Mangroves: Obligate or facultative halophytes? A review

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DOI: 10.1007/s00468-011-0570-x
Abstract
Salinity plays significant roles in regulating the growth and distribution of mangroves, and the salt tolerance mechanisms of mangroves have been the focus of research for several decades. There are contradictory views regarding the relationship between mangroves and salt: (1) Mangroves are facultative halophytes, i.e. freshwater is a physiological requirement and salt water is an ecological requirement for mangroves because they are capable of growing in freshwater. The former prevents excess respiratory losses while the latter prevents invasion and competition from non-halophytes. (2) Mangroves are obligate halophytes, i.e. salt is necessary for their growth. Mangroves cannot survive in freshwater permanently and salt water is a physiological requirement. Up to now, mangroves are usually considered as facultative halophytes. In this review, we provided five lines of evidence to evaluate these two contradictory views: (1) the results of laboratory culture experiments and field investigations; (2) the viviparous nature of mangroves; (3) the salt accumulation of mangroves under freshwater or low salinity; (4) the effect of salinity on the photosynthetic rate and in vitro enzyme activities, and (5) the effects of salinity fluctuation on mangrove growth and physiology. Contrary to widely accepted view, our evaluations of the aforementioned evidence suggest that mangroves are obligate halophytes. Mangroves can grow in freshwater for a limited time by drawing upon the nutrients and salt reserves in their hypocotyls while prolonged culture in freshwater is fatal to them. Mangroves have the ability to absorb Na+ and Cl− rapidly and preferentially under low-salinity conditions. Not all of the enzymes in mangroves are sensitive to salt. In fact, the activities of some enzymes are even stimulated by low or moderate salinity. Plants grown under constant salinity in a laboratory setting are unlikely to behave in the same way as those in their natural habitat with fluctuating salinity. Thus, studies on the effects of freshwater or low salinity and salinity fluctuation on mangroves, as well as the physiological mechanisms that allow maintenance of function under fluctuating salinity conditions should be strengthened in future research.
REVIEW
Mangroves: obligate or facultative halophytes? A review
Wenqing Wang
Zhongzheng Yan
Siyang You
Yihui Zhang
Luzhen Chen
Guanghui Lin
Received: 5 July 2010 / Revised: 15 April 2011 / Accepted: 20 April 2011 / Published online: 7 May 2011
Ó Springer-Verlag 2011
Abstract Salinity plays significant roles in regulating the
growth and distribution of mangroves, and the salt toler-
ance mechanisms of mangroves have been the focus of
research for several decades. There are contradictory views
regarding the relationship between mangroves and salt: (1)
Mangroves are facultative halophytes, i.e. freshwater is a
physiological requirement and salt water is an ecological
requirement for mangroves because they are capable of
growing in freshwater. The former prevents excess respi-
ratory losses while the latter prevents invasion and com-
petition from non-halophytes. (2) Mangroves are obligate
halophytes, i.e. salt is necessary for their growth. Man-
groves cannot survive in freshwater permanently and salt
water is a physiological requirement. Up to now, man-
groves are usually considered as facultative halophytes. In
this review, we provided five lines of evidence to evaluate
these two contradictory views: (1) the results of laboratory
culture experiments and field investigations; (2) the
viviparous nature of mangroves; (3) the salt accumulation
of mangroves under freshwater or low salinity; (4) the
effect of salinity on the photosynthetic rate and in vitro
enzyme activities, and (5) the effects of salinity fluctuation
on mangrove growth and physiology. Contrary to widely
accepted view, our evaluations of the aforementioned
evidence suggest that mangroves are obligate halophytes.
Mangroves can grow in freshwater for a limited time by
drawing upon the nutrients and salt reserves in their
hypocotyls while prolonged culture in freshwater is fatal to
them. Mangroves have the ability to absorb Na
?
and Cl
-
rapidly and preferentially under low-salinity conditions.
Not all of the enzymes in mangroves are sensitive to salt. In
fact, the activities of some enzymes are even stimulated by
low or moderate salinity. Plants grown under constant
salinity in a laboratory setting are unlikely to behave in the
same way as those in their natural habitat with fluctuating
salinity. Thus, studies on the effects of freshwater or low
salinity and salinity fluctuation on mangroves, as well as
the physiological mechanisms that allow maintenance of
function under fluctuating salinity conditions should be
strengthened in future research.
Keywords Mangrove Salinity Facultative halophyte
Obligate halophyte Vivipary Growth Photosynthesis
Osmotic regulation Enzyme Succulence Salinity
fluctuation
Introduction
Salinity has long been recognised as a vital factor regu-
lating growth and distribution of mangroves (Lugo and
Snedaker 1974; Bunt et al. 1982; Ball 1988a, b; Ukpong
1991; Jayatissa et al. 2008). Generally, mangroves are
Communicated by C. Lovelock.
