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Dispersal and germination syndromes of tree seeds in a seasonal
evergreen monsoon rainforest on Hainan Island, China
Wenjie Yang, Fude Liu, Shiting Zhang and Shuqing An
Seed Science Research / Volume 23 / Issue 01 / March 2013, pp 41 55
DOI: 10.1017/S0960258512000293, Published online: 03 January 2013
Link to this article: http://journals.cambridge.org/abstract_S0960258512000293
How to cite this article:
Wenjie Yang, Fude Liu, Shiting Zhang and Shuqing An (2013). Dispersal and germination syndromes of tree seeds in a
seasonal evergreen monsoon rainforest on Hainan Island, China. Seed Science Research, 23, pp 4155 doi:10.1017/
S0960258512000293
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Seed Science Research (2013) 23, 41 – 55
q Cambridge University Press 2013
doi:10.1017/S0960258512000293
Dispersal and germination syndromes of tree seeds in a seasonal
evergreen monsoon rainforest on Hainan Island, China
Wenjie Yang1,2, Fude Liu1,3, Shiting Zhang1 and Shuqing An1*
1
Laboratory of Forest Ecology and Global Changes, School of Life Science, Nanjing University, 22 Hankou Road,
Nanjing, China; 2College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan, China;
3
Key Laboratory of Water Resources and Environment of Shandong Province, Water Resources Research
Institute of Shandong Province, Jinan 250013, China
(Received 31 July 2012; accepted after revision 7 November 2012; first published online 3 January 2013)
Abstract
This paper examines the dispersal – germination
strategy of seeds of 66 native tree species from a
seasonal evergreen monsoon rainforest on Hainan
Island, China, and assesses correlations among seed
germination and phylogeny, dispersal mode and
dispersal season. Seeds of 15, 7, 25 and 19 species
were dispersed during the warm dry (March–May),
rainy (June – September), late rainy (October – November) and cool dry (December – February) seasons,
respectively. Berries (16 species), drupes (14 species)
and capsules (12 species) were common and
represented about 64% of the species. Zoochory
was the most common dispersal mode (69.7%)
followed by anemochory (16.7%) and autochory
(13.6%). More than 65% of species had dormant
seeds. Based on germination speed and synchrony,
six patterns were recognized: rapid and synchronous
germination (13 species), intermediate and synchronous germination (3 species), intermediate and
intermediately synchronous germination (24 species),
intermediate and asynchronous germination
(2 species), slow and intermediately synchronous
germination (5 species), and slow and asynchronous
germination (19 species). One-way ANOVAs revealed
that the variance in germination percentages among
species was largely dependent upon phylogeny. The
mean and median length of germination (MLG) were
largely dependent upon phylogeny, dispersal mode
and dispersal season. Anemochorous seeds germinated faster than autochorous and zoochorous seeds.
Seeds dispersed in the late dry or early rainy season
(March– May) tended to germinate quickly, whereas
those dispersed towards the end of the rainy season
and into the cool dry season are likely to have a much
*Correspondence
Email: anshq@nju.edu.cn
longer length of dormancy. Correlation analyses
indicated that larger seeds germinated faster and
had higher germination percentages.
Keywords: dispersal strategy, germination
phylogeny, seed dormancy, seed mass
time,
Introduction
Seed dispersal and germination are critical periods of a
plant’s life cycle (Harper, 1977; Swaine, 1996). The
timing of seed dispersal and germination plays a key
role, not only in individual plant fitness but also in
plant population dynamics, which may ultimately
affect floristic diversity (Baskin and Baskin, 1998;
Fenner and Thompson, 2005). In temporally and
spatially variable natural environments, unfavourable
conditions for germination may occur unpredictably
(Venable and Brown, 1988). Species therefore have
evolved different strategies to offset these fluctuations
in habitat suitability (Fenner and Thompson, 2005).
Tropical tree seeds exhibit a variety of dispersal and
dormancy characteristics. The timing of dispersal is
often the way by which species synchronize germination timing with favourable conditions for seedling
establishment (Frankie et al., 1974). Dormancy is a
strategic alternative to dispersal (Harper, 1977),
regulating the timing of germination in the field
(Baskin and Baskin, 1998; Fenner and Thompson,
2005). Species also exhibit different germination
characteristics or syndromes (Angevine and Chabot,
1979; Salazar et al., 2011; Silveira et al., 2012); for
example, tropical forest plants display a wide array of
germination strategies, some species germinate just
after dispersal or may even germinate before dispersal,
whereas other species can stay in the soil seed bank
for several years before germination occurs (Garwood,
1983; Vázquez-Yañez and Orozco-Segovia, 1993).
W. Yang et al.
Species exhibit considerable variation in germination time. It is selectively advantageous to maintain
high variability in this trait (Vázquez-Yañez and
Orozco-Segovia, 1993; Baskin and Baskin, 1998; Norden
et al., 2009). Rapid germination may allow seedlings to
grow larger (Black and Wilkinson, 1963), and maintain
competitive dominance over seedlings from seeds that
germinate later (Ross and Harper, 1972). On the other
hand, fast-germinating species may result in the entire
seedling cohort suffering from high mortality in
unpredictable environments. In this case natural selection may favour slow germination (Daws et al., 2007).
Seed germination among species is not only related
to environmental factors, such as temperature, rainfall,
light and altitude (Baskin and Baskin, 1998; Kyereh
et al., 1999; Gutterman, 2000), but also to life-history
attributes, such as seed mass (Garwood, 1983; Leishman et al., 2000), dispersal strategy (Willson and
Traveset, 2000) and phylogeny (Figueroa, 2003;
Bu et al., 2008; Wang et al., 2009). Therefore, to assess
the role of natural selection on seed germination at the
community level, it is necessary to take into account
phylogeny and various biological and ecological factors
when measuring the effect of any single variable.
