Journal of
Ecology 2001
89, 681–707
BIOLOGICAL F LORA OF THE BRITISH ISLES *
Blackwell Science, Ltd
NO. 219
List Br. Vasc. Pl. (1958) 160, 2 – 5
Salicornia L. (Salicornia pusilla J. Woods, S. ramosissima
J. Woods, S. europaea L., S. obscura P.W. Ball & Tutin,
S. nitens P.W. Ball & Tutin, S. fragilis P.W. Ball & Tutin
and S. dolichostachya Moss)
A. J. DAVY, G. F. BISHOP and C. S. B. COSTA†
School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK; and †Departamento de
Oceanografia, Fundação Universidade Federal do Rio Grande, C.P. 474, 96201–900 Rio Grande, Brazil
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
© 2001 British
Ecological Society
Correspondence: Dr A. J. Davy (fax + 44 1603592250; e-mail
a.davy@uea.ac.uk)
*Abbreviated references are used for many standard works;
see Journal of Ecology (1975), 63, 335–344. Nomenclature of
vascular plants follows Flora Europaea and Stace (1997) for
British plants, where authorities are not cited.
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
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G. F. Bishop &
C. S. B. Costa
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
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 yellowgreen 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.
I. Geographical and altitudinal distribution
The composite distribution of all taxa of Salicornia in
Britain (Fig. 1) faithfully reflects the availability of saltmarsh 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
683
Salicornia L.
Fig. 1 The composite distribution of all taxa of the genus Salicornia in the British Isles. (O) Pre-1950; (d) 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.
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
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).
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).
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
684
A. J. Davy,
G. F. Bishop &
C. S. B. Costa
© 2001 British
Ecological Society,
Journal
of Ecology,
Fig.
2 The
distribution of Salicornia europaea agg. in the British Isles. (O) Pre-1950; (d) 1950 onwards. Each dot represents at least one record in a 10-km
89, 681–707
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.
685
Salicornia L.
© 2001 British
Ecological Society,
Fig.
3 The
distribution of Salicornia procumbens agg. in the British Isles. (O) Pre-1950; (d) 1950 onwards. Each dot represents at least one record in a 10Journal
of Ecology,
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.
89, 681–707
686
A. J. Davy,
G. F. Bishop &
C. S. B. Costa
Fig. 4 The distribution of Salicornia pusilla. in the British Isles. (O) Pre-1950; (d) 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).
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
Fig. 5 The distribution of the genus Salicornia in Europe. Each dot (d) 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.
687
Salicornia L.
Fig. 6 The distribution of Salicornia europaea agg. in Europe. Each dot (d) 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.
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
Fig. 7 The distribution of Salicornia procumbens agg. in Europe. Each dot represents at least one record in a 50-km square. (d)
S. dolichostachya, S. fragilis and S. nitens; (m) 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.
688
A. J. Davy,
G. F. Bishop &
C. S. B. Costa
Fig. 8 The distribution of Salicornia pusilla in Europe. Each
dot (d) 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.
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.
II. Habitat
( )
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
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 in the upper marsh; conversely,
near the winter solstice, the value is typically 0.2–0.3 .
The water content of the sediment shows the inverse
trend, with low values in summer. Such saline substrata
inevitably have exceptionally low water potentials.
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During hot, dry summers the water potential (ψw) of
the upper layers of the sediment can fall rapidly to
below –5.0 MPa (–50 bars); in cooler, wetter summers
ψw potential remains barely below that of sea water,
c. –2.3 MPa (Jefferies et al. 1979). There are many
reports of hypersaline soil conditions in sites dominated
by S. europaea. For instance, Tsuda (1961) recorded
up to 8.2% NaCl in the soil solution in Japan (cf. 3.5%
total salts in seawater). Salinities in an Ohio salt pan
(Ungar et al. 1979), measured as electrical conductivity,
reached 143 mS cm –1 (approximately equivalent to
–5.1 MPa ψw). Crusts of crystallizing salts are commonly seen at the sediment surface in dry weather.
In inland salines, a variety of ions other than Na+ and
Cl– may predominate.
In coastal marshes, the substrates of Salicornia span
the tidal range and are often waterlogged for much
or all of the time, depending on elevation and drainage
conditions. The saturated sediments are typically hypoxic
and may develop low redox potentials, even in the surface
layers, with concomitantly high levels of potentially
toxic reduced ions such as S2– and Mn2+ (Ingold &
Havill 1984; Singer & Havill 1985). See VII (E).
III. Communities
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
The classification of salt marsh vegetation in the
British National Vegetation Classification (Rodwell 2000)
is based substantially on the work of Adam (1978, 1981)
who made a phytosociological analysis of relevés
from salt marshes all round the British coast. The only
community dominated by Salicornia is the ‘Annual
Salicornia salt marsh’ (SM8) or Salicornietum europaeae. Its constant species are at least one of the taxa
of Salicornia, which can be of greatly varying density,
in a generally open, ephemeral community. Sometimes
there are no other species. There is often an algal mat over
the substrate surface; in some areas turf fucoids (Fucus
vesiculosus ecad caespitosus) may be abundant. Scattered
plants of Puccinellia maritima, Suaeda maritima and
Spartina anglica may occur, with occasional individuals
of Atriplex portulacoides and Aster tripolium (including
var. discoideus). Sarcocornia perennis may be present as
a rare species. In 81 samples, the mean total cover was
53%, the mean vegetation height was 7 cm and the mean
number of species was three. Within the low marsh,
where it characteristically pioneers the colonization
of mud flats, the Salicornietum may occur as a distinct
zone (from a few metres to several hundred metres
wide) or in a mosaic with Spartinetum townsendii or
Puccinellietum maritimae (Adam 1981). Extensive pure
stands of Salicornia may occur in shallow, poorly drained
pans and depressions in higher parts of the marsh.
Salicornia is a constant species in two other communities (SM10 and SM11). ‘Transitional low-marsh
vegetation with Puccinellia maritima, annual Salicornia
species and Suaeda maritima’ (SM10) is species-poor
and always dominated by complementary proportions of the three constants. It is widespread on lower
marshes, where it may be a pioneer community on
sandy substrates; on heavily grazed lower marshes with
a hummocky Puccinellia maritima community, it tends
to occupy the hummock tops, whereas in muddier
marshes of south-east England it is found in slight
depressions within a variety of other communities. It
is also widespread on the sides of large creeks where
it occupies a distinct zone above the Salicornietum
europaeae. ‘Aster tripolium var. discoideus salt marsh’
(SM11) or Asteretum tripolii also occurs as an extensive zone on the lower marsh or on creek sides at varying
levels in the marsh, with a maximum development at
about 350 tidal submergences per year. In addition,
‘Zostera noltii stands’ (SM1) at their upper elevational
limits may grade into Salicornietum. Another essentially
annual community, ‘Suaeda maritima salt marsh’ (SM9)
or Suaedetum maritimae can also grade into Salicornietum on the lower marsh. ‘Spartina anglica salt marsh’
(SM6) or Spartinetum townsendii colonizes marshes
at the same elevation as Salicornietum and has now
replaced much of it.
The seeds of Salicornia are widely distributed on salt
marshes and so it is a variable or minor component of
many other communities, where it may find ephemeral
niches within the matrix of perennial species: ‘Spartina
maritima salt marsh’ (SM4); ‘Arthrocnemum perenne
(Sarcocornia perennis) stands’ (SM7); ‘Rayed Aster
tripolium on salt marshes’ (SM12); ‘Puccinellia maritima
salt marsh’ (SM13) or Puccinellietum maritimae (in
both the ‘Limonium vulgare-Armeria maritima subcommunity’ or General Salt Marsh, as well as the ‘Puccinellia
maritima-Spartina maritima subcommunity’); ‘Halimione (Atriplex) portulacoides salt marsh’ (SM14); ‘Juncus
maritimus-Triglochin maritima salt marsh’ (SM15);
‘Festuca rubra salt marsh’ or Juncetum gerardi (SM16);
‘Artemisia maritima salt marsh’ or Artemisietum maritimae (SM17); ‘Suaeda vera-Limonium binervosum salt
marsh’ (SM21) of the north Norfolk coast; ‘Halimione
(Atriplex) portulacoides-Frankenia laevis salt marsh’
(SM22); ‘Spergularia marina-Puccinellia distans salt
marsh’ (SM23); ‘Suaeda vera salt marsh’ (SM25); ‘Inula
crithmoides on salt marshes’ (SM26).
Adam 1981 described the vegetation of British salt
marshes in terms of 49 ‘noda’. Salicornia occurred in 34
of these noda and in association with 44 other species
of angiosperm, each of which occurred with a frequency
greater than 81% in at least one of the 49 noda.
Salicornia can have an important role as a salt-marsh
pioneer, as it is frequently the first higher plant to
colonize intertidal mud and sand flats. Carey & Oliver
(1918) first described accretion around S. ramosissima
plants to form ephemeral hummocks on a sand bank in
the Bouche d’Erquy, Brittany, France. These, however,
did not make a permanent contribution to the relief
of the marsh, unlike those of the perennial Sarcocornia
perennis. Salicornia species were the first colonists of
sand flats after embankment removed tidal influence
from the Grevelingen Estuary, in the Netherlands
(Stienstra 1987). Direct observation of a naturally
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developing salt marsh in the macrotidal environment
of the Severn Estuary, at Berrow, Somerset, UK,
chronicled succession from bare sediment, through
Salicornietum, to a species-poor Phragmitetum in fewer
than 90 years (Willis 2000). Nevertheless, large stands
of Salicornia on low-lying sand and mud flats may be
ephemeral and do not necessarily initiate succession.
