Annals of Botany 96: 69–80, 2005
doi:10.1093/aob/mci150, available online at www.aob.oupjournals.org
Wind-dispersed Seed Deposition Patterns and Seedling Recruitment of
Artemisia halodendron in a Moving Sandy Land
F E N G - R U I L I 1,*, T A O W A N G 1, A I - S H E N G Z H A N G 1, L I - Y A Z H A O 1,
L I N G - F E N K A N G 1 and W E N C H E N 1,2
1
Key Laboratory of Desert and Desertification, Cold and Arid Regions Environmental and Engineering Research Institute,
Chinese Academy of Sciences, 260 Donggang West Road, Lanzhou 730000, China and 2School of Agriculture and Wine,
Faculty of Sciences, the University of Adelaide, Roseworthy Campus, Roseworthy, SA 5371, Australia
Received: 9 October 2004 Returned for revision: 19 January 2005 Accepted: 25 February 2005 Published electronically: 27 April 2005
Background and Aims Artemisia halodendron is a native sub-shrub that occurs mainly in moving and semi-fixed
sandy lands in Inner Mongolia, China. Information on the spatial patterns of wind-dispersed seed deposition and
seedling recruitment of A. halodendron inhabiting moving sandy lands is very limited. The aim of this study was to
examine wind-dispersed seed deposition patterns and post-dispersal recruitment of A. halodendron seedlings.
Methods The spatial patterns of wind-dispersed seed deposition and seedling recruitment of A. halodendron were
examined by investigating the numbers of deposited seeds, emerged and surviving seedlings using sampling points
at a range of distances from the parent plant in eight compass directions for two consecutive growing seasons.
Key Results Wind-dispersed seed deposition showed considerable variation between directions and years. Wind
transported A. halodendron seeds only a few meters away from the parent plant in all eight directions. Seedling
emergence and establishment also showed between-direction and between-year variability, but the spatial pattern of
seedling distribution differed from that of seed deposition. Only a very small fraction (<1 %) of the deposited seeds
emerged in the field and survived for long enough to be included in our seedling censuses at the end of the growing
season.
Conclusions The spatial variation in wind speed and frequency strongly affects the pattern of seed deposition,
although the variation in seed deposition does not determine the spatial pattern of seedling recruitment. Seeds of
A. halodendron are not dispersed very well by wind. The low probability of recruitment success for A. halodendron
seedlings suggests that this species does not rely on seedling recruitment for its persistence and maintenance of
population.
Key words: Artemisia halodendron, Horqin Sandy Land, moving sand dunes, population dynamics, post-dispersal recruitment, recruitment success, sand-stabilizing plant, seed deposition, seedling emergence, seedling survival, wind dispersal.
INTRODUCTION
The Horqin Sandy Land of eastern Inner Mongolia is one of
the four well-known sandy areas in northern China (Li et al.,
2003a). Over the last few decades, the areas being affected
by desertification in this region have been spreading at an
annual average rate of about 2000 km2 per year, primarily
due to poor land management, such as over-cultivation
(conversion of grassland to farmland), intensive firewood
collection and overgrazing (Wang et al., 2003). The consequences of land desertification are a substantial loss of
the region’s biodiversity and productivity, as well as a range
of negative environmental and socio-economic impacts
(Jiang et al., 2003). For example, once the vegetation in
sandy grasslands has been destroyed by overgrazing or other
human activities, the soils become less stable and highly
erodable (Li et al., 2003a, 2005a), which, in the long-term,
will result in a new source of material that could contribute
to the dust-storms that occur frequently in the arid and semiarid lands of northern China (Xuan et al., 2000). Efforts
have been made since the late-1970s (particularly in recent
years) to combat desertification in the Horqin region. One of
the most effective practices has been to plant native species
that are adapted to a sandy land environment on severely
* For correspondence. E-mail [email protected]
degraded land (T. H. Zhang et al., 2004). However, the
success of this technique is strongly dependent on the
selection of the right species for re-vegetation.
Artemisia halodendron is a native sub-shrub that occurs
primarily on moderately-to-severely degraded semi-fixed
and moving sandy lands in the Horqin Sandy Land and
is often the dominant species in these grassland types
(Li, 1991). Due to its low nutrient requirements and high
capacity to produce offspring through vegetative propagation under conditions of sand burial, A. halodendron easily
colonizes bare patches to establish populations in unstable,
nutrient-poor moving sandy lands (Li and Zhang, 1991;
Chang et al., 1994; Li et al., 2002). Thus A. halodendron,
as an ideal sand-fixing plant, has been widely used for
re-vegetation on severely degraded sandy land. The value
of this species is that once a population has been established,
it will act both as a seed accumulator by physically trapping
dispersing seeds (Aguiar and Sala, 1997; Pugnaire and
Lázaro, 2000) and as a sink for resources, either actively
through root uptake of soil water and nutrients (Hook et al.,
1991; Gutiérrez et al., 1993; Burke et al., 1995) or passively
by accumulating wind-blown dust and litter (Barth and
Klemmedson, 1982; Garner and Steinberger, 1989) in a
feedback mechanism that facilitates invasion and colonization by other plant species under or near its canopy. This
ª The Author 2005. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved.
