DSpace at VNU: Growth and population dynamics during early stages of the mangrove Kandelia candel in Halong Bay, North Viet Nam

Estuarine, Coastal and Shelf Science 58 (2003) 435–444

Growth and population dynamics during early stages of the
mangrove Kandelia candel in Halong Bay, North Viet Nam
Hoang Thi Haa, Carlos M. Duarteb,*, Nguyen Hoang Tria,
Jorge Terradosb, Jens Borumc
a

Mangrove Ecosystem Research Division, Centre for Natural Resources and Environment Studies,
Viet Nam National University, Hanoi, So 7, Ngo115, Pho Nguyen Khuyen, Hanoi, Viet Nam
b
IMEDEA (CSIC-UIB), Grupo de Oceanografı´a Interdisciplinar, Instituto Mediterra´neo de Estudios Avanzados,
C/ Miquel Marque´s 21, 07190 Esporles (Mallorca, Islas Baleares), Spain
c
Freshwater Biological Laboratory, University of Copenhagen, Helsingørsgade 51, DK-3400 Hillerød, Denmark
Received 17 May 2002; accepted 31 March 2003

Abstract
Quantifying the dynamics of the early stages in the life cycle of mangroves is essential to predict the distribution, species
composition and structure of mangrove forests, and their maintenance and recovery from perturbations. The growth and population
dynamics of two stands of the mangrove Kandelia candel in Halong Bay (Viet Nam) were examined for 1 year. Growth was highly
seasonal, with high growth rates and fast internode formation in the summer, dropping to extremely low growth during January–
February, the coldest and driest months in the year. In addition, growth and internode formation rates showed important interannual variability during the last decade. The complete reproductive period required 7–8 months. Flower initiation was maximal in
June and peak propagule maturity occurred in December–January. Only one mature propagule developed for every 67 and 127
inflorescence buds formed at Site 1 and Site 2, respectively. Kandelia candel propagules begun to sink 10 days after being released,
and after 18 days all propagules had negative buoyancy. The propagules developed roots within 19–68 days, depending on whether
they were held on the water or sediment, and were capable of long range dispersal, for 15–20% of them dispersed more than 100 m
within 1 day. The median age of K. candel plants ranged between 8.7 and 5.6 years, with a density of 1900 and 470 plants haÿ1, in
Sites 1 and 2. Plant mortality was high, with 64 and 74% of the plants surviving after a year at Sites 1 and 2. Life expectancy (i.e.
median age-at-death) of only 2.2 and 2.7 years at Sites 1 and 2, respectively, indicates that mortality of young K. candel plants was
specially high. Recruitment occurred in early spring, and did not suffice to balance the mortality within the annual period examined.

These results suggest that the K. candel stands in Halong Bay might be maintained by a few years of high recruitment which would
compensate for generally high mortality rates.
Ó 2003 Elsevier Ltd. All rights reserved.
Keywords: growth; recruitment; mortality; mangrove; Kandelia candel

1. Introduction
Mangrove forests are important components of
shallow, tropical coastal areas, which have experienced
an important decline, largely due to logging and other
human-derived transformations, over the last 50 years
(Aksornkoae, 1993; Arrhenins, 1992; Go´mez, 1988). The
loss of mangroves has been particularly large in
* Corresponding author.
E-mail address: (C.M. Duarte).
0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0272-7714(03)00109-4

Southeast Asia, to the extent that many countries have
lost most of their original mangrove cover (Adeel &
Pomeroy, 2002). Realization of the detrimental ecological consequences of mangrove loss has led to the
development of large-scale afforestation projects in
many Southeast Asian countries, as well as measures
to conserve the natural forests still existing and promote
the recovery of perturbed mangrove systems (Field,
1998; Ong, 1995).
Knowledge of the population dynamics of mangroves
is essential to forecast their dynamics and eventual


