全 文 ：Received 26 Nov. 2003 Accepted 27 Feb. 2004
Supported by the Environment and Conservation Fund of the Hong Kong Special Administrative Region (9210007) and the National
Natural Science Foundation of China (40276036).
* Author for correspondence. Tel (Fax): +86 (0)592 2185622; E-mail: .
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Acta Botanica Sinica
植 物 学 报 2004, 46 (8): 896-906
Diaspore Traits and Inter-tidal Zonation of Non-viviparous Mangrove Species
YE Yong1* , LU Chang-Yi1, WONG Yuk-Shan2, TAM Nora-Fong-Yee2
(1. Key Laboratory for Marine Environmental Science of Ministry of Education, Xiamen University, Xiamen 361005, China;
2. Department of Biology and Chemistry, City University of Hong Kong, Hong Kong, China)
Abstract: Diaspore traits and germination of four non-viviparous mangrove species in Hong Kong,
Lumnitzera racemosa (Jack.) Voigt., Heritiera littoralis (Drgand.) Ait., Excoecaria agallocha L. and Acanthus
ilicifolius L., were investigated. L. racemosa fruits planted immediately after collection failed to germinate
but those stored in wet condition for 35 or 50 d were successfully germinated. This suggested that L.
racemosa had endogenous and morphological seed dormancy, with embryos continued to develop during
the dormant period. Germination rates of L. racemosa decreased with increasing salinity and no germina-
tion was found at salinities over 25 ppt (ppt, parts per thausand). H. littoralis seeds were easily germinated
if the fruit coat was artificially removed. Fruit dissection significantly shortened time for root initiation and
leaf expansion. E. agallocha and A. ilicifolius seeds were also easy to germinate, initiating roots within 2 and
3 d, respectively. In terms of germination, A. ilicifolius had more tolerance to high salinity than L. racemosa.
The four species exhibited three types of adaptation to unstable environments: (1) prolonged diaspore
longevity as shown in L. racemosa and H. littoralis ; (2) shortened rooting time as in E. agallocha and A.
ilicifolius ; and (3) produced sinking diaspores in L. racemosa. Diaspore buoyancy was one of the most
important factors in determining inter-tidal zonation of non-viviparous mangrove species. Among the four
species, L. racemosa was distributed in the most seaward zones because its diaspores were sinkers while
diaspores of H. littoralis, E. agallocha and A. ilicifolius, more abundant at backshore locations, were floaters.
Root initiation was also important in influencing the inter-tidal zonation of the three species whose
diaspores were floaters. H. littoralis with the longest rooting time, as compared to E. agallocha and A.
ilicifolius, was distributed in the most backshore zone. None of other factors including salinity of seawater,
animal predation, diaspore size and seedling dimension could account for inter-tidal zonation of these
species.
Key words: Lumnitzera racemosa ; Heritiera littoralis ; Excoecaria agallocha ; Acanthus ilicifolius ;
mangrove; inter-tidal zonation; seed dormancy
Mangrove swamps are unique inter-tidal wetland eco-
systems found in sheltered tropical and subtropical shores.
They maintain a rich and diverse biological resource with
significantly ecological, environmental, social and economic
values. However, mangrove habitats are decreasing around
the world. Losses in many tropical countries exceed 1% of
mangrove areas every year due to human activities
(Spalding et al., 1997). In Hong Kong and other cities along
southeast coasts of China, mangroves have been reclaimed
and used as agricultural fields, fishponds, new town and
infra-structural developments (Tam and Wong, 2000; 2002).
In recent years, ecological restoration of mangroves has
become increasingly important. Replanting of mangroves
by governmental authorities and local green groups has
taken place in the areas where natural mangrove swamps
were destroyed (Tam and Wong, 2000).
Vegetative propagation is uncommon in mangroves
(Tomlinson, 1986) and mangrove replanting depends on
the survival and growth of the established seedlings. Due
to the availability of seedlings, mangrove replanting in
China was mainly done for viviparous mangrove species
including Kandelia candel, Bruguiera gymnorrhiza,
Aegiceras corniculatum and Rhizophora stylosa (Liao et
al., 1996; 1998; Mo and Fan, 2001), and only those in
Sonneratia were replanted for non-viviparous mangrove
species (Zan et al., 2003). In Hong Kong, eight true man-
grove species, namely K. candel, B. gymnorrhiza, A.
corniculatum, Avicennia marina, Lumnitzera racemosa,
Heritiera littoralis, Excoecaria agallocha, and Acanthus
ilicifolius, are naturally distributed along the coastlines
(Tam et al., 1997; Tam and Wong, 2002). However, only the
first four species have been replanted because of their vi-
viparous characteristics, large-sized propagules ,
abundance, and easy germination. The germination
YE Yong et al.: Diaspore Traits and Inter-tidal Zonation of Non-viviparous Mangrove Species 897
techniques of non-viviparous species, namely L. racemosa,
H. littoralis, E. agallocha, and A. ilicifolius, have not been
established, despite the fact that these species are classi-
fied as rare ones and must be conserved in Hong Kong
(Tam et al., 1997; Tam and Wong, 2002). Natural regenera-
tion of these four species is low and only a few seedlings
are found in mangrove swamps. Although techniques on
vegetative propagation were developed for some mangrove
species difficult to germinate such as E. agallocha (Rao et
al., 1998; Basak et al., 2000), Laguncularia racemosa (Elster
and Perdomo, 1999) and Heritiera (Basak et al., 2000), it is
still important to understand their seed germination and
explore successful germination methods because vegeta-
tive propagation will eventually decrease the genetic di-
versity of mangrove populations and hinder mangrove
conservation.