For Permissions, please email: [email protected]
Li et al. — Seed Deposition and Seedling Recruitment
70
25
Wind speed
Wind frequency
20
6
15
4
10
2
0
5
5
0
15
B
NNW
NW
W
WSW
WNW
Wind direction
SW
SSW
0
S
0
SSE
3
SE
1
ESE
6
E
2
ENE
9
NE
3
NNE
12
N
4
Wind frequency (%)
Wind speed (m s–1)
A
Wind frequency (%)
Wind speed (m s–1)
8
F I G . 1. Wind speed and frequency (the number of hourly measurement points at which wind was blowing from that direction) for 16 compass directions over
the potential dispersal period from late-October to May between 1997 and 2002 (mean 6 s.e.). (A) Based on the data set excluding winds that occurred
with a speed less than 4 m s1 at 2 m height. (B) Based on the complete data set. N = 350–11 , NNE = 12–34 , NE = 35–56 , ENE = 57–79 , E = 80–101 ,
ESE = 102–124 , SE = 125–146 , SSE = 147–169 , S = 170–191 , SSW = 192–214 , SW = 215–236 , WSW = 237–259 , W = 260–281 , WNW = 282–304 ,
NW = 305–326 , NNW = 327–349 .
results in an increase in biodiversity of the moving sandy
land ecosystem (Pugnaire et al., 1996; Li et al., 2003b).
A number of recent studies of A. halodendron have
examined its ecological and morphological attributes (Li
and Zhang, 1991), its variation patterns of reproductive
allocation under different habitats (Li et al., 2005b), its
distribution patterns of populations in differently degraded
sandy lands (Chao et al., 1999), and its mechanisms of
physiological adaptation to the harsh sandy land environments, which are characterized by frequent drought, high
temperature and sand burial (Wang and Zhou, 1999; Zhou,
1999; Zhou et al., 1999). However, few studies have
examined the combination of the spatial patterns of seed
deposition by wind dispersal of A. halodendron and its postdispersal germination and seedling establishment. The aim
of this study was to address the following: (1) the spatial
pattern of wind-dispersed seed deposition; (2) the consequences of post-dispersal seedling recruitment, including
seedling emergence and establishment; and (3) to determine
if there is spatial concordance between seed deposition and
seedling distribution (i.e. does the spatial variation in seed
deposition determine recruitment pattern?).
MATERIALS AND METHODS
Study site and experimental species
The study was conducted from 2002 to 2003 on a natural
moving sandy land at Shelihu in Naiman County, Inner
Mongolia Autonomous Region, China (42 550 N, 120 440 E;
altitude approx. 360 m a.s.l.), 520 km north-east of Beijing
(Li et al., 2003a). Naiman is situated in the southern part of
the Horqin Sandy Land, which is roughly 400 · 400 km in
size and represents one of the worst examples of land desertification in northern China (Andrén et al., 1994). The landscape in this area is characterized by sand dunes alternating
with gently undulating lowland areas. The soils are sandy,
loose in texture, and particularly susceptible to wind erosion
(Li et al., 2003a). The climate is temperate, semi-arid and
continental, receiving 360 mm annual mean rainfall, with
75 % of this falling in the June–September period. Highly
variable rainfall in the growing season (April–September:
coefficients of variation 75 %, 54 %, 51 %, 60 %, 51 % and
124 %) results in unreliable plant growth and development
in most years. Climatic conditions in both years of the study
were dry, with 2002 receiving only 58 % (207 mm) of the
long-term average and 2003 receiving 69 % (249 mm).
There is little rain or snow in the late autumn–early spring
period and this is coupled with frequent and high winds.
Hence the period from late October to May has been shown
to be the major wind-erosion season (Li et al., 2003b), as
well as the major dispersal season for plant seeds (diasporas). Based on wind data (1997–2002) from the weather
station of the Naiman Desertification Experiment Station,
the annual mean wind speed ranges between 34–41 m s1
at 2 m height, and the prevailing wind directions over the
erosive season are S, SSW, SW, NNW, WNW, NW, N and
NNE. These winds occur with high speeds in excess of
4 m s1 at 2 m height (a threshold wind speed to initiate
sand movement; H. Zhang et al., 2004) in most days of the
erosive season (Fig. 1).
