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

Growth and population dynamics during early stages of the mangrove Kandelia candel in Halong Bay, North Viet Nam , Jorge Terradosb, Jens Borumc a Mangrove Ecosystem Research Division, Ce

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

, 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 inter-annual 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 ha
1, 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

Southeast Asia, to the extent that many countries have lost most of their original mangrove cover (Adeel & Pomeroy, 2002) Realization of the detrimental ecolog-ical 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

* Corresponding author.

E-mail address: cduarte@uib.es (C.M Duarte).

0272-7714/03/$ - see front matter Ó 2003 Elsevier Ltd All rights reserved.

doi:10.1016/S0272-7714(03)00109-4

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

re-main, 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

estab-lishment 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 &

All-away, 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 prop-agules 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 ( Dahdouh-Guebas, Verneirt, Tack, Van Speybroeck, & Koedam, 1998; Osborne & Smith, 1990; Robertson, Giddins, & Smith, 1990; Siddiqi, 1995; Smith, 1987a), or the local pre-dator 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 man-grove propagules and seedlings could determine the spatial distribution of adult trees (Smith, 1987b), a con-tention 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 percent-age 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 seeClarke, 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 candelis 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

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 15C 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

candelwas abundant were selected (other species present

were Rhizophora stylosa, Bruguiera gymnorrhiza,

Aegi-ceras corniculatum and Avicennia marina): Site 1

(2051.449N, 10659.119E) 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 (2051.429N, 10659.229E), 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 m2was 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

man-grove stand) and all of the K candel individuals present

inside were tagged (n¼ 94 plants) The height of the

tagged plants was measured and the number of

inter-nodes 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

esti-mation of mortality and recruitment A subset of 10

tagged K candel plants randomly selected from those

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 long-term 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 inDuarte

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 con-taining only seawater; and (3) 18 propagules were transferred between the sediment tank to the seawater

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:

r¼ 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

candelstands

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 year
1 at Sites 1 and 2,

respectively The patterns of inter-annual variation were

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 Pear-son’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 year
1) and Site 2 (5.5 cm year
1) 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

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 (  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).

internodes year
1 at Sites 1 and 2, respectively, and

annual rates for the period 1999–2000 of 8.4 internodes

year
1at Site 1 and 6.6 internodes year
1at 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

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 0.027 (SE) cm day
1during 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 mortal-ity 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

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).

Fig 3 The reconstructed mean (  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).

Site 1, where plant density is much higher (1900 and 470

plants ha
1in 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

ex-amined (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 candelpropagules had positive buoyancy at

the initiation of the experiment, but some began to sink

after 10 days, and after 18 days all propagules had

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 experi-enced Propagules maintained constantly over the sur-face 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 sea-water, 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 contin-uously 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

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).

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).

The monitoring of the distances moved by Kandelia

candel propagules over three consecutive tidal cycles

showed that 52.3 3.6% of the propagules at Site 1 and

36.7 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

growth during the cold, dry months, and fast growth during the warm, rainy months Strong, unimodal sea-sonality 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 & Wium-Andersen, 1977; Duke, 1990; Ellison & Farnsworth, 1996; Wium-Andersen, 1981; Wium-Andersen & Chris-tensen, 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 candelresults 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 pat-terns in the abundance of the reproductive organs as well (Clarke, 1994; Duke, 1990), while those growing in

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).

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 &

Wium-Andersen, 1977; Wium-Wium-Andersen, 1981; Wium-Andersen

& Christensen, 1978) The observation that the annual

maximum of leaf production of A marina and Aegiceras

corniculatumin 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 &

Christen-sen, 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,

Chris-tensen & 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 candelpropagules 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

Avicen-nia 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 distribu-tion 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 age-specific mortality or the occurrence of important inter-annual 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 repro-duction 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 candelwere 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

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

(ERBIC18-CT98-0292) 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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