Salicornia spp. is the character-taxon of the class
Thero-Salicornietea Tx. 1954; the order TheroSalicornietalia and alliance Thero-Salicornion Br.-Bl.
1933 em. Tx. 1950, whose eulittoral Salicornia-dominated
communities extend from the north Atlantic and west
Baltic coasts to the west coast of France and, locally,
the coasts of Portugal and the north Mediterranean
(Westhoff & Schouten 1979). Ellenberg (1988)
recognizes low-marsh, pure stands as Salicornietum
dolichstachyae. In the same order, communities of the
alliance Salicornion ramosissimae Tx. 1974 comprise
swards of Puccinellia maritima with S. ramosissima at
higher elevations (Ellenberg 1988). The inland saline
area east of the Neusiedlersee in Austria supports
Salicornietum prostratae Soó 1964, a rare community
dominated by Salicornia prostrata (S. europaea agg.),
with subdominant Puccinellia peisonis, Phragmites
australis always present and sometimes with Suaeda
pannonica present (Mucina et al. 1993). Bernatksy
(1905) concluded that Salicornia was local and uncommon in halophytic communities of central Europe
because seasonal fluctuations in water level were
generally too wide. S. ramosissima is the dominant
species of the Salicornietum europaeae hungaricum of
Hungary (Soó 1960) and, in the Sarcocornio perennisSalicornietum ramosissimae, the Salicornia characteristic of coastal marshes in north-west Spain (Sánchez
et al. 1996).
IV. Response to biotic factors
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
The lower limit of Salicornia europaea on tidal mud
flats at the seaward margin of salt marshes may be
determined by bioturbation. Gerdol & Hughes (1993),
working in the estuary of the River Crouch, Essex,
found that this lower limit corresponded with the upper
limit of the abundant amphipod Corophium volutator
(Pallas), at approximately mean high water neap tide
level (MHWNT). Seedlings transplanted below this
level were disturbed by the activity of Corophium but
those in areas treated with insecticide to remove the
Corophium had a doubled survivorship, similar to that
of seedlings transplanted above MHWNT. The populations of Corophium of up to about 14 000 m–2 were
effectively able to prevent seedling establishment.
There are varied biotic relationships between
Salicornia and algae on lower marshes. Algal mats (of
Enteromorpha linza, E. torta, E. prolifera, Rhizoclonium
riparium and Ulothrix speciosa) may contribute to
mortality of Salicornia seedlings by pulling them from
the sediment as the mats float on the incoming tide,
as at Skallingen, Denmark (Jensen & Jefferies 1984).
Costa (1992) found that patches colonized by Fucus
vesiculosus ecad muscoides provided favourable sites for
the trapping and germination of seeds of Salicornia.
Mortality rates of seedlings of S. europaea were reduced
in the algal patches. Temperatures inside Fucus patches
were 2–4 °C lower than on the adjacent mud surface on
sunny spring days (Costa 1992); fucoid algae intertwined
with Salicornia may reduce evaporation and maintain
salt concentrations closer to that of sea water (Chapman
1960). Salicornia plants themselves may facilitate
colonization by dominant, perennial halophytes in
physically stressful mid- and upper marshes, by reducing evaporation from the sediment surface and limiting
salinity stress (Hacker & Bertness 1999).
A study of neighbourhood effects in mixed stands
of the annuals S. europaea and Suaeda maritima at
Stiffkey, Norfolk, by Costa (1992) demonstrated that
their coexistence was maintained mainly by the earlier
germination of the smaller-seeded, slower-growing
Salicornia and its consequent pre-emption of resources;
when germinated at the same time, Salicornia was a
poor competitor with Suaeda. Particularly in the low
marshes of south-east England, large areas previously
dominated by Salicornia have been invaded and replaced
by Spartina anglica. According to Ball & Brown (1970),
Salicornia europaea is better able than S. dolichostachya
to withstand competition from the perennial grasses
Spartina anglica and Puccinellia maritima.
Greater species diversity and increased trophic
complexity of upper marshes can lead to complex biotic
interactions. Proudfoot (1993) investigated a 4-species
interaction close to creek banks dominated by the
shrubby perennial Atriplex portulacoides. The microlepidopteran Coleophora atriplicis (Meyrick) has
successive instars of case-bearing larvae that feed on
salt-marsh chenopods; early in the summer larvae
feed on pollen and flowers of Atriplex portulacoides but
in late summer they may migrate to Suaeda maritima
and Salicornia, where they mine and consume the
developing seeds. Proudfoot (1993) showed that a cline of
decreasing abundance of Suaeda away from creek banks
was due to increasing competition from Salicornia;
populations of Salicornia close to the Atriplex were
depressed as a result of preferential seed predation by
Coleophora larvae. Rand (1999), working on New England salt marshes, has recently shown that the presence
of S. europaea had an adverse effect on the annual
Atriplex patula; this effect was also mediated indirectly
through a shared herbivore, in this case the chrysomelid
beetle Erynephala maritima. Mature stands of Salicornia
and their seeds can be an important food resource for
passerine birds and geese (see IX A). On salt marshes
in northern Germany, intense sheep grazing promoted
communities containing S. europaea and its population
density decreased after reduction of the grazing intensity,
as Festuca rubra and other more competitive perennials
replaced Puccinellia maritima (Kiehl et al. 1996).
Mats of tidal detritus deposited by high tides may
remain long enough to kill the vegetation and create
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bare patches in which Salicornia stands can become
established (Truscott 1978). Experimental burial with
wrack (tidal litter) of Spartina alterniflora (using a 5–
10 cm thick layer) favoured germination and establishment of S. europaea on a Rhode Island Spartina patens
marsh (Brewer et al. 1998); the success of Salicornia
after disturbance by wrack burial was attributed to its
ability to compete with Juncus gerardii under the more
saline conditions of exposed sediments that are subject to
high rates of evaporation. Here, S. europaea is regarded
as a fugitive species of hypersaline bare patches and
pans, because of its inability to compete with the
dominant perennials (Bertness et al. 1992).
V. Responses to the environment
( )
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
Salicornia is generally highly gregarious but local
distributions may be random or aggregated (Brereton
1971; Joenje 1978). Seedling population densities may
be greater than 100 000 m–2 in suitable habitats. Very
local high-density clumps may occur where senescing
mother plants have fallen over and been incorporated
into surface sediments, releasing their embedded seed
complements in situ as they decompose. Algal patches
may also trap seeds and increase local density. Population density varies greatly, with the potential for strong
regulation from a combination of negatively densitydependent seed production and density-independent
seedling mortality (Jefferies et al. 1981; Davy & Smith
1985, 1988; Smith 1985; Watkinson & Davy 1985). The
effects of density on seed production arise from the
great morphological plasticity: at high density, individuals are unbranched with a single, terminal spike
that can produce only a few seeds; at low density, the
3-dimensional branching structure can result in large
individuals with hundreds of fertile terminal spikes
(see VIII C). Watkinson & Davy (1985) modelled the
relationship between the reproductive output per plant
(Ns /N ) and the density of surviving plants (N ) as:
Ns /N = λ(1 + aN )–b where λ is the number of seeds
produced by an isolated plant, a is the area required to
produce λ seeds and b describes the effectiveness with
which resources are taken up from a given area.
Mortality tends to be of the Deevey type I pattern,
preponderantly before flowering (Jefferies et al. 1981;
Beeftink 1985). The mortality in young plants at high
density is largely independent of density, resulting mainly
from disturbance, herbivory, interspecific competition
and water stress (Jefferies et al. 1981; McGraw &
Ungar 1981; Ellison 1987a; Ungar 1987a). Even at the
highest densities found in the field (> 10 000 m–2),
populations of S. europaea agg. show little evidence of
self-thinning, despite closely approaching combinations
of mass and density where thinning would normally be
predicted, according to the –3/2 power rule (Watkinson
& Davy 1985). The fact that size inequalities within
populations (expressed as Gini coefficients) did not
change with density, or with growth during the season,
is another manifestation of this (Ellison 1987b). The
failure of Salicornia to self-thin may be explained in
terms of growth geometry: because it lacks leaves and its
stems branch sparsely, at high densities its biomass per
unit area tends to increase as a linear function with height,
rather than as the cubic function that describes more
conventional morphology and which is believed to
underlie the –3/2 self-thinning rule (Ellison 1987b, 1989).
Harley & Bertness (1996) found that plants in
crowded stands of S. europaea on a New England salt
marsh were thinner and more susceptible to breakage,
becoming dependent on their neighbours for mechanical support. The breaking force for individuals that
had developed in isolation was much greater than for
those in crowded stands; all individuals from crowded
stands had collapsed and fallen over one week after
experimental removal of their neighbours.
( )
Salicornia is confined to saline habitats and, as an
annual, its performance is constrained by the length
of the growing season. At its northern limit in the
Canadian Arctic, where the growing season is effectively
only 3 months and conditions are generally severe,
individuals reach a height of 1–10 cm and produce
simple branches only at the cotyledonary node, if at all
(Wolff & Jefferies 1987b). In such marginal habitats,
plants colonize north-facing slopes poorly, where they
do not branch and can ripen little seed; most of the populations are on south-facing slopes, where many individuals branch and seed is ripened reliably (Jefferies et al.
