Annals of Botany 95: 649–659, 2005
doi:10.1093/aob/mci060, available online at www.aob.oupjournals.org

Seed Germination and Seedling Emergence of Three Annuals Growing
on Desert Sand Dunes in China
K A Z U O T O B E 1,*, L I P I N G Z H A N G 2 and K E N J I O M A S A 3
1

Laboratory of Intellectual Fundamentals for Environmental Studies, National Institute for Environmental Studies,
16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan, 2Cold and Arid Regions Environmental and Engineering
Research Institute, Chinese Academy of Sciences, Lanzhou 730000, China and 3Graduate School of
Agricultural and Life Sciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo, Tokyo 113-8657, Japan

Received: 11 July 2004 Returned for revision: 7 September 2004 Accepted: 1 November 2004 Published electronically: 11 January 2005

 Background and Aims Information on the initial growth characteristics of annuals found in Chinese deserts is very
limited. The aim of this study was to investigate seed germination and interactive effects of irrigation and seed burial
depth in sand on seedling emergence and seedling survival in three annuals (Agriophyllum squarrosum, Bassia
dasyphylla and Aristida adscensionis) commonly growing on sand dunes in these regions.
 Methods Effects of temperature, light and polyethylene glycol-6000 on seed germination were examined byirrigating seeds sown on filter paper in Petri dishes. Seedling emergence was examined for seeds sown on the surfaceof, or at different depths (5, 10, 20, 30, 40 and 50 mm) in, sand-filled pots, which were irrigated under different
regimes. For seeds buried at a depth of 50 mm, seed viability was examined after irrigation of the pots.
 Key Results Seeds of three species germinated at most temperatures recorded between spring and autumn in theirnative habitats. No seed dormancy was found in any species. For all three species, seedling emergence was mostfavoured when seeds were buried at a depth of 10 mm. When seeds sown on the sand surface were irrigated, seedgermination was considerably suppressed due to water deficiency, but many seeds remained viable. For
A. squarrosum and B. dasyphylla, many seeds that were deeply buried and irrigated remained ungerminated but
viable, while for A. adscensionis deeply buried seeds germinated, but the seedlings did not emerge due tounfavourable seedling growth in deep sand.
 Conclusions Precipitation is the most crucial factor in determining the seasonal emergence of seedlings of the threetested species in the field. The vertical distribution of seeds in sand determines the proportion of seeds that germinate
after precipitation and acts to maintain seed banks over multiple years.
ª 2005 Annals of Botany Company
Key words: Agriophyllum squarrosum, Aristida adscensionis, Bassia dasyphylla, irrigation regimes, mechanical resistanceof sand, oxygen deficiency, sand hardening, seed burial depth, seedling survival, temperature effects.

INTRODUCTION
In desert environments, plant survival is strongly limited bytemporal changes in water availability. Compared withmature plants, seedlings are more likely to suffer fromwater deficiency (Beatley, 1967; Ackerman, 1979; Jordan
and Nobel, 1981) because their short roots are distributed
only in dry shallow soil layers. Since seed germination
determines when and where seedling growth begins, thesuccess of seedling establishment depends greatly onseed germination responses to the environment. For annual
plants, which produce seed only once, seed germination
responses to environmental conditions are crucial for
recruitment.
Many studies have been reported on seed germination andseedling emergence of annuals growing in deserts in North
America (Tevis, 1958; Beatley, 1967; Freas and Kemp,
1983; Baskin et al., 1993; Philippi, 1993a, b), Australia(Mott, 1972, 1974; Mott and McComb, 1974) and Israel(Koller, 1957; Loria and Noy-Meir, 1979/1980; Gutterman
and Evenari, 1994); however, information is limited on
the initial growth of plants found in deserts of China andneighbouring countries (Kigel, 1995).
* For correspondence. E-mail tobe@nies.go.jp