Transplantation success is dependent on the supply of
healthy and young seedlings, which is affected by the size,
availability and lifespan of the diaspore (i.e. any spore, seed,
fruit or plant part able to produce a new plant when
dispersed), storage and germination methods. Tomlinson
(1986) stated that most mangrove species do not have in-
nate dormancy and will germinate immediately after maturity.
However, recent studies by Clarke et al. (2001) found that
all L. racemosa seeds failed to germinate, probably due to
seed dormancy.
The adaptation of mangrove species to the very un-
stable environments and their distribution along the shore
are controlled by effects of tidal action on the dispersal,
lifespan and germination of diaspores. Inter-tidal zonation
of mangrove species has been noted for a long time and
many hypotheses on “tidal sorting and zonation” were pro-
posed that mangrove zonation is controlled by tidal sort-
ing of the diaspores according to dispersal characteristics
such as size and buoyancy and by differential ability of
diaspores to establish in deep water (Rabinowitz, 1978a;
1978b; Jimenez and Sauter, 1991). However, confusions and
failure in zonation explanation were also reported, and fac-
tors related to diaspore buoyancy and size, root initiation,
and environmental factors are unable to give a complete
account for some mangrove zonation (Bunt, 1996; Ellison
et al., 2000; Clarke et al., 2001). In Hong Kong, the four
non-viviparous mangrove species, L. racemosa, H.
littoralis, E. agallocha and A. ilicifolius, are naturally dis-
tributed at the back of the mangrove swamps, but H.
littoralis is found only at the very high tide position (Tam
and Wong, 2000). Whether such difference in inter-tidal
zonation is related to the “tidal sorting and zonation” hy-
pothesis or due to different reproduction and germination
pattern is unknown.
The present study therefore attempts (1) to investigate
the germination of four non-viviparous mangrove species
in Hong Kong aiming to shorten the germination time and
provide seedlings for mangrove replanting, and (2) to com-
pare diaspore traits of these species to explain their inter-
tidal zonation.
1 Materials and Methods
1.1 Collection and dispersal characteristics of diaspores
Mature diaspores of four non-viviparous mangrove
species, Lumnitzera racemosa (Jack.) Voigt., Heritiera
littoralis (Drgand.) Ait., Excoecaria agallocha L., and
Acanthus ilicifolius L. were collected from Kei Ling Ha
Hoi, one of the typical mangrove swamps in Hong Kong
with permission of the Agriculture, Fisheries and Conser-
vation Department, Hong Kong Government. All of the eight
true mangrove species present in Hong Kong are found in
this swamp, with four non-viviparous species distributed
at the backshore and the viviparous species, Avicennia
marina, Kandelia candel, Bruguiera gymnorrhiza and
Aegiceras corniculatum, in seaward zones. Few seedlings
were found for non-viviparous species while a large num-
ber of young seedlings of the viviparous species were ob-
served in this swamp. Diaspores of L. racemosa, E.
agallocha and A. ilicifolius were considered mature if they
fell from parent trees by gently shaking the branches. Ma-
ture diaspores of H. littoralis were collected on the forest
floor. The shape, weight, size and other traits of mature
fruits were measured from 20 diaspores for each species
immediately after collection. Buoyancy of diaspores was
tested in tanks filled with 15 ppt (ppt, parts per thousand)
seawater. For storage experiments, diaspores of H. littoralis,
E. agallocha and A. ilicifolius were stored at room tem-
perature without any pretreatment and effects of storage
on L. racemosa were described as follows.
1.2 Germination experiments
Some freshly collected fruits of L. racemosa were planted
directly in a greenhouse by four different treatments, each
in triplicate: (1) 40 fruits in sandy soil collected from Sai
Keng mangrove swamp, at the southwest of Kei Ling Ha
Hoi; (2) 40 fruits in 15 ppt seawater; (3) 40 fruits in silty soil
collected from Mai Po mangrove swamp, another typical
mangrove in western Hong Kong; and (4) 40 fruits were
immersed in beakers containing 15 ppt seawater for about
10 h everyday for different days to promote germination
prior to planting in silty soil. The fruits were placed on soil
substrate in the same orientation as those naturally floated
onto tidal water. They were irrigated by 15 ppt seawater on
Acta Botanica Sinica 植物学报 Vol.46 No.6 2004898
the first day and any evaporation loss was compensated
by daily addition of tap water. Percentages of surviving
seedlings were recorded.