Li et al. — Seed Deposition and Seedling Recruitment
The study area was originally a grass-dominated steppe
community with sparsely distributed woody species (mainly
elm, Ulmus spp.). When the study was initiated, the original
vegetation had been substantially degraded, primarily due to
overgrazing by livestock (Li et al., 2000). Degraded grassland is generally classified into three main forms: fixed or
stabilized (light degradation), semi-fixed or semi-stabilized
(moderate degradation) and moving or unstabilized (severe
degradation), and these three forms represent a realistic
range of historical grazing activities and impacts (Zhao
et al., 2003). The severely degraded moving sandy land
is characterized by a very low vegetation cover dominated
by annual plant species. The most abundant species are
the annual chenopods Corispermum macrocarpum Bge.,
Salsola collina pall. and Agriophyllum squarrosum (L.)
Moq., and the annual grass Setaria viridis (L.) Beauv.,
which accounted for over 90 % of the total cover.
At the study site, Artemisia halodendron Turcz. ex Besser
(Asteraceae) is distributed primarily in moving and semifixed sandy lands, but rarely in fixed sandy lands. It is a
deciduous sub-shrub, with well-developed rhizome system.
In general, A. halodendron flowers in early July and sets
seed in early August, and seed matures in early October
(Li and Zhang, 1991). After ripening, A. halodendron seeds
(achenes) naturally fall on the ground around the parent
shrubs. According to our estimation from sampling 60 individual adult plants, mean seed production was 29 g per plant
and mean thousand-seed weight was 61 g 6 021 (6s.e.).
Experimental design and data collection
The experiment was conducted on a natural moving
sandy land that had been protected from livestock grazing
since 2000. The experimental site is open and level, covering an area of about 30 ha. In early spring 2002, six
individual adult A. halodendron plants of similar sizes
(plant height /canopy diameter: 70/278 cm, 84/310 cm,
85/290 cm, 63/241 cm, 64/269 cm, 67/281 cm) were chosen
to be ‘target plants’. Each of the six target plants was growing at least 30 m away from any other A. halodendron
shrubs, to ensure seed deposition patterns around each target
plant were not being affected by seed rain from other plants.
To determine the spatial patterns of wind-dispersed seed
deposition, sampling lines were set up along eight compass
directions (at 45 intervals, i.e. north, north-east, east, southeast, south, south-west, west, north-west) centred on each
target plant. In each of the eight directions, six sampling
points were placed at distances of 05, 1, 2, 3, 45 and 6 m
away from the target plant.
Measurements of densities of deposited wind-dispersed
seeds were made during the first week of April 2002 and
2003, before the seed rain and germination period. Thus, all
viable seeds found in the soil can reliably be assumed to
have originated from previous years, and all had passed
through at least one winter season with the cold stratification
needed to break dormancy (Baskin and Baskin, 1998). At
each of the six sampling points for each direction, a soil seed
bank sample of 20 · 20 cm and 5 cm deep was collected.
This sampling depth was chosen for two reasons. One is that
most A. halodendron seeds are retained at this depth, based
71
on a previous field study (Li et al., 2003c). The other is that
almost no seedlings emerged when A. halodendron seeds
were buried at a depth of >5 cm according to a laboratory
germination experiment (L. Y. Zhao, unpubl. res.). The
collected soil samples were germinated in plastic trays.
The trays were first filled with seed-free fine loam about
70 mm deep, and then the soil samples were spread to form a
uniform, thin layer (4–6 mm) and covered with 1–2 mm of
seed-free fine sand. All trays were placed in an unheated
greenhouse and the viable seed density estimated from
counts of seedlings that emerged over the following 12week period. The seedlings were counted at 3–4 d intervals
(Zhao et al., 2003). Interpretation of seed deposition patterns requires caution as variation in deposited seed density
may include both variations in pre- and post-dispersal seed
losses from the soil.
To examine the consequences of post-dispersal seedling
recruitment, we investigated the number of A. halodendron
seedlings that emerged at each of the six sampling points
of each direction in both years. For each year, seedling
censuses were made at two dates: one at the end of June
(representing mid-stages of the growing season) and again
at the end of August (representing late stages of the growing
season), using 1 m2 quadrats that were placed in close
vicinity to the sampling points of the seed bank. To assess
the success of recruitment, the recruitment process was
divided into two distinct phases: seed to emergent seedlings,
and emergent seedlings to established seedlings. The first
phase includes the process of emergence, and the probability of emerging success (the mean number of seedlings per
viable seed) is described as the emergence, which was calculated as a percentage of the cumulative number of
emerged seedlings over a period from late-April to the
end of June across all six sampling points of each direction
relative to the cumulative number of deposited seeds in the
5 cm soil layer. The second phase, including the process of
post-emergence establishment and the probability of establishing success (the mean number of established seedlings
per emerged seedling), is described as the seedling survival,
which was calculated as a percentage of the cumulative
number of established seedlings at the end of the growing
season relative to the cumulative number of emerged seedlings. The overall recruitment success relies not only on
emergence success but also establishment success, so the
probability of recruitment success can be described by the
recruitment index (RI), which is decomposed into the product of emergence and survival.