The montane region of Hainan Island, China, with
its high species richness, represents a key biodiversity
hotspot (Jiang and Lu, 1991; Li, 2002). Demands for
reforestation and restoration of Hainan Island are
increasing following extensive deforestation and longterm intensive agricultural land use (Jiang and Lu, 1991;
Li, 2002). Propagation of native Hainan species from
seeds is important in the conservation of rare species
and in production of plants needed for restoration
projects. However, studies on seed traits, especially
seed mass, germination and dormancy of native species
in Hainan Island of China are limited so far. This study,
at a regional scale, presents information about various
aspects of the whole-seed biology of 66 tree species
native to the Hainan Island, China. Given the wide
variation in seed traits among these species, we tested
differences in seed mass and germination patterns
among different fruit types and species with different
germination syndromes. The objective was also to
determine to what extent dispersal and dormancy
characteristics of seeds of various species fit into the
overall strategy of survival in this biome, and to assess
whether differences in seed germination among species
from the same community are related to phylogeny,
dispersal mode and dispersal season.
west of Hainan Island, China. The tropical evergreen
monsoon forest occurs at 300–700 m altitude. The soil
type of this region is latosol, the mean annual
temperature and annual rainfall are 228C and
2000 mm, respectively (Fig. 1). Rainy and dry seasons
are clearly demarcated, with the dry season occurring
from December to April and the rainy season from May
to October. The vegetation is dominated by species of
Dipterocarpaceae (Hopea hainanensis and Vatica mangachapoi), Lauraceae, Euphorbiaceae, Annonceae and
Myrtaceae (Jiang and Lu, 1991; Li, 2002).
Seed dispersal, maturation and germination
Seeds of 66 endemic species, belonging to 29 families
and 49 genera, were collected from 1 –5 parent trees
when fruits were mature and ripe, between December
2006 and December 2007. All species were selected
because of their commercial and ecological importance, as well as availability of mature seeds during the
period of the experiment. All species are planted in, or
considered feasible for, restoration and timber species
plantations within the tropical rainforest of Hainan
Island, China (Zhou, 2000).
Fruits were cut from branches or collected from the
ground only if they were ‘fresh’ and not decayed.
Species (as reported by Chun, 1964, 1965; Guangdong
Institute of Botany, 1974), their life-form, family, seed
mass, maturation time, possible mode of dispersal and
extraction method from fruits were recorded. The seed
extraction method, depending on the type of fruit,
followed the protocol of Thapliyal and Phartyal (2005):
(1) a single/double/multiple indehiscent fruit,
described as ‘seed’ in the functional sense, required
only drying; (2) dry fruits were split open, followed
by drying in the sun (30 – 358C) for 2 d and seeds were
then extracted by shaking, tumbling, flowing, threshing, etc.; (3) the seeds from dry indehiscent fruits
were extracted by rubbing them dry on a wire-net
cloth and gently pounding with wooden clubs or
hammering; (4) fleshy fruits, sometimes with bony
30
Rainfall
Max temp
Min temp
600
500
20
400
15
300
10
200
Materials and methods
5
100
Study site
0
Temperature (°C)
25
Rainfall (mm)
42
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month
Our study was carried out in the tropical rainforest of
Jianfengling National Natural Reserve (636.84 km2 area;
188200 –188570 N, 1088410 –1098120 E), located to the south-
Figure 1. Monthly rainfall and temperature in the seasonal
evergreen monsoon forest of Hainan Island, China.
Dispersal and germination of tropical tree seeds
endocarp, burst open or required extraction methods
as above; (5) seeds from pulpy fruits were extracted
by heaping the fruits in shade or by soaking to make
the pulp soft and then macerating by hand or on a tray
on wire-net cloth with constant washing in running
tap water.
Following extraction and cleaning, seeds were
dried in the laboratory under a fan or in the sun.
Usually seeds derived from fruits that dry as they
mature were dried in the sun, while those from fruits
that are pulpy at maturity were dried in the shade.
Four replicates of 100 seeds were sown on sand in
plastic trays under 50% of full sunlight. Large seeds
were pushed into the sand for one-half of their
diameter. Small seeds were covered by 1– 3 mm of
sand, if seeds were uncovered after watering they were
covered with sand again. Due to shortage of seeds
from Acmena acuminatissima, Calophyllum inophyllum,
Quercus patelliformis, Sindora glabra and Drypetes
perreticulata, we sowed four replicates of 50 seeds.
Conditions in the nursery were similar to those of the
natural environment. Average monthly rainfall and
temperature (outdoor) data for the past 25 years in the
study area, recorded by the Jianfengling Experimental
Station (Research Institute of Tropical Forestry,
Chinese Academy of Forestry), are presented in Fig. 1.
Germination was defined as emergence of any part of
the shoot, since roots were buried in the sand, and was
monitored every day, based upon interspecific differences until 1 month without any germination. The days
to first germination and last germination of each species
were recorded. The median length of germination time
(the median value of all the times to germination, MLG)
and the mean length of germination time (the mean
value of all the times to germination, mean LG) were
calculated (pooling individuals of each species from
the four replicate batches) from the germination times of
all seeds that germinated. Median lengths of germination time (MLG) for all the seeds that germinated were
calculated as measures of dormancy. Seeds with a
MLG # 30 d were considered to be non-dormant, while
those with MLG . 30 d were considered to be dormant
(Baskin and Baskin, 2004).
For the purposes of nursery production, germination was defined as rapid if the MLG was # 21 d, and
slow if the MLG was $ 84 d. For tree production in
the nursery, germination was defined as synchronous
if all seedlings of a given species emerged within
21 d, and highly asynchronous if this occurred over a
period of more than 84 d (Blakesley et al., 2002).
Following Blakesley et al. (2002), we calculated the
month of peak germination for each species, taking
into consideration month of collection and MLG. For
example, seeds collected in November with an MLG of
62 d will have a peak of germination in January. Then
we plotted the number of species that had their peak of
germination for each month.
43
Statistical analyses
One-way ANOVAs were used to determine the effects
of phylogeny, dispersal mode and dispersal season
on germination percentage, days to first germination,
MLG, mean LG and days to last germination.
(1) Phylogenetic group: to evaluate phylogenetic effect
on germination, each of the 65 angiosperm species
was assigned to an Order according to Angiosperm
Phylogeny Group III (2009): Ericales, Fabales,
Fagales, Gentianales, Gunnerales, Lamiales,
Laurales, Magnoliales, Malpighiales, Malvales,
Myrtales, Oxalidales, Rosales, Sapindales, Saxifragales.