For storage experiments on L. racemosa, fruits were kept
in sealed plastic bags, with 100 fruits per bag. The bags
were stored in three conditions, each in triplicate: (1) in a
laboratory cabinet at room temperature of about 25 ℃ (dry
room storage); (2) in a cold room of around 5 ℃ (dry cold
storage); and (3) in shade at room temperature after wetting
the fruits with tap water (wet storage). In addition, some
fruits (100 fruits per replicate and also prepared in triplicate)
were buried in wet sand at a depth of about 2 cm on which
some water was daily sprinkled (sand buried). The appear-
ance of the fruit and the embryo were examined at regular
time interval during a 35-d storage period. At the end of the
storage period, fruits were planted in plastic pots contain-
ing sand and were irrigated with tap water (0 ppt salinity)
for germination. Each pot had ten fruits and six replicate
pots were prepared. The percentage germination, time of
root initiation and time for expansion of the first pair of
leaves were recorded.
Some fruits of L. racemosa were kept under “wet stor-
age” for 50 d, then germinated in pots containing sand.
They were irrigated with water of different salinities: 0 (fresh
water), 5, 15, 25, and 35 ppt. Each pot had ten fruits. Three
replicate pots for each salinity treatment were prepared.
The percentage germination, time for root initiation and
time for expansion of the first pair of leaves were recorded.
A parametric one-way analysis of variance (ANOVA) test
was used to examine the effect of salinity on percentage
germination. Difference in percentage germination between
the two storage time (35 d vs 50 d) under fresh water irriga-
tion was examined by a student t-test.
The fruits of H. littoralis were divided into two portions:
one dissected to remove the hard fruit coat and the second
left intact. The dissection was done by carefully cutting
along the “keel” of the fruit with a sharp knife to avoid
damaging the embryo. Both intact and dissected fruits were
germinated in two soil types, namely sandy mangrove soil
collected from Sai Keng mangrove swamp and terrestrial
soil mixed with compost, with one fruit per plastic bag. When
planted, half of the fruit was buried in soil with the “keel”
upward and the embryo in the downward side. For each
soil type and each fruit treatment (dissected or non-
dissected), 24 bags were prepared. Due to limited availabil-
ity of the fruits, salinity experiment for this species was not
set up.
Fruits of E. agallocha were dissected to remove their
fruit coats, planted in pots containing wet sand (25 fruits
per pot), and irrigated with tap water. Nine replicate pots
were set up. The percentage germination and early seed-
ling growth in each pot were observed. Due to limited avail-
ability of fruits, salinity experiment for this species was not
set up.
Fruits of A. ilicifolius were dissected to remove their
coats, and seeds were germinated in pots containing sand.
They were irrigated with water of different salinities: 0 (fresh
water), 5, 15, 25, and 35 ppt (ten seeds per pot). Three rep-
licate pots for each salinity treatment were prepared. The
percentage germination, time of root initiation and time for
expansion of the first pair of leaves were recorded. ANOVA
test was used to examine the effect of salinity on percent-
age germination.
2 Results
2.1 Diaspore traits
Every adult L. racemosa tree produced thousands of
fruits. Mature fruits were small, with an average weight of
about 0.1 g (Table 1). The seed was well protected by a hard
layer of sclerenchyma tissue inside the outer corky layer of
fruit wall that was very difficult to remove. The mature fruits
were spindly with pale green embryos and sank in seawater.
After the fruits were kept in seawater for more than 20 d,
their embryos died.
In Kei Ling Ha Hoi mangrove swamp, natural recruit-
ment of H. littoralis was less successful than for other true
mangrove species. Only seven seedlings were found in a
natural H. littoralis stand of about 3 hm2. Mature fruit was
ellipsoidal, large and heavy with an average length, width
and height of about 5.5, 4.0 and 3.5 cm, respectively, and
unit weight of about 30 g (Table 1). Over 90% of the mature
fruits fallen on the forest ground was eaten by insects and
dead before germination despite their fruit coats were hard
and thick (about 0.5 cm thick). The fruits had low density,
Table 1 Traits of mature diaspores of the four non-viviparous mangrove species in Hong Kong (n = 20)
Species Type Length Weight Buoyancy
Viable period in Coat
(cm) (g) 15 ppt seawater (d)
Lumnitzera racemosa Fruit 1.5 ± 0.4 0.10 ± 0.03 Sinker <20 Green, thin but hard, difficult to dissect
Heritiera littoralis Fruit 5.5 ± 1.2 30 ± 6 Floater >150 Brown, thick and hard, difficult to dissect
Excoecaria agallocha Seed 0.35 ± 0.03 0.03 ± 0.00 Floater <7 Brown, thin, easy to dissect
Acanthus ilicifolius Seed 1.5 ± 0.3 0.02 ± 0.00 Floater <11 Grey, thin, easy to dissect
ppt, parts per thousand.
