalin, and on the Japanese islands of Hokkaido, Honshu and Shikoku (Vergl. Chor.; Hultén 1970). Recently Salicornia has been discovered in Saudi Arabia, in salt marshes on the Arabian Gulf coast and in the sabkha of Al-Aushaziya, some 400 km from the coast (Al-Turki 1992, 1997). Three (Tolkën 1967) or four (O’Callaghan 1992) species of Salicornia occur around the coast of southern Africa (Tanzania, Madagascar, Mozambique and South Africa). One of these, S. uniflora Tolkën, is analogous with S. pusilla in having single-flowered cymes (Tolkën 1967). S. europaea (s.l.) is distributed along the Atlantic coast of N. America and the St. Lawrence seaway. Plants from populations in this complex in arctic coastal marshes around Hudson Bay have been distinguished as S. borealis Wolff & Jefferies and S. maritima Wolff & Jefferies (Wolff & Jefferies 1987b). The form widely distributed in the prairies and salt flats of western North America is generally referred to S. europaea ssp. rubra (Nelson) Breitung. Salicornia (s.s.) is absent from Australia, although there are perennial members of the tribe Salicornieae in five other genera (Wilson 1980). Similarly, it is absent from South America, as all species referred to Salicornia there are perennial (i.e., strictly Sarcocornia or Arthrocnemum) (Costa & Davy 1992). The altitude of the vast majority of British Salicornia populations is below the level of the highest tides. The inland site at Northwich, Cheshire is at 10 m. However, populations in the sabkha of Al-Aushaziya, Saudi Arabia, are at 650 m and S. rubra in Montana, USA reaches 1277 m. Salicornia has very wide climatic tolerances: subarctic to subtropical and oceanic to continental. Its tolerance of water stress (see VII E) and its annual life history presumably contribute to its ability to survive extreme conditions in adverse seasons. The northern limit of Salicornia corresponds with the 10 °C July isotherm; populations at this range limit are virtually confined to low, south-facing slopes, where temperatures may be as much as 7 °C higher than the north-facing aspect (Jefferies et al. 1983). It is generally limited to unshaded sites with relatively high daily radiant energy availability during the growing season. Individual populations and taxa of Salicornia may be very sensitive to elevational variations associated with microtopography on the gradient from land to sea of tidal salt marshes. Populations low in the tidal frame need to be more tolerant of prolonged submergence, tidal scour and waterlogging, whereas those at high elevations may experience hypersalinity in summer (Jefferies et al. 1979). In Norfolk, England, S. dolichostachya is among the vascular plants that occurs lowest in the tidal frame, where it experiences more than 600 tidal submergences per annum (Smith 1985; Davy & Smith 1988). Rozema, van der List et al. (1987) record it occurring mainly below the mean High Water Level in the Netherlands. Salicornia europaea in Norfolk is characteristic of large areas of low marsh, whereas S. ramosissima is more typical of pans and interfluves of the upper marsh at slightly higher elevation; S. pusilla is restricted to low hummocks and the landward margin, the highest parts of the tidal frame, where it is often inundated only by spring tides (Davy & Smith 1988; Noble et al. 1992). Similarly, Rozema, van der List et al. (1987) reported that S. europaea agg. (‘S. brachystachya (Meyer) König’) occurs above Mean High Water Level. Various forms of Salicornia in intertidal habitats grow on a wide range of marine sediments, ranging from gravels and shelly sands, through silts to fine clays. In inland salines, the substrates can also vary from fine clays to coarse sands, depending on their origin. Although Salicornia is an early colonist of soft, unconsolidated sediments, the densest stands tend to be on firm silts and clays (Adam 1981). Salicornia is invariably associated with saline, brackish or alkaline substrates. The ionic composition of coastal salt marsh substrates generally reflects the ionic balance of seawater, dominated by sodium chloride, but actual concentrations can vary greatly, depending on complex tidal cycles, local evapotranspiration, precipitation and any supply of fresh groundwater. The concentration of Na+ ions in the interstitial water from coastal marsh sediments fluctuates greatly, both seasonally and from year to year (Jefferies 1977; Jefferies et al. 1979; Smith 1985). In mid-summer, when successive spring high tides fail to cover the upper marsh and evapotranspiration exceeds rainfall, Na+ concentrations in the interstitial water may exceed 1 m in the upper marsh; near the the is typically m. The water of the shows the with low in saline have low water the water of the upper of the can to below in below that of sea (Jefferies et al. 1979). are of conditions in sites dominated by S. europaea. recorded up to in the in in in an salt et al. as to of are at the surface in In inland salines, a of ions other than Na+ and may In coastal marshes, the substrates of Salicornia the tidal range and are often for much or all of the depending on elevation and The sediments are typically and may develop low even in the surface with high levels of reduced ions as and & & 1985). VII The of salt marsh in the British National is on the of a analysis of from salt marshes all the British The only dominated by Salicornia is the Salicornia salt or Its species are at least one of the taxa of Salicornia, which can be of in a generally there are no other is often an over the in some areas may be plants of maritima and may with individuals of and Sarcocornia may be present as a In the mean cover was the mean was 7 cm and the mean number of species was Within the low marsh, where it the of the may occur as a distinct a few to several or in a with or (Adam 1981). stands of Salicornia may occur in pans and in higher parts of the Salicornia is a species in two other and with annual Salicornia species and is and dominated by of the three It is on lower marshes, where it may be a on on lower marshes with a maritima it tends to occupy the whereas in marshes of it is found in within a of other It is also on the sides of large where it a distinct above the salt or also occurs as an on the lower marsh or on sides at levels in the marsh, with a development at about tidal submergences per In at their upper elevational may into annual maritima salt or can also into on the lower salt or marshes at the same elevation as and has much of The seeds of Salicornia are widely distributed on salt marshes and so it is a variable or of other where it may within the of perennial maritima salt on salt maritima salt or both the maritima or as well as the maritima salt maritima salt rubra salt or maritima salt or salt of the north Norfolk salt salt salt on salt described the of British salt marshes in of Salicornia in of and in with other species of each of which with a than in at least one of the Salicornia can have an as a salt-marsh as it is frequently the higher to intertidal and & described around S. ramosissima plants to form hummocks on a in the not make a to the of the marsh, those of the perennial Sarcocornia Salicornia species the of flats after tidal from the in the of a salt marsh in the of the at from through to a in than years large stands of Salicornia on and flats may be and not Salicornia is the of the the and from the north Atlantic and coasts to the coast of France the coasts of and the north Mediterranean & 1979). stands as In the same of the of maritima with S. ramosissima at higher elevations 1988). The inland saline east of the in a dominated by Salicornia (S. europaea with present and sometimes with present et al. that Salicornia was local and in halophytic of central Europe in water level generally wide. S. ramosissima is the species of the of in the the Salicornia characteristic of coastal marshes in et al. The lower limit of Salicornia europaea on tidal flats at the of salt marshes may be by & in the of the found that this lower limit with the upper limit of the abundant at mean high water level transplanted below this level by the of but those in areas with to the had a similar to that of transplanted above The populations of of up to about to are between Salicornia and on lower marshes. and may contribute to of Salicornia by from the as the on the as at & Jefferies found that by provided sites for the and of seeds of Salicornia. of of S. europaea reduced in the 2–4 °C lower than on the surface on spring (Costa with Salicornia may and salt concentrations to that of sea water Salicornia plants may by perennial in and upper marshes, by from the surface and stress & A of in stands of the S. europaea and maritima at Norfolk, by that their was mainly by the of the Salicornia and its of when at the same Salicornia was a with in the low marshes of England, large areas dominated by Salicornia have been and by to Ball & Salicornia europaea is than S. dolichostachya to from the perennial and species and of upper marshes can to complex a to dominated by the perennial The has successive of that on salt-marsh early in the summer on pollen and of but