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recovery from perturbation. While much research has
been done on the primary productivity of mangroves
(Ball, 2002; Bunt, 1995; Christensen, 1978; Christensen &
Wium-Andersen, 1977; Clarke, 1994; Clough, Ong, &
Gong, 1997; Clough, Tan, Phuong, & Buu, 2000; Coulter
et al., 2001; Duarte et al., 1998; Feller, 1995; O’Grady,
McGuinness, & Eamus, 1996; Onuf, Teal, & Valiela,
1977; Saenger & Snedaker, 1993; Twilley, Lugo, &
Patterson-Zucca, 1986), their population dynamics remain, in contrast, relatively poorly known. In particular,
quantifying the dynamics of the early stages in the life
cycle of mangroves is essential to predict the distribution,
species composition and structure of mangrove forests.
Mangroves propagate by sexual reproduction mainly,
and both the maintenance and recovery of mangrove
forests depend on propagule production, dispersal and
establishment, and the successful recruitment of
mangrove seedlings into the reproductive tree status
(Tomlinson, 1994).
The phenology and rates of propagule production
are known for a few species only (Avicennia marina:
Clarke, 1994; Clarke & Myerscough, 1991a; Duke,
1990; Aegiceras corniculatum: Clarke, 1994; Rhizophora
apiculata: Christensen & Wium-Andersen, 1977). The
dispersal and establishment capacity of mangrove
propagules have been characterized, and their power
to explain adult tree distribution has been discussed for
a larger number of species (Clarke, 1993; Clarke,

Kerrigan, & Westphal, 2001; Clarke & Myerscough,
1991b, 1993; Maxwell, 1996; McGuinness, 1997a;
McKee, 1995a; Minchinton, 2001; Rabinowitz, 1978).
Overall, these studies suggest that the maintenance of
mangrove populations depends less on their dispersal
properties and their rate of supply to a given mangrove
stand, and more on the factors that influence the establishment of propagules and their early survival and
growth.
The growth and survival of mangrove seedlings
depends on several factors such as tidal position and
desiccation (Ellison & Farnsworth, 1993, 1996; McKee,
1995a), salinity (Ball, 2002; Ball & Pidsley, 1995;
Clarke & Allaway, 1993; McGuinness, 1997a), redox
potential and sulfide concentration in pore water of the
sediment (McKee, 1993, 1995a, 1996; Youssef &
Saenger, 1998), nutrient availability (Clarke & Allaway, 1993; Duarte et al., 1998; Feller, 1995; McKee,
1995b; Onuf et al., 1977), light availability (Ball, 2002;
Ellison & Farnsworth, 1993; McKee, 1995b; Minchinton,
2001; Smith, 1987a; Tamai & Iampa, 1988), wave
exposure (Clarke & Myerscough, 1993; Tamai & Iampa,
1988; Thampanya, Vermaat, & Terrados, 2002),
decreased sedimentation (Ellison & Farnsworth, 1996),
burial by sediment (Terrados et al., 1997; Thampanya,
Vermaat, & Duarte, 2002), sediment disturbance
(McKee, 1995a; Minchinton, 2001) or fouling (Clarke
& Myerscough, 1993).

Herbivory, in particular the predation of mangrove
propagules by crabs, larval insects and snails is a source of
mortality in the early stages of mangrove life cycle that has

received close attention. First, there are species-specific
differences in the frequency of predation for the propagules of Avicennia species are always more preyed on
than those of other species while those of Rhizophora
species are usually less preyed on (McGuinness, 1997b;
McKee, 1995c; Smith, 1987b; Sousa & Mitchell, 1999).
Second, intensity of herbivory can vary widely between
different locations depending on several factors, such as
nutrient content (Feller, 1995), availability of propagules
of other, more preferred species (McGuinness, 1997b),
tidal position and predator abundance (DahdouhGuebas, Verneirt, Tack, Van Speybroeck, & Koedam,
1998; Osborne & Smith, 1990; Robertson, Giddins, &
Smith, 1990; Siddiqi, 1995; Smith, 1987a), or the local predator guild (Sousa & Mitchell, 1999). Then, herbivory
can reduce seedling growth and survival (Ellison &
Farnsworth, 1996; McGuinness, 1997b; McKee, 1995c;
Minchinton & Dalby-Ball, 2001; Osborne & Smith, 1990).
Furthermore, it was suggested that herbivory on mangrove propagules and seedlings could determine the
spatial distribution of adult trees (Smith, 1987b), a contention which seems to hold for Avicennia species only
(McGuinness, 1997b; McKee, 1995c; Sousa & Mitchell,
1999).
In spite of this wide knowledge of the environmental
conditions and ecological processes that can potentially
influence the growth and survival of mangrove seedlings,
the dynamics of mangrove seedling populations under
natural conditions remains to a large extent unknown
(Clarke, 1995). Certainly, naturally occurring mangrove
propagules or seedlings chosen according to particular
objectives have been selected, tagged, and the percentage of them surviving after a given time and/or their size
has been quantified on several occasions (Clarke &
Myerscough, 1993; McGuinness, 1997a; McKee, 1995c;
Minchinton & Dalby-Ball, 2001; Osborne & Smith,