YE Yong et al.: Diaspore Traits and Inter-tidal Zonation of Non-viviparous Mangrove Species 899
consistently floated and kept viable in seawater for over
three months.
Among the four non-viviparous species, the weights of
diaspores were in the descending order of H. littoralis > L.
racemosa, > E. agallocha > A. ilicifolius (P < 0.001, by
one-way ANOVA) (Table 1). The last two species had very
small diaspores (seeds) with average fresh weights of only
0.03 and 0.02 g for E. agallocha and A. ilicifolius,
respectively. The former species had spherical seeds while
the latter seeds were flat. Mature seeds of both species
were floaters and kept floating in seawater at all times.
However, all seeds of E. agallocha in seawater died within
7 d while that of A. ilicifolius survived for 11 d. Under dry
conditions, the stored seeds of E. agallocha lost water
rapidly and died within 2 d. Similarly, seeds of A. ilicifolius
turned to black and became rotten within two weeks under
dry storage. The order of longevity of diaspores of the four
non-viviparous mangrove species was H. littoralis > L.
racemosa > A. ilicifolius > E. agallocha while the buoy-
ancy was in the order of H. littoralis = A. ilicifolius = E.
agallocha > L. racemosa.
2.2 Germination
All mature fruits of L. racemosa planted in seawater,
sandy soil (from Sai Keng mangrove) and silty soil (from
Mai Po mangrove) immediately after collection as well as
those planted in silty soil after promoting sprouting in sea-
water for several days failed to germinate and the embryos
were found dead two months after planting. This observa-
tion suggested that freshly collected diaspores were un-
able to germinate.
When L. racemosa fruits were stored under dry condi-
tions at either room temperature or in a cool room, all be-
came black in color with dead embryos after one month of
storage, and seeds shrunk and disappeared. However,
about 30% of the fruits buried in wet sand (sand buried)
had “good” seeds with a size double the original and con-
sisted of viable deep-green colored embryos. When fruits
were under “wet storage”, all became black in color after
35- and 50-d storage, and about 95% of the stored fruits
had “good” seeds with double-sized and deep green
embryos, similar to those of “sand buried”. In both “sand
buried” and “wet storage” treatments, the sclerenchyma-
tous fibers at the tip of the fruit were exposed. These re-
sults suggested that fruits of L. racemosa must be stored
for a period of time under wet conditions to break their
dormancy prior to germination.
After “wet storage” for 35 d, L. racemosa fruits started
to germinate with roots initiated within 12 d of planting
(Fig.1A; Table 2). The average time needed to expand the
first pair of leaves was about 19 d. The cotyledons were out
of the sands while germinating but the fruit coat was still in
the sands after seedling establishment. The final percent-
age germination, about 20% germination on 23 d, was still
low despite the effort to break the dormancy.
The salinity of irrigation water during planting had sig-
nificant effects on germination of “wet stored” fruits of L.
racemosa (Fig.1B; Table 2). The germination rates de-
creased with increased salinities (P < 0.001 according to
one-way ANOVA), and fruits were unable to germinate at
salinities over 25 ppt. According to t-test, the diaspores
Fig.1. Germination pattern of Lumnitzera racemosa diaspores (A) after 35-d “wet storage” under 0 ppt (ppt, parts per thousand)
salinity and (B) after 50-d “wet storage” under different salinities.
Acta Botanica Sinica 植物学报 Vol.46 No.6 2004900
stored for 50 d had significant higher percentage of germi-
nation at 0 ppt than those stored for 35 d (P = 0.049).
Dissected H. littoralis fruits had 100% germination re-
gardless of whether they were planted in mangrove or ter-
restrial soils (Fig. 2A; Table 2). More rapid germination was
found in terrestrial soil than that in Sai Keng mangrove soil
for both dissected and non-dissected fruits (Fig.2A, B).
Dissected fruits had much more rapid germination than non-
dissected fruits. Almost all dissected fruits planted in ter-
restrial soil had root initiations took place 25 d after plant-
ing and the first leaf expansion time was about 63 d, while
the corresponding time of root initiation and leaf expansion
for fruits planted in mangrove soil were 63 and 85 d,
respectively. The non-dissected fruits planted in terrestrial
and Sai Keng soils had average root initiation time of 71
and 109 d, respectively, and the respective time for the first
leaf expansion were 104 and 144 d. These results suggested
that dissecting fruits planted in terrestrial soil mixed with
compost not only enhanced the germination success but
also shortened the germination time.