(2) Dispersal mode: each species was assigned to a
dispersal category – anemochorous seeds with
wings, hairs or a pappus; autochorous seeds
having no obvious morphological structure for
dispersal; zoochorous seeds with an aril or flesh.
(3) Dispersal season: according to rainfall and temperature (Fig. 1), dispersal mode was assigned to a
dispersal season category – March–May, June–
September, October–November, December–February.
Pearson correlation analysis was used to determine
the correlation between all variables for germination
studies. Data of germination were checked for
normality and homogeneity of variances, and were
log-transformed when necessary to correct deviations
from these assumptions. All statistical methods were
performed using SPPS Base 15 for Windows (SPSS,
Inc., Chicago, Illinois, USA).
Results
Pattern of seed dispersal syndromes
Overall, berries (16 species), drupes (14 species) and
capsules (12 species) were common and represented
about 64% of the species, followed by legumes
(7 species), nuts (7 species), figs (4 species) and
follicles (4 species). Pomes and samaras were
represented by only one species each. Zoochory was
the most common dispersal mode (69.7%), followed
by anemochory and autochory (16.7 and 13.6%,
respectively). Seeds of 15, 7, 25 and 19 species were
dispersed during the warm dry (March –May), rainy
(June –September), late rainy (October – November)
and cool dry (December –next February) seasons,
respectively (see Appendix).
Dormancy and germination synchrony categories
The MLG ranged from 7 to 272 d, and mean LG ranged
from 10 to 353 d (Table 1). Based on the MLG and 30 d
W. Yang et al.
44
Table 1. Germination data of seeds of 66 species from a seasonal evergreen monsoon forest in Hainan Island, China. Species are
divided into six germination and synchrony categories
Days to first
germination
Days to last
germination
MLG (d)
Mean LG(d)
60.5
24.6
93.2
71.5
65.3
86.7
43.6
95.5
94.5
77.5
82.1
85.5
90.4
10
12
4
9
7
12
6
4
4
10
15
12
12
25
33
15
28
27
24
24
19
19
31
30
47
27
16
18
7
15
11
21
11
7
8
16
20
20
15
18
21.5
9.5
16.5
12.5
20
13.5
9
9
18
22.5
22
17.5
Intermediate germination and synchrony (IG/S)
Castanopsis hystrix
77.3
Beilschmiedia roxburghiana
93.3
Madhuca hainanensis
92.3
19
20
37
40
34
58
24
26
26
25.5
27
29.5
Intermediate germination and intermediate synchrony (IG/IS)
Pithecellobium clypearia
90.5
Pterospermum heterophyllum
86.1
Polyspora balansae
42.3
Schima superba
52.5
Dalbergia hainanensis
65.3
Castanopsis hainanensis
75.2
Tarrietia parvifolia
80.8
Canarium album
86.5
Canarium pimela
86.2
Bridelia balansae
88.4
Endospermum chinense
73.3
Cinnamomum burmanni
80.8
Cryptocarya chinensis
77.6
Cryptocarya concinna
72.1
Machilus chinensis
83.5
Machilus salicina
85.2
Aglaia tsangii
87.3
Ficus altissima
12.1
Ficus benjamina
15.8
Syzygium cumini
80.4
Syzygium bullockii
80.5
Syzygium odoratum
83.1
Eriobotrya deflexa
91.5
Tutcheria multisepala
46.6
26
32
31
18
25
21
25
20
25
26
22
12
40
40
27
30
22
15
12
21
20
20
28
24
56
62
112
58
46
46
50
65
71
56
64
42
118
121
50
54
86
51
48
41
43
55
63
63
40
41
71
31
35
33
35
35
41
36
20
27
65
80
35
35
54
29
29
30
25
29
40
44
41
43.5
71.5
34
37
33.5
36
37.5
43.5
40
24
27
70
80.5
36.5
38
54
29
29
33.5
27.5
32
42.5
43.5
Intermediate germination and asynchrony (IG/AS)
Castanopsis formosana
76.2
Cyclobalanopsis patelliformis
63.6
32
32
128
121
80
77
80
76.5
Slow germination and intermediate synchrony (SG/IS)
Euodia meliaefolia
36.9
Mitrephora thorelii
56.9
Garcinia oblongifolia
81.5
Microcos chungii
25.2
Ardisa densilepidotula
28.6
120
278
180
164
182
162
310
224
190
212
142
290
200
177
197
141
294
202
177
197
Slow germination and asynchrony (SG/AS)
Sapium discolor
82.4
Ormosia balansae
76.2
80
150
196
346
138
248
138
248
Type/species
Germination
percentage (%)
Rapid germination and synchrony (RG/S)
Altingia obovata
Homalium hainanense
Sterculia lanceolata
Aquilaria sinensis
Winchia calophylla
Dolichandrone caudafelina
Radermachera hainanensis
Hopea hainanensis
Vatica mangachapoi
Castanopsis fissa
Bischofia javanica
Syzygium araiocladum
Nephelium topengii
Dispersal and germination of tropical tree seeds
45
Table 1. Continued
Type/species
Ormosia pinnata
Ormosia semicastrata f. litchiifolia
Magnolia lotungensis
Manglietia hainanensis
Michelia balansae
Gleditsia microcarpa
Sindora glabra
Dillenia turbinata
Elaeocarpus sylvestris
Hydnocarpus hainanensis
Garcinia multiflora
Artocarpus styracifolius
Artocarpus nitidus ssp. lingnanensis
Acmena acuminatissima
Syzygium championii
Syzygium chunianum
Symplocos lancifolia
Germination
percentage (%)
Days to first
germination
Days to last
germination
MLG (d)
Mean LG(d)
73.6
86.8
48.5
49.4
45.3
87.8
80.6
55.6
3.5
75.8
80.5
78.6
93.1
73.3
50.2
75.4
30.6
35
150
36
35
85
45
40
54
185
50
180
55
30
90
45
39
68
229
387
183
160
215
60
55
235
441
268
360
159
152
245
183
262
180
132
266
109
97
150
90
86
144
313
159
270
107
91
110
114
150
124
132
269
110
97.5
150
90
86
145
313
159
270
107
91
128
114
151
124
as the time-line, more than 65% (43 of 66) species had
dormant seeds. Based on germination time and
synchrony categories exhibited, six patterns could be
