JEC584.

fm Page 648 Saturday, July 14, 2001 1:42 PM

Journal of
Dispersal potential and early growth in 14 tropical
Blackwell Science, Ltd

Ecology 2001
89, 648 659 mangroves: do early life history traits correlate with
patterns of adult distribution?
PETER J. CLARKE, RAELEE A. KERRIGAN and CHRISTINE J. WESTPHAL
Botany, The University of New England, Armidale 2351, Australia

Summary
1 We characterized the dispersal potential and early growth traits of 14 tropical
mangrove species in experiments where diaspores were immersed in various solutions of
seawater and subsequently stranded onto surfaces with the same salinity.
2 Viviparous and non-viviparous species had similar buoyancy, seed weight and rates
of root and shoot initiation, as well as early growth and salinity tolerance. This trait
convergence may be related to selection against small, dormant diaspores in the unstable
regeneration niche.
3 Differences in dispersal potential and early growth of 12 species were compared with
known patterns of distribution (across the shore, along estuaries, regional occurrence
and continental range size) to test if tidal sorting of diaspores could account for adult
spatial patterns.
4 Diaspore buoyancy, orientation, lateral root initiation, shoot initiation and early
shoot extension differed among species but none correlated with adult zonation across
the shore or along estuaries. However, some back-shore species had diaspores that were
buoyant and were slow to initiate lateral roots and shoots. Patterns of early growth were
partially related to the distribution along estuaries but salinity responses contributed to
this zonation in only three species.
5 Regional distributions were unrelated to dispersal potential. However, the tend-
ency of infrequent species to show slow growth in full seawater may account for the
under-saturation of species in estuaries with appropriate habitats. The range size of
the tropical mangroves appears unrelated to their dispersal potential and early growth
traits.
6 Early life history traits of 12 mangroves showed poor correlation with patterns of
adult distribution across all spatial scales. Traits related to establishment were, however,
stronger predictors of distribution than those associated with dispersal.
Key-words: mangrove zonation, propagules, range size, vivipary, water dispersal
Journal of Ecology (2001) 89, 648659

variation in species distribution (104106 m) (Tomlinson

Introduction
Dispersal and early growth are plant life history stages
that fundamentally determine where species grow and
in what abundance in mangrove systems. Differences in
diaspore (seeds, fruits and seedlings) dispersal potential
and early growth traits may help explain pronounced
stand patterns ranging in scale from shore-parallel
zonation of species (101102 m), to estuary zonation
of species (102104 m), to between estuary (regional)
Correspondence: Peter J. Clarke, Botany, The University
2001 British of New England, Armidale 2351, Australia (e-mail
Ecological Society pclarke1@metz.une.edu.au).
1986; Duke 1992).
Ecological sorting at early life-history stages
(regeneration niche models) may lead to the habitat
differentiation or zonation commonly observed in
mature stands of mangroves (Rabinowitz 1978a;
Smith 1987; Clarke & Allaway 1993; McKee 1995;
McGuinness 1997). The tidal sorting of diaspores
(Rabinowitz 1978a,b,c; Tamai & Iampa 1988; Jimenez &
Sauter 1991) has largely been replaced as an explanation
by the sorting of species along a salinity gradient as a
result of competitive interactions (Ball 1988) or due to
the interactions of multiple variables (for example Smith
1987; Smith et al. 1989; Osborne & Smith 1990). More

648
JEC584.fm Page 649 Saturday, July 14, 2001 1:42 PM

649 recently the combined effects of sorting due to dispersal
Early life history of and early growth have been used to explain small-scale
tropical mangroves patterns of recruitment (McGuinness 1997; Minchinton
2001) and zonation (Clarke 1995; McKee 1995).
Many regeneration niche models have been tested
using elaborate manipulative field experiments in
which diaspores are stranded in early growth sites to
which experimental treatments (disturbance, predators,
competitors, etc.) are applied. Dispersal potential may,
however, influence the behaviours of these diaspores
and thus interpretation of field experiments involving
diaspore transplants (McKee 1995). Tidal action may
not deliver diaspores of all species to all sections of the
intertidal zone (cf. Smith 1992) and tidal sorting of
diaspores in relation to dispersal ability, as emphasized
by Rabinowitz (1978a,b), may need revisiting. Initial
factors that may influence the distribution and fate
of diaspores include dispersal potential (weight, shape,
orientation, time to shoot emergence, and buoyancy
of diaspores) and early growth (time and numbers of
plants with initiated roots and shoots), as these traits
interact with the environments where dispersal and
stranding occur.
In addition to the potential effects of tidal sorting
on shore-parallel zonation, it may affect distribution
of species along estuary tidal and salinity gradients
(see Duke 1992), although this has rarely been examined
(Smith 1992). In part this was due to the lack of com-
prehensive quantitative information about regional
patterns of species along estuaries, which for tropical
mangroves have only recently been published (Bunt
1996). These data show that mangrove species often
have distributions along estuary gradients that are
consistent with general accounts (for example Chapman
1976; Tomlinson 1986; Duke 1992) and may be related
to salinity (for example Bunt et al. 1982; Duke 1992),
although the cause remains speculative (Smith 1992).
Surveys in northern Australia ( Wells 1995; Bunt
1996; Ball 1998) have also revealed patterns of species
distribution between estuaries and enable species to
be ranked in order of their relative frequency within
the absolute bounds of their geographical distribution.
These surveys suggest that habitats (estuaries) were
under-saturated with mangrove species, possibly because
some species are unable to disperse and establish from
supply populations. Furthermore, the variable range
size of mangrove species ( Tomlinson 1986) is well docu-
mented for species in northern Australia (Duke 1992).
Several hypotheses have been advanced for these
geographical ranges (Tomlinson 1986; Duke 1992) but
the potential effects of dispersal potential and early
growth have not been tested.
The aim of our study was to compare the early life
history traits (dispersal potential and early growth)
of tropical mangroves with adult distributions at four
scales: (i) shore parallel zonation, (ii) estuary or river
zonation, (iii) frequency of species occurrence among
estuaries and (iv) geographical range around a coastline.
We also examined whether diaspore characteristics of
weight, size and dispersal potential are correlated with
early growth traits in mangroves, and whether viviparous
and non-viviparous mangrove species have different
dispersal and early growth abilities.
Materials and methods
,
Diaspores from 14 tropical species of mangroves
(Table 1) were subjected to immersion in different
salinity treatments at the Australian Institute of Marine
Science, Townsville. Nomenclature follows Tomlinson
(1986) and Duke (1992), with the exception of the
reclassification of Ceriops tagal var. australis as C. australis
by Ballment et al. (1988). None are known to be
dispersed other than in water, but a range of plant
families and germination types was included (Table 1).