1983). In temperate latitudes, such as the salt marshes
of north Norfolk, the growing season is typically 7–
8 months and under otherwise favourable conditions
individuals can reach 40 cm, with up to 4th-order
branching at the nodes. Such large individuals tend
to occur in isolation, on nitrogen-rich drift lines of
hyposaline estuarine marshes or on the sides of creeks
in other relatively eutrophic marshes. Performance can
be severely limited by summer hypersalinity in inland
marshes and on the higher elevations of coastal marshes,
especially at lower latitudes. The marshes and mangal
of the Saudi Arabian Gulf coast potentially enjoy a
12-month growing season, allowing the development
of massively branched individuals, with woody basal
internodes 7 mm in diameter, that display a wide
variety of morphologies; these plants can apparently
persist for more than one year (Al-Turki 1992), despite
their determinate growth. No seed dormancy has been
detected in such populations and this is presumably
an evolutionary response to a relatively benign and
reliable environment (Al-Turki 1992).
There have been few reliable measurements of net
primary production. Jefferies (1972) estimated the
annual net productivity of Salicornia spp. on the
marshes of the north Norfolk coast at 876 g m–2 year–1,
on the basis of frequent measurements of total standing
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C. S. B. Costa
crop. Similarly, annual net aerial primary production
of S. ramosissima on the Cantabrian coast (north Spain)
was estimated as 486 g m–2 year–1 by Benito & Onaindia
(1991) using Smalley’s method.
Species or populations characteristic of low marsh,
where hypersalinity is unlikely and a moderate supply
of nitrogen from seawater is assured (e.g. S. europaea
and S. dolichostachya), tend to have faster growth rates
than those of species abundant at higher elevations
(e.g. S. ramosissima) (Jefferies 1977; Jefferies et al. 1981).
There are numerous differences in demographic performance associated with the elevation of populations,
or species, in the tidal frame (e.g. Beeftink 1985; Davy
& Smith 1985, 1988).
( )
, .
Freezing is less of a hazard in the habitats generally
affected by Salicornia than in non-saline habitats with
the same climate, because of depression of the freezing
point by high concentrations of solutes in both soils
and plants. In addition, coastal locations are generally
buffered, by proximity to the thermal capacity of the sea,
from the lowest extremes of temperature experienced
inland at similar latitude. Nevertheless, cohorts of
seedlings that have germinated between December and
March may be killed by exceptionally hard frosts on
the north Norfolk coast; later germinating cohorts are
rarely damaged. Seedlings may also be removed by ice
scour. Autumn frosts hasten the senescence and collapse
of plants, thus releasing the seeds into the sediment.
The seeds overwintering in the surface sediments appear
to be extremely tolerant of low temperatures, even
those prevailing in the arctic. The annual distribution
of frost is undoubtedly one of the determinants of the
length of the growing season (cf. V B). As a halophyte,
Salicornia is tolerant of exceptionally low water potentials in its root environment, whether they arise from
salinity, drought or a combination of both (see V1 E).
Hydraulic forces generated by tidal flow, perhaps
associated with scouring of the sediment and wave
action, can be a major source of mortality for Salicornia
seedlings at lower elevations on a salt marsh (Wiehe
1935). Salicornia is very susceptible to marine pollution
from oil spills or refinery effluent and is killed quickly
by a single spillage (Baker 1979). Salicornia ramosissima
in a polluted estuarine marsh in south-west Spain
accumulated high concentrations of As, Cr, Cu, Fe,
Mn, Ni, Pb, Ti and Zn without apparent harm (Luque
et al. 1999).
VI. Structure and physiology
( )
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
Each succulent, photosynthetic ‘segment’ is an internode
separating consecutive pairs of oppositely arranged,
but very reduced, leaves or scale leaves. In older, mainly
basal, segments the outer tissues wither, leaving brown,
non-succulent stems. The morphological nature of the
photosynthetic tissue associated with each internode
has been controversial. Fahn & Arzee (1959) regarded
it as entirely cortical in origin, attributing all photosynthesis to the stem. Duval-Jouve (1868) considered
the outer cortex of each segment to be foliar in origin, a
sheath being formed from the fused bases of the leaves
immediately above. This ‘foliar sheath’ theory of the
succulent cortex of Salicornia was given credence by de
Fraine (1912) in a classical morphological study (using
several species of Salicornia) on development at the
shoot apex and of the vascular system. It was also supported by Halket (1928) after studying an abnormal
plant of S. europaea in which the terminal parts of
some leaves were clearly separated from the stem.
Evidence from other succulent chenopods agrees
(James & Kyhos 1961).
The vascular anatomy of a segment is well known (de
Fraine 1912; Fahn & Arzee 1959; Ellison et al. 1993). A
transverse section of the stem, taken mid-way within a
segment, shows a central ring of eight primary vascular
bundles enclosed by pericycle cells and an endodermis,
or ‘limiting layer’, surrounded by a layer of water
storage cells and then by a layer of photosynthetic cells.
Between the inner (water storage) and outer (photosynthetic) layers lies vascular tissue originating at the
distal end of the segment. Whilst it is agreed that this
vascular tissue is foliar in origin, the true nature of the
tissues it serves (water storing cells to the inside and
photosynthetic cells towards the outside) is controversial: these non-vascular tissues are considered to be
foliar by de Fraine (1912) but cortical by Fahn & Arzee
(1959). At each node, two of the eight vascular bundles
diverge as leaf traces opposite each other. Each leaf
trace divides into three: the central trace curves upwards
to supply the much reduced leaf tip whilst the lateral
pair curve downwards between the water storage and
palisade layers of the foliar sheath or cortex to form a
closed network of anastomosing vascular tissue (Fahn
& Arzee 1959). In curving downwards there is also
effectively a rotation of each bundle of the lateral pair
so that the phloem is outermost as in the leaf tip itself
(de Fraine 1912). Above the node, two of the six surviving
vascular bundles bifurcate, restoring the total to eight.
Ellison et al. (1993) determined, by serial sectioning,
changes in the mean diameters of vessel members of
the primary vascular traces between consecutive nodes:
hydraulic constrictions in S. europaea occur two nodes
below the morphological emergence of a branch, differing in this respect from those in trees and palms.
The bulk of the mature stem originates from a secondary meristem immediately surrounding the system
of primary bundles. Anomalous secondary thickening,
widespread among members of the Chenopodiaceae,
results in a concentric series of collateral vascular
bundles embedded in a lignified ground tissue; the
precise behaviour of the cambium during the formation of these bundles is disputed. The outer side of the
vascular cambium is inactive except where it forms
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© 2001 British
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Journal of Ecology,
89, 681–707
aerenchyma. Aerenchyma is present, particularly in
S. europaea and S. ramosissima, in the lower regions of
the stem and the upper part of the main root. It is
surrounded by a thin layer of cork which is very readily
torn off in cutting sections. In some cases aerenchyma
of a special kind is present: the aerenchyma cells are
drawn out at each end and appear to be covered with
large ‘pores’ which are actually the result of cutting
across tubular outgrowths connecting the loosely
arranged cells (de Fraine 1912). Broad and short
tracheid-like cells (Fahn & Arzee 1959; Fahn 1974),
‘stereids’ and ‘spiral cells’ (de Fraine 1912) are found
among the palisade cells in both vegetative and
reproductive shoots. Their function is unknown and
taxonomic significance uncertain (Ball & Tutin 1959).
Among halophytes, S. europaea has an exceptionally
high shoot to root (dry mass) ratio of about 10 : 1
(Cooper 1982). The root is diarch with a well marked
endodermis and aerating tissue consisting of large
intercellular spaces bridged by trabeculae. Although
the presence of aerenchyma is generally associated
with tolerance to flooding, in Salicornia this ability may
be more related to superficial rooting and metabolic
adaptations (Pearson & Havill 1988). The root has
anomalous secondary thickening, as in the stem.
Stomata are most numerous towards the distal end
of segments. They are arranged with their long axes at
right angles to the axis of the stem. A stomatal density of
49 ± 2 mm–2 (n = 30) has been recorded for S. europaea.
Dalby (1962) measured stomatal volumes (calculated
as that of a sphere from a diameter equal to that of the
stoma length) ranging from 3 to 16 × 103 µm3 in diploids
to 8 –39 × 103 µm3 in tetraploids, with a changeover value
around 13 × 103 µm3 (= 29.17 µm for length of stoma).
Ball & Brown (1970) reported the length of stomatal
guard cells as (20 –)24–28(–31) µm in S. europaea and
(27–)29 –36(–42) µm in S. dolichostachya.
Branching patterns are highly plastic and greatly
affected by plant density; crowding reduces the degree
of branching in both monospecific (Jefferies et al. 1981;
Jensen & Jefferies 1984; Smith 1985; Ellison & Niklas
1988) and mixed (Costa 1992) stands. S. europaea s.l.
growing early in a succession were bushy, profusely
branched and the younger internodes were much
shorter than older ones; plants in late succession were
unbranched, etiolated and had internodes of equal size
(Ellison & Niklas 1988; see VI E).
There has been a plethora of morphometric studies
of Salicornia (e.g. Langlois 1961a,b; Wilkon-Michalska
1985; Ungar 1987a), mainly in attempts to determine
the morphological characteristics of subtaxa and local
populations. Recent studies have applied numerical
methods to morphometric data (Huiskes et al. 1985a;
Ingrouille & Pearson 1987; Ingrouille et al. 1990).
( )
Endotrophic mycorrhiza in the roots of S. europaea
(‘S. herbacea’) was first reported by Klecka & Vukolov
(1937) in Czechoslovakia. Rozema et al. (1986) recorded
between 0.1 and 1% colonization of root length with
AM mycorrhiza in S. europaea (‘S. brachystachya’)
on a Dutch middle marsh; S. dolichostachya on a low
marsh showed 0.1–30% root colonization, external
hyphae and a low incidence of spores. S. europaea at
two inland salt marshes in north Germany had extensive
root colonization (extra- and intraradical hyphae),
with vesicles and arbuscules, whereas specimens
from a marsh on the Baltic coast had only 3% colonization, with sparse vesicles and arbuscules (Hildebrandt
et al. 2001). Spores present at high densities in soils at
the inland sites were mainly identifiable as Glomus
geosporum (Nicolson & Gerdemann) Walker, using
RFLP analysis of the ITS region of the rDNA of individual spores after amplification by PCR (Hildebrandt
et al. 2001).