1990, to cite only a few), but these studies hardly ever
chose a naturally occurring population of mangrove
seedlings, or a randomly chosen part of it, as the subject
of study (but see Clarke, 1995 and Osunkoya & Creese,
1997) to evaluate recruitment and mortality, which are
the basic demographic variables needed to characterize
the dynamics of any population. As a result, even if
previous studies suggest that mortality of early stages
(e.g. seedlings) might be very high, it is not clear
altogether its relevance to the actual dynamics of the
population. Additionally, few estimates of recruitment
are available (Clarke, 1995).
Kandelia candel is a common mangrove species in the
central and north coasts of Viet Nam, where it is widely
used for shoreline protection (Hong & Hoang, 1993).
This species forms small pockets of vegetation in the
bays of Halong Bay (North Viet Nam), which differ in


H.T. Ha et al. / Estuarine, Coastal and Shelf Science 58 (2003) 435–444

exposure and sediment characteristics, and may thus
affect the dispersal of propagules, and their subsequent
survival and growth. Here, an examination of the growth
and population dynamics, with an emphasis on early
stages, of K. candel in Halong Bay (North Viet Nam) is
provided. Using reconstruction techniques (Duarte,
Thampanya, Terrados, Geertz-Hansen, & Fortes, 1999;
Duke & Pinzo´n, 1992), the growth dynamics of the plants
over the past decade is examined, and then the seasonality

of seedling growth using marking techniques is reported.
Finally, the age distribution of the stands and the
dynamics of sexual reproduction and early survival of
the plants are examined.

2. Methods
Gia Luan is a bay on the northern coast of Cat Ba
Island in Halong Bay (Quang Ninh Province, North Viet
Nam). Bay waters are calm, with high levels of suspended
sediment, and seasonally changing temperature, which
drops to as low as 15  C in winter. The maximum depth
of the bay at high tide is less than 2 m, the maximum tidal
amplitude is 4.6 m, and the salinity ranges from 22.3 to
32. Two adjacent mangrove stands where Kandelia
candel was abundant were selected (other species present
were Rhizophora stylosa, Bruguiera gymnorrhiza, Aegiceras corniculatum and Avicennia marina): Site 1
(20 51.449N, 106 59.119E) was located inside the bay
and the sediment was muddy (silt and clay particles: 75%
of dry weight; coarse (>2 mm) particles: 3% of dry
weight), while Site 2 (20 51.429N, 106 59.229E), with
coarser sediments (silt and clay particles: 22% of dry
weight; coarse (>2 mm) particles: 62% of dry weight),
were located at the mouth of the bay. These stands were
dominated by seedlings (plants less than 0.5 m in height)
and saplings (plants less than 1 m in height), and none of
the adult trees present exceeded 2.5 m in height.
In April 1999, a plot of 819 m2 was established at Site
1 and all Kandelia candel seedlings, saplings and adult
tress present inside the plot ðn ¼ 165Þ were tagged to
allow individual identification. The plot extended from

the seaward side to the center of the mangrove stand.
One month later (May 1999), a plot of 1998 m2 was
delimited at Site 2 (the plot included the whole mangrove stand) and all of the K. candel individuals present
inside were tagged (n ¼ 94 plants). The height of the
tagged plants was measured and the number of internodes of the main stem counted to estimate their age
(Coulter et al., 2001; Duarte et al., 1999). The study sites
were visited monthly until June 2000 and which of the
tagged plants had died since the previous sampling date
was assessed as well as, many new plants, which were
also tagged, had recruited into the plots, allowing estimation of mortality and recruitment. A subset of 10
tagged K. candel plants randomly selected from those