W. Wang S. You Y. Zhang L. Chen G. Lin
Key Laboratory of the Ministry of Education for Coastal
and Wetland Ecosystems, School of Life Sciences, Xiamen
University, Xiamen 361005, Fujian, China
W. Wang
Australian Rivers Institute, Griffith University, Gold Coast,
QLD 4222, Australia
W. Wang (&) Y. Zhang L. Chen G. Lin
Key Laboratory of Marine and Environment, Xiamen University,
Xiamen 361005, Fujian, China
e-mail: mangroves@xmu.edu.cn
Z. Yan
Department of Biology and Chemistry, City University
of Hong Kong, Hong Kong, China
123
Trees (2011) 25:953–963
DOI 10.1007/s00468-011-0570-x
categorised as ‘exclusive’ species that are limited to the
mangrove habitat (referred as obligate mangroves or true
mangroves) and ‘nonexclusive’ species that occur in ter-
restrial or aquatic habitats as well as in the mangrove
habitat (referred as semi-mangroves or mangrove associ-
ates) (Tomlinson 1986; Lacerda et al. 2002). There are two
contradictory views regarding why true mangroves are
restricted to the mangrove habitat: (1) Mangroves are
facultative halophytes, i.e. salt is not required for their
growth (Chapman 1975; Field 1984; Mitsch and Gosselink
2000; Mohammadizadeh et al. 2009). Freshwater is a
physiological requirement while salt water is an ecological
requirement (Saenger 2002). The former prevents excess
respiratory losses and the latter prevents invasion and
competition from non-halophytes. Since they are capable
of growing in freshwater areas, salt is not a physiological
requirement for their development (Bowman 1917; Egler
1948; Stern and Voigt 1959; Chapman 1975; van Steenis
1984; Taylor 1986; Nybakken 1993; Mohammadizadeh
et al. 2009). Mangroves cannot develop in strictly fresh-
water communities because of competition for space from
freshwater vascular plants and because mangroves have a
competitive advantage over other plants in saltwater areas
(Simberloff 1983; Tomlinson 1986); (2) Mangroves are
obligate halophytes, i.e. salt is required for their growth
(Lugo and Snedaker 1974). Mangroves cannot grow in
permanent freshwater, and salt is a physiological
requirement.
The issue whether mangroves are obligate or facultative
halophytes is a controversial. Although Benecke and
Arnold (1931) discussed this as early as in 1931, scientists
still have not yet reached a consensus. It is generally
believed that mangroves are facultative halophytes (Beard
1955; Galloway 1982; Lugo et al. 1989; Jensen et al. 1991;
Clough 1992; Nybakken 1993; Smith and Snedaker 1995;
Atreya et al. 2009; Hao et al. 2009; Mohammadizadeh
et al. 2009). However, this view can only explain part of
the existing experimental findings and is also challenged by
the results of some recent findings.
Although Hogarth (2007) declared that it is impossible
to provide a general idea about salt tolerance of mangroves
because of large variations in salt tolerance among species,
there is still a need to integrate the numerous data into a
more general picture of the salt-tolerant nature of man-
groves which will make the research results widely avail-
able to resource managers and mangrove rehabilitation
(Aziz and Khan 2001a; Jayatissa et al. 2008). In this
review, we provided five lines of evidence to evaluate these
two contradictory views: (1) the results of laboratory cul-
ture experiments and field investigations, (2) the viviparous
nature of mangroves, (3) the salt accumulation of man-
groves under freshwater or low salinity, (4) the effect of
salinity on the photosynthetic rate and in vitro enzyme
activities, and (5) the effects of salinity fluctuations on
mangrove growth and physiology. We also provide some
suggestions for future studies in this field. To avoid con-
fusion, the mangroves we discuss in this paper only include
true mangrove from the genera Kandelia, Bruguiera,
Ceriops, Rhizohora, Avicennia, Sonneratia, Lumnitzera,
Laguncularia and Aegiceras, which dominate the majority
of mangrove forests globally.
Relations between salt and mangrove
Laboratory experiments and field investigation
The growth of plants under salt stress is a sensitive indi-
cator of salt tolerance (Hagemeyer 1997). Our under-
standing on mangrove salt tolerance mainly stems from
laboratory culture experiments. In general, growth response
to salinity has been used to identify a plant as either a
facultative or obligate halophyte (Ungar 1978; Mitsch and
Gosselink 2000). Facultative halophytes can grow in saline
environments, but their optimum growth usually occurs in
salt-free or low-salinity environment. They do not require
salt water for survival but are able to tolerate high salinity
(Mitsch and Gosselink 2000). Obligate halophytes are
defined as plants with optimal growth at moderate or high
salinity and that are incapable of growth at low salinity or
in freshwater (Ungar 1978; Mitsch and Gosselink 2000;
Sabovljevic
´
and Sabovljevic
´
2007).
Laboratory culture experiments with seedlings (less than
2 years old) showed that mangroves differ greatly in their
extent of salt tolerance (Tomlinson 1986; Ye et al. 2005;
Hogarth 2007; Krauss et al. 2008). The classic growth
response of most mangroves to increasing salt concentra-
tion in the soil is similar to that shown for nutrients, with
variation in the shape of the response curve reflecting
concentrations which are deficient, saturating and toxic to
growth (Clough 1992; Ball 2002; Krauss et al. 2008)
(Table 1). There is ample evidence for a nonobligatory
relationship between mangroves and salt. Avicennia ger-
minans can root in distilled water and grows well in
freshwater conditions (McMillan 1971). Bruguiera cyl-
indrica seedlings grow normally in soils irrigated with
freshwater (Atreya et al. 2009). Bruguiera gymnorhiza can
be cultivated in freshwater tanks for more than a decade
(Ng and Sivasothi 2002). In botanical gardens, Bruguiera
and Rhizophora could grow and flower regularly in pots of
sand irrigated only with freshwater (Lear and Turner 1977).