Table 1 Germination type and seed and seedling characteristics of mangrove species used in experiments. Vivipary, germination descriptions and
propagule type are from Tomlinson 1986. Nomenclature for Avicennia from Duke 1992

Propagule Propagule Growth

Species Family Vivipary Propagule type Germination elongation curvature form

Aegialitis annulata Plumbaginaceae Cryptoviviparous Seed Epigeal Elongated Curved Shrub

Aegiceras corniculatum Myrsinaceae Cryptoviviparous One-seeded fruit Epigeal Elongated Curved Shrub
Avicennia marina var. Avicenniaceae Cryptoviviparous One-seeded fruit Epigeal Not elongated Tree
eucalyptifolia
Bruguiera exaristata Rhizophoraceae Viviparous Seedling Epigeal Elongated Straight Tree
Bruguiera gymnorrhiza Rhizophoraceae Viviparous Seedling Epigeal Elongated Straight Tree
Bruguiera parviflora Rhizophoraceae Viviparous Seedling Epigeal Elongated Curved Tree
Ceriops australis Rhizophoraceae Viviparous Seedling Epigeal Elongated Straight Tree
Ceriops decandra Rhizophoraceae Viviparous Seedling Epigeal Elongated Straight Tree
Ceriops tagal Rhizophoraceae Viviparous Seedling Epigeal Elongated Straight Tree
Cynometra iripa Leguminosae None One-seeded fruit Epigeal Not elongated Shrub
Heritiera littoralis Sterculiaceae None One-seeded fruit Hypogeal Not elongated Tree
2001 British
Lumnitzera racemosa Combretaceae None One-seeded fruit Epigeal Not elongated Tree
Ecological Society,
Rhizophora stylosa Rhizophoraceae Viviparous Seedling Epigeal Elongated Straight Tree
Journal of Ecology
Xylocarpus ,
mekongensis Meliaceae None Seed Hypogeal Not elongated Tree
89, 648 659
JEC584.fm Page 650 Saturday, July 14, 2001 1:42 PM
650 Diaspores were generally collected by picking mature
P.J. Clarke, fruit from trees to prevent exposure to the osmotic
R.A. Kerrigan & effects of tidal water once they had fallen. However,
C.J. Westphal Heritiera littoralis and Cynometra iripa were only avail-
able by collecting dry intact fruits recently deposited
underneath parent trees and Ceriops australis had to
be collected from the strandline, but this species was
excluded from correlative analyses due to potentially
confounding effects of pre-exposure to tidal water.
The fresh weights of all diaspores were recorded
within 3 days of collection. All diaspores were collected
from mangrove stands (Lucinda and Cape Cleveland)
within 100 km of Townsville, Australia (1917 S,
14703 E).
Four salinity treatments were used (100%, 50%, 10%
and 0% seawater) in polythene storage bins (60 L). For
each species, treatment was replicated three times with
a total of five diaspores per bin. The bins each contained
a single species and were arranged in a randomized
block in a shade house where they were stirred by hand
each day and replenished with water if evaporation
reduced water levels. Buoyancy, orientation and initi-
ation of root or shoot primordia were recorded after 1,
2, 3, 5, 10 and 15 days.
The time taken for species to develop roots (the obli-
gate dispersal period, Rabinowitz 1978a) corresponds
with the period where diaspores are not able to derive
resources from sediments. Note that, in the cases where
vivipary or cryptovivipary results in the elongation
of the hypocotyl, the obligate dispersal period is the
time taken for development of lateral roots, not the
emergence of the radicle. These diaspores were added
to solutions and the time taken for lateral roots to
emerge (1 mm long) was measured, together with
numbers of roots.
The effects of salinity on the number of diaspores
floating, and the number of diaspores developing roots,
or lateral roots from hypocotyls, were analysed for each
species with a single factor . Cochrans test was
used to test for homogeneity of variances, no trans-
formations were required. The correlations among
continuous diaspore variables were also calculated.
-
At the end of the immersion experiment, stranding was
simulated by transferring five diaspores of each species
to each of three replicate trays per salinity treatment
(70 50 cm). Trays were filled with 5 cm of beach sand
and saturated with seawater of the same strengths as
used for the immersion experiments. We thus avoided
problems of osmotic shock that can occur by planting
seedlings into saline substrates. Salinities were randomly
allocated to trays arranged in blocks. Diaspores were
kept in a shadehouse under ambient summer temper-
2001 British
atures and moistened to maintain salinity levels.
Ecological Society, During a period of 15 weeks, survival, sprouting of
Journal of Ecology, shoots (elongation to 2 mm) and heights of seedling
89, 648 659 apical shoots were recorded.
The effects of salinity on the root development and
sprouting of each species after 15 weeks were analysed
with a single factor . Cochrans test was used to
test for homogeneity of variances and ln(x + 1) trans-
formations were applied where necessary.
Differences in buoyancy characteristics among popu-
lations were assessed for diaspores of A. corniculatum
(Lucinda, Townsville, Coffs Harbour 3018 S, 15308 E),
A. marina var. eucalyptifolia ( Townsville), A. marina var.
marina (Brisbane 2728 S, 15301 E, Coffs Harbour),
B. exaristata (Lucinda, Townsville) and R. stylosa.
(Townsville, Brisbane, Coffs Harbour). Forty diaspores
per population were collected from several trees and
distributed between containers filled with either 100%,
50%, 10% or 0% seawater under similar conditions to
those used for the more comprehensive study. The effect
of salinity and population on the number of diaspores
floating after 15 days was analysed for each species
with a two-way .
We tested for correlations between diaspore traits, i.e.
buoyancy (rank order), time to initiate roots (rank order),
mean diaspore weight, mean diaspore length, mean
proportion of diaspores initiating roots (across all
treatments), mean proportion of diaspores initiating
shoots (across all treatments). No attempt was made
to correlate these traits with other life history traits or
to adjust comparisons for phylogeny. Spearman rank
correlations were calculated where rank variables were
used, otherwise Pearson correlation coefficients were
calculated. C. australis and L. racemosa were excluded
from the analyses.
Quantitative zonation patterns described by Bunt (1996)
could not be correlated with diaspore data because of
the variable and inconsistent species zonation. Gener-
alized, qualitative positions in intertidal zones were
derived from tables presented in Duke (1992) and from
descriptions in Tomlinson (1986), providing they were
consistent with the results of Bunt (1996). These data
were qualitatively compared with the outcome of the
trait analysis.
The occurrence of mangrove species in downstream,
middle, and upstream locations of estuaries of north-
east Queensland (Bunt 1996) was used in correlations
of frequency in different tidal positions with diaspore
attributes of: buoyancy (rank order), dormancy (time
to radicle emergence), weight, % root initiation, % shoot
initiation and early growth. Data from systematic
surveys of two sets of independent estuaries in northern
Australia, a wetter coast in Queensland (Bunt 1996)
JEC584.fm Page 651 Saturday, July 14, 2001 1:42 PM