Data analysis
The repeated measures analysis of variance (ANOVA) of
the general linear model was performed to test for the
effects (using a random model) of year, direction and
their interactions on the number of deposited seeds at
each of the six sampling points. The repeated measures
ANOVA was also used to test for the effects of year, direction and their interactions on the cumulative numbers of
deposited seeds, emerged seedlings and established seedlings, as well as on emergence, survival and RI. Differences
between directions were compared using Tukey’s tests and
Li et al. — Seed Deposition and Seedling Recruitment
4000
Cumulative no. of
deposited seeds m–2
the significance of differences between the two years of the
study was determined using paired t-tests. When a significant interaction between year and direction was detected for a
response variable, we analysed the effect of direction within
years and the effect of year within directions. Regression
analysis was used to determine the relationship between
deposited seed density and dispersal distance. To explore
the relationship between seed deposition pattern and seedling distribution pattern, linear regression analysis was also
performed to test whether deposited seed density affected
emergence. The data were tested for normality using the
criteria of skewness (Webster, 2001). A log(n + 1) transformation was performed for the numbers of deposited
seeds, and emerged and established seedlings, and an arcsine square-root transformation was used for emergence,
survival and RI prior to analysis. However, untransformed
values are presented in the text.
Although the cumulative number of deposited seeds over all
sampling points and directions was similar between years
(mean 6 s.e.: 1262 6 154 vs. 972 6 88 seeds m2 in 2002
and 2003, respectively; F1,95 = 005, P = 03094), the cumulative number of deposited seeds over sampling points and
years varied between directions (F7,95 = 616, P < 00001).
The cumulative number of deposited seeds was significantly
higher in the south-west than in other directions, except for
the south-east and the west (Fig. 2). There was a significant
year–direction interaction (F7,95 = 873, P < 00001) on the
cumulative number of deposited seeds. In 2002, the maximum seed deposition density was noted in the south-west
and the minimum deposition density in the north, whereas
the maximum seed deposition density was found in the
north and the minimum deposition density in the south in
2003 (Fig. 2).
Over 90 % of the dispersed seeds were deposited within 2
m of the parent plant but deposition densities were very low
beyond 2 m when averaged across years (Fig. 3). Similar
results were observed when the data were analysed for each
year, despite some differences in the spatial pattern of seed
deposition between the two years (data not shown). Regression analyses showed a linear decrease of seed deposition
density with increasing distance in all eight directions,
although there were some differences in the relative rate
of decrease between directions (Fig. 4).
Spatial patterns of seedling emergence and establishment
Although seedling emergence in A. halodendron commences in late April, a major emergence period occurs
between May and June (according to our observations).
The cumulative emergence of seedlings over a period
from late-April to the end of June varied significantly
between years (F1,95 = 13934, P < 00001), with a 10-fold
higher cumulative emergence count in 2003 (58 6 6 seedlings m2) than in 2002 (6 6 07 seedlings m2). A significant difference in cumulative emergence of seedlings was
ab*
2000
1000
abc
bc*
bc
bc
cd
d*
3000
2003
2000
a
ab
abc
abc abc
abc bc
1000
c
0
Cumulative no. of
deposited seeds m–2
Spatial patterns of wind-dispersed seed deposition
a*
3000
3000
RESULTS
2002
0
Cumulative no. of
deposited seeds m–2
72
2002 + 2003 combined
a
ab
2000
abc
c
1000
c
bc
c
bc
0
N
NE
E
SE S SW W NW
Direction
F I G . 2. Cumulative number of deposited seeds across all six sampling
points for each direction in each of the two years, and the combined data
(mean 6 s.e.). Different letters indicate a significant difference between
directions (P < 005 from Tukey’s tests). *Indicates a significant difference
between means of the two years (P < 005 from paired t-tests).
also observed between directions (F7,95 = 438, P = 0035),
with a significantly higher cumulative number of emerged
seedlings in the north-east than in other directions except for
the east, south-east and north-west when averaged across
years (Fig. 5).
The spatial pattern in seedling emergence varied between
years (significant year–direction interaction: F7,95 = 244,
P = 00254). In 2002, the cumulative emergence counts
were significantly higher in the north-east than in other
directions except for the east and south-east, whereas in
2003 the corresponding value was significantly higher in
the north-east, east and south-east than in other directions
except for the north-west and north (Fig. 5). The spatial
pattern of seedling distribution differed remarkably from
that of seed deposition. Seed deposition density was lowest
in the north-east while the cumulative emergence of seedlings was highest in this direction. Likewise, seed deposition density was highest in the south-west, but the
cumulative emergence of seedlings was lowest in this
direction (Figs 2, 5).