The diaspores (seeds) of E. agallocha had a relatively
high germination percentage (about 81%), and rapid root
Table 2 Germination indicators of the four non-viviparous mangrove species in Hong Kong
Species Plantation method
Salinity Time for root Time for leaf Final
(ppt) initiation (d) expansion (d) germination (%)
Lumnitzera racemosa Wet stored for 35 d, sand 0 12.0 ± 0.0 (n = 6) 19.2 ± 1.8 (n = 6) 18.7 ± 9.9 (n = 6)
Wet stored for 50 d, sand 0 14.7 ± 3.2 (n = 3) 27.3 ± 7.5 (n = 3) 35.6 ± 10.2 (n = 3)
5 13.3 ± 3.2 (n = 3) 21.0 ± 4.6 (n = 3) 20.0 ± 6.7 (n = 3)
15 19.7 ± 8.5 (n = 3) 27.5 ± 5.0 (n = 3) 20.0 ± 11.5 (n = 3)
25 - - 0
35 - - 0
Heritiera littoralis Dissecting coats, terrestrial soil 0 24.7 ± 8.6 (n = 24) 62.8 ± 10.8 (n = 24) 100
Dissecting coats, mangrove soil 0 62.5 ± 19.7 (n = 24) 85.0 ± 20.5 (n = 24) 100
Not dissecting coats, terrestrial soil 0 71.2 ± 24.2 (n = 12) 104.2 ± 17.0 (n = 12) 50.0
Not dissecting coats, mangrove soil 0 108.5 ± 17.2 (n = 4) 143.8 ± 16.8 (n = 4) 16.7
Excoecaria agallocha Sand 0 2.0 ± 0.0 (n = 9) 11.6 ± 0.5 (n = 9) 81.3 ± 5.0 (n = 9)
Acanthus ilicifolius Sand 0 3.0 ± 0.0 (n = 3) 14.7 ± 0.6 (n = 3) 100.0 ± 0.0 (n = 3)
5 3.0 ± 0.0 (n = 3) 15.3 ± 0.6 (n = 3) 100.0 ± 0.0 (n = 3)
15 3.7 ± 0.6 (n = 3) 18.3 ± 0.6 (n = 3) 100.0 ± 0.0 (n = 3)
25 6.7 ± 0.6 (n = 3) 31.3 ± 2.3 (n = 3) 91.7 ± 8.3 (n = 3)
35 7.7 ± 0.6 (n = 3) 42.3 ± 2.5 (n = 3) 52.8 ± 4.8 (n = 3)
Mean ± SD are shown. Number of replicates per treatment was shown in bracket as n value.
Fig.2. Germination pattern of Heritiera littoralis diaspores planted in terrestrial soil and Sai Keng mangrove soil with (A) fruit coats
dissected and (B) fruit coats non-dissected.
YE Yong et al.: Diaspore Traits and Inter-tidal Zonation of Non-viviparous Mangrove Species 901
initiations of 2 d after planting (Fig.3; Table 2). Similarly,
germination of A. ilicifolius was very successful with 100%
germination at salinities at and less than 25 ppt (Fig.4; Table
2). Salinities had significant effects on germination of A.
ilicifolius (one-way ANOVA test, P < 0.05). The seeds had
100% germination and initiated roots 3-4 d after planting
at salinities below 15 ppt. At higher salinities, rooting and
leaf expansion rates and percentage germination dropped.
As compared to L. racemosa, A. ilicifolius had higher tol-
erance to salinity as the latter species had percentage ger-
mination of 52.8% and 91.7% at salinities of 25 and 35 ppt,
respectively, while the former species was unable to germi-
nate at these two high salinity levels.
Among the four species, L. racemosa had the lowest
seedling survival percentage (<10%). The survived seed-
lings also had the slowest early growth in terms of incre-
ments in stem height (average value of 0.02 cm/d) and di-
ameter (1.50 mm) compared to the other three species (Table
3). On the other hand, nearly 100% of the germinated
seedlings of H. littoralis, E. agallocha and A. ilicifolius
survived. H. littoralis seedlings had the most rapid growth
rate, followed by that of E. agallocha, and A. ilicifolius.
This is probably because more nutrients were available from
the large-sized seeds of H. littoralis for early seedling
growth. There was no significant difference in seedling
growth rates between the dissected and non-dissected H.
littoralis fruits as well as between those planted in terres-
trial and mangrove soils, with height increments of the dis-
sected fruit in terrestrial and mangrove soils of 0.30 and
0.31 cm/d, respectively, while the respective values for the
non-dissected fruits were 0.22 and 0.29 cm/d.
3 Discussion
3.1 Traits of diaspores and germination of non-
viviparous mangrove species
Mature fruits of L. racemosa were small (about 0.1 g)
and the seeds, even smaller, were protected by a hard layer
of sclerenchyma inside the outer corky layer of the fruit
Fig.3. Germination pattern of Excoecaria agallocha diaspores.
Fig.4. Germination pattern of Acanthus ilicifolius diaspores under different salinities. ppt, parts per thousand.