Results from half (13 out of 26) of the laboratory culture
experiments in Table 1 suggest that mangroves can grow
well in freshwater for an extended period of time.
Field observations also indicate that some mangroves
can grow normally in freshwater. In northern Irian Jaya,
954 Trees (2011) 25:953–963
123
van Steenis (1963) reported that the mangrove Sonneratia
caseolaris could grow at a freshwater lake around 75 m
above sea level. van Steenis (1984) also found a unique
stand of mangroves (Bruguiera gymnorhiza) on the eastern
shore terrace of Christmas Island located 120 m inland
with elevation of 24–37 m above sea level. The presence of
large Bruguiera gymnorhiza individuals and numerous
seedlings and samplings there indicates that Bruguiera
gymnorhiza can grow well in freshwater with normal
regeneration (Woodroffe 1988). Bruguiera sexangula was
also found growing in an inland freshwater stream at the
Bogor Botanic Gardens in Java for more than 100 years
(Ng and Sivasothi 2002).
However, there are also numerous studies in literature
showing that mangroves cannot grow vigorously in fresh-
water for an extended period of time. The absence of NaCl
initially accelerated the development of Avicennia marina,
but shoot growth and biomass production soon slowed
Table 1 Summary of selected laboratory culture experiments on the effects of salinity on the growth of mangroves
Species Material Culture time Optimum growth
salinity (psu)
Growth appearance
under freshwater
References
Aegiceras corniculatum Fruit 11 months 8.8 Normal Burchett et al. (1989)
Aegiceras corniculatum Fruit 3 months 0.0 Normal Ye et al. (2005)
Aegiceras corniculatum Fruit 3 months 7.0 Poor Clarke and Hannon (1970)
Avicennia marina Fruit precultivated in 25%
seawater for 4 weeks
11 months 8.8 Necrotic lesions
appeared on the stem,
leaves, and growing
points
Clough (1984)
Avicennia marina Seedling germinated on
deionised water
1–2 months 17.5 Connor (1969)
Avicennia marina Seedlings collected from
the field or germinated on
25% seawater
3 months 7.0–14.0 Poor Clarke and Hannon (1970)
Avicennia marina Fruit 100 days 17.5 Poor Yan et al. (2007)
Avicennia marina Fruit 11 months 8.8–17.5 Development of lesions
on leaves and growing
points, leaves dropped
and buds withered
Downton (1982)
Avicennia marina Fruit precultivated in 25%
seawater for 6–8 weeks
6 weeks 8.8 Normal Burchett et al. (1984)
Avicennia marina Fruit 6 months 17.5 Normal Khan and Aziz (2001)
Avicennia marina Fruit 3 months 5.0 Normal Ye et al. (2005)
Avicennia germinans Fruit 27 weeks 10.0 Normal Sua
´
rez and Medina (2005)
Bruguiera gymnorhiza Hypocotyl 40 days 10.0–20.0 Normal Zhang et al. (2004)
Bruguiera gymnorhiza Hypocotyl 4 months 7.3 Normal Takemura et al. (2000)
Bruguiera parviflora Hypocotyl precultivated in
tap water for 2 months
45 days 5.8 Normal Parida et al. (2004)
Ceriops australis Hypocotyl 12 weeks 8.8–17.5 Poor Ball (2002)
Ceriops decandra Hypocotyl 12 weeks 8.8 Poor Ball (2002)
Ceriops tagal Hypocotyl 6–12 months 17.5 Normal Aziz and Khan (2001a)
Kandelia candel Hypocotyl 4 months 5.0 Normal Hwang and Chen (1995)
Rhizophora apiculata Seedlings collected from
the field
1–3 months 26.3 Normal Manikandan et al. (2009)
Rhizophora mangle Hypocotyl precultivated in
freshwater for 9 months
11 months 11.7 Gradually died off Werner and Stelzer (1990)
Rhizophora mucronata Hypocotyl 6 months 17.5 Normal Aziz and Khan (2001b)
Rhizophora stylosa Hypocotyl precultivated in
25% seawater for 4 weeks
11 months 8.8 Poor Clough (1984)
Rhizophora stylosa Hypocotyl 6 months 17.5 Poor Khan and Aziz (2001)
Sonneratia alba 12 weeks 17.5 Ball and Pidsley (1995)
Sonneratia lanceolata 12 weeks 0–1.8 Ball and Pidsley (1995)
Trees (2011) 25:953–963 955
123
down and became negligible (Downton 1982; Clough
1984). The absence of NaCl was also associated with the
development of lesions on leaves and growing points of
Avicennia marina seedlings (Downton 1982). The overall
growth of Avicennia marina seedlings cultivated in fresh-
water was even less than that in 100% seawater (35 psu)
(Downton 1982; Clough 1984). Werner and Stelzer (1990)
precultivated propagules of Rhizophora mangle in a
greenhouse for 9 months before transplanting the seedlings
into nutrient solutions without salt and with 200 mM NaCl.
Growth of the salt-treated seedlings increased significantly,
while the seedlings under control died gradually (Werner
and Stelzer 1990). Ceriops decandra and Sonneratia alba
grew poorly in freshwater, and Bruguiera paviflora and
Ceriops tagal propagules even failed to grow in freshwater.