Deserts in China are characterized by a colder climate
compared with many other deserts in the world—mean
winter temperature in Chinese deserts is below 0  C, andwinter is an unfavourable season for seed germination andplant growth. This is in contrast to many other deserts, inwhich different annuals appear in winter and summer.
Precipitation is highest in summer due to a continental
monsoon (Fullen and Mitchell, 1994), especially in middle
to eastern parts of the desert regions in China. Anothercharacteristic of deserts in China is that a high proportionof the area is composed of sand dunes with different degrees
of stability (Fullen and Mitchell, 1994).
Precipitation moistens sand differently depending onsand depth—on the one hand, sand near the surface ismoistened even by a light rainfall, but moisture near thesand surface evaporates quickly; on the other hand, sand indeep layers will be moistened only after a heavier rainfall,but moisture in deeper sand is expected to persist longer due
to a lower evaporation rate. Thus, seeds located at different
depths in sand would be exposed to different moisture conditions after a precipitation event. In addition, seed germination and seedling emergence are expected to be affected by
the depth of seed burial in the sand.
Apart from moisture conditions, other depth-dependent
environmental factors may affect seed germination and

Annals of Botany 95/4 ª Annals of Botany Company 2005; all rights reserved

650

Tobe et al. — Initial Growth of Three Chinese Desert Annuals

seedling emergence in sand. While seeds of some species
will germinate irrespective of how deep they are buried(Watkinson, 1978; Maun and Riach, 1981), seeds ofother species when buried deeply do not germinate(Pemadasa and Lovell, 1975; Wang et al., 1998) or dormancy is induced (Maun and Lapierre, 1986; Zhang andMaun, 1990), even if the seeds do not require light for
germination. When seeds in sand germinate, the deeper
the seeds are buried, the farther the seedlings must elongate
to emerge from the sand surface.
This study investigated seed germination and seedlingemergence of three annuals commonly found on desert
sand dunes in China: Agriophyllum squarrosum(Chenopodiaceae), Bassia dasyphylla (Chenopodiaceae)
and Aristida adscensionis (Poaceae). Agriophyllum
squarrosum is found on mobile sand dunes, while theother two species are found on semi-stable or stable sanddunes. This study included examining (1) effects of temperature, light and polyethylene glycol (PEG)-6000 on seedgermination, and (2) emergence and survival of seedlings
when seeds were sown on the surface of, or at different
depths in, sand, and irrigated under different regimes. In
addition, an attempt was made to determine the fates ofseeds that were deeply buried but from which seedlings
did not emerge at the sand surface after irrigation.
MATERIALS AND METHODS
Seeds

Seeds of A. squarrosum were collected in October 1995
and of the other two species in October 1997 from desert
sand dunes in Shapotou, China (37 260 N, 104 570 E),
except the B. dasyphylla seeds used for expt 1 (a) andthe A. adscensionis seeds used for expt 1 (b) which werecollected in October 1995. Mean seed weights ofA. squarrosum, B. dasyphylla and A. adscensionis were18, 10 and 13 mg, respectively. The seeds collected
were initially stored at room temperature until they weretransported (within 2–3 months) to Japan. In Japan the seeds
were stored in a refrigerator (approx. 0  C), except for thoseused for seed longevity tests. During this storage period, theseeds stored in the refrigerator were periodically tested for
germination by incubating the seeds with deionized water at
20  C in darkness. Neither an indication of seed dormancy
nor a reduction in the ability of seeds to germinate(germination percentage >85 %) was found. Experiments
were carried out from April 1997 to March 2004.
Annual mean precipitation is 188 mm and annual mean
temperature is 104  C in Shapotou (1990–1995). Eightyseven per cent of annual precipitation occurred between
April and September and 55 % in July and August(1990–1995). Between October and early June, daily precipitation was usually <8 mm and periods of precipitation
were often interrupted by long dry days; however, between
late June and September, daily precipitation often exceeded
16 mm and precipitation occurred at shorter intervals. Annual variation in precipitation between April and September
in 1990–1995 was rather modest (max. 212 mm in 1995;
min. 104 mm in 1991), compared with those reported forother deserts in North America and Israel (Tevis, 1958;
Loria and Noy-Meir, 1979/1980).
Expt 1: germination experiments