Table 3 Early growth indicators of seedlings of the four non-viviparous mangrove species in Hong Kong
Species Time (d) Height (cm) Growth rate in height (cm/d) Stem base diameter (mm)
Lumnitzera racemosa* 118 2.6 ± 0.2 (n = 4) 0.02 1.50 ± 0.12 (n = 4)
Heritiera littoralis** 132 34.3 ± 3.8 (n = 48) 0.30 3.94 ± 0.30 (n = 48)
Excoecaria agallocha 98 10.9 ± 1.6 (n = 121) 0.11 2.76 ± 0.39 (n = 121)
Acanthus ilicifolius 78 6.3 ± 0.2 (n = 180) 0.08 2.39 ± 0.21 (n = 180)
Mean ± SD are shown. Number of replicates per treatment was shown in bracket as n value. *, only four of all seedlings successfully germinated
after 35 d and 50 d wet storage survived; **, only the seedlings germinated from dissected fruits were measured due to long germination period
for non-dissected ones.
Acta Botanica Sinica 植物学报 Vol.46 No.6 2004902
wall, thus root initiation took a relatively long time, 12 and
15 d after planting fruits stored for 35 and 50 d under wet
conditions (Table 2). This implies that in natural field
conditions, the embryos might be damaged by drought or
other unfavorable circumstances before germination. Field
observation showed that the quantity of seedlings in natu-
ral community was small. Many naturally recruited seed-
lings were found growing in the habitats with a thick growth
of grasses or in areas where the fruits were maintained wet
but not permanently waterlogged, such as stone lacunas.
This indicated that the diaspores of L. racemosa, the sink-
ers as described by Clarke et al. (2001), required some kind
of protection from tidal flushing to germinate. They could
be viable for less than 20 d before germination under condi-
tions without any shelters. Therefore, accurately simulat-
ing sheltered micro-circumstances is very important for this
species to germinate successfully. Although Tomlinson
(1986) classified the germination of L. racemosa as “modi-
fied hypogeal”, we considered it epigeal because the coty-
ledons were out of the sediment while germinating although
the fruit coat was still in the sediment after seedling
establishment, in accord with the description by Clarke et
al. (2001). Compared with the diaspores of other non-vi-
viparous mangrove species, mature fruits of H. littoralis
were large but took a long time to complete germination
because of the hard fruit coats (Table 1). Under natural
conditions, prolonged germination would enhance the
chances of insect infestation, drought damages and other
adverse environments leading to a low germination success.
Field observation showed that over 90% of the mature fruits
were damaged due to insect infection, animal grazing or
microbial degradation. Therefore, it is important to know
that the fruits have viable seeds when collecting and
germinating. Viable fruits could be judged preliminarily by
their weight (the heavier the better), color (the deeper brown
color the better), and integrity (the more the intact the better,
without any sign of infection). The fruit could also be ex-
amined by dissection and the removal of fruit coat to show
whether it consists intact seed or not. The present study
also demonstrated that fruit coat removal by dissection
significantly shortened the rooting and leaf expansion time
without affecting the germination percentage (Table 2).
E. agallocha is a dioecious species with poor seed set
and germination, probably due to the predominance of male
trees over female trees (Rao et al., 1998). Therefore, some
fruits might not bear any fertile seeds. Moreover, the tim-
ing of collecting mature fruits was very crucial for E.
agallocha. Once the fruits reach maturity, they open and
disperse the seeds that then lose the viability quickly if the
seeds have not a chance of germination. We observed that
almost all of the seeds on the forest ground lost their viable
embryos. Mature fruit with brown coats and readily germi-
nated seeds must be collected within a short period of time
(less than 10 d).
3.2 Seed dormancy of L. racemosa
Reduction in seed dormancy was associated with in-
creased seed weight, efficient spatial seed dispersal and
long-lived species (Rees, 1994; 1997). The present study
proved that L. racemosa was indeed a dormant species
although Tomlinson (1986) stated that mangrove species
have no innate dormancy. And all mature fruit planted im-
mediately after collection failed to germinate under various
conditions (silty soil, sandy soil or seawater) and the em-
bryos died two months later. However, if the fruits were
appropriately stored, they were successfully germinated
even after 50-d of “wet storage”. The embryos of L.
racemosa were pale green when collected but turned to
deep green with the embryo size increased to almost double
after “wet storage”. These results reveal that the embryos
in mature fruits picking from parent trees were under-devel-
oped and would continue to develop during the dormant
period. The dormancy was therefore endogenous and be-
longed to morphological dormancy according to the classi-
fication of seed dormancy types by Baskin and Baskin
(1998). Clarke et al. (2001) also regarded L. racemosa as a
dormant species as they found that the diaspores never
showed signs of root or shoot development after planting
but 60% of the fruits still had viable embryos. Nevertheless,
Clarke’s studies did not give sufficient evidence to con-
clude the seed dormancy of L. racemosa. There had not
been any other report on the dormancy type and L. racemosa
seemed to be the only innately dormant plant among all
mangrove species. Further studies on the dormancy of
mangrove plants are needed.