However, addition of as little as 5% seawater to culture
solution promoted vigorous growth of these species
(Bridgewater 1982; Hutchings and Saenger 1987). Similar
results have also been reported for other species, including
Avicennia officinalis (Teas 1977, 1979), Rhizophora man-
gle (Werner and Stelzer 1990) and Sonneratia alba (Ball
and Pidsley 1995). Ball (2002) argued that it was doubtful
whether Ceriops australis and Ceriops decandra could
grow to maturity in freshwater. Clough (1992) also indi-
cated that it is not clear whether the optimal salinity range
for seedling growth was the same as that for saplings and
mature trees. Thus, long-term studies are needed to monitor
the effects of salinity on the growth of mangroves (Biber
2006).
As mentioned above, some field observations showed
that mangroves could grow normally for a long time in
freshwater habitats (van Steenis 1984; Woodroffe 1988;Ng
and Sivasothi 2002). However, there is still no answer why
these mangroves have a competitive advantage over other
co-existing freshwater vascular plants nearby. What may
have been previously ignored is that the coastal plants on
the crest of steep ocean boundaries are not influenced by
tides but salt spray (Boyce 1954; Orcutt and Nilsen 2000).
Leaves of the plants grow in those habitats can accumulate
salts from salt spray (Boyce 1954; Orcutt and Nilsen 2000).
Leaf surface salt deposition has been reported for the
mangroves influenced by tides (Smith et al. 1989; Griffiths
et al. 2008). Based on the topographic analysis of Christ-
mas Island, Woodroffe (1988) suggested that the man-
groves in this island must be influenced by heavy salt
spray. Reports regarding the degree of salt spray on the
other mangrove leaves at other sites are not available.
Viviparous reproductive strategy
It is generally accepted that the seedling stage is the most
sensitive stage in growth and development of halophytes
(Ungar 1982, 1991; Vicente et al. 2004; Manikandan et al.
2009). Woody plants are usually relatively salt tolerant
during seed germination, turn to be much more sensitive
during the seedling stage, and become progressively more
tolerant with age through to the reproductive stage (Shan-
non et al. 1994) (Fig. 1). However, for viviparous man-
groves (particularly Bruguiera, Ceriops, Kandelia and
Rhizophora), their seedling stage (from mature hypocotyl
to a seedling with a few pairs of leaves) is the stage of
higher salt tolerance (Fig. 1). This is because these species
have larger propagules that store large amounts of nutrient
and energy (Tomlinson 1986; Ball 2002; Yan et al. 2007).
In mangroves, vivipary and cryptovivipary reproductive
strategies result in considerable parental nutrients and
energy investment for their seedlings (Tomlinson 1986;Ye
et al. 2005; Hogarth 2007; Yan et al. 2007). This invest-
ment provides the seedlings with ample nutrients and
energy to support their early growth under nutrient-poor or
salt-stressed conditions (Farrant et al. 1992; Milberg and
Lamont 1997; Wang et al. 2002; Bezerra et al. 2007; Yan
et al. 2007; Krauss et al. 2008). In addition to the nutrients
and energy reserves in hypocotyls, mangrove hypocotyls
contain large amounts of Na
?
and Cl
-
(Downton 1982;
Bhosale and Shinde 1983; Clough 1984; Wang et al. 2002).
Even growing in freshwater for a few months, mangrove
seedlings still maintain high levels of Na
?
and Cl
-
in their
tissues (Atkinson et al. 1967; Downton 1982; Clough 1984;
Ball et al. 1987; Naidoo 1987; Werner and Stelzer 1990;
Ger. See. Sap. Mat. Ger. See. Sap. Mat.
Relative salt tolerance
Relative salt tolerance
Non-viviparous plants Viviparous mangroves
Fig. 1 Hypothetical change in
relative salt tolerance during
different development stage of
non-viviparous pants and
viviparous mangroves. Ger,
germination; See, seedling; Sap,
sapling; Mat, Maturity
956 Trees (2011) 25:953–963
123
Aziz and Khan 2001a; Hwang and Chen 2001; Ye et al.
2005; Manikandan et al. 2009). For example, the salt
concentration in the leaf tissue of Avicennia marina and
Aegiceras corniculatum seedlings cultured in freshwater
for 90 days was about 2% (Ye et al. 2005). The concen-
trations of Na
?
and Cl
-
in the leaves and hypocotyls of
Rhizophora stylosa seedlings cultured in freshwater for
11 months were both greater than 100 mM (Clough 1984).
The viviparous nature of many mangrove species provides
their seedlings with the ability to grow in high or low
salinity or even in freshwater for an extended period (Ball
1988b, 2002; Hwang and Chen 1995; Wang and Lin 1999).
McMillan (1971) reported that Avicennia marina seed-
lings were able to root in distilled water. However, pro-
longed exposure of mangrove seedlings to freshwater will
result in nutrient depletion (Wang and Lin 1999; Yan et al.