The main colonist of Salicornia at all elevations on
Stiffkey salt marshes, Norfolk, is a previously unrecorded
but distinct ‘fine endophyte’ AM fungus, possibly Glomus
tenuis (Greenhall) Hall (Davy et al. 2000). It was also
present in Aster tripolium, along with a conventional
AM fungus.
( )
:
Therophyte. In Britain Salicornia is a summer annual
that perennates entirely as a seed bank in salt marsh
sediments. Seeds are shed between September and late
November. The sediment seed bank therefore increases
rapidly from a minimum in late summer to a maximum
in December and January. More than 95% of seeds are
concentrated in the upper 5 mm of the sediment. Mean
seed bank maxima at various elevations on the marshes
at Stiffkey range from 50 000 to 100 000 m–2, although
local densities may be higher (Smith 1985; Davy &
Smith 1988). When shed, the seeds are mostly innately
dormant but the proportion of dormant seeds declines
to less than about 5% by February. The relatively few
seeds that have not germinated by May have further
dormancy enforced by increasing sediment salinity.
In September, any seeds remaining after 1 year appear
to have lost viability, as judged by tetrazolium vital
staining. Similarly, there appears to be no significant
persistence of seeds from one year to the next in Danish
marshes (Jensen & Jefferies 1984).
In contrast, persistent seed banks of S. europaea
s.l. have been reported under more severe and less predictable conditions. Jefferies et al. (1983) found a seed
bank in sediments of an arctic, coastal marsh, although
the viability of the seeds was not certain. Substantial
seed banks throughout the year, with a minimum of
38 900 m–2 in August and a maximum of 128 000 m–2 in
November, were characteristic of an inland saline in
Ohio, USA; in this population, which shows seed
dimorphism (see VIII C, D), only the small (lateral)
seeds persisted in the seed bank after the winter and
this reserve played a significant role in maintaining
the population in this highly stressful habitat (Ungar &
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Riehl 1980; Philipupillai & Ungar 1984; Ungar 1987a,b).
The representation of S. europaea in the sediment
seed bank may be disproportionately large in comparison with the species composition of the vegetation,
especially in grazed marshes (Ungar & Woodell 1996).
Lee et al. (1992) have developed a method of mass
propagation of S. bigelovii clones by in vitro culture of
shoot tips (in the presence of 1-naphthaleneacetic
acid and N-(phenylmethyl)-1H-purine-6-amine) that is
useful in its development as a crop (see IX A) and for
experimentation.
( )
The taxonomic intractability of Salicornia is reflected
in the varied chromosome numbers reported for a
range of taxa (Wulff 1936, 1937; König 1939; Ludwig
1950; Hambler 1954; Nannfeldt 1955; Ball & Tutin
1959; Dalby 1962; Ferguson 1964a; Contandriopoulos
1968; Ball & Brown 1970; Parriaud 1971; Castroviejo
& Coello 1980; Smith 1985; Wolff & Jefferies 1987b;
Al-Turki 1992). The basic chromosome number for
the genus is x = 9 and British material may be either
diploid (2n = 18) or tetraploid (2n = 36). Aneuploid
numbers reported by Wulff (1936, 1937) and Hambler
(1954) are regarded as suspect (Dalby 1962). A triploid
type (2n = 27) has been reported from Italy (Cristofolini
& Chiapella 1970). The chromosomes of Salicornia are
small, ranging from about 0.6 –1.8 µm in length but
with some variation in shape (Dalby 1962).
Recent systematic treatments (Ball & Tutin 1959;
Ball 1964; Ferguson 1964a,b; Ball & Brown 1970; Dalby
1989; Stace 1997) use ploidy level in the delineation of
species: S. pusilla, S. ramosissima and S. europaea s.s.
are considered diploid and S. dolichostachya, S. fragilis
and S. nitens are defined as tetraploid. Material from
the field that is referred to S. europaea and S. ramosissima
on morphological criteria cannot always be reconciled
with this. Tetraploid types are more frequent than
diploids in open, low marsh, pioneer situations (e.g.
Ball & Brown 1970). Upright forms more often tend to
be diploid and prostrate forms more often tetraploid
(e.g. Parriaud 1971).
Diploid and tetraploid cytotypes may differ in the
size of pollen, stomatal guard cells and seeds (Dalby
1962), in fertile segment shape, number of fertile
segments in the terminal spike, length of anthers (Ball
& Brown 1970) and in the distance between the apex
of the middle floret and the apex of the segment
(Ingrouille et al. 1990).
( )
Salinity tolerance
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
As a halophyte, Salicornia is able to maintain low
water potentials in its tissues by accumulating solutes.
There are many reports of the accumulation of high
concentrations of inorganic ions, mainly sodium and
chloride in a variety of taxa (e.g. Albert 1975; Grouzis
et al. 1977; Gorham et al. 1980; Cooper 1982; Riehl
& Ungar 1982; Ayala et al. 1996). Salicornia has a
relatively high ratio of Na : K, typical of dicotyledonous
halophytes (Gorham et al. 1980; Rozema 1991). These
high concentrations of inorganic ions are accumulated
predominantly in the cell vacuoles; there is some
evidence that pinocytosis is instrumental in ion accumulation in the vacuoles of shoot cells (Kurkova &
Balnokin 1994). As in other halophytic chenopods,
high concentrations of compatible organic solutes
(mainly the form of the methylated quaternary ammonium compound, glycinebetaine) are maintained in
the cytoplasm (Stewart et al. 1979; Gorham et al. 1980;
Briens & Larher 1982). This asymmetric distribution of
solutes protects metabolic activity from the potentially
toxic effects of high concentrations of inorganic ions.
Optimal growth generally occurs at external salinities
equivalent to less than half that of seawater, depending
on other environmental conditions. Halket (1915)
first showed a response of growth to salt. Seedlings of
S. ramosissima on intact sods taken from a salt marsh
grew taller when watered with 1% sea-salt solution
(equivalent to c. 170 m NaCl) than when there was
no salt or when concentrations were higher (2–5%). In
water culture, the greatest growth in height and branch
length of S. dolichostachya (‘S. oliveri Moss’) was
obtained in the presence of 2% (340 m) NaCl; salt
concentrations of 3–5% (520–860 m) were progressively detrimental to growth. Plants of this species grew
very poorly and failed to flower when grown without
salt. Langlois (1967, 1971a) found that a daily, 90-minute
immersion of seedlings of S. europaea (‘S. stricta
Dumort.’) in nutrient solution containing 10 g L–1 NaCl
(170 m) gave growth more similar to that seen in the
field than treatments with no immersion or two immersions a day. Cooper (1982) reported that S. europaea
gave its maximum yield in the saline treatments of
growth experiments, applied as weekly waterings with
340 m NaCl. The North American form S. bigelovii
Torr. shows optimal growth at 200 m NaCl (Ayala
et al. 1996). Even in vitro callus cultures of S. europaea
have been reported to accrue dry mass maximally in
the presence of 0.75 –1.0% (129 –170 m) NaCl (von
Hedenström & Breckle 1974), although it is not clear
what proportion of this dry mass was accounted for
by accumulation of inorganic salts. In a comparison
of relative growth rates under standardized glasshouse
conditions with 15 salt marsh species, Salicornia was
amongst the most salt-tolerant, both under flooded
and well-drained conditions (Rozema et al. 1985).
Rozema, van der List et al. (1987) found that dry mass
was increased in S. europaea (‘S. brachystachya Meyer’)
and S. dolichostachya by treatment with 250 m NaCl
on a clay substrate; however, growth was reduced by
this salinity on a sandy substrate and S. dolichostachya
was the more adversely affected.
The effects of salinity and inundation by seawater
on different aspects of metabolism have been studied in
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Salicornia L.
various segregates of Salicornia: protein accumulation
(Langlois 1969, 1971a), sugar movement (Langlois
1971b) and plasma-membrane ATPase activity (Ayala
et al. 1996)
Tolerance of flooding and sediment hypoxia
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
As expected of plants that include forms capable of
colonizing the lowest parts of tidal marshes, Salicornia
is extremely tolerant of regular flooding. Nevertheless,
growth of S. europaea is reduced by cultivation under
continuous waterlogging, in comparison with free
drainage at the same salinity (Brereton 1971; Cooper
1982). A combination of waterlogging and non-saline
conditions results in very poor growth and survival
(Cooper 1982; Keiffer et al. 1994).
Salicornia may avoid root hypoxia by relatively
shallow rooting, despite poorly developed aerenchyma.
Schat et al. (1987) found that experimental deoxygenation of the root environment reduced relative growth
rate and the elongation rate of roots, but no effects
were detected on CO2 exchange or inorganic nutrient
uptake; neither was there any difference in response
between S. dolichostachya from the lower marsh and
S. ramosissima from the upper marsh. Nevertheless
Salicornia is tolerant of toxic reduced substances resulting from chemical transitions at low sediment redox
potentials, including those of sulphate to sulphide and
manganic to manganous ions. Ingold & Havill (1984)
found that the addition of 100 µ sulphide to a sealed
water-culture system did not have an adverse effect on
the growth and root development of S. europaea, unlike
three other salt marsh species examined; S. europaea
was also the only vascular plant rooted in sulphidecontaining sediments on a lower marsh. Havill et al.