651 and a seasonally arid coast in the Northern Territory

% of propagules

SE = standard error. *Ceriops australis was collected from dispersed propagules and this may confound comparisons. Avicennia marina initially sinks but then refloats. Averaged over all salinity treatments.
Early life history of (Wells 1995), were also used to calculate the relative

23 days (SE)
with roots at

38.0 (19.8)

58.3 (10.9)

98.3 (11.3)
tropical mangroves occurrence of mangrove species within each region.

18.3 (8.7)

100.0 (0.0)
70.7 (7.2)
68.7 (6.3)
86.7 (6.9)
23.3 (7.3)

8.3 (3.3)
3.3 (3.0)
8.3 (3.5)

3.3 (2.2)
These data were then correlated with diaspore attributes

0
of: buoyancy, dormancy (time to radicle emergence),
weight, % root initiation, % shoot initiation and early
growth. Note that the term dormancy is used in the
broadest sense to infer a resting or dispersal phase of

Did not develop

root initiation
the life cycle. In viviparous mangroves, development

Time until
is often continuous and there is no strict dormancy.

(days)
Nevertheless, there are differences in the time taken for
shoots to emerge (the apparent dormant phase).

10
8
4
8
14
8
8
8
14
23
23

14
4
Finally, measures of the range of species along the
coastline of Australia were used to correlate geo-
graphical range with diaspore attributes of: buoyancy,

Prone to vertical

Prone to vertical
Prone to vertical

Prone to vertical
orientation of
dormancy, weight, % root initiation, % shoot initiation

Predominant

propagules
and early growth. Data were obtained from Tomlinson

Vertical

Vertical
(1986), Wells (1995) and our own field observations.