437

present in the plots at the beginning of the study at each
site were used to estimate growth by recording the
height of the main stem and the number of internodes
on them at each sampling event.
To estimate the growth and internode production
rates using reconstruction techniques (Coulter et al.,
2001; Duarte et al., 1999) 10 of the oldest Kandelia
candel trees present (>30 internodes) at each site were
also selected at the beginning of the study and the length
of all the internodes along the main stem of the plants
measured from the apical meristem of the main stem
down to the point where node rings were unclear. The
series of internodal lengths were filtered through a longterm running average (150% of the number of
internodes produced during 1 year, 12 internodes) and
a short-term one (30% of the number of internodes
produced during 1 year, three internodes) to remove

inter-annual and sub-seasonal variations, respectively,
from the series, and the cycles present in the filtered
series were used to infer the internode production and
elongation over the past decade, as described in Duarte
et al. (1999) and Coulter et al. (2001). In brief, the
average number of data points (i.e. internodes) between
two consecutive maxima or minima in the filtered series
of internodal lengths is an estimate of the average
number of internodes produced per year if the cycles in
the series are of an annual nature. The correctness of
this assumption is tested using the data provided by the
plants tagged and monitored for 1 year. Once the annual
nature of the cycles is established, the correspondence
between any individual cycle in a given series and year is
straightforward, as it is the estimation of the number of
internodes produced and the elongation of the main
stem in that year (Duarte et al., 1999).
To quantify the seasonality of reproductive effort and
seedling production of Kandelia candel in Halong Bay,
30 branches on at least 10 different reproductive trees at
each site were selected, tagged and the number of
inflorescence buds, flowers and stages of fruits and
propagules counted monthly during the reproductive
season (from May 1999 to March 2000). The length of
the hypocotyl was measured to quantify propagule
development. Rainfall, air temperature and insolation
data were derived from a nearby meteorological station.
Fifty-six mature propagules were collected in Site 1 in
May 2000 and transported to the laboratory to estimate
how long the propagules maintained positive buoyancy,

and the time needed to develop roots. The propagules
were maintained in three different regimes: (1) 20
propagules were placed in a tank which contained
sediment collected at the same site as the propagules
and which was maintained wet during the experiment by
adding small amounts of seawater (salinity of 26) when
needed; (2) 18 propagules were placed in a tank containing only seawater; and (3) 18 propagules were
transferred between the sediment tank to the seawater


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tank to simulate the alternation of exposure to air (low
tide) and seawater (high tide) that they would experience
at the collection site in Gia Luan. The development of
the propagules was monitored for 2 months at intervals
increasing from 4 to 18 days in between observations
(nine events) to record if they floated or not and the state
of development of the roots, quantified as the number
and length of the roots.
In May 2000, 30 propagules which seemed to have
fallen to the sediment recently at each site were randomly
selected, painted and their position marked on the
sediment with a chopstick bearing the same number as
that painted on the propagule. The short-term dispersal
of these propagules was evaluated by measuring at low
tide the distance the propagules moved during three
consecutive days.

3. Results
3.1. Growth patterns: seasonal and decadal
There was a clear shift in weather conditions during
the year, with very warm temperatures and abundant
rainfall in the summer dropping to dry and cool
temperatures in the winter (Fig. 1). Together with
a pattern of decreasing insolation from summer to
winter (Fig. 1), these data show strong seasonality in
weather conditions at the study sites. The analysis of
growth and internode formation of the marked seedlings
revealed very clear seasonal patterns, with high growth
rate and fast internode formation in the summer,
dropping to an extremely low growth during January–
February, the coldest and driest months in the year
(Fig. 1). The formation of internodes by the main stem
of K. candel was positively correlated (P < 0:05, Fig. 1)
with air temperature, rainfall and insolation in both
sites; the elongation of the main stem, however, was
positively correlated with air temperature only (Site 1:
r ¼ 0:83, P < 0:01; Site 2: r ¼ 0:88, P < 0:01). Both the
growth rate and the rate of internode formation tended
to be somewhat higher at Site 1 than at Site 2 (Fig. 1).
The examination of the sequence of internodal
lengths along the tree stems revealed clear cyclic patterns
(Fig. 2), similar to those described already for this
(Coulter et al., 2001) and other (Duarte et al., 1999;
Duke and Pinzo´n, 1992) mangrove species. The presence
of these clear signals reflected the strong seasonality of
plant growth at the study site (Fig. 1), and allowed the