distinguished (Table 1). The first group is characterized by rapid and synchronous germination (RG/S),
e.g. Winchia calophylla, Dolichandrone caudafelina, Radermachera hainanensis, Hopea hainanensis, Vatica mangachapoi, Bischofia javanica, Castanopsis fissa, Altingia
obovata, Syzygium araiocladum, Homalium hainanense,
Nephelium topengii, Sterculia lanceolata and Aquilaria
sinensis. The second group is characterized by
intermediate but synchronous germination (IG/S),
e.g. Castanopsis hystrix, Beilschmiedia roxburghiana and
Madhuca hainanensis. The third group, intermediate
and intermediately synchronous germination (IG/IS),
includes Canarium album, Canarium pimela, Bridelia
balansae, Endospermum chinense, Pithecellobium clypearia,
Dalbergia hainanensis, Castanopsis hainanensis, Cinnamomum burmanni, Cryptocarya chinensis, Cryptocarya
concinna, Machilus chinensis, Machilus salicina, Aglaia
tsangii, Ficus altissima, Ficus benjamina, Syzygium
cumini, Syzygium bullockii, Syzygium odoratum, Eriobotrya deflexa, Pterospermum heterophyllum, Tarrietia
parvifolia, Polyspora balansae, Schima superba and
Tutcheria multisepala. The fourth group is characterized
by intermediate but asynchronous germination (IG/
AS), e.g. Castanopsis formosana and Cyclobalanopsis
patelliformis. The fifth group, slow and intermediately
synchronous germination (SG/IS), e.g. Mitrephora
thorelii, Garcinia oblongifolia, Microcos chungii, Ardisia
densilepidotula and Euodia meliaefolia. The sixth group
was characterized by slow and asynchronous germination (SG/AS), e.g. Dillenia turbinata, Elaeocaepus
sylvestris, Sapium discolor, Gleditsia microcarpa, Sindora
glabra, Ormosia balansae, Ormosia pinnata, Ormosia
semicastrata f. litchiifolia, Hydnocarpus hainanensis,
Garcinia multiflora, Magnolia lotungensis, Manglietia
hainanensis, Michelia balansae, Artocarpus styracifolius,
Artocarpus nitidus ssp. lingnanensis, Acmena acuminatissima, Syzygium championii, Syzygium chunianum and
Symplocos lancifolia. Germination percentages among
species with the six patterns were not significantly
different (F ¼ 1.916, P . 0.05) but the differences in
seed mass among the six patterns were significant
(F ¼ 3.055, P ¼ 0.016). Seeds characterized by intermediate but asynchronous germination (IG/AS) were
the largest, followed by seeds characterized by IG/S,
IG/IS, SG/AS and SG/IS, whereas seeds characterized
by rapid and synchronous germination (RG/S) were
the smallest.
Correlation between germination and phylogeny,
dispersal mode and dispersal season
One-way ANOVAs showed that phylogenetic group
had statistically significant effects on germination
percentages of the 66 species; dispersal season and
dispersal mode had statistically significant effects on
days to first germination; phylogenetic group, dispersal season and dispersal mode had statistically
significant effects on MLG, mean LG and days to last
germination (Table 2).
Species in the Laurales presented the highest
germination percentage (81%), and species in the
Ericales presented the lowest germination percentage
(48%) (Fig. 2a); the days to first germination were not
significantly different among phylogenetic groups;
the MLG and mean LG displayed a significant
difference among phylogenetic groups, species in the
W. Yang et al.
46
Table 2. One-way ANOVAs showing effect of phylogeny, dispersal mode and dispersal season on germination variables among
species
Phylogenetic group
Dispersal mode
2
Source of variation
df
F
Sig.
R
Germination percentage
Days to first germination
MLG
Mean LG
Days to last germination
14
14
14
14
14
5.03
2.13
2.7
2.61
2.85
***
ns
**
**
**
0.58
0.11
0.43
0.42
0.44
df
F
2
2
2
2
2
0.54
7.08
7.95
7.05
7.59
Dispersal season
2
Sig.
R
ns
**
**
**
**
0.02
0.18
0.21
0.19
0.19
df
F
3
3
3
3
3
0.16
2.85
2.91
3.52
3.62
Sig.
R2
ns
*
*
*
*
0.01
0.12
0.12
0.15
0.15
MLG, median value of all the times to germination; mean LG, mean value of all the times to germination.
ns, Not statistically significant. Significance (Sig.) at *, P # 0.05; **, P # 0.01; *** P # 0.001.
Seed mass and germination of species
Correlation analyses showed that seed mass was
positively correlated with germination percentage,
days to first germination, MLG and mean LG.
Germination percentage was negatively correlated
with days to first germination, MLG and mean LG
(Table 3).
Month of peak seed maturation and germination
The number of species with a germination peak in
each month is shown in Fig. 5. Fruits of five species
matured in the hot, dry months (March – April),
36 matured during the rainy season (May –October)
and 25 matured during the cool season (November–
Germination percentage (%)
(a)
90
80
70
60
50
40
30
20
10
MLG
es
Sa
pi
nd
al
es
s
os
al
le
Mean LG
R
M
yr
va
al
M
ta
le
le
s
s
s
ia
gh
pi
al
M
M
ag
no
lia
al
ur
La
First germination
(b) 250
le
es
s
s
le
le
ga
Fa
ba
Fa
Er
ic
al
es
0
Germination time (d)
Last germination
200
150
100
50
s
La
ur
a
M
ag les
no
lia
M
le
al
s
pi
gh
ia
le
s
M
al
va
le
s
M
yr
ta
le
s
R
os
al
Sa
es
pi
nd
al
es
le
s
le
ga
Fa
ba
Fa
ic
al
es
0
Er
Magnoliales presented the longest MLG and mean LG
(44 and 45 d, respectively), species in the Laurales
presented shortest MLG and mean LG (13 and 12 d,
respectively) (Fig. 2b).
