Download Effects of sand burial depth and seed mass on seedling emergence

 Springer 2006
Plant Ecology (2006) 185:191 –198
DOI 10.1007/s11258-005-9094-z
Effects of sand burial depth and seed mass on seedling emergence and growth
of Nitraria sphaerocarpa
Q.Y. Li1,2,*, W.Z. Zhao1,2 and H.Y. Fang3
1
Cold and Arid Regions Environmental and Engineering Research Institute, Chinese Academy of Sciences,
Lanzhou, 730000, China; 2Chinese Ecosystem Network Research Linze Inland River Basin Comprehensive
Research Station, Lanzhou, 730000, China; 3Institute of Geographical Sciences and Natural Resources
Research, Chinese Academy of Sciences, Beijing, 100101, China; *Author for correspondence (e-mail:
[email protected])
Received 8 September 2005; accepted in revised form 22 December 2005
Key words: Biomass allocation, Optimal burial depth, Sand burial, Seed size, Seedling emergence, Seedling
size
Abstract
A greenhouse experiment was conducted to test the effects of sand burial depth and seed mass on seedling
emergence and growth of Nitraria sphaerocarpa. Seeds of Nitraria sphaerocarpa were sorted into three sizeclasses (large, medium, small) and artificially buried at 0, 1, 2, 3, 4, 5 and 6 cm depths in plastic pots filled
with unsterilized sand. In the seven treatments, the percent emergence, seedling mass and seedling height,
significantly affected by both burial depth and seed size, were highest at the optimal burial depth of 2 cm
burial depth, and decreased with increasing burial depth in each seed size-class. Although seedling mass was
usually greatest for large seeds and least for small seeds at each burial depth, little difference was observed
in seedling height at shallow burial depths of 0 –3 cm. In each seed size-class, with increasing burial depth,
both root-mass ratio and aboveground stem-mass ratio decreased, while belowground stem-mass ratio
increased. In each burial depth, with decreasing seed size, belowground stem-mass ratio increased, while
root-mass ratio decreased.
Introduction
In dune systems, sand accretion and deflation
mediated by wind may be important selective
forces in the evolution of the species (Zhang
et al. 2002). The germination of seeds is directly
related to the depth at which seeds are buried
(Zhang and Maun 1994). Shallow burial, particularly improves the germination of seeds and the
subsequent emergence and survival of seedlings.
Seeds beneath a prospective layer of sand experience a much more moderate environment (e.g.
temperature, moisture), because it prevents them
from drying out (Harper and Benton 1966).
However, deep burial depth may prevent seedlings from emergence above the sand and affect
survival, because pre-emergence mortality results
from a cessation of seedling growth before it
reaches the soil surface or the seeds are unable to
germinate due to lack of oxygen, light and temperature fluctuation (Maun and Riach 1981; Van
Assche and Vanlerberghe 1989; Zhang and Maun
1990; Vleeshouwers 1997). These traits suggest
that there is an optimal range of burial depth to
maximize the seedling emergence and subsequent
seedling growth.
192
The optimal burial depth of seedling emergence could be strongly influenced by seed mass
(Chen and Maun 1999). Seed mass plays a key
role in the establishment of the juvenile phase of
a plant’s life cycle, and seed mass is a parameter
that profoundly influences both germination
characteristics and seedling traits. Larger seeds
are generally superior to smaller seeds by having
a higher probability of emergence (Dolan 1984;
Stanton 1984; Winn 1988), and by developing
into seedlings with better competitive ability
(Stanton 1984), higher survival (Simons and
Johnston 2000), and better performance in later
life stages (Wulff 1986; Vaughton and Ramsey
2001). Often, larger seeds have higher germination rates than smaller seeds (Simons and Johnston 2000), but the opposite has also been
observed (Dolan 1984; Susko and Lovett-Doust
2000). Several researches have observed that,
within populations, large seed mass confers an
advantage during at least one stage of the life
cycle, principally under conditions where resources are scarce (Sivertown 1989; Manga and
Yadav 1995; Grubb and Coomes 1997; Meyer
and Carlson 2001). However, in contrast to the
advantages of relatively larger seed mass, several
studies have detected ecological factors that can
lead to the opposite trend, particularly during the
phase when seeds remain in the soil. The predation has been observed to be greater on large
seeds, presumably because of richer energy resource or large seeds are more visible to the
predators than small seeds (Hulme 1993; Vander
Wall 1994). For any given species, the effect of
seed mass on plant performance may depend
both on the intrinsic effects of seed mass on
seed-seedling behavior and on its interactions
with other ecological factors. The selective pressures influencing the evolution of seed mass are
likely to differ among species and habitats
(Foster 1986).