reconstruction of the past growth history of the Kandelia
candel stands.
The examination of the average growth of the trees
revealed important inter-annual fluctuations (twofold)
in plant growth (Fig. 3) about the long-term average
values of 13.2 and 12.5 cm yearÿ1 at Sites 1 and 2,
respectively. The patterns of inter-annual variation were

Fig. 1. Monthly average air temperature (solid circles), rainfall (open
squares) and insolation (sun hours per month, open circles) from June
1999 to May 2000, and mean ( Æ SE) growth and internode production
of Kandelia candel at Site 1 (solid circles) and Site 2 (open circles) in
Cat Ba Island, Halong Bay (Northern Viet Nam).

also different between the two sites, with a tendency
towards declining growth rates in the past 5 years at Site
2, while mean annual growth rates first decreased and
then increased during the same period at Site 1 (Fig. 3).
This variation was statistically independent (i.e. Pearson’s r, P > 0:05) of climatic fluctuations, as represented
by mean annual temperature, rainfall and the number of
sun hours, further indicating the role of site-specific
factors. The decadal-average (1990–1999) growth rates
tended to be higher than the annual rates determined for
the period 1999–2000 at Site 1 (9.4 cm yearÿ1) and Site 2
(5.5 cm yearÿ1) and the difference between these last two
followed the recent trend observed in the years previous
to the study, when differences between Sites 1 and 2 were
greater than the average decadal values indicate (Fig. 3).
In contrast, the variation of the internode formation
rate was small and not statistically significant between

years (Fig. 3), with a long-term average of 6.7 and 5.4


H.T. Ha et al. / Estuarine, Coastal and Shelf Science 58 (2003) 435–444

Fig. 2. Examples of the series of internodal lengths measured in the
main stem of Kandelia candel (open circles), and of the filtered (to
evidence its seasonality) series of internodal lengths (solid circles) at
Site 1 and Site 2 in Cat Ba Island, Halong Bay (Northern Viet Nam).

internodes yearÿ1 at Sites 1 and 2, respectively, and
annual rates for the period 1999–2000 of 8.4 internodes
yearÿ1 at Site 1 and 6.6 internodes yearÿ1 at Site 2.

3.2. Sexual reproduction and propagule development
Flower development was at its maximum in June, and
was followed by peak flowering in July, which led to peak
fruit formation in August and maximum abundance of
mature propagules in December–January (Fig. 4). It
took, therefore, 7–8 months for mature propagules to
form from flowers. The abundance of structures in the
different stages of the sexual reproduction (inflorescence
buds to mature propagules) declined drastically along
their development (Fig. 4). The ratios of peak abundance
of these structures were found to be 67 buds : 18
flowers : 4 fruits : 1 propagule at Site 1, and 127 buds : 34
flowers : 10 fruits : 1 propagule at Site 2. Provided that
each inflorescence bud leads to four flowers, on average,
these ratios indicate that only one mature propagule is

439

Fig. 3. The reconstructed mean ( Æ SE) annual growth and internode
production of Kandelia candel at the study sites in Cat Ba Island,
Halong Bay (Northern Viet Nam). Asterisk indicates that data
corresponding to the year 2000 were obtained after measuring tagged
plants, and not using reconstruction techniques (see Section 2).