2007). Once the seedlings become mature and the reserves
are depleted, the seedlings that develop predominantly at
the expense of hypocotyl reserves may not have sufficient
resources to compete effectively with fully autotrophic
seedlings (Ball 1988b, 2002; Yan et al. 2007). The Na
?
concentrations in the leaves and stems of Kandelia candel
seedlings cultured in NaCl-deficient solution decreased
over time (Hwang and Chen 1995). In freshwater, the early
seedling development of Avicennia marina was fastest in
the absence of NaCl, but shoots growth and biomass pro-
duction soon slowed and then became negligible (Downton
1982; Clough 1984; Ghowail et al. 1993). To reduce or
eliminate complications arising from involvement of
hypocotyl reserves, Werner and Stelzer (1990) used Rhi-
zophora mangle seedlings that had been precultivated in
freshwater for 9 months, and found that the seedlings died
gradually after growing in freshwater for another
11 months. These results indicate that the response of
mangrove seedling growth to salinity varies with the stage
at which salt stress is initiated (Vicente et al. 2004).
Our current understanding of the salt tolerance of
mangroves is mainly based on short-term growth experi-
ments with seedlings during periods varying from a few
weeks to several months (Table 1). Such a short period
does not take into account the early, rapid, but short-lived
growth of seedlings on salt-free media (Downton 1982).
The presence of propagule reserves may cause the results
to differ considerably from those of older seedlings
dependent on autotrophic growth (Tomlinson 1986; Ball
2002).
This has been overlooked in many reports. Thus, when
describing the salt tolerance of mangroves, the stage of
development being tested must be defined carefully (Ungar
1991). To eliminate the complications arising from the
presence of hypocotyl reserves, the use of growth as a
parameter to measure salinity stress is necessary for long-
term studies to achieve meaningful results (Biber 2006).
The callus or cell culture approach is an effective way to
study salt tolerance at the cellar or tissue levels (Mimura
et al. 1997a; Kawana and Sasamoto 2008; Hayashi et al.
2009). Another advantage of this approach is that it elim-
inates the effects of hypocotyl reserves. Salt-stimulated
growth was also shown in callus or cell culture experi-
ments. As examples, the growth rate of calluses of Bru-
guiera sexangula was the highest in the medium containing
100 mM NaCl (Mimura et al. 1997a, b). Akatsu et al.
(1996), and Yasumoto et al. (1999) cultivated the calluses
of the non-viviparous mangrove Sonneratia alba on solid
Murashige and Skoog medium supplemented with NaCl,
and the maximum growth was observed at 50 mM NaCl.
Similar results were also observed in suspension-cultured
Sonneratia alba and Avicennia alba cells (Kawana and
Sasamoto 2008; Hayashi et al. 2009). Because the culture
medium contained 3 mM NaCl, no fatal effects were
detected in the control (Mimura et al. 1997a, b; Kawana
and Sasamoto 2008).
Physiology
Increasing salt-tolerance appears to occur at the expense of
growth and competitive abilities under low salinity (Ball
and Pidsley 1995). The measurement of leaf stomatal
conductance and chlorophyll fluorescence, two important
physiological parameters used to assess photosynthetic
function, are regarded as rapid and reliable substitutes as
parameters to measure salt tolerance (Krause and Weis
1991; Govindjee 1995; Biber 2006; Manikandan et al.
2009). Reductions in photosynthetic gas exchange rates
(measured by leaf photosynthetic gas exchange) on an area
basis, PSII efficiency and electron transport rate in man-
groves subjected to salinity have been widely reported and
thus mangroves are interpreted as giving support to the idea
that mangroves are facultative halophytes (Sobrado 2005;
Biber 2006; Li et al. 2008; Manikandan et al. 2009).
However, growth is a combined effect of the effective
photosynthetic area and photosynthetic rate on an area
basis (Kriedemann 1986). The specific influence of salinity
on photosynthesis alone cannot explain all the changes in
growth (Orcutt and Nilsen 2000). Salt stress has an effect
not only on photosynthetic rate, but also on photosynthetic
leaf area. Lower or moderate salinity stimulates leaf
growth (Clough 1984; Burchett et al. 1989; Werner and
Stelzer 1990; Wang and Lin 1999; Yan et al. 2007).
Although there were no differences in the photosynthetic
rates observed between the control and salt treatments, leaf
area per plant and also the net carbon assimilation per plant
increased (Aziz and Khan 2001a, b;Ball2002; Parida et al.
2004; Yan et al. 2007). This finding partially explains why
some halophytes grow better under moderate salinity
conditions than in freshwater. Stem, leaf and root growth of
Trees (2011) 25:953–963 957
123
Rhizophora mangle seedlings were significantly enhanced
in low salinity (Smith et al. 1996). A study on another
mangrove, Bruguiera gymnorhiza, indicated that leaf area,
leaf mass per plant and relative leaf longevity all increased
with increasing salinity (Wang and Lin 1999). Stimulation
of leaf growth was also observed in Ceriops australis and
Ceriops decandra growing under 5–75% seawater (Ball
2002). Prolonged exposure to freshwater results in smaller
leaf size, and shorter leaf longevity, subsequently resulting
in a smaller active photosynthetic area than that observed
for plants growing in low or moderate salinity environ-
ments (Clough 1984; Burchett et al. 1989; Werner and
Stelzer 1990; Wang and Lin 1999; Yan et al. 2007). Clough
(1984) recorded that leaf development was inhibited and
leaf numbers and sizes in Avicennia marina and Rhizo-
phora stylosa were reduced in freshwater compared with
those plants grown in 25, 50 and 75% seawater. Similar
results were also found by Pezeshki et al. (1990). Indeed,
changes in rates of leaf area expansion with increasing
salinity have been considered the major cause of change in
the growth of several plant species (Rawson and Munns
1984). It would be incorrect to assume that the growth rate
decreases solely because of a decrease in the photosyn-
thetic capacity (Ball 1988a, b).