Replicates of 25 seeds were sown on three layers of filter
paper (no. 1) in a 90-mm glass Petri dish. About 15 ml ofdeionized water or a PEG-6000 solution was added to eachdish so that about half the volume of each seed was
immersed. The Petri dishes were covered with lids andmaintained at a constant or diurnally alternating temperature regime in the dark or in 12 h light/12 h dark in an
incubator. When the temperature was alternated, theseeds were exposed to a lower temperature for 12 h in
the dark and to a higher temperature for 12 h in thelight. In the light, the seeds were illuminated with fluorescent lamps (photon flux density (PFD) at wavelengths 400–
700 nm at the surface of the seeds: 80–90 mmol m2 s1).
During exposure to light, the temperature of the fluid in the
Petri dishes was approx. 2  C higher than that in the incubator. For all treatments, except for (c) below, seeds wereobserved daily through a magnifying glass with a scale, andseeds with radicles longer than 5 mm were regarded ashaving germinated and were discarded; about two-thirdsof the volume of the fluid in each Petri dish was replaced
daily. For dark treatments, daily seed observation was performed under dim light (PFD; approx. 2 mmol m2 s1);during each day’s observation, seeds were usually illuminated with dim light for 15–60 s. After 10, 14 or 20 dof incubation, the final germination percentage (GF) was
determined. Each treatment was replicated four times.
(a) Seed longevity. Agriophyllum squarrosum andB. dasyphylla seeds collected in October 1995 were initiallystored at room temperature for 2 months in China, and thenin a refrigerator (approx. 0  C) for 4 months in Japan;
thereafter, some of the seeds were stored in the refrigerator
and others were stored at room temperature (approx. 23  C).
Seed germination was examined by incubating the seeds at
20  C in the dark for 14 d for seeds stored at approx. 23  C
for 08, 63 or 71 years (13, 69 or 77 years after seedmaturation). Seed germination was evaluated by GF.
(b) Effects of temperature and light on seed germination.
To examine the effects of temperature and light on seedgermination, seeds were incubated with deionized water inthe dark or in 12 h light/12 h dark under a different temperature regime. GF was determined after 10 d of incubationfor B. dasyphylla and after 14 d of incubation for the othertwo species.
(c) Seed germination in complete darkness. Even brief
illumination with dim light, such as that used to observeseeds daily, can stimulate seed germination (Dixit andAmritphale, 1996); therefore seed germination in darkness
in the above experiment (b) may not be illustrative of thegermination behaviour of seeds completely deprived oflight. Thus, seed germination was examined when seeds
were incubated at 12 h 15  C/12 h 25  C in darkness for
14 d without daily observation. Seed germination was
evaluated by GF.

Tobe et al. — Initial Growth of Three Chinese Desert Annuals(d) Effects of PEG and light on seed germination. Seeds
were incubated at 20  C in either darkness or 12 h light/12 hdark with deionized water or a PEG-6000 solution of known
water potential (CW) (0 to 10 MPa for A. squarrosum and
0 to 17 MPa for the other two species). The PEG solutionof known CW was prepared according to a calibration curvethat was determined from isopiestic psychrometer measurements (Boyer and Knipling, 1965) at 20  C. After incubation for 20 d, GF was determined.
Expt 2: examination of seedling emergence