Germination percentage of seeds did not differ
among dispersal mode (Fig. 3a). The days to first
germination and days to last germination were
significantly different among dispersal mode: anemochorous seeds presented shortest days to first
germination and days to last germination (16 and
44 d, respectively), and autochorous seeds presented
longest days to first germination and days to last
germination (71 and 184 d, respectively). MLG and
mean LG showed significant differences among
dispersal mode: autochorous seeds presented the
longest MLG and mean LG (both 115 d) whereas
species with anemochorous seeds displayed shortest
MLG and mean LG (26 and 30 d, respectively) (Fig. 3b).
Germination percentage of seeds did not differ
among dispersal season (Fig. 4a). The days to first
germination and days to last germination were
significantly different among dispersal season: seeds
dispersed in March–May presented shortest days to
first germination and days to last germination (16 and
38 d, respectively); seeds dispersed in October –
November presented longest days to first germination
and days to last germination (58 and 145 d, respectively). MLG and mean LG showed significant
differences among dispersal season: seeds dispersed
in March–May presented shortest MLG and mean LG
(26 and 27 d, respectively) and seeds dispersed in
October– November presented longest MLG and mean
LG (both 102 d) (Fig. 4b).
Phylogenetic group
Figure 2. Differences in (a) mean germination percentage
and (b) germination time among phylogenetic groups
(five orders – Gentianales, Gunnerales, Lamiales, Oxalidales
and Saxifragales – with a low number of species were
excluded). MLG, median value of all the times
to germination; mean LG, mean value of all the times
to germination.
Dispersal and germination of tropical tree seeds
80
70
60
50
40
30
20
10
0
Zoochory
(b) 200
180
Germination time (d)
160
Autochory
Anemochory
Autochory
Anemochory
First germination
MLG
Mean LG
Last germination
140
120
100
80
60
40
20
0
zoochory
Dispersal mode
Figure 3. Differences in (a) mean germination percentage and
(b) germination time among dispersal mode groups. MLG,
median value of all the times to germination; mean LG, mean
value of all the times to germination.
February). This seasonal variation resulted in a peak
in nursery germination and seed dispersal, with
the germination peak in March and October, while
seed dispersal peaked in June and December (Fig. 5).
to germination (MTG) ranged from 5 to 207 d (Yu et al.,
2008). For 157 species in a tropical seasonal moist forest
in Panama, the mean length of dormancy (time
between sowing and germination) ranged from 2 to
370 d (Garwood, 1983). Sautu et al. (2006) reported
that mean and median (MLG) lengths of germination
period for 94 species in the same forest type in Panama
were 3.7 – 253 d and 3 –203 d, respectively. For 18
species in a Ghanaian tropical seasonal forest, MTG
ranged from 16 to 79 d in forest understorey and from
15 to 100 d in a forest gap with 30% irradiance (Kyereh
et al., 1999). For 36 tree species in a tropical seasonal
forest in Thailand, the median length of dormancy
(MLD) ranged from 7 to 219 d (Blakesley et al., 2002).
Similarly, in the present study, the MLG ranged from 7
to 313 d and mean LG ranged from 9.5 to 353 d.
Baskin and Baskin (2005) indicated that about
60% of the seeds of tropical rainforest and about 50%
of those of tropical semi-evergreen forest are nondormant at maturity. Here, more than 65% of the 66
studied species had dormant seeds. The proportion
of species with dormant seeds was much higher than
has been reported in several other tropical seasonal
forests. Garwood (1983) reported that about 50% of
157 species had dormant seeds, based on length of
(a)
Germination percentage (%)
Germination percentage (%)
(a)
47
90
80
70
60
50
40
30
20
10
0
Discussion
(b) 160
140
Germination time (d)
In our study, seed dispersal occurred throughout the
rainy and dry seasons. Similarly, Thapliyal and
Phartyal (2005) reported that seeds of 77 studied tree
species matured in the hot, dry summer months
(April –June), rainy season (July – September), cold
season (October – February) and late spring (March) in
a monsoonal forest in northern India. Blakesley et al.
(2002) reported that seeds of the 36 tree species they
studied were dispersed throughout the wet and dry
seasons in a tropical seasonal forest in Thailand. Sautu
et al. (2006) also reported that roughly equal
percentages of seeds of 95 forest tree species were
dispersed during the dry, early rainy and late rainy
seasons in a tropical seasonal forest in Panama.
Considerable variation in mean time to germination has been reported in tropical forests around the
world. For example, for eight species in a tropical
seasonal rainforest in south-west China, the mean time
120
March-May
JuneSeptember
OctoberNovember
DecemberFebruary
OctoberNovember
DecemberFebruary
First germination
MLG
Mean LG
Last germination
100
80
60
40
20
0
March-May
JuneSeptember
Dispersal season
Figure 4. Differences in (a) mean germination percentage and
(b) germination time among dispersal season groups. MLG,
median value of all the times to germination; mean LG, mean
value of all the times to germination.
W. Yang et al.
48
Table 3. Pearson correlation coefficients between seed mass, germination percentage, days to first germination, MLG, mean LG
and days to last germination, calculated from germination data of 66 species from a seasonal evergreen monsoon forest in
Hainan Island, China
Seed mass (g)
Germination percentage (%)
Days to first germination
MLG (d)
Mean LG (d)
Germination
percentage (%)
Days to first
germination
0.435**
0.255*
20.252*
MLG (d)
Mean LG (d)
0.246*
2 0.258*
0.912**
0.248*
20.275*
0.942**
0.980**
Days to last
germination
0.242
2 0.265
0.949**
0.988**
0.995**
MLG, median value of all the times to germination; mean LG, mean value of all the times to germination.
*, Correlation is significant at the 0.05 level. **, Correlation is significant at the 0.01 level.
represented in the three subfamilies of Fabaceae
(Caesalpinoideae, Mimosoideae and Papilionoideae)
(Baskin and Baskin, 1998). In our study, seeds of
S. glabra, P. clypearia, D. hainanensis, O. balansae,
O. pinnata and O. semicastrata f. litchiifolia can be
assigned to physical dormancy. Such dormancy is
caused by one or more layers of palisade cells in the
seed or fruit coat that are impermeable to water
(Baskin et al., 2000). Previous studies of species from
several environments have shown that alternating
temperatures between 15 and 358C can break physical
dormancy of seeds in tree species growing in gaps in
a rainforest in Mexico (Vázquez-Yañes and OrozcoSegovia, 1982) and in non-climax tree species from the
evergreen Atlantic forest (Paula et al., 2012; Souza et al.,
2012). Seeds with physical dormancy in the present
study were dispersed in the late rainy season and
cool dry season. These seeds experience natural
fluctuating temperatures before germination, resulting
in synchronization of the peak of germination with
high rainfall.