Prone
Prone

Prone
Prone

Prone

Prone

Prone

Prone
Spearman rank correlations were calculated where
rank variables were used, otherwise Pearson correlation
coefficients were calculated. C. australis was excluded
from all analyses and L. racemosa, which remained

buoyancy pattern
dormant, was excluded from the analyses where shoot

Predominant
and root initiation were involved.

freshwater

Floater**
Floater

Floater
Floater
Floater
Floater
Floater

Floater
Floater
Sinker
Sinker

Sinker
Sinker

Sinker
Table 2 Mangrove diaspore attributes of mass, length, buoyancy, immersion orientation, dormancy and root initiation

Results

,

buoyancy pattern
Predominant

Diaspore characteristics are summarized in Table 2.

in saltwater

Floater

The buoyancy patterns of the diaspores ranged from

Floater
Floater

Floater
Floater
Floater
Floater
Floater

Floater
Floater
Sinker
Sinker

Sinker

Sinker
obligate floaters to those that sink (Fig. 1, Table 2). All
species with elongated straight propagules (Table 1)
floated and orientated the dispersal unit to a vertical
position, whereas the three species with curved prop-
of propagules
Mean length

agules remained in a prone position and sank during

the experiments (Table 2). The timing of root initiation
ranged from 4 days to more than 3 weeks and the
(cm)

3
4
3
9
18
21
13
15
19
2
5
1
23
6

proportion of propagules initiating roots was highly

variable within and between species (Table 2). Patterns
of root initiation among species appear unrelated to
Mean fresh mass

buoyancy and propagule orientation.

of propagules

Salinity treatments had differential effects on buoyancy

0.25 (0.01)
0.51 (0.01)
5.16 (0.14)
4.30 (0.15)
24.96 (0.97)
2.53 (0.05)
1.60 (0.03)
2.74 (0.06)
4.65 (0.09)
6.72 (0.19)
20.93 (1.08)
0.17 (0.01)
35.37 (1.09)
24.49 (0.79)

in some species (Fig. 1cj) and these were mostly related

(g) (SE)

to the physical effects of denser solutions, i.e. greater

buoyancy in full seawater. Species with variable buoyancy
were defined as floaters if more than 50% of diaspores
remained buoyant after 15 days of enforced dispersal.
Avicennia marina var. eucalyptifolia

Interactive effects between salinity and time suggested

biochemical changes in diaspores in relation to the sur-
rounding medium, as in Avicennia marina which initially
Xylocarpus mekongensis

sank but then refloated. Three broad groups of species

Aegiceras corniculatum

Bruguiera gymnorrhiza

Lumnitzera racemosa
Bruguiera exaristata

emerged: (i) those with diaspores that are buoyant and

Bruguiera parviflora

Rhizophora stylosa
Aegialitis annulata

Heritiera littoralis
Ceriops australis*
Ceriops decandra

float for the period observed, (ii) those that sink within
Cynometra iripa
Ceriops tagal

2001 British
5 days of release, and (iii) those where buoyancy changes
Ecological Society, through time and/or with salinity (Fig. 1, Table 2).
Species

Journal of Ecology, Diaspores of A. marina, C. tagal, C. iripa, H. littoralis,

89, 648 659 R. stylosa and X. mekongensis tended to float irrespective
JEC584.fm Page 652 Saturday, July 14, 2001 1:42 PM

652
P.J. Clarke,
R.A. Kerrigan &
C.J. Westphal

Fig. 1 Proportion of diaspores floating in tanks of 100%, 50%, 10% and 0% seawater. Mean values shown from five diaspores
placed in each of three replicate tanks. Species arranged in order of response from floaters to sinkers.

Table 3 Correlations among diaspore traits for 12 mangrove species

Mass Length Root initiation (%) Shoot initiation (%) Buoyancy

Length 0.30
Root initiation (%) +0.05 0.23
Shoot initiation (%) +0.44 0.45 +0.65
Buoyancy* +0.69 0.05 0.20 +0.14
Time for root initiation* 0.09 +0.23 +0.87 +0.63 +0.14

*Spearman rank correlations.