Because of the dormancy, suitable ways to store fruits
of L. racemosa must be identified. From the present results,
wet storage under room temperature or buried in wet sand
were possible, and the “wet storage” seemed to be more
convenient because the latter required daily irrigation and
had a lower percentage of viable seeds. The time needed
for the 35-d stored fruits to have their root and first leaf
expansion were similar to those stored for 50 d, but the
former fruits had lower percentage germination than the
latter one (Table 2). Therefore, “wet storage” for 50 d was
more preferable. However, the maximum storage time and
other methods for dormancy interruption should be further
explored because the highest germination percentages ob-
tained were less than 40% (Table 2), still far from
YE Yong et al.: Diaspore Traits and Inter-tidal Zonation of Non-viviparous Mangrove Species 903
satisfactory.
3.3 Reproductive adaptations of non-viviparous species
to habitats
Mangroves have two reproductive types, namely vi-
viparous (including true- and crypto-viviparous) and non-
viviparous. The focus of mangrove reproduction was mainly
on the viviparous species because it was considered as
one of the important characteristics of mangrove plants
(Tomlinson, 1986). For the viviparous species, the embryo
produced from normal sexual reproduction has no dormancy
but grows to seedling while still attached to the parent
plant. Therefore, their diaspores are neither seeds nor fruits
but seedlings. For viviparous species especially the true-
viviparous ones, the diaspores with special shapes and
morphology can readily anchor the sediment and escape
from tidal flushing. On the other hand, the mature diaspores
of the non-viviparous species, the fruits or seeds but not
seedlings, generally cannot anchor the sediment immedi-
ately after falling from parent trees and are subject to tidal
flushing. It is interesting to know how these diaspores adapt
to mangrove habitats during the inundation periods.
The present study suggested that the four non-vivipa-
rous mangrove species in Hong Kong had three different
mechanisms to adapt the very unstable and ever changing
environment. They were: (1) prolonged longevity and vi-
ability of diaspores as in L. racemosa and H. littoralis by
seed dormancy and hard fruit coat, respectively; (2) short-
ened rooting time for rapid establishment in soil as in E.
agallocha and A. ilicifolius, with roots initiated within sev-
eral days of germination; and (3) produced diaspores of
sinkers as in L. racemosa. These mechanisms allow the
diaspores to have a rapid escape from the adverse circum-
stances especially tidal flushing. In addition to these three
mechanisms, the diaspores of Sonneratia, another non-
viviparous genus, had different adaptive mechanism. In
this genus, the entire seed capsule containing several hun-
dreds of seeds falls from parent trees when the diaspores
(seeds) ripe, sinks very quickly and releases individual di-
aspores which initiate roots and anchor the sediments very
rapidly (Smith, 1992). The sinkable capsule protects the
diaspores from tidal flushing, allowing them to routinely
colonize the lowest inter-tidal zone in spite of their small
size which is only 1.0-1.5 cm in length (Tomlinson, 1986).
3.4 Inter-tidal zonation of non-viviparous species
Inter-tidal zonation has been considered as a common
feature in mangrove swamps, which is often attributed to
dispersal characteristics, animal predation and establish-
ment capacity of diaspores, seedling dimensions, and
physico-chemical factors (Rabinowitz, 1978a; Smith, 1987;
1992; McKee, 1993; 1995; Clarke et al., 2001). However, it
has also been proposed that none of the factors including
rooting time, animal predation, buoyancy and size of
diaspores, and salinity give a satisfactory account for the
zonation of all mangrove species (Bunt, 1996; Ellison et al.,
2000; Clarke et al., 2001). Bunt (1996) summarized that the
distribution pattern of mangrove species across an inter-
tidal mudflat was highly variable, influenced by many fac-
tors and often occurred as multiple distribution centers. In
Hong Kong, the four non-viviparous mangrove species,
distributed at the more backshore locations, shared some
similar diaspore characteristics as the viviparous species
which colonized in the more seaward regions such as larger
diaspores in H. littoralis, sinker diaspores in L. racemosa,
rapid root initiations in E. agallocha and A. ilicifolius. Clarke
et al. (2001) also suggested that viviparous and non-
viviparous mangrove species had similar buoyancy, seed
weight and rates of root and shoot initiation, as well as
early growth and salinity tolerance. These suggested that
zonation explanation for both viviparous and non-vivipa-
rous mangrove species is complicated and it is difficult to
explain why the non-viviparous species were more land-
ward distributed than the viviparous ones.
Nevertheless, the obvious zonation among four non-
viviparous species from seaward to landward in the order
of L. racemosa, E. agallocha, A. ilicifolius, and H. littoralis
might be explained by the diaspore characteristics.
Rabinowitz (1978a) suggested that diaspore characteris-
tics especially buoyancy determined mangrove zonation,
and sinking diaspores would be restricted to lower eleva-
tions while consistently buoyant diaspores were only es-
tablished at higher positions in the inter-tidal zone. The
present study also showed that diaspore buoyancy could
partially explain the zonation of non-viviparous species in
Hong Kong. L. racemosa with sinking diaspores had rela-
tively seaward distribution but the other three non-vivipa-
rous species with buoyant diaspores were more at the back
of the shore.