(1985) similarly did not detect any adverse effects of this
concentration of sulphide on its growth and metabolism.
Experiments by van Diggelen et al. (1987) indicate that
the growth of neither S. europaea (‘S. brachystachya’)
nor S. dolichostachya from The Netherlands was
affected by sulphide concentrations of up to 500 µ.
On the other hand, Pearson & Havill (1988) were
able to distinguish between the responses of the
species: root alcohol dehydrogenase (ADH) activity
of S. europaea was little affected by culture in sulphidecontaining (100 µ) nutrient solution, whereas the
corresponding ADH activities of S. dolichostachya and
S. fragilis were increased more than 7- and 14-fold,
respectively, compared with non-sulphide treated
controls.
Similarly, S. europaea was the most tolerant, of eight
salt marsh halophytes examined, to Mn2+ in saline
culture solution, its growth being unaffected up to a
concentration of 10 m (Cooper 1984). Presumably
high concentrations of Na+ ameliorate the toxicity of
Mn2+, because Singer & Havill (1985) reported that
root and shoot growth was inhibited by concentrations
above 0.5 m Mn2+ after 6 weeks in Hoagland (nonsaline) culture solution.
Water relations
Water is conserved by low transpirational losses associated with the absence of leaves and is stored in succulent tissues. The water content of stems (succulence)
varies with external conditions; that in S. europaea
(‘S. stricta’) main stems in the Orne estuary of northern
France ranged from about 700–1100% of dry mass
(Langlois 1968a). Likewise, tissue water potentials
depend on external salinity and the accumulation of
solutes through osmoregulation but they can become
very low without resulting in death. Langlois (1968a)
recorded solute (osmotic) potentials no lower than –
2.67 MPa for S. europaea in the Orne estuary. Material
from a coastal salt marsh at Seal Beach, California
had a water potential (ψw) of –4.23 ± 0.24 MPa, with
a component solute potential (ψs) of –5.32 ± 0.10 MPa
(Kuramoto & Brest 1979). Tsuda (1961) reported an
extreme solute potential of expressed sap as –7.6 MPa,
with sodium chloride content contributing –7.2 MPa
of this, under extremely hypersaline conditions in
Japan. Riehl & Ungar (1982) recorded midsummer
tissue ψw as low as –9 MPa in an inland saline in Ohio,
USA. Momonoki & Kamirura (1994) reported an
increase in the osmolality of stem and branch sap from
about 650 mOsm kg–1–2600 mOsm kg–1 (approximately
equivalent to ψw of –3 to –13 MPa) during the growing
season, in plants growing at the edge of Lake Notoro-ko,
Japan. The NaCl concentration required for incipient
plasmolysis of epidermal cells rose from 1.6 to 2.2%
during the growing season (Momonoki et al. 1994)
and these values were high in comparison with other
halophytes. Rozema, van der List et al. (1987) detected
a diurnal cycle in S. europaea (‘S. brachystachya’), with
2.7% increase in stem thickness during the dark and
shrinkage during the day.
Gas exchange
As expected, stomatal conductance decreased with
increasing external salinity in S. bigelovii, producing
a concomitant decrease in the rate of transpiration
(Ayala & O’Leary 1995). Carbon dioxide fixation is by
the C3 pathway, with a ∂13C ratio of –26.62 determined
for S. europaea (Carolin et al. 1982). Guy et al. (1986)
reported a range of ∂13C ratio (–29 to –23) in S. rubra
(S. europaea ssp. rubra), with less negative values at
higher salinity reflecting differences in long-term wateruse efficiency. Low activities of PEP carboxylase, without fluctuations due to endogenous rhythms, have been
reported (Kuramoto & Brest 1979). Net photosynthetic
rates have been shown to decrease slowly with lowering of external water potential; CO2 uptake in the
absence of salt was 7.59 ± 0.64 mg dm–2 h–1 on a leaf
area basis (14.22 ± 1.66 mg g–1 h–1 on a dry mass basis)
and this was reduced to 4.75 ± 0.12 mg dm–2 h–1
(8.47 ± 1.30 mg g –1 h–1) after equilibration for 72 h
at seawater salinity (Kuramoto & Brest 1979). Dark
respiration declined similarly. Schat et al. (1987) found
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that net photosynthetic and dark respiration rates (on
a fresh mass basis) declined with increasing plant fresh
mass. They also observed mid-day stomatal closure,
exceptionally, in certain individuals of S. ramosissima
under hypoxic stress.
Response to inorganic nutrients
Salicornia plants growing on salt-marsh sediments,
in situ or on cores removed for experiments, typically
respond to additions of nitrogen and phosphorus only
in the absence of significant competition from perennial
species (e.g., Pigott 1969). In sand culture, growth of
S. europaea and S. ramosissima responds to increasing
nitrate concentration up to at least 1 m (Jefferies 1977).
Addition of inorganic nitrogen and phosphorus to lower
marsh plots on the north Norfolk coast significantly
increased shoot frequency over 5 years but did not have
any effect on higher marsh plots; at the end of the
experiment there was significantly greater Salicornia
biomass in nutrient treated lower-marsh plots, particularly those that had received nitrate (Jefferies & Perkins
1977). Regular additions of nitrate- or ammonium-N
within a single growing season can markedly stimulate
biomass accumulation and, especially, seed production
(Jefferies et al. 1979). Similarly, at the limits of its distribution on the shores of Hudson Bay, seed production
of S. europaea agg. was increased greatly by experimental addition of sodium nitrate (Jefferies et al. 1983).
S. europaea demonstrated the ability to accumulate
nitrogen with increasing external nitrate availability
(Costa 1992). Total concentrations of N in shoots of
S. dolichostachya range from 1.0 to 1.35% (dry mass)
in the field (Pigott 1969) to 6.5% in nitrogen-rich hydroponic culture (Schat et al. 1987).
Induction of flowering
The conditions that promote flowering are poorly
understood. In cultivation, plants typically flower
precociously at a few weeks old, thus terminating
vegetative growth and limiting the capacity for seed
production. Langlois (1968b) suggests that the high
radiant flux densities found in its natural environment are
necessary to prevent precocious flowering. S. europaea
plants from both Britain (Costa 1992) and the Netherlands (Joenje 1978) have shown a minimum threshold
size for successful seed production. This can lead to
oscillatory population dynamics where increasing numbers of individuals fail to reach the threshold size as
density increases or environmental factors limit growth.
Response to shade
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
Growth and branching vary enormously, depending
on population density (especially at low elevation in
marsh zonation, or in early successional sites) and the
presence of other species (especially higher in the
zonation, or in later successional sites). Branching
responses appear to be mediated substantially by light
availability. A computer simulation of the 3-dimensional
branching patterns in S. europaea generated forms that
corresponded well with those found at different stages
in a salt marsh succession, by simultaneously maximizing light interception and minimizing total bending
moment (Ellison & Niklas 1988).
( )
The distinctive violet-red colouration of many
forms of Salicornia is mainly due to the presence
of a betacyanin pigment, betanidin-5-O-[2-O-(β-glucopyranosyl uronic acid)]-β--glucopyranoside
(Chiji 1976). The reddish stems of S. europaea also
contain two 2,3-unsubstituted chromones, identified
as 6,7-methylenedioxychromone and 6,7-dimethoxychromone, respectively (Chiji et al. 1978; Arakawa et al.
1983). Arakawa et al. (1982) determined the structure
of two new isoflavones (2′-hydroxy-6, 7-methylenedioxyisoflavone and 2′, 7-dihydroxy-6-methoxyisoflavone)
and one flavanone (—)-(2S)-2′-hydroxy-6, 7-methylenedioxyflavanone, from S. europaea in Japan. Geslin &
Verbist (1985) found that flavonoids represent 1.2% of
the dry mass of S. europaea and isolated eight flavonoids, of which the most abundant was (malonyl-6″β-glucoside)-3-quercetol. Borkowski & Drost (1965)
identified two distinctive alkaloids from S. europaea
(‘S. herbacea’), salicornin and saliherbin.
Weete et al. (1970) found differences between shoot,
root and seed tissues of S. bigelovii in the relative
distribution of paraffin hydrocarbons (chain lengths
C21 to C33) and total fatty acids (chain lengths C14 to C24);
there were also substantial differences between two
populations in both hydrocarbons and fatty acids.
Salicornia europaea seeds are rich in oil, containing
26–30% total lipids; the di-unsaturated linoleic acid
accounted for 70% of the fatty acid content (Austenfeld
1986, 1988). Seed oil of Salicornia (SOS-7), a form
selected for cultivation as an oil-seed crop, has been analysed in great detail (El-Shami & El-Negoumy 1993;
El-Mallah et al. 1994). Its fatty acid composition is likewise dominated by linoleic acid (66.9%), with 17.5%
oleic acid, only 1.4% linolenic acid and traces of stearic
and palmitic acid; 22 different triglycerides were detected
by HPLC. In common with other members of the
Chenopodiaceae, the photosynthetic tissues of Salicornia
contain a remarkable diversity of sterol biosynthetic
capacity. Eight different 24-α-ethylsterols have been identified, with spinasterol and stigmasterol most abundant;
S. europaea apparently differs from S. bigelovii in lacking isofucosterol (Salt & Adler 1985). According to ElMallah et al. (1994) the seeds of SOS-7 also contain a
range of tocopherols (mainly alpha and gamma), sterols
(mainly 7-stigmastenol and sitosterol) and sterylglycosides (mainly B-sitosterol and campestigmasterol).