It is generally recognised that salinity inhibits the in
vitro activity of enzymes and the metabolic processes of
mangroves. Mangrove enzymes are as sensitive to salts as
non-halophyte enzymes (Flowers et al. 1977; Ball and
Anderson 1986;Lu
¨
ttge 1997; Larcher 2001). To protect
enzymes from the negative effects of high salt concentra-
tions, Na
?
and Cl
-
are sequestered in vacuoles and the salt
concentrations in non-vascular regions were reduced (i.e.
cytoplasm and chloroplasts) (Shannon et al. 1994; Koz-
lowski 1997). The in vitro sensitiveness of mangrove
enzymes to salinity was interpreted as biochemical evi-
dence that mangroves are facultative halophytes (Hogarth
2007). However, this argument is challenged by recent
findings. The isolated superoxidate dismutase (SOD) from
Bruguiera gymnorhiza leaves were not affected by
1000 mM NaCl in the measurement system, and catalase
kept high activity under 500 mM NaCl in the measurement
system (Takemura et al. 2000). In contrast, SOD and cat-
alase from some glycophytes were both sensitive to NaCl.
In Vigna unguiculata, mitochondrial Mn-SOD was signif-
icantly decreased by 35 mM (up to 35%) and 100 mM
NaCl (up to 60%) (Herna
´
ndez et al. 1994). In Phaseolaris
vulgaris, leaf catalase activity was reduced more than 50%
with NaCl doses higher than 150 mM, whereas in Medi-
cago sativa this inhibition occurred with doses higher than
25 mM (Garcı
´
a et al. 2007). These results indicate that
some enzymes of mangrove may be less sensitive to salt
than those of glycophytes. Increases of enzyme activity by
adding 50 mM NaCl into measurement systems were also
reported even in non-halophyte (Phaseolus vulgaris) and in
halophytes (Atriplex spongiosa and Salicornia australis)
(Greenway and Osmond 1972). Further research is neces-
sary to confirm whether mangrove enzymes are less sen-
sitive to NaCl than glycophytes and if this is a general
phenomenon or restricted to enzymes in particular
organelles.
Na
?
and Cl
-
requirements
Although numerous reports have documented the necessity
of Na
?
and Cl
-
for mangrove growth, the molecular and
physiological bases of growth inhibition in the absence of
Na
?
and Cl
-
are not well known for mangroves (Ball
2002). A recent study showed that Cl
-
was required for
proper functioning of the catalytic centre of PSII to cata-
lyse the oxidation of water to dioxygen (Ferreira et al.
2004). Cl
-
was also shown essential for the optimal oxy-
gen-evolving activity of PSII (Roose et al. 2007). Thy-
lakoids from Avicennia marina leaves require high levels
of Cl
-
for photosynthetic electron transport around PSII
(Critchley 1982) and are much more resistant to salt than
thylakoids from glycophytes (Critchley 1982, 1983). The in
vitro effect of Cl
-
on photosynthetic electron transport in
mangrove thylakoids was explained as a physiological
requirement for high levels of Cl
-
(Critchley 1982).
However, no further reports showed that mangroves have
higher salt requirements for fundamental photosynthetic
processes. In addition to its role in osmotic regulation, a
metabolic involvement of Na
?
has been proposed to
explain its requirement for growth (Maggio et al. 2000).
Mangroves show a greater ability to accumulate Na
?
and Cl
-
under low salinity or freshwater than do glyco-
phytes (Downton 1982; Hwang and Chen 1995; Patel and
Pandey 2009). Even when only traces of NaCl were present
in the growth medium, the tissue concentrations of Na
?
and Cl
-
were relatively high (Clough 1984; Werner and
Stelzer 1990; Aziz and Khan 2001a; Patel and Pandey
2009). The Na
?
contents in roots and stems of Aegiceras
corniculatum seedlings cultivated under 3.0 mM NaCl
were 10.0 mg/g, which is comparable with those cultivated
under 24.0 mM NaCl (12.0 mg/g) (Patel and Pandey
2009). The tap water used to make up the 0% seawater
treatment contained \1mMNa
?
and Cl
-
, and the tissues
of Avicennia marina and Rhizophora stylosa seedlings
growing under the treatment contained appreciable con-
centrations of both ions ([200 mM in Avicennia marina
and [100 mM in Rhizophora stylosa) (Clough 1984). It
was suggested that a certain amount of salt was translo-
cated from the salt reserve of hypocotyls under the treat-
ment of tap water (Clough 1984). However, this
preferential absorption was also identified in suspension
cultured Bruguiera sexangula cells in an experiment that
958 Trees (2011) 25:953–963
123
eliminated the effect of hypocotyl salt reserves (Kura-Hotta
et al. 2001). Energy-dispersive X-ray microprobe analyses
showed that the root vacuoles of Rhizophora mangle in
freshwater revealed Na
?
preference, while those of salt-
treated plants revealed a strong Na
?
exclusion (Werner and
Stelzer 1990). Under low external Cl
-
concentration,
plants show active and rapid uptake of Cl
-
(White and
Broadley 2001). Takemura et al. (2000) transferred Bru-
guiera gymnorhiza seedlings precultivated in distilled
water for 4–6 months into a medium with 500 mM NaCl.
