Journal of
Plant Ecology
VOLUME 4, NUMBER 4,
PAGES 292–301
DECEMBER 2011
doi: 10.1093/jpe/rtq008
Advanced Access published
on 29 March 2010
available online at
www.jpe.oxfordjournals.org
Differentiation between true
mangroves and mangrove
associates based on leaf traits and
salt contents
Liangmu Wang1, Meirong Mu1, Xiaofei Li1, Peng Lin1 and
Wenqing Wang1,2,*
1
Key Laboratory of Ministry of Education for Coastal and Wetland Ecosystems, School of Life Sciences, Xiamen University,
Xiamen 361005, Fujian, People’s Republic of China
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, Fujian, People’s Republic
of China
*Correspondence address. Tel: +86-592-2181431; Fax: +86-592-2181430; E-mail: [email protected]
2
Abstract
Aims
Mangrove species are classified as true mangroves and mangrove
associates. However, as for some fringe species found mainly on
the landward transitional zones of mangroves, no consensus among
scientists could be reached in favor of this classification and much
debate arises. We hypothesized that true mangroves differ from mangrove associates physiologically and ecologically in their ability to
survive in mangrove environment.
Methods
To test this hypothesis, leaf structural traits and osmotic properties
were used to describe variation in 33 mangrove species (17 true mangroves, 6 mangrove associates and 10 controversial species).
Important Findings
Specific leaf area (SLA) of true mangroves as well as leaf nitrogen
concentration on a leaf mass (Nmass) were lower than that of man-
INTRODUCTION
To know the exact plant species composition of mangroves is
a basic and important prerequisite to understanding all the
aspects of structure and function of mangroves, as well as their
biogeographical affinities and their conservation and management (Jayatissa et al. 2002; Wang et al. 2003a). This is also
a promise of research on the origin and evolution of mangroves
(Duke 1992).
Generally, mangrove species are categorized as ‘exclusive’
species that are limited to the mangrove environment (referred
as strict mangrove, obligate mangrove or true mangrove) and
‘nonexclusive’ species that are mainly distributed in a terres-
grove associates; leaf succulence was, in general, twice as high in
true mangroves compared to mangrove associates; true mangroves
accumulated 8–9 times more Na and Cl than mangrove associates
and the former had K/Na ratios <0.5, but the latter had K/Na ratios
>0.5. These results indicated that true mangroves differed reliably
from mangrove associates in leaf traits and osmotic properties. True
mangroves are true halophytes and mangrove associates are glycophytes with certain salt tolerance. Combining distribution pattern information, the 10 controversial species were reclassified.
Keywords: mangrove d leaf trait d chemical
composition d osmotic adaptation d classification
Received: 2 September 2009 Revised: 3 December 2009 Accepted: 4
December 2009
trial or aquatic habitat but also occur in the mangrove ecosystem
(referred as semi-mangrove, back mangrove or mangrove
associate) (Lacerda et al. 2002; Parani et al. 1998; Tomlinson
1986). Tansley and Fritsch (1905) first introduced the criteria
to classify mangrove species in Ceylon into true mangroves and
mangrove associates (semi-mangroves). Tomlinson (1986)
used fairly rigid criteria to distinguish true mangroves from
mangrove associates. In his criteria, true mangroves possess
all or most of the following features: (i) occurring only in mangrove environment and not extending into terrestrial communities; (ii) morphological specialization (aerial roots, vivipary);
(iii) physiological mechanism for salt exclusion and/or salt
excretion; (iv) taxonomic isolation from terrestrial relatives.
Ó The Author 2010. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
All rights reserved. For permissions, please email: [email protected]
Wang et al.
|
Differentiation between true mangroves and mangrove associates
To some extent, Tomlinson’s criteria gave a very ‘clear’ standard to classify true mangroves and mangrove associates and it
hasbeenacceptedwidely(Duke 2006; Kathiresan and Bingham
2001; Lacerda et al. 2002; Parani et al. 1998; Saenger 2002;
Wang et al. 2003a) and most taxa have been classified clearly
(Parani et al. 1998; Saenger 2002). However, as for some fringe
species found mainly on the landward transitional zones of
mangroves, no consensus among scientists could be reached
in favor of this classification and much debate arises (Table 1)
(Duke 2006; Heads 2006; Mu et al. 2007; Parani et al. 1998). As
there is no acceptable classification to include these species,
they are referred to as controversial species in this paper before
a clear classification is made. In addition, although Hernandia
nymphaeifolia and Clerodendrum inerme were classified as mangrove associates by some researchers (Pillai and Sirikolo 2001;
Saenger 2002; Thomson and Evans 2006), they were even not
be classified as mangroves by others (Parani et al. 1998; Satyanarayana et al. 2002; Tomlinson 1986). We also consider them
as controversial species.
Clear classification results in unclear results. Why?