formed for each 268 and 508 flowers at each site. The
reproductive success, therefore, was greater at Site 1,
where the number of propagules developed per flower
bud initiated was twice as that at Site 2. The propagules
elongated at a constant average rate of 0.098 Æ 0.027
(SE) cm dayÿ1 during the period 1999–2000.
3.3. Stand age structure and seedling demography
The age structure of the Kandelia candel plants,
established in April 1999, indicated a median age of 8.7
years at Site 1 and 5.6 years at Site 2 (Fig. 5). The
maximum plant age, however, was similar at both sites
(Site 1: 21.6 years; Site 2: 21.7 years; Fig. 5). The age
distributions suggested—if stable in time—that mortality was higher at Site 2 than at Site 1 during the first 3–4
years of life, reversing afterwaters. Although the relative
contribution of young plants to the population was
greater at Site 2, their absolute abundance was greater at


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Fig. 4. The changes in the average number of reproductive structures
(inflorescence buds, circles; flowers, squares; fruits, triangles; mature
propagules, diamonds) of Kandelia candel at sites 1 and 2 in Cat Ba
Island, Halong Bay (Northern Viet Nam).

Site 1, where plant density is much higher (1900 and 470
plants haÿ1 in Sites 1 and 2, respectively).
The examination of plant survivorship indicated
a comparable pattern of plant depletion in both sites
(Fig. 6), with 64 and 74% of the plants surviving
within a year at Sites 1 and 2, respectively. Mortality
occurred throughout the year but it seemed lowest
during August and September (Fig. 6). The distribution
of age-at-death indicated that most of the plants that
died were young, with the life expectancy (i.e. median
age-at-death) of 2.2 and 2.7 years for Sites 1 and 2,
respectively (Fig. 5). Recruitment occurred in early
spring, with a distinct period of recruitment about 3
months after the peak in propagule maturity (cf. Figs.
4 and 6). The number of new recruits was insufficient
to balance the mortality within the annual period examined (Fig. 6), over which the number of new recruits
was only 46 and 26% of the number of plants lost, for
Sites 1 and 2, respectively.
3.4. Propagule buoyancy, root development
and dispersal
Kandelia candel propagules had positive buoyancy at
the initiation of the experiment, but some began to sink
after 10 days, and after 18 days all propagules had

Fig. 5. The cumulative age distribution (upper panel, Site 1: 165

plants; Site 2: 92 plants) and the age-at-death (lower panel: Site 1: 52
plants; Site 2: 23 plants) of Kandelia candel at Site 1 (solid circles) and
Site 2 (open circles) in Cat Ba Island, Halong Bay (Northern Viet
Nam).

negative buoyancy, both when maintained constantly in
seawater and when maintained alternatively in seawater
and on the surface of wet sediment. Root initiation was
dependent on the conditions the propagules experienced. Propagules maintained constantly over the surface of the sediment developed at least one root within
19 days. Propagules that were maintained alternately
in seawater and on the sediment surface started to
develop roots after 13 days, and after 28 days all of them
had developed at least one root. Root initiation was
slower in the propagules maintained constantly in seawater, which started to develop roots after 19 days and
all propagules had developed at least one root only after
68 days. When propagules were maintained continuously in seawater, the roots elongated linearly with time
reaching lengths greater than 10 cm during the first 45
days. Root elongation could only be reliably assessed for
seedlings maintained in seawater, for those in sediments
broke when pulled to measure the root length.


H.T. Ha et al. / Estuarine, Coastal and Shelf Science 58 (2003) 435–444

Fig. 6. Depletion curves for surviving plants (upper panel), and
mortality and recruitment (central and lower panels) of Kandelia
candel in Cat Ba Island, Halong Bay (Northern Viet Nam).

The monitoring of the distances moved by Kandelia
candel propagules over three consecutive tidal cycles

showed that 52.3 Æ 3.6% of the propagules at Site 1 and
36.7 Æ 4.7% of the propagules at Site 2 did not move;
from those that dispersed, 56% at Site 1 and 77% at Site
2 moved less than 100 m, while the rest moved more
than 100 m.