Hagène (1958) reported that early in the growing
season, the ascorbic acid content of S. pusilla (‘S. disarticulata’) was consistent at about 250 mg 100 g–1 but
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Salicornia L.
in the autumn the concentration was correlated with
the total hours of sunshine on the day of collection
and the previous two or three days. The cell walls of
S. ramosissima are rich in arabinose, galacturonic acid,
glucose and proteins, and contain 0.7% ferulic acid and
3.8% acetic acid (Renard et al. 1993).
Ion transport within Salicornia at nodes and at
the parting points of lateral roots from the main stem
may be facilitated by acetylcholinesterase activity
(Momonoki et al. 1996). There are several reports
of the distributions of ions and elements in different
tissues and organs of S. europaea agg. (Gorham et al.
1980; Austenfeld 1986).
Nitrogen content depends on the material, its age and
environmental conditions (Langlois & Ungar 1976).
Under various submergence treatments, main stems and
branches of young plants of inland origin (referred to
S. ramosissima) accumulated total N of 3.0 –4.3% (dry
mass), representing 1.8–3.0% as protein N and 1.0–2.1%
as soluble N; corresponding values for S. europaea
(‘S. stricta Dumort.’) of coastal origin were total N
4.7–5.5%, protein N 1.0–4.7% and soluble N 0.4–
4.5%. Mature plants had generally lower nitrogen concentrations. Patterns of serological and electrophoretic
variation in seed proteins (Cristofolini 1968; Cristofolini
& Chiapella 1970) in 13 Italian populations corresponded
neither with each other nor with those for morphology
or geographical and ecological distributions. Schat
et al. (1987) reported total phosphorus concentrations
equivalent to 0.51–0.53% (dry mass) for S. ramosissima
and 0.42– 0.59% for S. dolichostachya.
VII. Phenology
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
The life cycle of Salicornia is typically summer-annual,
although in subtropical environments plants can persist
for more than a year. Germination tends to coincide
with low sediment salinities, in winter in Britain (Smith
1985) and from February to June in Ohio salt pans
(Ungar et al. 1979). The germination period can be
protracted in mild winters: at Stiffkey in Norfolk, seedlings are occasionally found as early as November
but are most abundant from early January to late April.
Characteristically lower-marsh populations, such as
S. dolichostachya and S. europaea, tend to germinate
earlier than upper marsh ones, e.g. S. ramosissima and
S. pusilla (Jefferies et al. 1981; Smith 1985).
Vegetative growth proceeds by the addition of new stem
segments and, except at very high population densities,
lateral branches develop. In lower marsh populations
growth is usually continuous, whereas higher marsh
populations often show slow growth in the period when
hypersaline conditions can occur, when spring tides fail
to cover the marsh surface around the summer solstice.
In late July or August, vegetative growth is terminated
by the production of fertile segments at the ends of
all branches. Benito & Onaindia (1991) found that
the standing crop of S. ramosissima peaked in early
September in a Cantabrian salt marsh (north Spain);
the highest rate of increase in standing live crop was
in July.
In Britain, flowering occurs mainly from mid-August
to mid-September but flowers may be seen from late July
until well into October. Salicornia europaea (‘S. stricta’)type flowers a fortnight earlier than S. ramosissima-type
(Dalby 1955). Populations flower first on the seaward edge
of the marsh at Stiffkey, Norfolk, where S. dolichostachya
flowers earliest; S. pusilla, found characteristically on
the drier, upper interfluves, is the last to flower (Smith
1985). Neotenous flowering of plants has been observed
by Langlois (1968b) in S. europaea (‘S. stricta’) grown
in artificial culture. Seeds reach maturity from midSeptember onwards and fall out of the dead or dying
parent plant although some may remain in situ for
germination the following spring (Ball & Brown
1970).
VIII. Floral and seed characters
( )
Flowers are normally bisexual but plants in the field
or in cultivation may exceptionally have unisexual
flowers as a result of male or female organs failing to
develop (Ferguson 1964b). Some populations are
undoubtedly cleistogamous, their anthers dehiscing
before exsertion, or failing to exsert (e.g. Ball & Tutin
1959). Chasmogamous flowers are usually weakly
protogynous but the stigmas are persistent and often
seen in contact with dehiscing anthers such that self
pollination is easily possible (Knuth, Poll. 3) and is
probably the norm (Dalby 1962; Ferguson 1964b).
Pollen may also fall onto the stigmas of flowers
immediately below on the same plant. Ferguson (1964b)
found that in tetraploid plants resembling S. lutescens
and S. dolichostachya, both in the field and in cultivation, either the stigmas protruded just before the
undehisced anthers were exserted or the anthers and
stigmas emerged together.
The pollen grains are almost spherical, differing from
other chenopodiaceous pollen only in size and details
of sculpturing (Al-Turki 1992). Dalby (1962) detected
large quantities of wind-borne chenopodiaceous pollen
under circumstances where it is reasonable to assume
that it must have come from Salicornia. This indicates
that outbreeding is potentially possible. Pollen grain
diameter in S. europaea is (20–)24–28(–31) µm; in
S. dolichostachya it is (27–)31–34(–42) µm (Ball & Brown
1970). Dalby (1962) recorded smaller pollen-grain
volumes in diploids (2–12 × 1000 µm3) than in tetraploids (6–19 × 1000 µm 3) with the changeover at
c. 10.5 × 1000 µm3 (= 27.2 µm diameter). By mounting
fresh pollen grains in acetocarmine and considering
those which took up the stain deeply to be fertile, 90–
100% of pollen grains were generally found to be fertile,
whether taken from diploid or tetraploid individuals.
Some tetraploid individuals showed exceptionally low
pollen fertility.
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A. J. Davy,
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‘Bagging’ experiments with plants on several British
salt marshes have demonstrated self compatibility,
with only a slight depression of seed-set associated with
enclosure of the shoots in polythene bags (Dalby 1962).
There is no evidence of apomixis. Excision of the stigmas from protogynous flowers of S. europaea resulted
in failure to set seed in 16 flowers out of 17; the single
seed set may have resulted from pollination before
excision of the stigma (Dalby 1962).
Despite a capacity for wind pollination, the floral
biology of Salicornia apparently favours the production
of inbred lines, which may be regarded as microspecies
or locally differentiated populations, with gene exchange
at low frequency between them. Noble et al. (1992)
typed the nuclear rDNA (using RFLP analysis) in 38
maternal plants from Stiffkey in Norfolk and 2112 of
their progeny and found no instance of progeny differing from their maternal type. The method was capable
of discriminating 1% of a different DNA type within
a sample and so any out-breeding must have been at
a lower frequency than 1%. This strong tendency to
inbreeding undoubtedly contributes to the taxonomic
complexity of the group.
( )
Uncertainty regarding the delimitation of species
within Salicornia makes the identification of hybrids
even more uncertain. A putative hybrid S. pusilla ×
S. ramosissima has cymes with different numbers of
flowers (1, 2 or 3) on the same individual (Hyb. Br. Isl.).
Such plants are not uncommon on the higher parts of
the salt marsh at Stiffkey, Norfolk. Four other putative
crosses from British material are listed by Stace (Hyb.
Br. Isl.).
( )
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
A fertile segment produces a maximum of 6 seeds (2
cymes with 3 flowers each), except in S. pusilla, where
only 2 seeds per fertile segment can be produced. The
fecundity of individual plants is strongly and negatively
density-dependent, as it reflects the highly plastic
number and the length of fertile branches produced.
Hence seed production per unit ground area may
remain approximately constant over a 20-fold range
of plant density, or greater. Plants at very high density,
with a single fertile segment, may produce 6 seeds or
fewer; isolated individuals potentially may produce
more than 1000, depending on growth conditions. At
typical field densities (300 –30 000 m–2 mature plants)
between 300 and 10 seeds may be produced on average
per individual (Jefferies et al. 1981; Jensen & Jefferies
1984; Smith 1985; Davy & Smith 1988).
The proportion of flowers that set seed declines at
high density but individual seed mass can increase with
the resulting redistribution of resources (Smith 1985).
Dalby (1962) reported that diploids tend to have smaller
seeds (1–1.8 mm) than tetraploids (1.2–2.7 mm) and
this has been supported by comparisons of particular
taxa: S. ramosissima (‘S. appressa Dumort.’) has smaller
seeds than S. fragilis (‘S. stricta Dumort.’) on the
Normandy coast of France (Binet & Langlois 1962);
S. europaea (‘S. brachystachya Meyer’) has smaller
seeds than S. nitens (‘S. emerici Duval-Jouve’) on the
Mediterranean coast of France (Knoerr 1968) and
S. europaea has smaller seeds (1.0–1.7 mm) than
S. dolichostachya (1.5–2.3 mm) in the Dee Estuary
(Ball & Brown 1970).
Similarly, within cymes the mean mass of central
(median) seeds is greater than that of the lateral ones
(König 1960; Dalby 1962; Ungar 1979). The magnitude
of this seed dimorphism is extremely variable. In a
range of nine populations from the north Norfolk
coast, Smith (1985) found mean masses of central
(median) seeds of 0.25–0.57 mg and corresponding
mean masses of lateral seeds of 0.20 –0.50 mg; only
S. dolichostachya did not have significantly heavier
central seeds. In contrast, Ungar (1979) found that
in North American S. europaea the central seeds
(0.78 ± 0.1 mg) and the lateral ones (0.24 ± 0.4 mg)
did not overlap in mass range. The composition (see
VI F) as well as the concentration of nutrient reserves
is the same in both small, lateral (mean air-dry mass
0.25 ± 0.01 mg) and large, median (mean air-dry
mass 0.31 ± 0.01 mg) seeds of S. europaea (Austenfeld
1988).