Duke (1992) claimed that the greater problem is in the classification itself. What is mangrove environment? The landward edge of the mangrove environment is the ‘most highly
variable’ of the zones in terms of salinity, freshwater flows, soil
types and soil moisture contents (Macnae 1968). It is rather
arbitrary to define the physical boundaries of mangrove environments (Mueller-Dombois and Fosberg 1998; Saenger
2002). Additionally, just as mentioned by Duke (1992), the
above-mentioned classification did not tell us the distinction
between true mangroves and mangrove associates clearly.
Present classification on mangrove species mainly based on
wide-ranging field observations on species zonation patterns
293
(Duke 1992; Lin 1999; Smith 1992) and experience of observers but not on scientific facts (Lacerda et al. 2002). Mu et al.
(2007) compared leaf Cl content and leaf traits between true
mangroves and mangrove associates in China and classified
the controversial species accordingly. However, limited by
the number of parameters, this classification could not give
a clear distinction between the two groups.
Salinity is one of the outstanding environmental features of
mangrove ecosystem. There are many reports indicating the importance of salinity for mangrove species as well as evidence that
various mangroves may have different tolerances and optima
salinity (Ball 2002). So researches on the physiology of their
ability to survive in saline environment may shed light on
the evolution of mangroves from terrestrial species (Parani
et al. 1998). Osmotic properties (succulence and ion content)
are the key parameters in salt tolerance of mangroves. Leaf
structural traits (leaf nitrogen concentration on a leaf mass
(Nmass), specific leaf area (SLA) and succulence) have been
proven to reflect the long-term adaptive strategy successfully
(Cunningham et al. 1999; Wang et al. 2003; Wright et al.
2004). In this study, we hypothesized that true mangroves differ from mangrove associates physiologically and ecologically
in their ability to survive in mangrove environment. To test
this hypothesis, leaf structural traits and osmotic properties
were used to describe variation in 33 mangrove species (17 specific true mangroves, 6 specific mangrove associates and 10
controversial species), and a dendrogram depicting the relationship between them has been established. Our objective
is to determine differences in leaf traits and osmotic properties
between specific true mangroves and specific mangrove associates and to classify the controversial species according to
these differences.
Table 1: major controversies on the classification of some species as true mangrove or mangrove associate
Species
True mangrove
Mangrove associate
Heritiera littoralis
Giesen et al. (2007); Jayatissa et al. (2002); Lin
(1999); Peter and Sivasothi (1999); Saenger et al.
(1983); Tomlinson (1986)
Chang (1997); Francis (2007); Mu et al. (2007);
Mukherjee et al. (2003); Tansley and Fritsch
(1905); Wang et al. (2003a)
Acrostichum spp.
Duke (1992); Giesen et al. (2007); Lin (1999); Peter
and Sivasothi (1999); Tomlinson (1986)
Chang (1997); Jayatissa et al. (2002); Kathiresan
and Bingham (2001); Mu et al. (2007); Saenger
et al. (1983); Tansley and Fritsch (1905)
Excoecaria agallocha
Giesen et al. (2007); Jayatissa et al. (2002); Lin
(1999); Peter and Sivasothi (1999); Pillai and
Sirikolo (2001); Satyanarayana et al. (2002);
Tomlinson (1986)
Chang (1997); Francis (2007); Hong and San (1994);
Mu et al. (2007); Tansley and Fritsch (1905); Wang
et al. (2003a); Zhang et al. (2005)
Xylocarpus granatum
Chapman (1984); Giesen et al. (2007);
Jayatissa et al. (2002); Lin (1999); Parani et al. (1998);
Peter and Sivasothi (1999); Saenger et al. (1983);
Tomlinson (1986); Wang et al. (2003a)
Chang (1997); Francis (2007); Hong and San (1994)
Acanthus spp.
Chapman (1984); Giesen et al. (2007); Lin (1999); Mu et al.
(2007); Parani et al. (1998); Saenger et al. (1983);
Satyanarayana et al. (2002); Tansley and Fritsch (1905)
Chang (1997); Das et al. (1996); Jayatissa et al. (2002);
Peter and Sivasothi (1999); Tomlinson (1986);
Wang et al. (2003a)
Pemphis acidula
Chapman (1984); Jayatissa et al. (2002); Peter and Sivasothi
(1999); Tomlinson (1986)
Lin (1999); Pillai and Sirikolo (2001); Saenger et al.
(1983); Wang et al. (2003a)
294
Journal of Plant Ecology
MATERIALS AND METHODS
RESULTS
Study sites and plants
Comparison of leaf traits between true mangroves
and mangrove associates
Field investigation and sample collection were performed in
northeastern part of Hainan Island of China, Qinglan Bay
(19°22#;19°35#N, 110°40#;110°48#E). This bay has the highest mangrove species diversity in China (Wang and Wang
2007). The climate is tropical with an average annual rainfall
of 1 974 mm and a mean annual temperature of 24.0°C.