They found that Na
?
concentration in leaves increased
rapidly and reached a stable value in 3 days.
Fluctuation in salinity
In estuarine ecosystems, there are often large spatial,
temporal and seasonal variations in water salinity, where
soils may vary from freshwater to hypersaline conditions.
These large fluctuations are characteristic of mangrove
habitats, particularly in riverine mangroves (Lugo et al.
1989; Naidoo 1989; Gordon 1993; Orcutt and Nilsen
2000; Medina et al. 2005; Hogarth 2007). Many man-
groves penetrate considerable distances inland along river
banks where water is permanently fresh and tidal fluctu-
ations are minimal or absent (Tomlinson 1986). This
distribution offers strong support for the view that man-
groves are facultative halophytes. However, after carefully
monitoring the salinity of river water, many researchers
found that the upstream penetration distance of salt water
determined the range of the distribution of true mangrove.
In other words, the upstream limit of true mangrove dis-
tribution is the upstream limit of salt water penetration.
This has been observed in many rivers (Carter et al. 1973;
Bunt et al. 1982; Ball and Pidsley 1995; Ball 1988a, b;
Duke et al. 1998). Significant spatial and temporal (daily
and seasonal) variations in salinity from the river mouth to
the upstream limit of mangrove distribution existed in
these rivers. Carter et al. (1973) investigated the effect of
salinity on mangroves in a region in Florida dominated by
mangrove wetlands. Mangroves were found grow well in a
site 14 km downstream of the wetland, where salinity was
about 5–10 psu in dry season while near 0 psu in wet
season. Scholander et al. (1964) suggested that even
though mangroves grow well in river estuaries they sel-
dom penetrate inland beyond the direct action of ocean
tides. Neither species with higher salt tolerance (e.g.
Sonneratia alba) nor species with low salt tolerance (e.g.
S. lanceolata) occurred permanently in freshwater (Ball
and Pidsley 1995). Among the species occurring along the
Adelaide River in northern Australia, few species grew
well in the absence of NaCl (Ball and Pidsley 1988).
These results indicate that true mangroves do not occur
where freshwater is permanent.
Plants grown under constant salinity are unlikely to
behave in the same way as those in field situations, where
fluctuating rather than constant salinity occurs (Beckett
et al. 1995). Variation in salinity may be more difficult to
cope with than high salinity only (Hogarth 2007). A fluc-
tuating salinity regime had a significantly negative effect
on photosynthesis (as measured by leaf gas exchange) and
plant growth rates in Rhizophora mangle relative to con-
stant salinities with the same mean (Lin and Sternberg
1993). Trees surrounded by saline or even hypersaline
water may satisfy their requirements from freshwater
seepage, or from a subterranean lens of brackish water
(Hogarth 2007; Lambs et al. 2008). Orcutt and Nilsen
(2000) argued that many plants may use windows of low
salinity to survive in such habitats. Using stable isotope
technique, Sternberg and Swart (1987) showed that man-
groves in Florida Swamp could use water with a wide
variation in salinity. Despite this, most studies of the
effects of substrate salinity on mangroves were carried out
under constant salinity. Little work has been carried out on
the effects of fluctuations in substrate salinity on man-
groves in the field.
Leaf succulence is a common characteristic in many
mangroves (Tomlinson
1986). Their leaf cells enlarge suf-
ficiently, achieved through increasing water uptake of
leaves, such that absorbed salt was diluted (Levitt 1980;
Sua
´
rez and Sobrado 2000;La
¨
uchli 2004). Consequently,
succulence may be a mechanism to avoid excessively high
salt concentrations in plant organs (Hagemeyer 1997) and
mangroves growing under higher salinities should have
higher leaf succulence levels. However, this simplistic
conclusion avoids the questions of how succulence is
induced or when mangroves absorb this extra water for leaf
succulence (Tomlinson 1986). There are two possible
explanations: (1) If the salinity around mangrove roots is
constant, the development of succulence has only one
advantage: preparing for even higher salinity. In laboratory
culture, leaf succulence increased with the increase of
salinity, but the highest leaf succulence was not detected at
the highest salinity but at intermediate salinity levels (Bur-
chett et al. 1984; Sua
´
rez and Sobrado 2000; Sobrado 2005).
(2) If the salinity around mangrove roots is variable, man-
groves may absorb water during low salinity and then
develop succulence for even higher salinity. A few recent
findings illustrated that under fluctuating salinity, plants can
use times when salinity is low to take up water. Trees sur-
rounded by saline or even hypersaline water may satisfy
their requirements from freshwater seepage, or from a sub-
terranean lens of brackish water (Hogarth 2007; Lambs et al.
2008). Orcutt and Nilsen (2000) argued that many plants
may use windows of low salinity to survive in hypersaline
habitats. Using stable isotope technique, Sternberg and
Swart (1987) showed that mangroves in Florida Swamp
Trees (2011) 25:953–963 959
123
could use water with a wide variation in salinity. Kathiresan
and Bingham (2001) inferred that mangrove species, par-
ticularly those that are less tolerant of high-salinity condi-
tions, could opportunistically uptake and store water when
they are exposed to low-salinity conditions.