Seeds with different dispersal strategies have
been generally viewed as showing an adaptation to
avoid unfavourable conditions (i.e. natural enemies,
sibling interactions, any limitation of available
12
Number of species
dormancy (MLD, days from sowing to germination)
of 4 weeks, in her study of a seasonal tropical forest in
Panama. In another example, of a seasonal moist
tropical forest in Panama, Central America, Sautu et al.
(2006) reported about 48% of 94 tree species with
dormant seeds, based on the median length of
germination (MLG) of 30 d as the time-line between
dormancy and non-dormancy. Seed dormancy can be
an important survival strategy because it prevents
seeds from germinating shortly after maturation,
when seedlings might be exposed to unfavourable
establishment conditions (Clauss and Venable, 2000).
Our results clearly show that seed germination
percentage and germination time (except days to
first germination) among species was strongly related
to phylogenetic group (Order). Previous studies on
various communities, for example, temperate rainforests (Figueroa, 2003), alpine meadows (Bu et al.,
2008) and arid and semi-arid zones (Wang et al., 2009,
2012), have shown that there is a phylogenetic pattern
of seed germination. Our results suggest that variation
in seed germination may be closely related to
phylogeny, i.e. inherent characters of species may
play a prominent role in evolution and phylogeny
of species may play an important role in natural
selection for the regulation of seed germination. Thus,
germination behaviour will be similar in more closely
related species, regardless of ecological factors, than
in distantly related species.
Seeds of M. hainanensis, M. lotungensis, H. hainanensis and M. thorelii were dormant and began to
germinate after 1 –3 months of sand burial in our
study. Seeds of these species belonging to the
Magnoliales have physiological dormancy, requiring
2– 3 months of cold stratification to break dormancy
(Baskin and Baskin, 2005). These species shed their
seeds in the late rainy season and must experience
a period of natural low temperature and a moist
environment to come out of dormancy, which might
ensure that they germinate in the next rainy season.
Physical dormancy has been recorded in 15 families
of angiosperms (Baskin et al., 2000) and is well
Germination
Dispersal
10
8
6
4
2
0
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
Month
Figure 5. Number of species with seed dispersal and
germination peaks in each month (calculated based on
month of seed collection and median length of germination
period).
Dispersal and germination of tropical tree seeds
resources to the parents), as well as to increase the
probability of finding a suitable establishment site
(Janzen, 1970; Cheplick, 1993; Willson and Traveset,
2000). In the present study, seed dispersal period
had no significant effect on seed germination
percentage, but did have a significant effect on
time to germination and could explain independently
12 –15% of the total variance in germination time in
the rainforest. Garwood (1983) recognized three
germination syndromes: the first is delayed-rainy,
seeds are dispersed in the rainy season but germination is delayed until the beginning of the next rainy
season. In our study, G. oblongifolia, M. lotungensis,
M. hainanensis, E. sylvestris, H. hainanensis, M. balansae,
G. multiflora and A. densilepidotula conformed to
the delayed rainy syndrome. The second germination
syndrome is intermediate-dry, seeds are dispersed
during the dry season and germination is delayed
until the beginning of the rainy season. In the present
study, O. semicastrata f. litchiifolia, M. chungii,
E. meliaefolia, S. chunianum, S. championii, S. discolor,
S. lancifolia, A. styracifolius, O. balansae, G. microcarpa,
O. pinnata and C. chinensis can be assigned to
the intermediate-dry syndrome. The third syndrome
is rapid-rainy, seeds are dispersed and germinate
in the rainy season. In our study, N. topengii,
F. benjamina, S. lanceolata, R. hainanensis, S. araiocladum,
B. roxburghiana, S. cumini, A. sinensis, H. hainanense,
V. mangachapoi, S. superba, A. obovata and C. fissa
appeared to be similar to this group. It is important
to link the likelihood of seedling establishment with
the ‘drought avoidance syndrome’ (Angevine and
Chabot, 1979).
Species exhibit considerable variation in dormancy
and germination synchrony. Results of our study show
that species with seeds dispersed in the late dry/early
wet season (March– May) tend to germinate quickly,
whereas those with seeds dispersed towards the end
of the wet season and into the dry season are likely to
have a much longer length of dormancy (Fig. 4), similar
to results of Blakesley et al. (2002) in a tropical seasonal
forest in Thailand. Troup (1921) also described natural
regeneration in many species; seeds of most species
belonging to monsoon forests germinated in nursery
beds near the onset of the rainy season. It is well
recognized that germination at the onset of the rainy
season is an evolutionarily selected trait in seasonal
forests (Garwood, 1983; Marod et al., 2002), which
maximizes the use of the first rainy season for seedling
establishment and increases the survival probability
in the next dry season (Garwood, 1983).
Harper (1977) suggested that germination during
the rainy season may reduce mortality and increase
seedling establishment. In this study, seed germination
occurred not just in the rainy season, but even in the
driest season, which indicates that rainfall itself is
not the only factor determining germination time, as
49
was observed in other dry forests (Garwood, 1983;
Van Schaik et al., 1993; Sautu et al., 2006). Some biotic
factors, such as seed predators and litter, may be an
additional factor affecting seed germination (Molofsky
and Augspurger, 1992; Vallejo-Marı́n et al., 2006).