At the naturally aggregated distribution site of each species,
three mature individuals of similar growing status were selected. In July to August 2006, mature fully expanded leaves
were sampled from the upper part of the plant canopy of all the
plants.
Measurements
A minimum of eight fully expanded leaves were collected
from each plant. Immediately after collection, leaves were
cleaned carefully with tissue papers and distilled water, then
fresh mass, leaf sap osmolality and area were determined.
Samples were oven-dried (80°C) and dry mass was determined. With these results, the leaf succulence (water content
on a leaf area basis, g dm 2) and SLA (expressed as leaf area to
leaf dry mass, cm2 g 1) were determined for each sample.
Dried samples were ground and homogenized for subsequent
analysis. Nitrogen content was determined on this
ground material by Nessler’s reagent colorimetric method.
Leaf nitrogen concentration was expressed on a dry mass basis (Nmass) and on a leaf area basis (Narea), by dividing
Nmass by SLA.
Calcium (Ca), magnesium (Mg), potassium (K) and sodium
(Na) were extracted with nitric acid from leaf samples after being ashed in a muffle furnace at 550°C and determined by Inductively Coupled Plasma Mass Spectrometry (ELAN DRC-e;
Perkin Elmer Inc., Waltham, MA, USA). Chloride (Cl) was
extracted with hot distilled water and determined by AgNO3
titration. The ion content was expressed on a leaf area basis
(g m 2) and on a molar basis per mass of water in fresh tissue
(mol m 3). Leaf sap osmolality of leaves was determined by
a dew point osmometry (VAPOR 5520; Wescor Inc., South
Logan, UT, USA).
Statistical analyses
The significance of the difference between the means of each parameter of different species (group) was tested using one-way
analysis of variance and an unpaired one-tailed t-test. To give
prominence to the difference between true mangroves and
mangrove associates, P < 0.001 were significant.
The data (11 variables including 4 leaf traits, 5 ion contents,
osmolality and K/Na ratios) of 33 species were log (10) transformed. From these data, a dendrogram was obtained by cluster analysis following the unweighted pair group with
arithmetic mean method, using MVSP (multivariate numerical
analyses) version 3.2 (Kovach Computing Services).
Table 2 shows the results of leaf succulence, SLA, Nmass and
Narea of 17 true mangroves and 6 mangrove associates. For the
statistic results, see Table 3.
The leaf succulence of 17 true mangroves ranged between
2.80 and 4.82 g dm 2 and the mean value was 3.92 g dm 2.
The leaf succulence of 6 mangrove associates ranged between
0.81 and 2.64 g dm 2 and the mean value was 1.75 g dm 2.
The present data indicated that true mangroves had significantly higher succulence than mangrove associates (P <
0.001). The leaf succulence was, in general, twice as high in
true mangroves compared to mangrove associates.
The true mangroves had significantly lower level of SLA than
that of mangrove associates (P < 0.001). SLA spanned from
40.32 to 93.24 cm2 g 1 in true mangroves and from 128.41
to 199.39 cm2 g 1 in mangrove associates (Table 2). True mangroves had lower SLA, which averaged 70.68 cm2 g 1 and
none was >100 cm2 g 1. The average values of SLA of mangrove associates were 156.85 cm2 g 1, which was 119% higher
than that of the true mangroves. Of the true mangroves,
Rhizophora stylosa had the lowest level of SLA (40.32 cm2 g 1),
and of the mangrove associates, Pongamia pinnata had the highest level of SLA (199.39 cm2 g 1). In comparison, true mangroves had smaller leaf size than mangrove associates.
There were significant differences in Nmass between the
two categories (P < 0.001). As for mangrove associates, Nmass
levels were all >20 mg g 1 except for Thespesia populnea. However, as for true mangroves, Nmass levels were all <20 mg g 1
except for the species of Sonneratia and Avicennia marina. The
mean Nmass level of 17 true mangroves (14.72 mg g 1)
was significantly lower than that of mangrove associates
(26.50 mg g 1) (Table 2). True mangroves had higher Narea
(averaging 2.26 g m 2) except for Scyphiphora hydrophyllacea,
Lumnitzera racemosa and Lumnitzera littorea and the mean Narea
in mangrove associates was 1.73 g m 2.