4. Discussion
The results obtained reveal a strong seasonality in the
elongation and internode production of the main stem of
Kandelia candel in Northern Viet Nam, with very low

441

growth during the cold, dry months, and fast growth
during the warm, rainy months. Strong, unimodal seasonality of the vegetative development of K. candel has
also been found in other locations (Okinawa, Japan)
where 70% of seasonal variation in leaf production could
be explained by the seasonal change in air temperature,
humidity and day-length (Gwada, Makoto, & Uezu,
2000). Other mangroves growing in subtropical locations
show strong seasonality in their vegetative development
(Avicennia marina: Clarke, 1994; Duke, 1990; Osunkoya
& Cresse, 1997; Aegiceras corniculatum: Clarke, 1994).
Mangroves growing in tropical locations, however,
usually show weaker and/or multimodal seasonal signals
in their vegetative development (Christensen & WiumAndersen, 1977; Duke, 1990; Ellison & Farnsworth,
1996; Wium-Andersen, 1981; Wium-Andersen & Christensen, 1978). Air temperature/humidity, rainfall, and
day-length/insolation have been consistently identified
by these studies as the environmental factors driving the
seasonality of mangrove growth and development.

The strong seasonality in the growth of Kandelia
candel results in the presence of distinct, annual cycles of
internodal length along the stems (Coulter et al., 2001;
Duarte et al., 1999) which allows the elucidation of past
growth patterns. This is an important feature for
mangroves lack clear annual growth rings (Tomlinson,
1994). The evaluation of the past growth rates identified
strong (twofold) inter-annual changes in K. candel
growth over the past decade, but these variations were
relatively independent at the two study sites and
unrelated to changes in climate, suggesting that they
relate to site-specific factors.
The reproductive success of Kandelia candel was low
at the Cat Ba Island, with only one mature propagule
formed for each 67 and 127 inflorescence buds initiated
at Site 1 and Site 2, respectively. The low number of
mature propagules recovered at the end of the study
(Fig. 4) advises to consider these values as preliminary.
However, low values of reproductive success have been
estimated (Avicennia marina: only 3% of flower buds
develop a viable fruit (Clarke & Myerscough, 1991a)
and the amount of propagules formed is two orders of
magnitude lower than that of ovules and zygotes,
(Clarke, 1995); Rhizophora apiculata: only 1–3% of
flower buds developed a fruit, (Wium-Andersen &
Christensen, 1978)) or suspected (Rhizophora mucronata,
Wium-Andersen, 1981) in other mangrove species,
which suggests this might be a general feature of
mangrove reproductive biology.
Similar to growth seasonality, the reproductive

phenology of Kandelia candel was characterized by
single annual peaks in the abundance of flower buds,
flowers, fruits and mature propagules. Mangrove species
growing in subtropical locations show unimodal patterns in the abundance of the reproductive organs as
well (Clarke, 1994; Duke, 1990), while those growing in


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tropical locations may show single but broader peaks in
the abundance of reproductive organs (Avicennia
marina: Duke, 1990; Wium-Andersen & Christensen,
1978) or single peaks but with flowers present all year
round (Rhizophora apiculata, Rhizophora mucronata,
Bruguiera cylindrica, Ceriops tagal, Lumnitzera littorea,
Scyphiphora hydrophyllacea: Christensen & WiumAndersen, 1977; Wium-Andersen, 1981; Wium-Andersen
& Christensen, 1978). The observation that the annual
maximum of leaf production of A. marina and Aegiceras
corniculatum in a subtropical location (Jervis Bay, New
South Wales, Australia) occurred during the period of
fruit maturity, and that leaf production was minimal at
the time of flower development and during initial stages
of fruit maturation led Clarke (1994) to suggest that
there might be a trade-off between leaf growth and
resource investment to sexual reproduction; this does
not seem to be the case for K. candel in Gia Luan for the
development of flowers and fruits occurred during
summer months, when plant growth was also fastest;