of salinity treatments. The curved diaspores of
2001 British
A. corniculatum, A. annulata and B. parviflora sank over
Ecological Society, time in all solutions, whereas buoyancy of L. racemosa,
Journal of Ecology, B. gymnorrhiza, B. exarista and C. decandra varied with
89, 648 659 the density of the solution. L. racemosa was considered
a sinker (50 80% of diaspores sink within 15 days)
and B. exaristata a floater (73100% remain buoyant),
while B. gymnorrhiza and C. decandra have more varied
patterns but generally float in seawater. Correlations
between diaspore traits (Table 3) show that weight and
JEC584.fm Page 653 Saturday, July 14, 2001 1:42 PM
653
Early life history of
tropical mangroves
Fig. 2 Mean proportion of diaspores with vertical orientation in tanks of 100%, 50%, 10% and 0% seawater. Mean values shown
from five diaspores placed in each of three replicate tanks.
Table 4 Summary of the effects of salinity on buoyancy of mangrove propagules from widely separated populations
Salinity Population
Aegiceras corniculatum <0.01 NS
Avicennia marina <0.01 NS
Bruguiera exaristata <0.01 <0.01
Rhizophora stylosa <0.001 <0.01
NS = not significant, P > 0.05.
buoyancy are positively correlated, i.e. small diaspores
are less buoyant than large ones.
For Rhizophoraceae species with buoyant diaspores,
orientation often changed from prone to vertical through
time (Table 2, Fig. 2). These patterns were, how-
ever, variable among species during the course of the
experiment but re-orientation was more marked in
less saline solutions (Fig. 2). Three sinker species
with elongated, but curved, diaspores never adopted
a vertical position.
The effects of salinity treatments on buoyancy patterns
were generally consistent across populations of a
species ( Table 4). Diaspores from both subtropical and
tropical populations of R. stylosa and B. exaristata
floated in full seawater, whereas A. marina sank and
refloated and A. corniculatum sank in all treatments.
Diaspores of R. stylosa showed interactions between
population and salinity with higher proportions of
diaspores sinking in more diluted seawater at sub-
tropical latitudes. Despite some differences in details
the overall buoyancy classification of species was con-
sistent among populations from locations that were
widely separated.
2001 British
Ecological Society,
Journal of Ecology, There were significant effects of both species (F12,143 =
89, 648 659 22.1, P < 0.001) and duration of immersion on initiation
Interaction Buoyancy pattern
NS Sinker
NS Sinks and refloats
NS Floater
<0.05 Floater
of roots. Salinity, however, had little effect except for
A. annulata (F3,8 = 16.0, P < 0.001), which developed roots
only in full seawater, and A. corniculatum (F3,8 = 3.3,
P < 0.1), which had few roots in full seawater.
Diaspores showed a wide range of times taken to
develop lateral roots (dormancy) during enforced
immersion (Table 2). A. marina had the shortest
dormancy period, with 20% of diaspores developing
roots by day 5, and X. mekongensis, a non-viviparous
species, also had a short dormant phase (1015 days
with 17% of diaspores developing roots by day 10). By
day 15 both species had initiated 45 roots per diaspore
(4 and 40 mm long, respectively) whereas the other
species had only one or two roots. All viviparous
species had begun to develop roots by day 15 (Table 2).
Of the remaining species, C. iripa and H. littoralis did
not develop roots at all until day 23, and L. racemosa
never showed signs of root or shoot development.
Dissection of L. racemosa fruits revealed a viable
embryo in 60% of fruits and this is therefore regarded
as the only innately dormant species.
There were significant effects of both species (F12,26 = 9.0,
P < 0.001) and salinity on initiation of shoots following
stranding (Fig. 3). The effect of salinity on the propor-
tion of diaspores initiating apical shoots was significant
at P < 0.05 for four species and for a further three
species if probability of type one error was reduced
to P < 0.1 (Table 5). The remaining species did not
differ significantly in their response to the salinity
treatments even if the high variances associated with
some treatments are taken into account (P > 0.5).
JEC584.fm Page 654 Saturday, July 14, 2001 1:42 PM

654
P.J. Clarke,
R.A. Kerrigan &
C.J. Westphal

Fig. 3 Mean (SE) proportion of diaspores that initiated shoots after 15 days of enforced dispersal in tanks of (a) 100%, (b) 50%,
(c) 10% and (d) 0% seawater. Species sorted in rank order of response.

Fig. 4 Mean (SE) height of shoots in (a) 100%, (b) 50%, (c) 10% and (d) 0% seawater after 15 days of enforced dispersal and
15 weeks in early growth trays. Species sorted into rank order.

Table 5 Summary of the salinity effects on shoot initiation and growth 4 months after mangrove diaspore stranding

% Apical shoot Apical shoot initiation in Shoot growth Initial shoot growth in
Species initiation (SE) relation to salinity index (mm/g fw) relation to salinity

Aegialitis annulata 15.0 (7.0) Few in fresh** 11 No growth in freshwater

Aegiceras corniculatum 28.3 (9.9) Decrease with seawater* 16 Optimal growth 5% sw
Avicennia marina var. 90.0 (5.2) No salinity effect 20 No salinity effect
eucalyptifolia
Bruguiera exaristata 75.0 (7.4) No salinity effect 6 Optimal growth 5% sw
Bruguiera gymnorrhiza 50.0 (11.1) Decease with seawater* 4 Optimal growth 050% sw
Bruguiera parviflora 28.3 (8.3) Optimal at 50% seawater** 2 Optimal growth 050% sw
Ceriops australis 63.3 (6.4) Decrease at 5% seawater* 1 No salinity effect
Ceriops decandra 36.6 (10.4) No salinity effect 2 Optimal growth 050% sw
Ceriops tagal 20.0 (6.0) No salinity effect 1 Optimal growth 050% sw
Cynometra iripa 21.7 (9.7) Decrease with salinity** 12 Optimal growth 010% sw
Heritiera littoralis 15.0 (6.1) Decrease with salinity** 4 Optimal growth 010% sw
Lumnitzera racemosa None No initiation 0 No growth
Rhizophora stylosa 73.3 (7.9) No salinity effect 2 Optimal growth 50100% s
Xylocarpus mekongensis 81.7 (9.9) No salinity effect 16 Optimal growth 050% sw

Ceriops australis was collected from dispersed propagules and this may confound comparisons. SE = standard error. Mean value
averaged over all salinity treatments. Index calculated as height of main shoot (mm) divided by mass of propagule (g fw).
*Significant difference P < 0.1, **significant difference P < 0.05.

2001 British
Trends in shoot emergence related to salinity are also increases the number of species with greater than
Ecological Society, shown in the shifting rank order of species in the 25% of diaspores sprouting is reduced.
Journal of Ecology, proportion initiating apical shoots (Fig. 3). Most Differences in growth (height of shoots) were observed
89, 648 659 species initiate shoots at low salinity, but as salinity among both species and salinity treatments (Fig. 4)
JEC584.fm Page 655 Saturday, July 14, 2001 1:42 PM

655
Early life history of
tropical mangroves

Fig. 5 Mean shoot height : fresh weight of diaspore ratios at (a) 100%, (b) 50%, (c) 10% and (d) 0% seawater after 15 days of
floating and 15 weeks in early growth trays. Species sorted into rank order.