Comparison of element accumulation between true
mangroves and mangrove associates
True mangroves had higher ion elements than mangrove associates (Fig. 1). Except for a few species, true mangroves had
higher contents of K, Ca and Mg than mangrove associates
(P < 0.02). This difference was even more notable in Na and
Cl. All true mangroves showed significantly higher Cl and
Na contents than mangrove associates (P < 0.001). The mean
Na contents were 2.83 in true mangroves and 0.28 g m 2 in
mangrove associates. The former was as many as 10 times
the latter. Of the 17 true mangroves, Sonneratia gulngai had
the lowest Na content (1.97 g m 2), and S. alba had the highest
Na content (3.74 g m 2). Of the 6 mangrove associates, P. pinnata had the lowest Cl content (0.09 g m 2), and T. populnea
had the highest Na content (0.64 g m 2). The mean Cl contents
in true mangroves and mangrove associates were 4.55 and
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Wang et al.
Differentiation between true mangroves and mangrove associates
295
Table 2: leaf succulence, SLA, Nmass and Narea for specific true mangroves and specific mangrove associates
Groups
Species
Plant
code
Succulence
(g dm 2)
SLA (cm2 g 1)
True mangroves
Aegiceras corniculatum
Ac
2.81 6 0.04
Avicennia marina
Am
2.82 6 0.19
Bruguiera gymnorrhiza
Bg
Bruguiera3 rhynchopetala
Nmass (mg g 1)
Narea (g m 2)
66.19 6 4.72
13.35 6 0.41
2.02 6 0.07
73.63 6 7.38
22.86 6 1.37
3.14 6 0.23
3.48 6 0.71
69.44 6 8.17
14.11 6 2.04
2.17 6 0.33
Bv
2.53 6 0.27
84.74 6 16.62
13.92 6 1.17
1.66 6 0.19
Bruguiera sexangula
Bs
2.41 6 0.30
68.23 6 13.06
13.19 6 0.44
1.98 6 0.38
Ceriops tagal
Ct
4.39 6 1.46
44.16 6 12.28
8.56 6 0.93
2.12 6 0.42
Kandelia obovata
Ko
3.43 6 0.08
64.01 6 1.01
18.96 6 1.48
2.96 6 0.27
Rhizophora apiculata
Ra
4.68 6 0.27
43.68 6 1.83
12.13 6 2.30
2.77 6 0.41
Rhizophora stylosa
Rs
5.03 6 0.02
40.32 6 1.18
14.22 6 1.35
2.83 6 0.04
Lumnitzera racemosa
Lr
4.82 6 0.84
93.14 6 8.24
14.03 6 1.67
1.41 6 0.13
Lumnitzera littorea
Ll
4.73 6 0.29
60.41 6 2.30
9.56 6 0.84
1.47 6 0.10
Sonneratia alba
Sa
4.28 6 0.48
90.40 6 2.84
30.89 6 1.43
4.10 6 0.16
Sonneratia caseolaris
Sc
4.65 6 0.36
88.48 6 10.37
26.66 6 0.92
3.04 6 0.40
Sonneratia 3 gulngai
Sg
3.59 6 0.39
93.24 6 8.16
24.99 6 2.89
2.69 6 0.43
Sonneratia 3 hainanensis
Sk
4.08 6 0.30
70.76 6 2.04
18.96 6 4.49
2.70 6 0.68
Sonneratia ovata
So
4.28 6 0.07
47.09 6 2.21
13.00 6 0.97
1.73 6 0.08
Scyphiphora hydrophyllacea
Sh
4.58 6 0.19
80.92 6 1.31
10.06 6 1.43
1.24 6 0.16
Average
Mangrove associates
3.92
71.48
14.72
2.26
Barringtonia racemosa
Br
2.65 6 0.13
144.89 6 8.43
23.69 6 1.18
1.64 6 0.06
Cerbera manghas
Cm
2.39 6 0.26
164.60 6 28.97
29.78 6 3.22
1.80 6 0.14
Dolichandrone spathacea
Ds
1.47 6 0.04
160.41 6 4.33
30.04 6 3.04
1.87 6 0.20
Hibiscus tiliaceus
Ht
1.70 6 0.18
128.41 6 4.10
25.95 6 1.74
2.02 6 0.11
Pongamia pinnata
Pp
0.81 6 0.11
199.39 6 3.63
36.07 6 6.41
1.81 6 0.31
Thespesia populnea
Tp
1.59 6 0.02
143.39 6 13.92
15.93 6 1.81
1.11 6 0.04
1.75
156.85
26.50
1.71
Average
Values are mean 6 SD. SD, standard deviation.
Table 3: comparison of leaf characteristics and osmotic properties between 17 specific true mangroves and 6 specific mangrove associates
2
1
SLA (cm g )
Succulence (g dm 2)
Nmass (mg g 1)
True mangroves
Mangrove associates
70.68 6 15.21 (43.68;93.24)
157.02 6 24.62 (128.41;199.39)
3.92 6 0.87 (2.41;5.03)
1.77 6 0.66 (0.81;2.65)
15.72 6 5.27 (8.56;26.66)
26.91 6 6.84 (15.93;36.07)
Na (g m 2)
2.83 6 0.59 (1.97;3.74)
0.28 6 0.20 (0.09;0.64)
Cl (g m 2)
4.55 6 1.43 (2.61;6.63)
0.52 6 0.28 (0.19;0.88)
0.25 6 0.13 (0.07;0.51)
1.10 6 0.50 (0.56;2.01)
K/Na
Osmolality (mmol kg 1)
1 195 6 246 (785;1 709)
648 6 81 (566;751)
Values are mean 6 SD. Figures in the brackets are the ranges of various parameters. To accent their differences, this table only shows the parameters with a P value <0.001. SD, standard deviation.