Approximately 50% of the seeds fall within 100 mm
of the parent plants (Ellison 1987b) but small, fairly
consistent numbers spread up to 400 mm and a few can
disperse considerable distances (Smith 1985). Rand
(2000) found that numbers of S. europaea seeds caught
by sticky traps correlated well with the sizes of the corresponding germinable seed banks, at sites of different
elevations across a New England salt marsh. Separate
Salicornia seeds have little buoyancy. Hilton (1975)
reported that fresh seeds of S. dolichostachya sank
immediately and air-dried seeds sank within a few
minutes; sinking rates in seawater at 9 °C were 12.5 –
15 mm s–1. Koutstaal et al. (1987) reported that 50% of
Salicornia seeds sank within 2 h and all sank within a
day. Submerged seeds may be rolled along the sediment
surface by tidal currents but are apt to be trapped by
depressions, sessile algae and perennial vegetation
(Brereton 1971; Hilton 1975; Costa 1992). The testa is
covered with mucilaginous and hooked hairs (Fig. 9),
which assist in anchoring the seed to the sediment
surface. Germinating seedlings that do not establish
immediately are buoyed up by the expanding cotyledons
(Petch & Swann 1968) and are likely to be carried away
by tidal currents. Floating seedlings of S. dolichostachya
can remain alive, without further growth, and able to
establish for up to 3 months; this provides a potential for
long-distance transport not afforded by ungerminated,
shed seeds (Hilton 1975). In S. pusilla the disarticulated
fertile segments retain their seeds and may float in sea
water for 3 months (Dalby 1963); they are characteristically deposited on high points and the strand line
699
Salicornia L.
Fig. 9 Germination and seedling development in Salicornia europaea agg. (a) seed, (b) germination, and (c–g) developing
seedling.
where the seeds germinate in situ. The central seeds
of dimorphic S. europaea (S. patula) found in Mediterranean environments are dispersed attached to a
persistent perianth, which also aids buoyancy (Berger
1985). Such floating seeds have also been noted in
Norfolk, UK (Petch & Swann 1968).
( )
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
:
The germinability of Salicornia seeds is generally high:
collections from diverse populations have achieved
90 –100% germination within a few days under laboratory conditions (Langlois 1961b; Smith 1985; Al-Turki
1992). Viability has been reported to be high after several
weeks of dry storage at room temperature (Langlois
1961b; Al-Turki 1992), although this is not a realistic
simulation of over-wintering conditions in British
salt marshes. On salt marshes in north Norfolk
seeds released into the sediment seed bank early in the
autumn tend to be innately dormant. This dormancy
can be broken by up to 5 weeks of chilling at c. 3 °C in
the imbibed state, which promotes both the amount
and rate of germination; seeds released later in the
autumn require less chilling, suggesting that the requirement has been fulfilled partially by declining field
temperatures (Smith 1985). Cold stratification to relieve
seed dormancy has been widely reported in populations
of Salicornia species (Langlois 1966; Grouzis 1973;
Grouzis et al. 1976; Ungar 1977). Air-drying of fresh
seed and pre-treatment with high salinity (equivalent
to seawater) may also break dormancy (Smith 1985;
Huiskes et al. 1985b; Keiffer & Ungar 1997).
Once the requirements for breaking dormancy
have been satisfied, diurnally fluctuating temperature
regimes between 5/15 and 20/30 °C appear to have little
effect on overall germination but germination is faster
at higher temperatures (Huiskes et al. 1985b; Smith
1985; Al-Turki 1992). Continuous low temperatures
inhibit germination (Huiskes et al. 1985b), which leads
to conditional dormancy in the field in winter. Light
appears to stimulate germination, at least in certain
populations of S. dolichostachya (‘S. emerici’), S. pusilla
(‘S. disarticulata’) and S. europaea (‘S. patula’ and
‘S. stricta’) (Langlois 1966; Grouzis et al. 1976; Berger
1985). Salicornia seeds, like those of most halophytes
(Ungar 1978), germinate best at low salinity: Langlois
(1961b, 1966) recorded up to 100% germination in rainwater and Lötschert (1970) reported that S. europaea
(‘S. stricta ssp. typica’) germinated best in pure
water; Grouzis (1973) found progressive inhibition in
S. dolichostachya (‘S. emerici’) with increasing salinity,
starting from c. 8.5 m NaCl; Berger (1985) reported
an optimum salinity of 34 m NaCl in ‘S. patula’,
whereas Huiskes et al. (1985b) and Smith (1985)
independently found very similar germination at 0 and
c. 50 m NaCl in S. europaea and S. dolichostachya.
Although above this concentration increasing salinity
decreased the amount and rate of germination, a proportion of seeds that had been pre-treated for 10 days
at 3 °C in distilled water germinated in solutions of
NaCl up to 1 , about double that of sea water (Smith
1985). Increasing salinity appears to lower the optimum
temperature for germination (Langlois 1966; Rivers &
Weber 1971; Huiskes et al. 1985b). Ungar (1977, 1978)
found that application of 10–4–10–3 gibberellic acid
substantially alleviated the depression of germination
associated with high salinity but kinetin had no effect.
The effect of salinity on germination is a conditional
dormancy, as ungerminated seeds from high salinity
treatments are usually able to germinate when transferred to distilled water (e.g. Smith 1985; Garcia-Tiburcio
& Troyo-Dieguez 1993); as in other halophytes this
reversibility indicates that inhibition is due to low water
potential rather than ion toxicity. Keiffer & Ungar
(1997) found that subsequent germination in distilled
water was stimulated by prolonged exposure to high
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A. J. Davy,
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salinity (3–10% NaCl) in North American material of
S. europaea.
Populations or taxa with well-developed seed dimorphism generally have different germination requirements
for the larger (central) and smaller (lateral) seeds in a
cyme. This probably represents a bet-hedging strategy
that has evolved in less predictable environments, with
readily germinable central seeds and highly dormant
lateral seeds for dispersal in time. The central seeds of
dimorphic S. europaea (‘S. patula’) from a Mediterranean
environment (Camargue) had low sensitivity to salt,
needed no cold pre-treatment and were relatively indifferent to light, whereas lateral ones were highly sensitive
to salinity, needed pre-treatment with cold and showed
a positive response to light (Grouzis et al. 1976; Berger
1985). Similarly, the large seeds of dimorphic S. europaea
from an inland salt marsh in Ohio, USA were more salt
tolerant and yielded higher germination percentages
under salinities of 0–5% than the small ones (Ungar
1979); the small seeds were more dormant and remained
in a persistent seed bank, unlike the large ones which
germinated in the Spring after production (Philipupillai
& Ungar 1984). Smith (1985) found no significant
differences in germination behaviour between central
and lateral seeds in a wide range of populations in the
relatively predictable environment of a north Norfolk
salt marsh, nor in initial rates of elongation of seedling
radicles. Huiskes et al. (1985b) found that seeds of
S. europaea (‘S. brachystachya’) and S. dolichostachya
buried under a layer of sediment of 10 mm germinated
but the seedlings failed to emerge.
Sodium chloride may be important for the establishment of seedlings. NaCl concentrations of 0.1–
0.2 stimulated hypocotyl elongation of S. europaea
(‘S. herbacea’) especially in the dark (Kawasaki et al.
1978). In S. bigelovii seedlings, the cotyledons failed
to expand and growth was impaired, because water
movement into plants was inhibited by lack of inorganic
solutes (Stumpf et al. 1986).
( )
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
The seedling (Fig. 9) normally has two fleshy cotyledons
and a short, thick hypocotyl. Seedlings with three
cotyledons occur regularly at low frequency. The
cotyledons are fused laterally towards the base to form
a cotyledonary tube which is united with the hypocotyl
and forms a succulent ‘cortex’ around it. The cotyledons
have no palisade layer but aqueous tissue is well marked.
The arrangement of vascular strands in the cotyledons
is the same as that described for mature vegetative
segments, the hypocotyl having a double series of
bundles (de Fraine 1912). Transition from stem to root
takes place high in the hypocotyl and is of the van
Tieghem Type III (de Fraine 1912). Seedlings from one
parent plant usually resemble each other closely but
differ from those of other parent plants grown in
similar conditions in cotyledon size and shape, presence or absence of pigmentation (betacyanin) in the
hypocotyl and the number and origin of primary
branches (Dalby 1955).
The lower limit of establishment of Salicornia on salt
marshes often appears to be set by the time necessary
for the seedlings to penetrate the sediment and develop
a ring of root hairs, in order to become fully anchored.
Wiehe (1935) suggested a threshold period of tidal
exposure of 2–3 days for rooting sufficient to resist
tidal action on the low part of an estuarine marsh. The
more rapid radicle growth in S. dolichostachya than in
S. europaea may give the former an establishment
advantage and account for its predominance at the
lowest levels of marshes (Ball & Brown 1970).
IX. Herbivory and disease
( )
Nematoda
Heteroderinae: Cactodera salina Baldwin, MundoOcampo & McClure has adverse effects on oilseed crops
of S. bigelovii at Sonoro, Mexico (Baldwin et al. 1997).
Hemiptera
Miridae: Orthotylus rubidus (Fieber in Puton) can
have two generations on Salicornia that is not regularly
submerged by the tide; the larvae are found June–August
and adults July–October (Southwood & Leston, Land
and Water Bugs).
Cicadellidae: Macrosteles sordidipennis (Stål) [= M.
salinus (Reuter) ] has been found on Salicornia in
France (Ribaut 1952) and has also been recorded in
Britain, although not on Salicornia (Kloet & Hincks
1964).
Lepidoptera
Coleophoridae: Larvae of Coleophora salicorniae
Wocke typically feed on small plants of Salicornia
colonizing well-drained patches in mixed vegetation.