Seeds of desiccation-sensitive species are much
more likely to be dispersed in the wet season, whereas
those of desiccation-tolerant species are more likely to
be dispersed in the dry season. However, in a tropical
seasonal moist forest in Panama, very short-lived
seeds were reported to be dispersed in the dry (DS),
early rainy (ERS) and late rainy (LRS) seasons (Sautu
et al., 2006). Seed of some desiccation-sensitive species,
for example, V. mangachapoi, N. topengii, A. sinensis, M.
hainanensis, H. hainanensis and S. lanceolata in the
present study were dispersed in less wet (humid)
months. Seeds of these species exhibited rapid
synchronous germination. These species may rely on
a seedling bank rather than a seed bank to persist and
respond to favourable growth conditions and, therefore, require minimal time in the germination stage
when they are particularly susceptible to pests and
diseases (Daws et al., 2005). Rapid germination and
high synchrony is an adaptation for avoidance of seed
predation.
In this study, seed dispersal mode had no
significant effect on the interspecific variation of
germination percentage, but dispersal mode had a
significant effect on germination time and could
explain independently 18 –21% of the germination
time. Wind-dispersed seeds have faster germination
than both unassisted-dispersed seeds and vertebratedispersed seeds. It has been suggested that in some
species seed dormancy may have evolved to reduce
the risk of sibling competition by spreading germination out in time (Venable and Brown, 1988). Venable
and Lawlor (1980) noted that there was a strong
tendency for the poorly dispersed morph to have
delayed germination and the well-dispersed morphs
to have rapid germination.
A majority of fleshy and pulpy fruits produced
seeds that take a long time to germinate, similar to
results reported by Thapliyal and Phartyal (2005) in a
monsoonal forest in northern India. Seeds with fleshy
and pulpy fruits exhibited slow germination and
asynchronous/intermediate synchrony. A long time to
germinate is possibly because of their dependence on
frugivores for dispersal. Seeds that have hard,
mechanically resistant coats that protect the embryo
from damage during chewing or enzymatic action
while passing through the gut, or depend on slow
decomposition or insect action for release of seeds, can
take a long time to germinate. Seeds of some species in
this category take several years to germinate (Troup,
1921) and length of dormancy could be the secondary
effect of a defence mechanism. The germination of
vertebrate-dispersed seeds with fleshy fruit, which
50
W. Yang et al.
may be swallowed by birds or other vertebrates, is
promoted by passage through the animal’s digestive
system (Willson and Traveset, 2000). These requirements have led to selection for delayed germination.
Some seeds of fleshy and pulpy fruits ripen and are
dispersed in the cold season (November or December).
In this case, low temperature and/or lack of moisture
may be another reason leading to slow decomposition
or insect action for release of seeds; thus, they take
a long time to germinate.
Theoretical models predict that small seeds are
more likely to show delayed germination than large
seeds (Venable and Brown, 1988; Rees, 1994; Norden
et al., 2009) and early emergence of large seeds can
compensate for the lower number of seeds by
increasing seedling survival (Westoby et al., 2002).
Conversely, small-seeded species may be more
persistent in the soil seed bank (Venable and Brown,
1988; Rees, 1994), and delayed germination has been
an important factor for the formation of a persistent
soil seed bank. Swanborough and Westoby (1996)
considered that large seeds take a longer time to
germinate than small ones because large seeds need a
longer time for water to permeate than small ones.
Faster germination might give small-seeded species a
survival advantage, especially if conditions for seedling establishment remain favourable for only a short
time (Moles and Westoby, 2004). Seed mass was
weakly correlated with MLG and mean LG in the
present study (Table 3), which is similar to results by
Chen et al. (2002) who found a weak correlation
between germination and seed mass in subtropical
forests in China. Seed mass was significantly positively
correlated with germination percentage across species.
The higher germination percentage of large seeds than
small ones can compensate for the lower number of
seeds by increasing seedling survival (Verdú and
Traveset, 2005).
Acknowledgements
This research was funded by the National Natural
Science Foundation of China (Nos 30570298 and
30430570) and the Special Research Program for
Public-Welfare Forestry (‘Responses of forests to
climate change and adaptive strategy of forestry in
China’, Grant No. 200804001). The authors are grateful
to Professor Yide Li for assistance in this study, and to
Professor Shiman Huang and Mr Chaoyong Wang
for assistance in seed collection and identification of
tree species.
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Appendix
Fruit type, dispersal agent, seed mass, reported fruiting time, month of collection and seed extraction procedure for 66 species from a seasonal evergreen monsoon
forest in Hainan Island, China. Fruiting as reported by Chun (1964, 1965), Guangdong Institute of Botany (1974) and Zhou (2000).
Family/species
Fruiting
as reported
(month)
Month of
collection
Extraction
method
Fruit type
Tree
Bacca
Animal
322.3
5-8
8
5
Tree
Follicle
Wind
3.151
11-2
2
2
Tree
Tree
Capsule
Capsule
Wind
Wind
85.55
1.254
3-4
4-6
3
6
2
2
Tree
Tree
Drupe
Drupe
Animal
Animal
1693
1674
9-11
9-10
11
10
4
4
Tree
Tree
Shrub or tree
Tree
Tree
Tree
Tree
Legume
Legume
Legume
Legume
Legume
Legume
Legume
Gravity
Gravity
Gravity
Wind
Gravity
Gravity
Gravity
91.67
2473
2.635
75.48
803.1
490.8
206.3
11-4
7-9
4-8
11-12
9-11
11
12-1
1
8
6
12
11
1
12
3
3
2
3
2
2
2
Tree
Bacca
Animal
13.25
6-7
6
5
Tree
Tree
Nut
Nut
Wind
Wind
312.1
252.7
3-4
8-9
4
9
1
1
Tree
Drupe
Animal
878.0
8-10
9
4
Tree
Shrub or tree
Tree
Tree
Bacca
Drupe
Drupe
Capsule
Animal
Animal
Animal
Animal
16.07
65.82
13.22
43.05
10-12
11
8-9
5-12
12
11
9
11
5
5
5
2
Tree
Tree
Tree
Tree
Tree
Nut
Nut
Nut
Nut
Nut
Animal
Animal
Animal
Animal
Animal
1346
1388
1714
613.3
3477
10-12
9-10
8-10
11-12
10-11
10
10
9
11
11
1
1
1
1
1
Tree
Bacca
Animal
1232
8-10
10
5
53
Plant form
Dispersal and germination of tropical tree seeds
Annonaceae
Mitrephora thorelii Pierre
Apocynaceae
Winchia calophylla A.DC.