0.52 g m 2, respectively. The former was as many as 8.7 times
the latter.
K/Na ratio
True mangroves had significantly lower K/Na molar ratios
than mangrove associates (P < 0.001). The mean values of
K/Na ratios of true mangroves and mangrove associates were
0.25 and 1.10, respectively. The K/Na ratios of the 17 true
mangroves were not >0.25, while they were >0.56 in the
6 mangrove associates. Of the true mangroves, S. hydrophyllacea had the lowest K/Na ratio (0.07). Of the mangrove associates, P. pinnata had the highest K/Na ratio (2.01).
Cluster
Cluster analysisusingthedataofleaf traits andosmoticproperties
revealed that these 33 mangrove species fell into two groups
296
Journal of Plant Ecology
-2
K content (g.m )
4.00
1.00
-2
Ca content (g.m )
7.00
6.00
Mangrove associates
3.00
2.00
1.00
-2
Mg content (g.m )
True mangroves
Ht Pp Tp Br Cm Ds
4.00
4.00
Ra Rs Bg Bs Bv Ko Ct Sh Lr Ll Sc Sg Sa So Sk Am Ac
True mangroves
Ht Pp Tp Br Cm Ds
Mangrove associates
3.00
2.00
1.00
0.00
Na content (g.m-2)
Ra Rs Bg Bs Bv Ko Ct Sh Lr Ll Sc Sg Sa So Sk Am Ac
5.00
0.00
-2
Mangrove associates
2.00
0.00
Cl content (g.m )
True mangroves
3.00
6.00
5.00
Ra Rs Bg Bs Bv Ko Ct Sh Lr Ll Sc Sg Sa So Sk Am Ac
True mangroves
Ht Pp Tp Br Cm Ds
Mangrove associates
4.00
3.00
2.00
1.00
0.00
10.00
Ra Rs Bg Bs Bv Ko Ct Sh Lr
Ll
Sc Sg Sa So Sk Am Ac
True mangroves
Ht Pp Tp Br Cm Ds
Mangrove associates
8.00
6.00
4.00
2.00
0.00
Ra Rs Bg Bs Bv Ko Ct Sh Lr
Ll
Sc Sg Sa So Sk Am Ac
Ht Pp Tp Br Cm Ds
Figure 1: element contents of the mature leaves on leaf area basis of 17 true mangroves and 6 mangrove associates in Hainan, China. For plant
codes, see Table 2. Vertical lines correspond to the standard error of the average, n = 3.
(Fig. 2). One group was a clustering of 11 species representing
5 controversial species Acrostichum aureum, Acrostichum speciosum, H. nymphaeifolia, Heritiera littoralis and Excoecaria agallocha and 6 specific mangrove associates P. pinnata, T. populnea,
Dolichandrone spathacea, Cerbera manghas, Barringtonia racemosa and Hibiscus tiliaceus. Because six specific mangrove
associates were included in this group, this group was named
as mangrove associate group. The other group was a clustering
of 17 specific true mangroves and 4 controversial species,
Xylocarpus granatum, Acanthus ilicifolius, Acanthus ebracteatus
and Pemphis acidula. Because most specific true mangroves
were included in this group, this group was named as true
mangrove group. Surprisingly, C. inerme, even not classified
as mangrove associate by some researchers, was classified into this group. The clustering of all the specific true mangroves
into a group also implied that the homology among the true
mangroves is more than that between the true mangroves
and mangrove associates.
Wang et al.
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Differentiation between true mangroves and mangrove associates
297
Figure 2: clustering of data of leaf traits and ion contents by log (10) transformation using Euclidean distance of 33 mangrove species in China. For
species name, see Tables 2 and 4.
DISCUSSION
Differences in true mangroves and mangrove
associates
As early as 1906, Guppy (1906) claimed that it was not possible
to draw a definite line between the plants of the mangrove
swamp and those of the tracts around. There was no sharp demarcation between mangrove plants and other coastal plants
(Whitmore 1984). Tomlinson (1986) concluded that ‘The ecological literature seems incapable of being reduced to a simple
set of rules to account for the diversity of vegetation types
within the broad generic concept of mangroves’. A precise definition for the word ‘true mangrove’ may not exist (Pillai and
Sirikolo 2001) and it was desirable to give a hazy definition for
it (Mepham and Mepham 1985). Heads (2006) claimed that ‘a
satisfactory definition of mangroves is elusive but, in any case,
less important than analysis of the morphological, ecological,
and biogeographical affinities involved’.