Replicates with 16 seeds were sown on the surface of or atdifferent depths (5, 10, 20, 30, 40 and 50 mm) in sand incylindrical plastic pots (inner diameter, 80 mm; sand surface
area, approx. 50 cm2) with a height of 50 mm (short pots) or
100 mm (long pots). At the bottom of each pot was a circulardrainage hole (diameter, 12 mm) covered with cloth. Sand,
collected from a seashore in Japan, was washed repeatedly
to remove salt and mud and air-dried before being put into
the pots to a depth of 45 mm (short pots) or 90 mm (longpots). The particle-size distribution of the sand (91 %wt
was 63–250 mm) was similar to that of the sand dunes in
Shapotou (Buckley et al., 1986).
The pots were placed in an incubator and maintained at
12 h 25  C (light)/12 h 15  C (dark), which is representativeof the temperature conditions in Shapotou from late spring
to early summer when seeds are expected to germinate. The
pots were illuminated with light in the light period as
described in expt 1 (PFD at the surface of the sand, 80–
130 mmol m2 s1). Relative humidity in the incubator wasusually 40–70 % in the 25  C (light) and 90–95 % in the
15  C (dark) periods (mean relative humidity in Shapotou
was 59 % in July 1996). Irrigation was performed at the
beginning of a light period by slowly and evenly dripping
water on the sand with a pipette. The pots were observed
daily and the number of emerging and surviving seedlings ineach pot was counted. A seedling was regarded to haveemerged when its height exceeded 3 mm or it extended
cotyledons, and a seedling was regarded to have diedwhen it fell over or most of the seedling turned yellowish
or brownish. Treatments were replicated five or six times.
(a) Seedling emergence and survival when seeds weresown on the surface of or at a depth of 10 mm in sand andirrigated under different regimes. Replicates of 16 seeds
were sown on the sand surface or at a depth of 10 mm inshort pots. The pots were either initially irrigated with waterof 16 mmP (x mmP denotes irrigation equivalent to x mm
precipitation) and subsequently with water of 3 mmP at 1-dintervals for 14 d, or initially irrigated with water of 8 mmP
and subsequently with water of 3 mmP at 2-d, 4-d, or 6-dintervals for 14 d.
Where seeds were sown on the surface of the sand andirrigated for 14 d, these seeds which did not develop established seedlings were transferred to a Petri dish and were
held in an incubator (12 h 15  C/12 h 25  C in the dark) as
described in expt 1 (b), and seed germination and seedling
growth were observed daily for another 10 d. On the other
hand, to examine whether seeds remained viable after anunfavourable irrigation regime (seeds sown at a depth of651

10 mm and irrigated at 6-d intervals), pots were irrigatedwith 8 mmP water on the 14th day and subsequently with
3 mmP water at 1-d intervals for 10 d, and emergence of
seedlings was observed daily.
(b) Seedling emergence and survival when seeds wereburied at different depths in sand and irrigated under
different regimes. Replicates of 16 seeds were sown at different depths (5, 10, 20, 30, 40 and 50 mm) in pots (longpots). The pots were either initially irrigated with deionizedwater of 8, 16 or 24 mmP and subsequently not irrigated at
all for 16 or 20 d ([8+0], [16+0] and [24+0] treatments,
respectively), or they were irrigated initially with deionizedwater of 16 mmP and subsequently with water of 3 mmP at
1-d intervals for 20 or 35 d ([16+3] treatment).
To investigate the fate of seeds that were deeply buried
and did not generate emerging seedlings after irrigation,
seeds sown at a depth of 50 mm in pots and treated withthe [16+3] irrigation for 35 d or with the [16+0] or [24+0]
irrigation for 20 d were dug out from the sand, and examinedfor evidence of germination. Ungerminated seeds and seeds
with emerging seedlings <30 mm long were transferred toa Petri dish and were held in an incubator (12 h 15  C/12 h
25  C in the dark) as described in expt 1 (b), and seedgermination and seedling growth were observed daily for
another 10 d.
To evaluate the moisture content of the sand at different
depths during this experiment, long pots in which no seeds
were sown were irrigated under the same conditions as ineach irrigation regime of this experiment. On different days
after the beginning of irrigation, sand at each of the different
depth ranges in the pot was weighed to determine the moist
sand weight, and after the sand was dried at 100  C for >1 d,
the dry sand weight was determined; the weight of water inthe sand was determined by subtracting the dry sand weightfrom the moist sand weight. The moisture content in eachsand sample was determined as [(kg water in sand)/(kg drysand)] · 100 %. For the [16+3] treatment, the moisture
content in the sand was measured just before the daily
3-mmP irrigation (1 d after the last 3-mmP irrigation).
Statistical analysis