Post-emergence establishment of seedlings also varied
between years (F1,95 = 1494, P = 00062), with a significantly higher cumulative number of surviving seedlings at
the end of the growing season in 2003 (92 6 14 seedlings
m2) than in 2002 (13 6 02 seedlings m2). Although no
73
Li et al. — Seed Deposition and Seedling Recruitment
500
400
40
300
200
20
100
0
E
600
300
20
200
100
0
S
200
20
0
0
W
800
400
20
200
0
0·5 1·0 2·0 3·0 4·5 6·0
Distance from parent plant (m)
SE
40
600
20
300
0
SW
1500
1200
60
900
40
600
20
60
0
900
300
0
NW
600
40
400
20
200
0
0·5 1·0 2·0 3·0 4·5 6·0
Distance from parent plant (m)
No. of deposited seeds m–2
600
40
0
0
No. of deposited seeds m–2
Relative density (%)
60
100
No. of deposited seeds m–2
400
40
200
20
80
600
No. of deposited seeds m–2
Relative density (%)
60
300
0
Relative density (%)
0
Relative density (%)
Relative density (%)
400
40
No. of deposited seeds m–2
40
500
400
60
No. of deposited seeds m–2
500
NE
0
Relative density (%)
0
60
60
Relative density (%)
N
No. of deposited seeds m–2
Relative density
No. of deposited seeds
No. of deposited seeds m–2
Relative density (%)
60
0
F I G . 3. Relative density (% of cumulative number of deposited seeds) and absolute number of deposited seeds at each of the six sampling points at varying
distances from the parent plant in eight directions (mean 6 s.e.). Data from the two years are combined. N = 350–11 , NE = 35–56 , E = 80–101 , SE =
125–146 , S = 170–191 , SW = 215–236 , W = 260–281 , NW = 305–326 .
statistical difference was found in cumulative survival
counts between directions (F7,95 = 081, P = 06145), the
cumulative number of surviving seedlings was highest in the
north-east and lowest in the south-east when averaged
across years (Fig. 5). There was also a significant interaction
between year and direction on seedling survival (F7,95 =
931, P < 00001), indicating that the effect of year on
this variable varied between directions (Fig. 5).
Li et al. — Seed Deposition and Seedling Recruitment
74
Log no. of deposited seeds m−2
y = −0·328x + 2·314
N
4
y = −0·425x + 2·4439
S
R2 = 0·333, P < 0·0001
y = −0·244x + 2·438
W
R2 = 0·635, P < 0·0001
R2 = 0·288, P < 0·001
3
2
1
0
Log no. of deposited seeds m−2
4
y = −0·240x + 2·382
E
R2 = 0·407, P < 0·0001
NE
y = −0·299x + 2·394
SW
y = −0·416x + 2·853
y = −0·361x + 2·545
NW
R2 = 0·555, P < 0·0001
R2 = 0·625, P < 0·0001
3
2
1
0
Log no. of deposited seeds m−2
4
y = −0·406x + 2·952
SE
R2
= 0·686, P < 0·0001
All directions combined
y = −0·341x + 2·540
R2 = 0·633, P < 0·0001
R2 = 0·484, P < 0·0001
3
2
1
0
0
1
2
3
4
5
6
7
0
Distance from parent plant (m)
1
2
3
4
5
6
Distance from parent plant (m)
7
0
1
2
3
4
5
6
7
Distance from parent plant (m)
F I G . 4. Relationship between deposited seed density and dispersal distance from the parent plant for eight different directions. Data from the two years are
combined. N = 350–11 , NE = 35–56 , E = 80–101 , SE = 125–146 , S = 170–191 , SW = 215–236 , W = 260–281 , NW = 305–326 .
Recruitment success and the effect of seed deposition
density on recruitment
Although emergence was significantly higher (F1,95 =
16622, P < 00001) in 2003 (81 6 11 %) than in 2002
(08 6 01 %), seedling survival was similar in both years
(315 6 56 % vs. 263 6 41 % in 2002 and 2003, respectively). There were striking differences in emergence and
survival between directions (F7,95 = 623, P < 00001 for
emergence and F7,95 = 699, P < 00001 for survival;
Fig. 6A, B). Both emergence and survival showed a significant interaction between year and direction (F7,95 = 220,
P = 00426 for emergence and F7,95 = 516, P = 00023
for survival), indicating that the variation observed in
emergence and survival between directions varied between
years (Fig. 6A, B).