Table 2 showed that, as for 17 specific true mangroves and
6 specific mangrove associates, there existed significant differences in leaf characteristics and osmotic properties. Cluster
analysis using the data of leaf traits and osmotic properties
revealed that these 33 mangrove species fell into two groups,
true mangrove group and mangrove associate group (Fig. 2).
This implied that the homology among true mangroves is more
than between true mangroves and mangrove associates.
Results of molecular markers showed a rather distant relationship between true mangroves and mangrove associates (Parani
et al. 1998). To accent their differences, we only chose parameters with a P value <0.001 (Table 3). In comparison, specific true mangroves had lower SLA, higher succulence, lower
K/Na ratios, higher Na and Cl contents and higher osmolality.
This proved our hypothesis that true mangroves differ reliably
from mangrove associates in some aspects.
Salt-tolerant features of mangroves
As a true halophyte, it has two features: (i) showing higher salt
tolerance and optimal growth under moderate salinity (Parida
and Das 2005) and (ii) showing higher level inorganic ion accumulation for osmotic adjustment (Ueda et al. 2003). Field
observations and laboratory experiments show that the optimal salinity for growth of most true mangroves ranges between 10& and 20& or 10% and 50% seawater (Khan and
Aziz 2001 and the references cited in this paper). Many
researchers have demonstrated that true mangroves use inorganic salts (mainly Na and Cl) as energetically cheap osmolytes
for osmotic adjustment (Downton 1982; Medina and Francisco
1997; Niu et al. 1995; Wang and Lin 2003; Zhao et al. 1999).
The 17 specific true mangroves studied here behave as true
halophytes, accumulating NaCl for osmotic adjustment, which
298
were similar to the results of the 3 true mangroves (Medina
and Francisco 1997).
Available reports suggested that mangrove associates behave differently from true mangroves. Mangrove associates
did not show higher salt tolerance and grew best under freshwater (Li and Ong 1997; Lloyd and Buckley 1986; Paliyavuth
2001; Tomlinson 1986; Youssef 2007). Hibiscus tiliaceus does
not accumulate Na and Cl to lower its tissue water potential
(Dopp et al. 1985; Naidoo et al. 2002). Heritiera littoralis utilizes
organic solutes instead of inorganic salts in osmotic adjustment
(Dopp et al. 1985; Paliyavuth et al. 2004). After studying the
growth and metabolic responses of mangrove associate Ac. aureum to salt stress, Sun et al. (1999) concluded that it was not
a true halophyte.
In general, halophytes had lower K/Na ratios (<1.0), while
glycophytes had higher K/Na ratios (>1.0) (Albert and Popp
1977; Glenn and O’Leary 1984). Although all the 17 specific
true mangroves had lower K/Na molar ratios and higher
Na and Cl contents, true mangroves maintained higher K levels
than mangrove associates (Fig. 1 and Table 3). Although K/Na
molar ratios in some true mangroves varied with substrate salinities (Teas et al. 1995), they were all no >1.0 in higher substrate salinity, 0.1;0.4 in Rhizophora mangle (Medina and
Francisco 1997; Teas et al. 1995), 0.1;0.3 in Laguncularia racemosa (Medina and Francisco 1997), and 0.5 in Avicennia germinans (Medina and Francisco 1997). Naidoo et al. (2002) found
that true mangroves A. marina and Bruguiera gymnorrhiza kept
lower K/Na ratios in their leaves (0.1;0.25), while mangrove
associate Hi. tiliaceus showed a higher K/Na ratio (1.8;3.6).
After comparing the mineral ions of leaves of 23 mangroves
from Queensland, Dopp et al. (1985) found that 2 mangrove
associates, Hi. tiliaceus and He. littoralis, kept a higher K/Na ratio
(18.5;21.6 in the former and 4.3;11.9 in the latter), while it
was no >1.0 in other 21 true mangroves. This was also confirmed by hydroponic culture experiments with different saline waters in some true mangroves (Parida et al. 2004) and
mangrove associates (Youssef 2007). This suggested that true
mangroves grown under saline habitats were able to maintain
a higher K level independently of Na and Cl accumulation.
This lower K/Na ratio is not attributed to the reduction in
K+ uptake but apparently to the increase in Na+ uptake (Downton 1982; Parida et al. 2004). Maintenance of efficient uptake
of K under higher saline habitats is a key feature of salt tolerance (Glenn et al. 1994; Niu et al. 1995). Data of K/Na ratio
show that true mangroves have characteristics of halophytes,
while mangrove associates have characteristics of glycophytes.