The adaptation of the seedlings of dune species
to sand accretion may rely on their morphology
and biomass allocation (Maun and Riach 1981;
Maun and Lapierre 1986; Zhang et al. 2002). In
herbaceous species, the adaptation of seedlings to
burial has been attributed to the effective elongation of the coleoptile, subcoleoptile, first internode
or hypocotyls (Maun and Riach 1981; Maun and
Lapierre 1986). In large-seeded tree species, with
increasing burial depth and decreasing seed size,
the biomass allocation to stems increased, while
allocation to roots decreased (Seiwa et al. 2002).
In desert shrub species, little is known concerning
how buried seeds allocate reserves to the stems in
order to facilitate seedling emergence and to what
extent the allocation is changed in relation to the
availability of seed mass.
In this study, we buried seeds of different mass
of Nitraria sphaerocarpa at various depths in a
greenhouse to examine the effects of sand burial
depth and seed size on seedling emergence and
growth, to test the biomass allocation at various
sand burial depths, and to assess the optimal depth
for establishment success of Nitraria sphaerocarpa
affected by sand burial and seed size.
Materials and methods
Study site
This study was conducted in a greenhouse in the
Chinese Ecosystem Network Research Linze Inland River Basin Comprehensive Research Station
in northwest China (3921¢N, 10007¢E) with an
elevation of 1382 m. The mean annual temperature and rainfall are 7.6 C and 117.1 mm,
respectively. The mean monthly temperature ranged from )27 C (January) to 39.1 C (July). Soil
is dominated by blown sand with coarse texture
and loose structure. The vegetation is dominated
by shrubs, including Nitraria sphaerocarpa, Hedysarum scoparium, Nitraria tangutorum, Calligonum mongolicum, subshrubs, like Reaumuria
soongorica, and annuals such as Suaeda glauca,
Agriophyllum squarrosum, Bassia dasyphylla, Halogeton arachnoideus, and so on.
Plant species
Nitraria sphaerocarpa is one of the major sand
binding species in the sandlands of northwest
China. Seeds of Nitraria sphaerocarpa are dispersed by wind when they mature, and dispersed
single seed may be picked up again by wind and
moved over longer distances. Seeds and seedlings
of the species may be buried by sand to various
depths during the establishment. Burial by sand
may be a critical episode for the successful establishment of the seedlings. After emergence and
193
establishment, seedlings of Nitraria sphaerocarpa
can populate the mobile dunes or semi-mobile
dunes in the sandland habitat.
Experimental procedure
Fruits were collected in the fall of 2004 from multiple
individuals in desert. One fruit has only one seed.
Seeds were cleaned, dried at room temperature for
2 –3 weeks then stored at 8 C under dry, dark conditions. Seeds were weighed singly and sorted into
three seed size-classes based on mass per seed: large
(23.49 ± 2.999 mg, mean ± SE, n = 700), medium (17.31 ± 1.545 mg, mean ± SE, n = 700) and
small (10.78 ± 1.874 mg, mean ± SE, n = 700).
For each group, counted seeds (20 each) were planted
at 0, 1, 2, 3, 4, 5 and 6 cm depths in plastic pots
(15.5 cm in diameter, 20 cm in depth) filled with
unsterilized sifted sand. The drainage outlet at the
bottom of the pots was covered with strips of nylon
mesh to prevent the loss of sand while allowing
drainage of excess water. Sand was poured into each
pot up to the lower mark and moistened. Seeds were
then placed on the sand surface and the pots were
filled up to the upper mark with additional sand.