Recruitment index (RI) varied significantly between
years (F1,95 = 6142, P < 00001). In 2002, only 02 % of
the deposited seeds emerged in the field and survived for
long enough to be included in our seedling census at the end
of the growing season, compared with 16 % in 2003 when
averaged across directions. There was also a considerable
difference in RI between directions (F7,95 = 576, P <
00001), varying from 01 % in the south-east to 26 %
in the north-east when the data for the two years were
analysed together (Fig. 6C). A significant interaction between year and direction was found for RI (F7,95 = 338,
75
15
ab* abc*
10
bc* bc*
5
c*
0
2003
ab
120
90 abc
a
ab
ab
60
c
30
bc
c
a
4
ab
ab*
2
ab*
ab*
b*
b*
b*
0
2003
a
30
20
ab
ab
b
10
c
b
b
b
0
20
a
ab
ab
bc
cd
40
cd
20
N
NE
E
cd
d
SE S SW W NW
Direction
Cumulative no. of
survived seedlings m−2
2002 + 2003 combined
60
0
2002
6
40
0
80
Cumulative no. of
emerged seedlings m−2
bc*
c*
Cumulative no. of survived
seedlings m−2
150
2002
a*
Cumulative no. of
survived seedlings m−2
Cumulative no. of emerged
seedlings m−2
20
Cumulative no. of emerged
seedlings m−2
Li et al. — Seed Deposition and Seedling Recruitment
2002 + 2003 combined
a
15
10
a
a
a
a
5
a
0
N
NE
E
a
a
SE S SW W NW
Direction
F I G . 5. Cumulative numbers of emerged seedlings over a period from late-April to the end of June, and surviving seedlings at the end of the growing season
across all six sampling points for each direction (mean 6 s.e.). Data is presented for each of the two years, and for both years combined. Different letters
indicate a significant difference between directions (P < 005 from Tukey’s tests). *Indicates a significant difference between means of the two years (P < 005
from paired t-tests). N = 350–11 , NE = 35–56 , E = 80–101 , SE = 125–146 , S = 170–191 , SW = 215–236 , W = 260–281 , NW = 305–326 .
P = 00033). In 2002, no statistical difference was observed
in RI between directions, but RI was significantly higher in
the north-east than in other directions except for the east in
2003 (Fig. 6C).
Regression analyses indicated a negative relationship
between seed deposition density and emergence in both
years tested. A negative relationship between seed deposition density and emergence was also detected in six of the
eight directions, and in particular the relationship was much
stronger in the south-east and south-west, which had the
highest seed deposition densities (Fig. 7).
DISCUSSION
Wind-dispersed seed deposition patterns
This study indicated that the local deposition pattern of
wind-dispersed A. halodendron seeds was strongly affected
by the spatial variation in wind speed and frequency over
the dispersal season. In the study area the potential dispersal
season occurs during the period from late-October (after
seeds mature) to the end of May in the following year
(Zhao, 2004), which coincides with the erosive season
(Li et al., 2003a). A significantly higher density of deposited
seeds was found in the south-western and south-eastern
aspects than in the northern, north-eastern and southern
aspects when averaged across the two years (Fig. 2). The
spatial variation observed in seed deposition can largely be
explained by the spatial variation in the frequency and speed
of the prevailing winds over the dispersal season (Fig. 1).
Our study also showed a significant difference in the spatial
pattern of seed deposition between the two years tested by
finding that far more seeds were deposited in the southwestern aspects in 2002 and in the northern aspects in
2003 (Fig. 2). Although the present year study cannot
explain the cause of the year-to-year variation, we believe
that this between-year variability in seed deposition is most
likely to be a result of the combined effects of a range of
factors including annual wind conditions, seed production,
seed rain input, seed germination, secondary tumble dispersal, and pre- and post-dispersal seed losses. Further
research is needed to test the effects of individual factors
and the interactive effects of different factors on the spatial
and temporal pattern of seed deposition in A. halodendron.
The results have also shown large differences in dispersal
distances between directions. These differences might
Li et al. — Seed Deposition and Seedling Recruitment
76
Emergence (%)
A 25
North
East
South
West
20
15
North-east
South-east
South-west
North-west
a
ab
b
ab
b
10
a
b
5
a*
a
b
abc
bc c
a* a* a* a* a* a*
abc
bc
c
c c
0
a*
B 100
ab
Survival (%)
80
abc*
60
a
a
ab
40
20
a
a
bcd
cd*
ab ab
bcd*
d
bc
d*
ab
ab ab
bc
b b
b
c
0
Recruitment index (%)
C
8
a
6
ab
4
a
2
a*
a*
b
bc
a
a* a
a* a* a*
c
bc
b b
bc
ab
ab
c
bc
bc bc
0
2002
2003
2002 + 2003 pooled
F I G . 6. (A) Emergence, (B) survival and (C) recruitment index (RI) of Artemisia halodendron seedlings across directions and years (mean 6 s.e.). See
Methods for definition of RI. Different letters indicate a significant difference between directions (P < 005 from Tukey’s tests). *Indicates a significant
difference between means of the two years (P < 005 from paired t-tests).
reflect variation in wind speed with direction. Many studies
have suggested that wind dispersal distance is highly
dependent on wind speed (McEvoy and Cox, 1987; Greene
and Johnson, 1989; Yang and Zhu, 1995; Bullock and Clarke,
2000). The fact that wind transported A. halodendron seeds
only a few meters away from the parent plant suggests that
this species is not dispersed very well by wind because of
its relatively large seed mass. ‘Wind dispersal’ in this
study refers to a mixed effect of primary wind dispersal
(i.e. the ‘flight’ itself) and secondary tumble dispersal,
because we were unable to distinguish between the two.