Table 6 Distribution and occurrence of mangrove species within and between estuaries in northern Australia. Bunt (1996) data
are based on frequencies in 149 transects across 17 tidal waterways (estuaries) in north-east Australia. Wells (1995) data are from
the presence in 82 tidal estuaries in northern Australia

Position in estuary
Frequency Frequency (no. of sites) Position in intertidal
Coastal range* (fq among (fq among
Species (km) estuaries) sites) Up Low Mid High Down Mid

Aegialitis annulata 6600 0.97 0.14 82 14 4 + +

Aegiceras corniculatum 7400 0.90 0.20 27 32 41 +
Avicennia marina 10000 1.00 0.33 53 31 17 + + +
Bruguiera exaristata 4800 0.86 0.16 73 27 0 +
Bruguiera gymnorrhiza 4700 0.39 0.45 25 39 36 + +
Bruguiera parviflora 4100 0.60 0.24 35 46 19 +
Ceriops decandra 3100 0.47 0.22 30 57 13 + +
Cynometra iripa 1300 0.16 3 43 54 +
Heritiera littoralis 2200 0.26 4 4 92 +
Lumnitzera racemosa 5000 0.80 0.09 26 48 26 + +
Rhizophora stylosa 7000 1.00 0.21 70 26 4 + +
Xylocarpus mekongensis 4800 0.84 0.19 19 56 25 + +

*Data from Tomlinson (1986), Wells (1995) and personal observations. Data from Wells (1995). Data from Bunt (1996).
Data from Duke 1995. = absent from this region.

but were not statistically tested because of the varied
number of diaspores initiating shoots. Comparisons
of the rank order of shoot height in relation to salinity
show that some species have distinct tolerances for
particular treatments (Fig. 4). Shoot height and diaspore
weight are positively correlated and comparison of
growth might therefore benefit from expressing height
relative to diaspore weight, as in Fig. 5. This index of
early growth takes into account the maternal storage
effect of the diaspore, which may influence early
seedling performance. Two species (A. annulata and
R. stylosa) decreased while three species (H. littoralis,
A. corniculatum and C. iripa) increased in their rank
position from seawater to freshwater.
2001 British
Ecological Society,
Journal of Ecology, Correlations of abundance and habitat preferences
89, 648 659 within estuaries (Table 6) and individual diaspore
attributes often showed contrasting signs but were
rarely significantly correlated. Those species more
abundant in the downstream end of estuaries were pos-
itively correlated with species that could initiate shoots
over a range of salinities and could grow well in salin-
ities greater than 10% seawater (Table 7). Conversely,
those species abundant in the upstream locations of
estuaries were positively associated with diaspores that
grew taller in fresh and brackish water. Species more
common in downstream locations were also less buoy-
ant and were faster to initiate shoots than species more
abundant in upstream locations.
Correlation of individual diaspore attributes and
measures of relative occurrence of species within 17
estuaries (Bunt 1996) show a positive correlation with
the ability to initiate roots and, in particular, shoot
initiation in brackish (10% seawater) conditions. In
contrast, the relative frequency of species occurrence
among estuaries in the survey of Bunt (1996) was also
positively correlated with shoot initiation and shoot
JEC584.fm Page 656 Saturday, July 14, 2001 1:42 PM

656
Table 7 Correlations of mangrove diaspore attributes and adult occurrences within estuaries, occurrences among estuaries and the range of species along
the
P.J.Australian
Clarke, coastline
R.A. Kerrigan &
Frequency in sections of estuaries Frequency Frequency Frequency
C.J. Westphal within among among Coastal
Downstream Mid-stream Upstream estuaries estuaries estuaries range

Buoyancy 0.46 +0.01 +0.17 +0.02 +0.23 +0.23 0.48

Time to initiate roots +0.55 +0.07 0.42 +0.39 +0.23 +0.17 +0.43
Diaspore mass 0.09 0.14 +0.17 +0.31 +0.40 0.01 0.59
Percentage root initiation +0.08 +0.39 0.33 +0.50 +0.33 0.13 +0.57
Percentage shoot initiation in freshwater 0.02 +0.22 0.17 +0.29 +0.33 0.04 0.03
Percentage shoot initiation in 10% seawater +0.47 +0.02 0.45 +0.71* +0.67* 0.07 +0.14
Percentage shoot initiation in 50% seawater +0.42 +0.20 0.55 +0.11 +0.48 +0.20 0.19
Percentage shoot initiation in seawater +0.59* 0.14 0.51 +0.01 +0.59* +0.65* +0.01
Shoot height in freshwater 0.53 0.12 +0.59 +0.05 +0.14 +0.13 +0.11
Shoot height in 10% seawater 0.48 0.44 +0.71 +0.09 +0.19 +0.16 +0.03
Shoot height in 50% seawater +0.30 0.01 0.28 0.01 +0.42 +0.15 0.01
Shoot height in seawater +0.31 0.08 0.25 +0.03 +0.54 +0.34 +0.24

*Significant correlation P < 0.05. Average values used across all salinity treatments.