There were five pots per treatment. Pots were watered daily with tap water. Temperature in the
greenhouse was maintained at 23 C during the day
(16 h photoperiod) and 14 C at night.
Emerged seedlings were counted daily. Seedling
emergence was defined as the first appearance of a
seedling at the sand surface. After 8 weeks of
seedling emergence and growth in the greenhouse,
the experiment was terminated. All the seedlings
were measured for their height above the sand
surface, and then they were harvested. At harvest,
the seedlings were dug out by hand and trowel,
and care was taken to collect as many roots
belonging to the seedling as possible. Roots were
cleaned with water. Seedlings were separated into
three parts: aboveground stems, belowground
stems and roots. After drying at 70 C for 48 h,
each fraction was weighed.
biomass allocation (root mass ratio, belowground
and aboveground stem-mass ratio) were analyzed
using two-way ANOVAs in the treatments.
Tukey –Kramer multiple comparison test was used
to determine differences in each trait among seed
size-classes within a single burial depth class. Since
no seedlings emerged from the small seeds in all of
the replicates at 6 cm burial depth, interaction
between seed sizes and burial depth was not
calculated.
Results
Seedling emergence
In the seven treatments, the percent emergence
was significantly affected by both burial depth
(F=98.134, d.f.=6, p<0.0001) and seed size
(F=18.668, d.f.=2, p=0.0002). Seedling emergence was highest at 2 cm burial depth, but decreased with increasing burial depth in each seed
size-class (Figure 1). The percent emergence was
not significantly different between large and
small sized seeds, although the emergence was
usually highest for large seeds, and lowest for
small seeds at each sand burial depth. In the
sand burial depth of 0 cm, the emergence was
lower for the drought. There was a significant
decline in emergence at 4 and 5 cm burial depths.
No seedlings emerged from 6 cm burial depth for
the small size seeds.
Time to emergence often determines whether a
plant competes successfully with its neighbors, is
consumed by herbivores, infected with diseases,
and whether it flowers, reproduces, and matures
properly by the end of the growing season.
The mean number of days to the first seedling
emergence was affected by sand burial depth
(F=25.235, d.f.=5, p<0.0002), but not by seed
size (F=2.648, d.f.=2, p=0.119). Seedling emergence occurred earliest for the seeds from shallow
burial depths (0 –2 cm), and delayed with the
increasing burial depth (Figure 2).
Statistical analysis
Seedling size
The effects of burial depth and seed size on the
mean number of days to emergence, percent
emergence, seedling mass, seedling height and
Seedling size was measured in terms of seedling
mass and seedling height. Seedling mass and
194
90
L
M
S
80
Emergence (%)
70
60
50
40
30
20
10
0
0
1
2
3
4
5
6
Sand burial depth (cm)
Figure 1. Mean (±SE) percent emergence of seedlings at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M)
and small (S) sized seeds of Nitraria sphaerocarpa.
16
L
M
S
Time to emergence (day)
14
12
10
8
6
4
2
0
0
1
2
3
4
5
6
Sand burial depth (cm)
Figure 2. Mean (±SE) number of days to the first emergence of seedlings at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large
(L), medium (M) and small (S) sized seeds of Nitraria sphaerocarpa.
seedling height were significantly affected by
both burial depth (F=22.660, d.f.=5, p<0.0001;
F=18.922, d.f.=5, p<0.0001, respectively) and
seed size (F=22.744, d.f.=2, p<0.0002; F=6.190,
d.f.=2, p=0.018, respectively). Both seedling
mass and seedling height were usually greatest at
2 cm burial depth, and decreased with an increase
in burial depth for all seed size-classes (Figures 3
and 4). Although seedling mass was usually
greatest for large seeds and least for small seeds at
each burial depth, little difference was observed in
seedling height at shallow burial depths (0 –3 cm).