In a recent study, Tackenberg et al. (2003) reported that
some Artemisia species are not dispersed very well by wind,
consistent with our results. Other studies have demonstrated
differential wind dispersal potentials for different plant
species because of different terminal velocities, resulting
primarily from the great differences in seed size, weight,
shape and surface roughness (e.g. Bond, 1988; Matlack,
1992; Greene and Johnson, 1993; Benkman, 1995; Lisci
and Pacini, 1997; Fort and Richards, 1998; Tackenberg
et al., 2003). A recent study by Vander Wall and Longland
(2004) has suggested that for many plant species the
dispersal of their seeds (propagules) is a complex, multistep process involving a range of alternative dispersers,
with wind dispersal as only the first step of the whole dispersal process. In this study, we only examined the spatial
pattern of seed movement away from the parent plant that
is the result of initial dispersed by wind; the secondary
dispersal pattern of A. halodendron seeds by seed-caching
rodents and birds, or other dispersal agents remain
unexplored.
Post-dispersal seedling recruitment patterns
There was a significant difference in either seedling
emergence or post-emergence establishment between the
two years tested, providing evidence that the process of
recruitment was strongly affected by annual climatic conditions. In this study, the significantly greater cumulative
emergence and survival in 2003 than in 2002 could largely
be attributed to the higher rainfall in 2003 (249 mm) than in
2002 (207 mm), which might result in a different soil moisture environment for emergence and establishment of
A. halodendron seedlings in the two years. The importance
77
Li et al. — Seed Deposition and Seedling Recruitment
Emergence (%)
10
R2
8
4
4
2
2
0
500
1000
2000
2500
W
y = −1·2597 + 2349·92/x
R2 = 0·515, P = 0·009
6
2000
3000
NE
R2 = 0·039
P = 0·540
30
1500
2000
R2 = 0·450, P = 0·016
0
0
500
1000
15
1500
2000
NW
R2 = 0·001
P = 0·921
12
9
20
6
10
0
3
0
500
1000
1500
0
500
1000
1500
2000
SW
y = 57·401e−0·0023x
8
y = −0·8391 + 3204·65/x
R2 = 0·818, P = 0·0001
6
R2 = 0·836, P = 0·0001
SE
30
0
10
40
Emergence (%)
1000
30
10
1000
500
= 0·499, P = 0·01
E
y = −9·2724Ln(x) + 69·634
2
0
0
S
40
20
40
20
4
10
2
0
0
1000
2000
3000
4
Emergence (%)
0
4
0
Emergence (%)
1500
R2
8
6
8
Emergence (%)
= 0·451, P = 0·017
6
0
y = 6·3779e−0·0019x
10
N
y = 0·002x + 0·3788
4000
2002
y = −0·5023Ln(x) + 4·1915
3
R2
= 0·237, P = 0·0001
0
1
10
1000 2000 3000 4000 5000 6000
Number of deposited seeds m−2
2000
3000
4000
5000
0
6000
2003
y = 12·9699e−0·0009x
30
20
0
1000
40
2
0
0
R2 = 0·315, P = 0·0001
0
1000
2000
3000
4000
Number of deposited seeds m−2
F I G . 7. Effects of deposited seed density on seedling emergence, which was calculated as a percentage of the cumulative number of emerged seedlings
relative to the cumulative number of deposited seeds. The data were analysed for each direction combined over the two years (n = 12) and for each year
combined over the eight directions (n = 48).
of the abiotic soil environment (e.g. water and nutrient
levels) in determining the performance of individual plants
and recruitment success of plant populations has been
well documented by many investigators (e.g. Winn, 1985;
Aguilera and Lauenroth, 1995; Bisigato and Bertiller, 1999;
Wijesinghe et al., 2005).
The results also demonstrated the between-direction
variability in cumulative emergence of seedlings. The
78
Li et al. — Seed Deposition and Seedling Recruitment
cumulative seedling counts were more than four times
higher in the north-eastern aspects than in the western
aspects (which had the lowest cumulative emergence)
when the data for the two years were analysed together.