growth in brackish (10% seawater) conditions (Table 7).
In the more seasonally dry region, the relative frequency
of species occurrence among estuaries (Wells 1995; n = 82
estuaries) was more strongly positively correlated with
shoot initiation in full seawater (Table 7).
No strong correlations were detected between geo-
graphical range of species and early life history traits
(Table 7).
Discussion
?
Mangrove diaspores vary in weight and shape, and
their ability to float and to initiate roots and shoots
(Tables 1, 2 and 4). The expectation from terrestrial
studies that larger diaspore weight would confer an
advantage in root and shoot initiation (Westoby et al.
1997) was not consistently observed here, either within
a phylogenetic group (six Rhizophoraceae species)
or across different families (Table 3). Larger diaspores
may, however, confer advantages in established life
stages, such as resistance to predation, taller plants and
larger leaf areas ( Westoby et al. 1997). This covariation
in traits needs to be measured in studies of other life
history stages in tropical mangroves.
-
?
Many mangrove species have embryos that develop
continuously without innate dormancy so that the
dispersal unit is a seedling, or propagule, rather than a
seed (Tomlinson 1986). However, not all mangrove
2001 British
species are viviparous and their dispersal unit, which
Ecological Society, is either a seed or a one-seeded fruit (Tomlinson 1986),
Journal of Ecology, may have some dormancy. Our study shows that, with
89, 648 659 the exception of the one dormant species (Lumnitzera
racemosa), non-viviparous mangrove species show
similar early growth traits to those of viviparous species.
Ranges for buoyancy, seed weight, rates of root and
shoot initiation, early growth and salinity tolerance also
do not differ between the two classes. This finding is
not consistent with the hypothesis of Joshi (1933) that
selection for vivipary arises from escape from germina-
tion in saline habitats (see also Tomlinson 1986; Elmqvist
& Cox 1996).
The presence of large viviparous diaspores in all
Rhizophoraceae is related to their common descent,
but similar traits are present in other lineages. This con-
vergence may be related to the intrinsic instability of
the regeneration niche selecting against small, dormant
diaspores. The lack of dormancy in mangroves also
appears to be consistent with the results of Rees (1994,
1997) who found that reduction in seed dormancy was
associated with increased seed weight, efficient spatial
seed dispersal and long-lived species.
Thirteen of the 14 mangroves tested had non-dormant
diaspores, suggesting that these tropical forests have
little or no buried seed bank and rely on regular cohorts
of diaspores for regeneration. The absence of a seed
bank in most mangrove stands reduces the temporal
storage effect and increases the importance of early
life history stages in determining spatial patterning
within and among mangrove forest stands (for
example Rabinowitz 1978a; Smith 1987; McKee
1995; McGuinness 1997; Clarke & Kerrigan 2000).
?
We wished to assess whether shoreline zonation
reflects differences in dispersal potential and subsequent
stranding (Rabinowitz 1978a,b). In a review of mangrove
structuring processes, Smith (1992) rejects dispersal
effects and suggests that tidal action delivers all species
to all portions of the intertidal zone. However, the 14
Indo-Pacific species tested showed a range of buoyancy
JEC584.fm Page 657 Saturday, July 14, 2001 1:42 PM
657 patterns, from floating for prolonged periods to sinking,
Early life history of and the combined effects of buoyancy, diaspore weight
tropical mangroves and differences in the time taken to initiate shoots
and roots, could influence stranding patterns across the
shoreline. These patterns could, in turn, reflect intertidal
habitat differentiation (zonation) by dispersal sorting
in the absence of physiological tolerance, predation
and competition.
Discussion of tidal sorting and zonation assumes
that shoreline zonation occurs. In a recent analysis,
Bunt (1996) showed that species sequences across an
intertidal location are highly variable and that multiple
centres of distribution often occur. It is now clear that
shore parallel species sequences (zonation sensu stricto)
are not as consistent as portrayed in general accounts of
mangrove shore zonation (see Watson 1928; Chapman
1976 for patterns and Macnae 1966; Semeniuk 1985;
Bunt et al. 1991; Ellison et al. 2000 for exceptions).
Nevertheless, several of the species used in the present
study (C. iripa, L. racemosa, H. littoralis) consistently
occur high on the shore, whilst others (R. stylosa,
A. marina) commonly extend from low to high shore
locations (Duke 1992; Bunt 1996) (see Table 6).
The diaspore dispersal potential characteristics of
weight, shape, orientation and buoyancy appear unre-
lated to shore parallel species zonation in northern
Australia. For example, species with small diaspores (for
example A. corniculatum, A. annulata and L. racemosa)
are not restricted to high shore habitats as suggested
by Rabinowitz (1978a) and are generally less buoyant
than species with large diaspores. Similarly, species with
diaspores that float (for example R. stylosa, A. marina
and B. gymnorrhiza) are not restricted to high shore
habitats. Whilst dispersal potential alone does not cor-
respond with zonation, the combination of buoyancy and
early growth may account for the distribution of some
high shore species (C. iripa, H. littoralis, L. racemosa).
These species all float for long periods and initiate
roots and shoots more slowly than other floating species.
Growing these species in intertidal locations will test
whether they are restricted to the backshore because
of physiological tolerance, predation, or competition
from low shore species. In general, however, the effect
of tidal sorting of diaspores on shore parallel zonation
does not appear to be important for low and mid-tidal
mangrove species in northern Australia.
? ?
Habitat differentiation of mangrove species along