Root initiation is an important factor, secondary to di-
aspore buoyancy, in determining shoreline zonation of non-
viviparous mangrove species. Clarke et al. (2001) reported
that time taken for a species to develop roots and anchor
sediments, i.e. the obligate dispersal period, corresponded
with the period when diaspores were unable to derive re-
sources from sediments, and considered that backshore
mangrove species had diaspores that were slow to initiate
roots and shoots. This was similar to H. littoralis, the most
backshore species in natural mangrove swamps in Hong
Kong, took an extremely long period to initiate their roots
Acta Botanica Sinica 植物学报 Vol.46 No.6 2004904
(109 d on average) even under favorable conditions.
However, it was strange to find that L. racemosa, the most
foreshore species among the four non-viviparous ones,
still needed more than 10 d for root initiation even after a
necessary long dormancy period (35 d “wet storage”), while
the other more backshore non-viviparous species, E.
agallocha and A. ilicifolius had their root initiations oc-
curred in 2 and 3 d, respectively, even more rapid than the
foreshore viviparous species. Rabinowitz (1978a) also ob-
served that Avicennia and Laguncularia restricted in higher
inter-tidal zones took 5-7 d to initiate their roots, while the
foreshore genera, Rhizophora and Pellciera needed 11-
15 d to become rooted, indicating that the zonation did not
necessarily relate to the rooting time of mangrove diaspores.
Therefore, root initiations could not completely explain
mangrove zonation.
Rabinowitz (1978b) hypothesized that zonation in
Panama mangrove forest was controlled by the size of the
diaspores due to tidal action, and the distribution of man-
grove species from low to high inter-tidal zones were highly
related to the size of their diaspores. She found that
Avicennia and Laguncularia were restricted to high inter-
tidal zone because their small diaspores would be carried to
the farthest land by high tides while species having large
diaspores such as Rhizophora and Pellciera would not be
carried into the high tide areas. The “tidal sorting” hypoth-
esis was resurrected by Jimenez and Sauter (1991) in their
study on zonation of R. racemosa and R. bicolor in Costa
Rica. However, observations on species distribution in
Australia and elsewhere indicated that “tidal sorting” was
not a mechanism influencing mangrove zonation, and the
genera Aegiceras and Avicennia, typically abundant in low
inter-tidal areas had small diaspores (Bunt and Williams,
1981; Wells, 1982). Saenger (1982) investigated seedling
recruitment in mangrove forests at Port Curtis in central
Queensland coast (Australia) and found that R. stylosa
with the largest diaspore among all species was distributed
in all portions of the inter-tidal zone. Smith (1992) also re-
jected the “tidal sorting” hypothesis based on the study
that Sonneratia species routinely colonized the lowest in-
ter-tidal zone had very small diaspores in comparison to
other mangrove plants. Results from the present study
showed that H. littoralis distributed in the highest inter-
tidal zone had heavier diaspores (with average weight of
about 30 g) while the two non-viviparous species, E.
agallocha and A. ilicifolius with very small diaspores were
more towards to seaward zones. These suggested that
mangrove zonation in Hong Kong was not related to the
size of diaspores.
McKee (1995) suggested that physico-chemical factors
influenced mangrove shoreline zonation in Twin Cays and
74% of the variation was explained by intensity of salinity-
related stresses. The present study showed that the inhibi-
tory effects of high salinities on seed germination were
stronger in L. racemosa than that in A. ilicifolius, but the
former species naturally colonizes in more seaward zone
with higher salinity. This suggested that salinity could not
explain non-viviparous mangrove shoreline zonation in
Hong Kong.
Animal predation of diaspores was an important factor
influencing the zonation of mangrove species because
predators (mainly grasped crabs) appears to be the least in
the lowest inter-tidal zone and increases to maximum
amounts in the high inter-tidal zone (Osborne and Smith,
1990). However, over 90% diaspores of H. littoralis distrib-
uted in high inter-tidal zone were attacked and killed by
insect predators. For the other three non-viviparous spe-
cies distributed in more seaward zones, mortality of di-
aspores was not due to animal predations. Therefore, pre-
dation was not sufficient to account for the distribution
pattern of non-viviparous species in mangrove forests of
Hong Kong.
McKee (1993; 1995) reported that seedling dimensions
after establishment would also influence mangrove
zonation, and seedlings with small height and diameter had
backshore distribution because the small stem diameter had
a lower cross-sectional area for oxygen diffusion and lim-
ited aeration of their root systems. However, H. littoralis
distributed in the highest inter-tidal zone had the largest
seedling dimensions among four non-viviparous mangrove
species in Hong Kong, while L. racemosa distributed in the
lowest inter-tidal zone had the smallest seedling
dimensions. These indicated that seedling dimensions also
could not well explain the shoreline zonation of non-vi-
viparous mangrove species in Hong Kong.
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(Managing editor: HAN Ya-Qin)