Classification of controversial species
Although many mangroves growing on seaward of mangrove
environments (e.g. true mangroves) have been researched extensively, very little information is available on the species
growing on seaward of mangrove environments (including
specific mangrove associates and some controversial species)
(Chapman 1976; Naidoo et al. 2002). Comparison on characteristics of physiology and ecology between true mangroves
Journal of Plant Ecology
and mangrove associates was practically nil. However, available data could help us do some conclusions.
Acrostichum spp.
Generally, Ac. aureum and Ac. speciosum grew in the landward
edge of mangrove environments (Lacerda et al. 2002; Medina
et al. 1990; Sun et al. 1999). However, Ac. aureum was by no
means restricted to mangrove environments and could survive
even in nonsaline conditions (Jayatissa et al. 2002; Medina
et al. 1990; Sun et al. 1999; Taylor 1986; Tomlinson 1986).
In Western Australia and the Northern Territory, Ac. speciosum
inhabits areas of freshwater seepage beyond the upper mangrove fringe (Duke 2006). The germination of spores and
growth of prothalli of Ac. aureum appear to be best in freshwater (Lloyd and Buckley 1986; Tomlinson 1986).
In comparison to the true mangroves growing in the same
site, Ac. aureum leaves showed a distinct pattern in the ionic
relationships (Medina et al. 1990). The C1/Na ratio in its cell
sap of leaves (averaging 2.5) is consistently higher than that
of R. mangle (1.2) and L. racemosa (1.5) (Medina et al. 1990).
In addition, the K/Na ratio averages 2.6 in Ac. aureum, while
in the true mangroves this ratio is consistently <0.5 (Field
1984). Similar results were revealed in our study. Compared
to the true mangroves, their leaves showed higher SLA, lower
leaf succulence, higher Nmass, lower Na content and Cl content, higher K/Na ratios and lower osmolality (Tables 2 and 3).
Result of cluster analysis showed they were included in the
mangrove associate group (Fig. 2). We classified them as mangrove associates.
Acanthus spp.
They grow especially well in areas with more freshwater input
(Tomlinson 1986). Table 4 showed that, except for leaf SLA,
which was higher than the mean value of true mangroves
and lower than the mean value of mangrove associates, all
the parameters fell into the range of the true mangroves.
Fig. 2 showed that it was closer to mangrove associates
than any other true mangrove. We classified them as true
mangroves.
Clerodendrum inerme
Clerodendrum inerme is something of an enigma among the species examined in the present study. It is found abundantly both
on the landward edge as well as deep inside the mangrove environment (Parani et al. 1998). Saenger (2002) considered it as
a mangrove, but he did not tell if it was a true mangrove or
a mangrove associate. Satyanarayana et al. (2002) did not consider it as a mangrove species. Parani et al. (1998) classified it as
a terrestrial species.
Except for SLA, which was similar to mangrove associates,
all the parameters showed in Table 4 fell into the ranges of the
true mangroves. It was clustered into the true mangrove group
(Fig. 2). These showed that C. inerme behaved like both true
mangroves and mangrove associates. It appears to have the
largest salinity tolerance. Further researches are needed.
Wang et al.
|
Differentiation between true mangroves and mangrove associates
299
Table 4: leaf traits and element accumulation of mature leaves for 10 controversial mangrove species
Species
Plant
code
SLA
(cm2 g 1)
Succulence
(g dm 2)
Nmass
(mg g 1)
Na
(g m 2)
Cl
(g m 2)
K/Na
Osmolality
(mmol kg 1)
Acrostichum aureum
Aa
113.06 6 32.62
2.23 6 0.12
16.14 6 1.31
0.63 6 0.12
1.26 6 0.28
2.14 6 0.33
879 6 28
Acrostichum speciosum
As
144.54 6 19.78
2.26 6 0.10
22.24 6 2.03
0.89 6 0.02
1.41 6 0.24
1.14 6 0.10
913 6 32
Acanthus ilicifolius
Ai
99.43 6 16.23
4.47 6 0.29
21.96 6 1.37
2.87 6 0.03
4.43 6 0.01
0.48 6 0.02
795 6 43
Acanthus ebracteatus
Ae
108.88 6 21.07
4.48 6 0.53
18.93 6 1.38
2.44 6 0.02
4.17 6 0.01
0.41 6 0.01
822 6 30
Clerodendrum inerme
Ci
146.06 6 28.74
3.74 6 0.93
24.48 6 2.81
2.45 6 0.74
3.70 6 1.24
0.16 6 0.05
1 005 6 58
Excoecaria agallocha
Ea
131.40 6 24.71
2.24 6 0.38
23.14 6 2.06
0.44 6 0.04
1.16 6 0.22
1.18 6 0.18
987 6 91
Heritiera littoralis
Hl
71.41 6 7.93
1.88 6 0.19
16.68 6 0.62
0.20 6 0.04
0.64 6 0.04
7.41 6 1.61
545 6 62
Hernandia nymphaeifolia
Hn
147.88 6 30.60
2.89 6 0.64
33.19 6 9.09
1.36 6 0.70
1.50 6 0.95
0.41 6 0.01
645 6 56
Pemphis acidula
Pa
76.97 6 0.70
4.04 6 0.29
14.08 6 1.87
3.34 6 0.33
3.74 6 0.41
0.28 6 0.05
1 136 6 21
Xylocarpus granatum
Xg
110.91 6 6.98
2.87 6 0.20
24.82 6 1.04
0.92 6 0.19
2.88 6 0.24
1.73 6 0.75
1 247 6 27
Excoecaria agallocha
Hernandia nymphaeifolia
This tree inhabits the landward edge of mangrove forests
(Tomlinson 1986) and is restricted to low-salinity areas (Joshi
and Ghose 2003). In Tonga and India, it may occur further inland and sometimes in association with rain forest species
(Franklin et al. 2006; Satyanarayana et al. 2002). Noticeably,
it is also recorded in disturbed open sites to an elevation of
400 m (Tomlinson 1986).