Biomass allocation
Both root-mass ratio and belowground stem-mass
ratio were significantly affected by both burial
depth (F=35.178, d.f.=5, p<0.0001; F=25.749,
d.f.=5, p<0.0001, respectively) and seed size
195
9
L
M
S
8
Seedling mass (mg)
7
6
5
4
3
2
1
0
0
1
2
3
4
5
6
Sand burial depth (cm)
Figure 3. Mean (±SE) seedling mass at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S) sized
seeds of Nitraria sphaerocarpa.
14
L
M
S
Seedling height (cm)
12
10
8
6
4
2
0
0
1
2
3
4
5
6
Sand burial depth (cm)
Figure 4. Mean (±SE) seedling height at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S)
sized seeds of Nitraria sphaerocarpa.
(F=18.561, d.f.=2, p=0.0004; F=7.162, d.f.=2,
p=0.012, respectively), while aboveground stemmass ratio was affected by only burial depth
(F=10.292, d.f.=5, p=0.001) but not by seed size
(F=0.465, d.f.=2, p=0.641). In each seed sizeclass, with increasing burial depth, both root-mass
ratio and aboveground stem-mass ratio decreased,
while belowground stem-mass ratio increased. In
each burial depth, with decreasing seed size,
belowground stem-mass ratio increased, while
root-mass ratio decreased (Figure 5).
Discussion
Seedling performance at sand burial depth
Seed burial has both positive and negative consequences for seedling emergence. The most obvious
negative consequence is burial so deep that seed
germination is prevented. Germination sometimes
occurs with deep burial but seed reserves may be
exhausted before the seedling reaches the soil
surface, which leads to seedling death. As might be
196
100%
90%
Biomass allocation
80%
70%
60%
50%
40%
30%
20%
10%
0%
L0 M0 S0
L1 M1 S1
L2 M2 S2
L3 M3 S3
Sand burial depth (cm)
L4 M4 S4
L5 M5 S5
L6 M6
Figure 5. Biomass allocation of seedlings at various sand burial depths (0, 1, 2, 3, 4, 5, 6 cm) for large (L), medium (M) and small (S)
sized seeds of Nitraria sphaerocarpa. () Aboveground stem; ( ) belowground stem; (j) root.
expected, deep burial is more detrimental to small
seeded than to large seeded species (King and
Oliver 1994; Forcella et al. 2000). The benefits of
burial are reduced exposure to air. Soil overlying
very young seedlings creates mulch that maintains
high humidity and allows growth to proceed relatively rapidly. Moreover, soil burial also provides
protection of seeds and seedlings from abnormally
low and high air temperatures as well as predators
that dwell on or near the soil surface. Consequently, emergence patterns of the species exhibit
parabolic relationships with soil burial depth
(Forcella et al. 2000).
The burial experiment of Nitraria sphaerocarpa
showed that deep burial reduced seedling emergence. Similar relationship was reported in other
species. The highest percent emergence of Calamovilfa longifolia seedlings occurred from 1 –2 cm
depths, however, as the depth of burial increased
from 2 to 12 cm there was a significant decrease in
seed percent emergence (Maun and Riach 1981).
Zhang and Maun (1990) showed that seedlings of
Panicum virgatum emerged from a mean depth of
4.73 and 11 cm was the maximum depth of in the
field.
Greater seedling emergence was observed for
large seeds compared with small seeds, probably
due to the greater food reserves that can produce
longer shoots thus facilitating their emergence
above the surface soil. Seedling mass and height
of the Nitraria sphaerocarpa were significantly
affected by burial depth, mainly due to the following reasons. A greater fraction of seed reserves
would be exhausted by the time of the seedling
emergence, because seedlings that emerged from
deep burial showed smaller plant size initially.
These seedlings would have less initial investment
to future growth. And since seedlings from deeper
burial depths usually emerge later than those from
shallower burial depths, the period of growing
season will be shorter and biomass gain and vertical growth will be lower than the seedlings from
shallow buried seeds.