They bore into the tissues, eating the seeds, and then
cut off the stem tip as a case, attaching it to another
stem to continue feeding (Emmet 1979); they have been
recorded generally on S. europaea agg. (Emmet 1980)
and specifically on S. europaea, S. ramosissima and
S. fragilis (Heal 1982, 1983). Females of Coleophora
atriplicis Meyrick oviposit in July on the flowers of
Atriplex portulacoides. The larvae build silk-lined cases
and feed successively on pollen, developing embryos
and seeds until diapause in October or November. In
autumn, they also migrate to adjacent S. ramosissima
plants, where they bore into the seeds and can have
considerable impact on reproductive output (Proudfoot
1993). In Rhode Island (USA) salt marshes, the spring
generation larvae of the bivoltine Coleophora caespititiella Zeller feed on Juncus gerardii, whilst the autumnal
generation feeds on S. europaea, consuming up to 25%
701
Salicornia L.
of the seeds (Ellison 1991). This species has been
recorded in Britain but apparently not on Salicornia
(Emmet 1979).
Gelechiidae: Eggs of Scrobipalpa salinella (Zeller)
have been found on Salicornia in Britain (Emmet
1979) and the larvae feed on S. europaea in central
Europe (Povolny 1980). Povolny also recorded larvae
of Scrobipalpa instabilella (Douglas) and S. nitentella
(Fuchs) on Salicornia europaea, and those of S. obsoletella (Fischer von Roslerstamm) on Salicornia spp.
Coleoptera
Chrysomelidae: Cassida nobilis L. and C. vittata de
Vill. feed on Salicornia spp. ( Walsh & Dibb 1954).
Erynephala maritima Lac. is a significant herbivore
of S. europaea on New England salt marshes (Ellison
1987a; Rand 1999). Larvae of Metachroma sp. have
been reported to kill Salicornia seedlings in the USA
(Stanghellini et al. 1988).
Curculionidae: Baris scolopacea Germar is found
on Salicornia (Walsh & Dibb 1954); Hoffmann (1954)
specified the presence of adults on S. europaea.
Diptera
Cecidomyiidae: Larvae of the gall midge Baldratia
salicorniae Kieffer inhabit the internodes of S. europaea
(Buhr, Gallen). Baldratia jaxarctica Fedotova has
recently been described from S. europaea in Kazakhstan
(Fedotova 1992).
Ephydridae: Clanoneurum cimiciforme (Haliday)
larvae feed on Salicornia (Uffen & Chandler 1978).
Acarina
Eriophyiidae: Eriophyes salicorniae Nalepa larvae
and adults cause witches’ brooms on S. europaea
(Davis et al. 1982).
Aves
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
Twite (Carduelis flavirostris), linnets (C. cannabina)
and shore-larks (Eremophila alpestris) feed on readily
disarticulating spikes of Salicornia (Petch & Swann
1968). Mallard (Ananas platyrhynchos), pintail
(A. acuta), teal (A. crecca), wigeon (A. penelope),
shoveller (Spatula clypea), redshank (Tringa totanus),
chaffinch (Fringilla coelebs) and thrush (Turdus sp.)
are all known to feed on the seeds (Hilton 1975). Brown
& Atkinson (1996) record that Suaeda /Salicornia salt
marshes are amongst the communities most used by
wintering coastal passerines, particularly twite and
skylark (Alauda arvensis). Mature plants of S. europaea
agg. containing seeds form much of the diet of darkbellied brent geese (Branta bernicla bernicla) on the
north Norfolk coast in autumn (Summers et al. 1993).
Rowcliffe et al. (1998) reported a strong aggregative
response to this preferred food. Salicornia europaea on
New England salt marshes is relatively unpalatable to
Canada geese (Branta canadensis), whilst S. bigelovii
has a positive chemical defence mechanism, including
a pungent odour, against being eaten by this species
(Buchsbaum et al. 1984); in S. europaea there is an
increase in the percentage of phenolic substances,
thought to render the plants unpalatable to Canada geese,
from May to September (Buchsbaum & Valiela 1987).
Mammalia
Testas of Salicornia seeds have been reported in the
faecal pellets of rabbits (Oryctolagus cuniculus) on a salt
marsh; yellow-necked fieldmice (Apodemus flavicollis)
sought out and consumed stored seed in preference to
potatoes, carrots and apples (Hilton 1975).
Domestic animals and Man
Salicornia bigelovii has been grown as an oil-seed and
forage crop in arid environments, as it may be irrigated
with seawater or other saline waters. It can yield 10 –20
t ha–1 of seed, containing 28% oil and 31% protein
with only 5–7% fibre and ash (Glenn et al. 1991, 1999).
It is acceptable as the forage component of diets fed to
goats (Glenn et al. 1992) and a by-product of oil extraction, Salicornia meal, may be used as an ingredient in
broiler chicken diets (Attia et al. 1997).
Salicornia has a long history of human consumption
as a vegetable and in pickles (Chevalier 1922). In Britain
it has long been collected as samphire for eating.
( )
Booth et al. (1988) provide a review of fungal records,
world-wide, on Salicornia europaea agg. and a detailed
analysis of fungal assemblages on populations in
sulphate-dominated, alkaline lakes in Manitoba and
Saskatchewan, Canada. Sixty-five species of fungi
have been reported from its rhizosphere and 80 taxa
from the root and stem surfaces, seeds, moribund plants
and dead material. Except where otherwise attributed,
the following summary is from this source. Rhizosphere
fungi are not included.
Zygomycotina
Mucorales: Mortierella (1 sp.), Mucor (1 sp.).
Ascomycotina
Chaetomium (1 sp.), Didymosphaeria (1 sp.), Hypoxylon
(1 sp.), Leptosphaeria (1 sp.), Mycosphaerella (1 sp.),
Pleospora (8 spp.), Protomyces (1 sp.).
Basidiomycotina
In Britain, the rust Uromyces salicorniae de Bary is
found uncommonly on leaves and stems of S. europaea
702
A. J. Davy,
G. F. Bishop &
C. S. B. Costa
and S. ramosissima; aecia are mostly on young plants in
May (Ellis & Ellis 1985).
Deuteromycotina
Stagnosporopsis salicorniae (P. Magnus) Died. occurs
on lower part of stems of S. europaea in July; scattered
pycnidia are visible (Ellis & Ellis 1985). Records from
Booth et al. (1988): Acremonium (7 spp.), Alternaria
(9 spp.), Arthrinium (1 sp.), Ascochyta (2 spp.),
Aspergillus (1 sp.), Aureobasidium (1 sp.), Botrytis (1
sp.), Camarosporium (3 spp.), Cladosporium (4 spp.),
Coniella (1 sp.), Coniothyrium (1 sp.), Dendryphiella
(2 spp.), Diplodina (1 sp.), Doratomyces (1 sp.),
Drechslera (2 spp.), Epicoccum (1 sp.), Fusarium (4
spp.), Gliocladium (1 sp.), Gliomastix (1 sp.), Monodictys (1 sp.), Papulaspora (1 sp.), Penicillium spp.,
Phoma (2 spp.), Phomopsis (1 sp.), Scopulariopsis (1
sp.), Scytalidium (1 sp.), Septoria (1 sp.), Stagonospora
(1 sp.), Stemphylium (3 spp.), Trichocladium (1 sp.),
Trichoderma (2 spp.), Tubercularia (1 sp.).
An indigenous, Mexican, soil-borne fungus,
Macrophomina phaseolina, infects roots and causes
mortality in S. bigelovii (Stanghellini et al. 1992).
( )
See (B) above.
X. History
Salicornia is recorded from Flandrian deposits of the
East Anglian Fenland. At Littleport, where it is accompanied by Suaeda maritima, it is in deposits close to the
margin of the Fen Clay that were laid down in a marine
transgression culminating about 2000 . At Saddlebow it has been found in deposits from the subsequent
marine transgression in Roman times (Godw. Hist.).
The vernacular name ‘samphire’ is derived from
‘sampere’, an early English name from the French
‘herbe de St. Pierre’ (Wilson 1980). The common name
‘glasswort’ arose from the use of its soda-rich ashes in
early glass making. William Turner’s Herball (part iii)
refers to it as ‘saltwurt’ and ‘glaswede’ in 1568; the
name Salicornia originates from the ‘Pemptades’ of
Dodonaeus in 1583 (First Rec.). Linnaeus described
the genus Salicornia (Species Plantarum edn 2, 1763) to
include all succulent and apparently leafless chenopodiaceous plants. Scott (1977) has provided an historical
survey of subsequent taxonomic revisions resulting in
its restriction to annual species. Pioneering taxonomic
work on Salicornia was undertaken by Woods (1851),
Dumortier (1868), Duval-Jouve (1868) and Moss
(1911, 1912).
© 2001 British
Ecological Society,
Journal of Ecology,
89, 681–707
given legal status and protection as ‘Special Areas of
Conservation’ under a Habitats Directive of the
European Union.
XI. Conservation
British and other European habitats supporting
low marsh and mud-flat stands of Salicornia have been
Acknowledgements
We thank Mrs J. M. Croft and Dr C. D. Preston for preparing the British distribution maps and Dr L. K. Ward
for information from the ITE (now, Centre for Ecology
and Hydrology) Phytophagous Insects Data Bank.
Dr I. Teräs, the Committee for Mapping the Flora of
Europe and Societas Biologica Fennica Vanamo kindly
allowed reproduction of the European distribution
maps. We are grateful to James Goodwin for the
excellent drawings of seedlings (Fig. 9). Paul Adam,
Bob Jefferies, Michael Proctor and Arthur Willis all
provided valuable comments and information.
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