the fruits continue their development through fall in
a context of decreasing plant growth rates, and
propagules reached maturity in winter, when plant
growth rate was lowest. The time needed by K. candel
to produce mature propagules from flowers (7–8
months) was shorter than that required by subtropical
A. marina (12 months: Clarke, 1994), although this last
species can produce mature propagules in 3–4 months
only in tropical locations (Wium-Andersen & Christensen, 1978). Other mangrove species living in tropical
locations can produce mature propagules in 3–6 months
(B. cylindrica, C. tagal, L. littorea: Wium-Andersen &
Christensen, 1978; S. hydrophyllacea: Wium-Andersen,
1981) or longer times (6–8 months in R. mucronata,
Wium-Andersen, 1981; 3 years in R. apiculata, Christensen & Wium-Andersen, 1977).
The propagules of Kandelia candel are capable of
long-range dispersal for between 33 and 46% of
dispersing propagules in Gia Luan dispersed to distances
larger than 100 m within 3 days. Similarly, 84% of fallen
K. candel propagules did not settle near the parental trees
in Ranong, Thailand (Maxwell, 1996). The distance
traveled by K. candel propagules might be considerable,
since they float for an average of 10 days at least. After
this time, they sink and can rapidly develop roots (2–3
weeks) when in contact with suitable sediments. Avicennia marina propagules shed their pericarp and sink
within 1–3 days when exposed to seawater, and it takes
7–10 more days to develop roots (Clarke, 1993; Clarke &
Myerscough, 1991b). The period of obligate dispersal
might be of about 2 weeks, and within it most propagules
strand within 500 m of the release site, usually during the
first tidal cycles (Clarke, 1993). The present results show

that the period of obligate dispersal of K. candel
propagules varies from 3 to 9 weeks depending on the
particular conditions experienced by the propagules,

which suggests that the dispersal capacity of K. candel
might be higher than that of A. marina. The duration of
the obligate dispersal period for propagules of other
mangrove species varies from 4 to 40 days (Clarke et al.,
2001; Rabinowitz, 1978). It must be realized that these
are minimum estimates based on the fastest-developing
propagules; the percentage of propagules which have not
developed a root after the estimated period of obligate
dispersal may be quite high in some species (Clarke et al.,
2001). Kandelia candel propagules developed roots at
the slowest rate when exposed to seawater only, a result
consistent with previous observations in other mangrove
species (Clarke et al., 2001; Rabinowitz, 1978). This
response of mangrove propagules might increase their
dispersal potential and has been considered as a possible
reason why propagules of some species are not able to
recruit in apparently suitable habitats near their release
site, making those species infrequent (Clarke et al., 2001).
The dispersal traits of mangrove propagules seem,
however, poor predictors of the geographical distribution of the adult trees (Clarke et al., 2001). Recruitment
occurred in spring, 2–3 months after the annual peak of
mature propagule abundance, which sets an estimate for
the overall time needed by the seedlings to disperse and
establish.
The uneven age distribution of Kandelia candel
observed, specially in Site 1, is indicative of either agespecific mortality or the occurrence of important interannual differences in seedling recruitment or mortality.

Mortality was high during the early stages of life (age <3
years) at both sites but decreased afterwards, which
suggests that the unevenness of the age distribution of
the population might be driven, then, by inter-annual
differences in propagule production and/or seedling
recruitment. Inter-annual differences in sexual reproduction output of mangroves have been described for
Avicennia marina in southeastern Australia (Clarke &
Myerscough, 1991a), a mangrove species which shows
Ôuneven size distributionsÕ (Clarke, 1995). It seems,
therefore, that events of high recruitment and/or
mortality might be a general feature of the dynamics
of mangrove populations.
The present results indicate that both populations of
Kandelia candel were not in demographic steady-state at
the annual scale, and that both were in regression
(mortality was higher than recruitment) over the period
studied. These observations of direct recruitment and
mortality, together with the reconstructed age structure
of the populations, suggest that the K. candel stands in
Ha Long Bay are probably maintained by a few years of
high recruitment, due to either unusually high sexual
reproduction or currents that bring imported propagules
to the sites, to compensate for generally high mortality
rates. This hypothesis remains, however, speculative and
requires sustained observations over long periods to be
tested.


H.T. Ha et al. / Estuarine, Coastal and Shelf Science 58 (2003) 435–444

Acknowledgements
This is a contribution to the PREDICT (Prediction of
the REcovery and Resilience of DIsturbed Coastal
Tropical) communities project, funded by the INCO
programme of the European Commission (ERBIC18CT98-0292). We thank Mr Nguyen Van Tang, Ms Tu
Lan Huong, Ms Sarah Coulter and Ms Cecile Padilla
for assistance in the field.
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