However, the spatial pattern of seedling distribution was
found to differ from that of seed deposition, suggesting
that there was no spatial correspondence between seed
deposition, seedling emergence and establishment; or in
other words the spatial variation in seed deposition did
not determine recruitment pattern. An explanation for
this result may be that A. halodendron seeds were deposited
much more in the south-western aspects because of the wind
direction, whereas seedlings emerged more in the northeastern aspects, most likely because of the higher soil moisture. Therefore, the observed between-direction variability
in seedling distribution could partly be related to soil
resource heterogeneity between different directions. However, our analysis of the relationship between seed deposition density and emergence provided a further explanation
for this result. In these analyses, a significant negative relationship was found between seed deposition density and
emergence in both years and in six of the eight directions
(Fig. 7), suggesting a negative effect of deposited seed
density on emergence of seedlings. In addition, the negative
relationship between seed deposition density and emergence was far stronger in high seed deposition directions
(e.g. south-western and south-eastern aspects) than in low
seed deposition directions (e.g. northern, north-eastern and
north-western aspects, Fig. 7). A possible explanation may
be that relative to the directions with lower seed deposition
densities, those with higher seed deposition densities had
much lower rates of emergence, most likely because of the
stronger below-ground (seed-to-seed) competition for resources such as soil moisture and nutrients. All these results
emphasize the importance of negative density-dependent
regulation in determining seedling distribution pattern.
Negative density dependence for emergence of seedlings
has been documented by many studies in both natural plant
communities and artificially constructed assemblages of
species (e.g. Linhart, 1976; Fowler, 1986; Murray, 1998;
Goldberg et al., 2001; Lortie and Turkington, 2002).
Another important result emerging from the present study
was the low probability of recruitment success of
A. halodendron seedlings. Overall, only a very small fraction (<1 %) of the deposited seeds in the top 5 cm of soil
germinated or emerged in the field and survived for long
enough to be included in our seedling census at the end of
the growing season. The low recruitment rate, resulting
primarily from a low emergence rate and a high post-emergence mortality rate, might suggest that A. halodendron
persists and maintains its population by not relying on seedling recruitment in moving sandy lands. A recent study by
Li et al. (2005b) has suggested that sexual reproduction
is relatively favoured in A. halodendron plants inhabiting
less-eroded semi-fixed sandy land, whereas vegetative propagation is the most important recruitment mechanism for
A. halodendron plants inhabiting highly erodable mobile
sandy land. Although the mechanism behind the lower
recruitment success of A. halodendron seedlings remains
unclear, the following factors could be important. Firstly,
the moving sandy land in which A. halodendron is growing
is characterized by a highly erodable environment, which
may lead to seeds landing on ground where they are more
likely to be buried by moving sand. Successful germination of the seeds would be more difficult following burial
at a significant depth. In a laboratory germination test
using a range of burial depths under controlled water
conditions, Zhao (2004) found that the germination rate
of A. halodendron seeds declined with increasing depth
and virtually no seedlings were able to emerge from a
depth of >5 cm. Secondly, low and highly variable rainfall
in the May–June period (a major seedling emergence period) may result in low emergence success. Thirdly, a high
post-emergence mortality rate of juvenile seedlings could
primarily be accredited to desiccation during dry spells over
the growing season. The study area has a strong continental
climate with highly variable rainfall over the growing season (Li et al., 2003b); hence short periods of drought occur
frequently. Furthermore, because of the low vegetation
cover on moving sandy lands, the rain-wetted surface
layer would soon dry out when exposed to sunshine and
high winds (Li et al., 2002). Consistent with this view, we
found that after rainfall, the wetted top 7–9 cm soil layer in
the bare sandy land dried out rapidly when exposed to direct
solar radiation in the summer months (pers. obs.). Fourthly,
evidence from other studies has suggested that A. halodendron plants have a relatively weak capacity to compete for
resources, such as water, from the surface soil layer compared with other herbaceous plants (Wang and Zhou, 1999;
Zhou, 1999). In a pot experiment using a range of water
supply treatments, Zhou et al. (2004) assessed the droughtresistance of two shrub species (A. halodendron and
A. frigida) that are distributed widely in the Horqin sandy
steppes by measuring changes in their gas exchange, shoot
water potential and leaf chemical characteristics. This study
indicated that A. frigida seedlings had superior capacity to
compete for water compared with A. halodendron seedlings
under severe water stress conditions.
In conclusion, this study improves our understanding of
the population dynamics of A. halodendron inhabiting moving sandy lands and is helpful for developing appropriate
management practices for conservation of A. halodendrondominant grasslands.
ACKNOWLEDGEMENTS
This study was funded by the China National Key Projects
for Basic Scientific Research (TG2000048705), the
National Natural Science Foundation of China (39730100
and 90102011), and an Innovation Research Project from
the Cold and Arid Regions Environmental and Engineering
Research Institute, Chinese Academy of Sciences
(2004121). We wish to thank two anonymous referees
for their critical reviews and valuable comments on a previous version of this paper.
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