Conclusions and future prospects
Salinity is a major abiotic factor influencing mangrove
growth. Mangroves can grow in freshwater for a limited
time but not throughout their entire life cycles. Salt stim-
ulation to growth is a common feature of all true man-
groves. Although critical experiments are still needed, the
evidence favours the tentative conclusion that mangroves
are obligate halophytes. This conclusion contradicts the
prevailing view that mangroves grow well without addi-
tional NaCl and are facultative halophytes.
Available reports illustrate and explain the facultative/
obligate nature of mangrove salt requirements is not
comparable and hence have led to confusion (Hagemeyer
1997). The viviparous nature of mangroves which include
substantial stores of salt in fruits and propagules is the
major source of this confusion. Laboratory culture exper-
iments under constant salinity do not give us the whole
picture on the salt tolerance mechanisms of mangroves.
Future studies should focus on the possible effects of
salinity fluctuations on mangroves, especially those in the
field. The physiological basis of apparent requirements for
saline conditions to support growth is still not well
understood, which also deserves more attention in future
research. Present research focuses on the effects of high
salinity on mangroves and on the mechanisms mangroves
use to cope with high salinity (Scholander 1968; Waisel
et al. 1986; Ball 1988a, b;Popp1994;Lo
´
pez-Hoffman
et al. 2006; Liang et al. 2008; Alongi 2009; Parida and Jha
2010), but very few studies have assessed the effects of low
salinity or freshwater on mangroves (Mallery and Teas
1984; Tuffers et al. 2001; Yan et al. 2007). In addition, the
long-term response of mangroves to the absence of NaCl is
also unclear.
Acknowledgments This research was jointly supported by the
National Natural Science Foundation of China (No. 40776046),
National Basic Research Program of China (No. 2009CB426306) and
the China State Administration of Oceanography’s Research Grant
(No. 200905009).
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    • "Mangroves are facultative halophytes that complete their life cycles under saline conditions (Krauss and Ball, 2013 ). Recent reports, however , suggest an obligate requirement for salt in some species (Wang et al., 2011; Nguyen et al., 2015). The optimum salinity for growth generally ranges from 5 to 50% seawater (Ball, 1988). "
    [Show abstract] [Hide abstract] ABSTRACT: Mangroves are unique, highly productive forests that interface between marine and terrestrial environments in protected and sheltered habitats of tropical and temperate regions. In Africa, mangroves reach their southern distributional limit in the warm temperate zone at Nahoon Estuary (32°56′ S) in South Africa. Temperate mangroves are less diverse, slower growing and of smaller stature than those in the tropics. This review gives an overview of mangrove distribution in South Africa and factors that constrain their spread. This is followed by an ecophysiological overview of mangrove adaptations to survive in an intertidal environment characterized by heterogeneous salinity, waterlogging and low nutrients. These adaptations play critical roles in salt exclusion, maintenance of low tissue water potentials and conservative water and nutrient use. Adaptations range from macro to micro levels and include root, stem and leaf morphology. It also discusses characteristics of mangroves at higher latitudes that distinguish them from their tropical equivalents. The effects of anthropogenic pollution, climate change and sea level rise, as well as local threats in South Africa are also discussed. This review also includes a detailed list of research conducted on South African mangroves and makes suggestions for future work.
    Full-text · Article · May 2016
    • "A number of researchers have published articles on OA in halophytes in general and mangroves in particular (Downton, 1982; Clough, 1984; Munns, 1988; Popp & Polania, 1989; Popp & Albert, 1995; Aziz & Khan, 2001a, b; Yancey et al., 2005; Slama et al., 2015) yet nature and contribution of solutes under different salinity regimes and plant age have not been discussed in detail. Avicennia marina, a salt secreting mangrove is considered as an obligate halophyte for its physiological requirement of salt to optimize growth although under higher salinities growth response slows down (Wang et al., 2011). This true mangrove is known to accumulate large amount of leaf Na + and synthesize glycinebetaine (GB) for its osmotic adjustment under salt stress (Popp, 1984b). "
    Full-text · Article · Jan 2016
    • "From month 8.5, the cover area of Deep turfs decreased, and by month 13.5, the turfs had either become smaller or died. Salt can be a physiological or an ecological requirement (Wang et al., 2011 ). The selected model related salinity to a slight increase in turf covering area. "
    [Show abstract] [Hide abstract] ABSTRACT: In this paper we investigated the role of competition to determine Bacopa monnieri L. Pennel (Plantaginaceae) zonation in a temporarily open/closed tropical estuary. In this estuary, B. monnieri occupies a given vertical zone in the saline stretch, where it forms dense monospecific stands, but is absent elsewhere. We transplanted turfs to areas outside of their natural occurrence in the estuary, both in the presence and absence of competition: a higher-elevation zone, a lower-elevation zone and a non-saline region. Turfs transplanted between naturally occurring stands served as controls. Turfs transplanted to the lower zone either died or became much smaller. As there was no competition under this condition, we conclude that the absence of this species from this zone is due to abiotic conditions, likely light limitation imposed by the turbid water column. Turfs transplanted to the higher zone under competition died; however, in the absence of competition, they survived. Turfs transplanted to the non-saline zone died, regardless of the presence or absence of competition, indicating an abiotic restraint. Our results indicate that the absence of B. monnieri from higher elevations is related to competitive displacement, whereas its absence from lower elevations and from non-saline areas is related to abiotic drivers.
    Full-text · Article · Jun 2015
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