Seed mass effects on establishment success
A bigger seed means more energy reserves and
hence, greater vigor and higher chance for
emergence of seedlings from deeper locations and
is better at tolerating a wide range of environmental stresses, such as predators, nutrient
deprivation, drought, or prolonged periods in
deep shade (Weller 1985; Leishman and Westoby
1994; Westoby et al. 1996; Leishman et al. 2000).
And smaller seeds give rise to seedlings more
liable to suffer high mortality from drought,
physical disturbance by predators, or to suffer
overtopping if they are adjacent to seedlings
from larger seeds under favorable conditions.
The same may be true for Nitraria sphaerocarpa
seeds. The seed mass of Nitraria sphaerocarpa
197
used in this study ranged from 8.906 to
26.489 mg per seed. Once seedlings emerged,
those from large seeds would probably have
better survivorship because they have the greatest
height and bigger root-mass ratio, showing the
selective advantages of large seeds for effective
resource acquisition, which would be of adaptive
significance on sand dune systems because it
would enhance absorption of water and nutrients
and avoid drought stress near the surface. Similar results were also reported that seedlings of
Strophostyles helvola from large seeds had greater
survival than smaller seeds when they were subjected to the burial treatment (Yanful and Maun
1996). However, the opposite evidences were
observed in other studies, which showed that
there was no relationship between seed mass and
percentage seedling emergence (Jurado and
Westoby 1992; Reader 1993; Jones et al. 1994;
Eriksson 1997; Chen et al. 2002) or no relationship between relative growth rate and seed mass
(Fenner 1983; Shipley and Peters 1990; Swanborough and Westoby 1996). This suggested that
the establishment success might depend on the
species assemblage as well as growth conditions.
Morphological changes in response to sand burial
depth
The seedlings from deep burial showed greater
biomass allocation to stem, particularly the part
below the ground surface, instead of the roots in
each seed size-class. Such plastic response in biomass allocation suggests that the seedlings allocates lower energy reserves to the roots and diverts
the rest to the stem to facilitate emergence from a
deep location, as suggested by Seiwa et al. (2002).
A similar phenomena has also been observed in
some grass species in sand dunes that seedlings
from a deeper location had a longer first internode
or subcoleoptile internode but shorter roots than
those in a more shallow planting (Maun and Riach
1981; Redmann and Qi 1992). This study, furthermore, revealed that the increasing investment
to belowground stems instead of roots was also
observed as the seed size decreased in each of the
burial depths, suggesting that seedling emergence
from small seeds is also facilitated by the morphologically adaptive allocation of the limited seed
reserve.
Optimal burial depth for establishment success
Seed burial has both positive and negative consequences for seedling emergence, so there is an
optimal range of burial depth to maximize the
seedling emergence and subsequent seedling
growth. In this study, the shallow burial depth
seems to be advantageous for seedling establishment of the Nitraria sphaerocarpa, because the
greatest emergence, height and mass were observed
at 2 cm burial depth in this experiment. If optimal
caching depth for a propagule is considered as the
probability of escaping predation by a forager
times the probability that it will emerge, grow and
survive in the absence of predation, is maximized
(Vander Wall 1993; Seiwa et al. 2002), the optimal
depth for a seed of Nitraria sphaerocarpa is in the
range of a shallow burial depth, approximately,
2 cm sand burial depth. In the optimal burial
depth of 2 cm, there was little difference in the
seedling emergence and the seedling height among
seed size-classes, although seedling mass was
dependent on seed size.
During the restoration of the dune systems,
Nitraria sphaerocarpa will be one of the most
important species. And suitable environmental
conditions can be selectively ameliorated to promote the seedling establishment success and seedling growth. The seeds of Nitraria sphaerocarpa
with bigger mass are buried at 2 cm sand burial
depth in practice will be valuable information.
Acknowledgements
This research was supported by the national natural science foundation of China (No. 40571026)
and the foundation of field research stations,
Chinese Academy of Sciences (No. 2005410).
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