Except for leaf osmolality, which was higher than the average value of mangrove associates and similar to true mangroves, all the parameters showed in Table 4 fell into the
ranges of the mangrove associates. Clustering results showed
it was clustered into the mangrove associate group. We classified E. agallocha as a mangrove associate.
In Samoa, H. nymphaeifolia usually grows on sandy or rocky
substrates in the narrow zone between low-growing littoral
vegetation on the seaward side and lowland forest inland
(Thomson and Evans 2006). In Fiji, it is restricted to beaches
or thickets and woods immediately behind beaches (Heads
2006). Table 4 showed that except for K/Na ratios, all the
parameters listed in this table showed the features of mangrove
associates. Result of cluster analysis showed it was included in
the mangrove associate group (Fig. 2). In conclusion, we classified it as a mangrove associate.
Heritiera littoralis
Heritiera littoralis is commonly found at the most landward
fringe of the mangroves, which is flooded by spring or equinoctial high tides (Jian et al. 2004). But it was also reported
occurring in terrestrial habitats or inlands. In Ishigaki Island
of Japan, it was found to be distributed along the streams in
Sokobaru (altitude 50–80 m) upstream of the Miyara
River (Mitsunori et al. 2001). In Taiwan, China, it occurs
from seashore to upland above 300 m (ZJ Li, personal
communication).
In water relations and ion concentrations, He. littoralis did
not show the same patterns displayed by other true mangroves
(Paliyavuth et al. 2004). Different from other true mangroves,
organic solutes play a particularly important role in osmotic
adjustment (Paliyavuth 2001; Paliyavuth et al. 2004; Popp
1984). Culture experiment showed that it grew best in freshwater (Paliyavuth 2001). Except for leaf SLA and Nmass, all the
parameters listed in Table 4 showed the features of mangrove
associates. The above mentioned indicated that He. littoralis
has the characteristics of glycophytes with lower salt tolerance.
It was included in the mangrove associate group (Fig. 2). In
conclusion, we classified it as a mangrove associate.
Pemphis acidula
Pemphis acidula is usually found at the landward edge of mangrove forests, sheltered beaches and seaward side of motus
(Saenger 2002; Stoddart 1980). Till now, there has been no report on its inland or terrestrial distribution. It has no aerial
roots, does not produce viviparous diaspores and does not have
large fruits (Tomlinson 1986; Wang and Wang 2007). However, it showed higher leaf succulence, lower SLA, higher
Na and Cl content, lower K/Na ratios and higher osmolality
(Table 4), which all fell into the ranges of true mangroves.
Result of cluster analysis showed that it was included in the
true mangrove group (Fig. 2). So, it was classified as a true
mangrove.
Xylocarpus granatum
Xylocarpus granatum is commonly described as occurring on the
landward edge of mangrove forests (Stoddart 1980). It mainly
accumulated Na and Cl as osmotic adjustment, which was similar to true mangroves A. alba and B. gymnorrhiza but different
from mangrove associate He. littoralis (Paliyavuth 2001). Although X. granatum was clustered into the true mangrove group
(Fig. 2), in fact it was different from the other true mangroves
greatly. Fig. 2 showed that it was closer to mangrove associates
than any other true mangrove. Its leaf succulence and Cl content showed the features of true mangroves, but it’s K/Na ratio
300
(1.73) fell into the range of mangrove associates (0.56;2.01);
it’s SLA and Na content ranked between the mean levels of true
mangroves and mangrove associates (Table 4). In the present
paper, we classified it as a true mangrove.
Journal of Plant Ecology
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National Natural Science Fund of China (40776046,
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Science (J0630649).
Guppy HB (1906) Observations of a Naturalist in the Pacific between 1896
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