Bignoniaceae
Dolichandrone caudafelina (Hance) Benth & Hook
Radermachera hainanensis Merr
Burseraceae
Canarium album (Lour) Raeusch
Canarium pimela Leenh
Fabaceae
Gleditsia microcarpa Metc
Sindora glabra Merr et De Wit
Pithecellobium clypearia (Jack) Benth
Dalbergia hainanensis Merr et Chun
Ormosia balansae Drake
Ormosia pinnata (Lour) Merr
Ormosia semicastrata f. litchiifolia How
Dilleniaceae
Dillenia turbinata Finet et Gagnep
Dipterocarpaceae
Hopea hainanensis Merr et Chun
Vatica mangachapoi Blanco
Elaeocarpaceae
Elaeocaepus sylvestris (Lour)
Euphorbiaceae
Bischofia javanica Bl
Bridelia balansae Tutch
Endospermum chinense Benth
Sapium discolor (Champ ex Benth) Muell- Arg
Fagaceae
Castanopsis fissa (Champ) Rehd & Wils
Castanopsis formosana (Skan) Hayata
Castanopsis hainanensis Merr
Castanopsis hystrix A.DC
Cyclobalanopsis patelliformis (Chun)
Flacourtiaceae
Hydnocarpus hainanensis (Merr) Sleum
Seed
mass (mg)
Dispersal
mode
54
Appendix Continued
Family/species
Fruit type
Dispersal
mode
Seed
mass (mg)
Fruiting
as reported
(month)
Month of
collection
Extraction
method
Tree
Tree
Bacca
Bacca
Animal
Animal
2880
801.1
10-11
8-10
10
9
5
5
Tree
Capsule
Wind
9.215
10
10
2
Tree
Tree
Tree
Tree
Tree
Tree
Drupe
Drupe
Drupe
Drupe
Drupe
Drupe
Animal
Animal
Animal
Animal
Animal
Animal
872.4
118.0
406.0
416.4
1664
318.8
5-7
3-4
8-12
10
2
7-8
6
4
2
6
3
7
4
4
5
5
4
4
Tree
Tree
Tree
Follicle
Follicle
Follicle
Animal
Animal
Animal
114.4
465.2
152.1
8-10
9-11
9-10
10
10
9
2
2
2
Tree
Bacca
Animal
2626
7-8
7
4
Tree
Tree
Tree
Tree
Figs
Figs
Figs
Figs
Animal
Animal
Animal
Animal
236.3
297.5
0.2615
0.3833
10-11
9-10
11-12
1-12
11
9
11
5
5
5
5
5
Tree
Bacca
Animal
113.3
8-10
10
5
Tree
Tree
Tree
Tree
Tree
Tree
Shrub or tree
Bacca
Bacca
Bacca
Bacca
Bacca
Bacca
Bacca
Animal
Animal
Animal
Animal
Animal
Animal
Animal
1309
442.3
50.25
200.7
279.0
608.8
120.8
12
6
12
6
6
12
11
12
12
5
5
5
5
5
5
5
Tree
Pome
Animal
522.3
10
10
4
Tree
Capsule
Gravity
8.533
11-12
12
2
Tree
Capsule
Wind
1.011
7-8
8
2
Tree
Drupe
Animal
777.1
5-6
5
5
12-1
W. Yang et al.
Clusiaceae
Garcinia multiflora Champ
Garcinia oblongifolia Champ
Hamamelidaceae
Altingia obovata Merr et Chun
Lauraceae
Beilschmiedia roxburghiana Nees
Cinnamomum burmanni (Nees) Bl
Cryptocarya chinensis (Hance) Hemsl
Cryptocarya concinna Hance
Machilus chinensis (Champ) Hemsl
Machilus salicina Hance
Magnoliaceae
Magnolia lotungensis Chun et C Ysoong
Manglietia hainanensis Dandy
Michelia balansae (A. DC.) Dandy
Meliaceae
Aglaia tsangii Merr
Moraceae
Artocarpus styracifolius Pierre
Artocarpus nitidus ssp. lingnanensis Merr.
Ficus altissima Bl
Ficus benjamina L
Myrsinaceae
Ardisia densilepidotula Merr
Myrtaceae
Acmena acuminatissima (Bl) Merr & Perry
Syzygium cumini (L) Skeels
Syzygium araiocladum Merr & Perry
Syzygium bullockii (Hance) Merr et Perry
Syzygium championii (Benth) Merr et Perry
Syzygium chunianum Merr et Perry
Syzygium odoratum (Lour) DC
Rosaceae
Eriobotrya deflexa (Hemsl) Nakai
Rutaceae
Euodia meliaefolia (Hance) Benth
Samydaceae
Homalium hainanense Gagnep
Sapindaceae
Nephelium topengii (Merr) H S Lo
Plant form
Appendix Continued
Family/species
Fruit type
Dispersal
mode
Seed
mass (mg)
Fruiting
as reported
(month)
Month of
collection
Extraction
method
Tree
Bacca
Animal
882.8
3-4
4
5
Tree
Tree
Tree
Capsule
Capsule
Samara
Wind
Animal
Gravity
65.32
503.5
3022
9-10
6
8-9
12
6
8
2
2
1
Tree
Drupe
Animal
33.51
9-10
11
5
Tree
Tree
Tree
Capsule
Capsule
Capsule
Wind
Wind
Animal
9.812
4.522
360.5
7-9
9-10
1-12
8
9
12
2
2
4
Tree
Capsule
Gravity
141.8
7-8
8
2
Tree
Drupe
Animal
130.4
11-12
10
5
Dispersal and germination of tropical tree seeds
Sapotaceae
Madhuca hainanensis Chun & How
Sterculiaceae
Pterospermum heterophyllum Hance
Sterculia lanceolata Cav
Tarrietia parvifolia (Merr) Merr & Chun
Symplocaceae
Symplocos lancifolia Sieb & Zucc
Theaceae
Polyspora balansae (Pitard) Hu
Schima superba Gardn et Champ
Tutcheria multisepala Merr et Chun
Thymelaeaceae
Aquilaria sinensis (Lour) Spreng
Tiliaceae
Microcos chungii (Merr) Chun
Plant form
55