rivers has been shown to have some basis from the
systematic surveys of rivers in northern Australia
(Bunt 1996) and may be related to salinity tolerance
(Bunt et al. 1982). The habitats for 12 of the species used
2001 British
in this study are shown in Table 6 (Bunt 1996) and
Ecological Society, several have upstream distributions (A. corniculatum,
Journal of Ecology, C. iripa, H. littoralis) whilst others are more frequent
89, 648 659 downstream (A. annulata, A. marina, B. exaristata and
R. stylosa). Upstream locations are more likely to
experience more freshwater influence, although cau-
tion should used because seasonal aridity can reverse
salinity gradients in some monsoon estuaries (Duke
1992).
Dispersal potential traits (diaspore buoyancy and
timing of root initiation) showed little relationship with
the relative frequency of species in down stream, mid-
stream and upstream locations (Table 7). The tendency
of some species (B. exaristata and C. decandra) to have
diaspores that sink in freshwater does not correspond
with the distribution of these species along the estuary
gradient (Table 6).
The differential growth responses to salinity observed
in many species generally correspond to results in
culture (see review by Smith 1992). Salinity preferences
at the early growth stages can, however, only be directly
related to river zonation in a few cases. For example,
A. annulata was rarely found upstream and will not
grow in freshwater, whereas C. iripa and H. littoralis are
commonly recorded in upstream locations and grew
best at low salinities. Across all species there was a
positive correlation between species abundances in the
downstream sections of estuaries and the initiation of
shoots in full seawater (Table 7). Conversely, upstream
abundance was negatively correlated with initiation
and growth shoots in seawater.
Growth in relation to salinity has been used to
explain the river zonation of Sonneratia (Ball 1995) and
Ceriops congeners (Smith 1988) and unrelated sym-
patric species (Hutchings & Saenger 1987; Ball 1988;
Ball et al. 1988). Alone, however, tolerance of edaphic
conditions is unlikely to explain distribution because
dispersal properties, early growth abilities and suscep-
tibility to predators vary among species. It is clear,
however, that salinity during dispersal and stranding
affects early growth of mangrove species in different
ways. Recently, the combined effects of dispersal
potential and early growth of diaspores have been used
to explain the distribution of co-occurring mangroves
(Clarke 1995; McKee 1995) and smaller scale pattern-
ing (Minchinton 2001). Thus, field experiments on the
effects of dispersal properties, early growth abilities,
tolerance of edaphic conditions and predation are
needed to clarify river, as well as shore, zonation.
The occurrence of mangrove species in northern
Australia is often sporadic among estuaries within their
geographical range (Wells 1995; Bunt 1996). Some
species occur commonly within their geographical
range but are less frequent within estuaries (for example,
R. stylosa), whilst others have more sporadic occur-
rences across their geographical range but are more
frequent within those estuaries where they occur (for
example, B. gymnorrhiza) (Table 6). Wells (1995)
JEC584.fm Page 658 Saturday, July 14, 2001 1:42 PM
658 suggests that although species with restricted discon-
P.J. Clarke, tinuous distributions could disperse to all estuaries,
R.A. Kerrigan & seasonal salinity leads to patchy distribution. Our study
C.J. Westphal also suggests that dispersal potential was not related to
species occurrences within or between estuaries but
may be related to early growth.
Species with the ability to initiate shoots and grow
in seawater appear to be more abundant in the mon-
soonal estuaries sampled by Wells (1995). This pattern
is also significant in the less seasonal estuaries of Bunts
study, where the ability to initiate roots and shoots
under low salinity conditions is also related to fre-
quency of occurrence. These results suggest that some
species are unable to colonize from supply populations
because of the inhibitory effects of full seawater on
early growth. This may account for the under-saturation
of species in estuaries with suitable habitats. This
hypothesis is counter-intuitive to the way distant dis-
persal often occurs, as those seeds that are dormant
have more time to be widely dispersed. In unstable
habitats, such as mangroves, lack of dormancy in the
dispersal medium (seawater) may be advantageous, as
it would increase the chance of successful early growth
upon stranding in a favourable site.
Finally, the geographical range of our study species
varied from a few thousand kilometres to about 10 000
kilometres along the continuous Australian coastline.
This range of distribution was, surprisingly, negatively
correlated with buoyancy and diaspore weight. This
negative correlation suggests that geographical limits
to the early growth of mangrove species are independent
of their dispersal abilities. Across all spatial scales early
life history traits of 12 mangroves showed poor cor-
relation with patterns of adult distribution. Traits
related to establishment tended to be stronger predictors
of occurrence than those associated with dispersal.
Acknowledgements
We wish to thank the staff at the Australian Institute of
Marine Science (AIMS) for their support throughout
the project. In particular we are grateful to Barry
Clough, Dan Alongi, Janet Ley and Alistair Robertson,
for sponsorship at AIMS and logistical support. We
are indebted to Paul Dixon and to Otto Dalhaus for
diaspore collection and their contribution to the care
of mangrove seedlings. Graeme Wells and John Bunt
had the vision to collect mangrove distribution and
abundance data in remote regions of the Australia. The
Queensland Department of Primary Industries and the
National and Marine Parks Services granted permis-
sion for diaspore collection. The project was funded by
an Australian Research Council grant A19530936.
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