Student’s t-test was used to statistically test the difference
between two means. For comparison of multiple means,
two-way ANOVA or Tukey’s test was used. Percentage
values were arcsine transformed prior to statistical analysis.
Statistical tests were conducted at P = 005.

RESULTS
Seed longevity

GF of seeds 70 years after maturation, following storage atapprox. 0  C, was 96 6 16 % for A. squarrosum and 95 6
19 % for B. dasyphylla (mean 6 s.e.). GF of B. dasyphylla
seeds stored at approx. 23  C was 85 6 47 % after 08 years
but fell to 0 6 00 % after 63 years. For A. squarrosum, GF
of seeds stored at approx. 23  C was 88 6 45 %, 76 6 56 %and 13 6 52 % after 08, 63 and 71 years, respectively.

Tobe et al. — Initial Growth of Three Chinese Desert Annuals

652
100

100

75

75

50

50

A

25

A

0
100

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10

15

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35

40

10/20 15/25 10/30 20/30 5/35

10

15

20

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35

15

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25

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35

40

100

75
75

50

GF

Percentage germination

25

25

B

B

50
25

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0

75

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50

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5

40

15/25 10/30 5/35

C

50

25

C
25

0
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4

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8

10

12

14

Day
F I G . 1. Changes over time in percentage germination of the three tested
species (A, A. squarrosum; B, B. dasyphylla; C, A. adscensionis) at 15  C/
25  C in either dark (filled circles) or light/dark (open circles).Each point
represents the mean of four replications; error bars indicating standard error
are shown only where it was larger than the point size.

Effects of temperature and light on seed germination

Seed germination in both darkness and light/dark wasmost rapid for B. dasyphylla, followed by A. adscensionis
and A. squarrosum at 15  C/25  C (Fig. 1) and at many othertemperatures. The effect of temperature was significant (P =005; two-way ANOVA, temperature · light) for GF in all
three species. No temperature fluctuation requirement forseed germination was found for any species. Seed germination of B. dasyphylla was favoured more at lower temperatures (GF in darkness was 94 % at 5  C and 15 % at 40  C)
(Fig. 2B), while GF of A. adscensionis seeds was high at
higher temperatures (GF in darkness was 33 % at 10  C and
73 % at 40  C; Fig. 2C). For A. squarrosum (Fig. 2A),
although GF in darkness was low at both high (e.g. 8 %at 30  C) and low (e.g. 4 % at 10  C) constant temperature
regimes, GF in darkness was high in alternating temperature
regimes with the high and low temperatures (e.g. 99 % at
10  C/30  C).
In Shapotou, the means of the daily lowest and highest
temperatures in April 1996 were, respectively, 42  C and174  C, and both the lowest daily mean temperatureand highest mean temperature were greatest in July
(180  C and 290  C, respectively, in 1996). Comparing
the data in the field with the results of the present experiment, it was found that seeds of these three species will
germinate, at least in the dark, at most temperatures
recorded between spring and autumn in Shapotou andmany other desert regions in China.
The effect of light on GF was significant only forA. squarrosum. Seeds of A. squarrosum showed a0
10

10/20 15/25 10/30 5/35

Temperature (°C)

F I G . 2. Final percentage germination (GF) of seeds (A, A. squarrosum;
B, B. dasyphylla; C, A. adscensionis) at different temperature regimes indark (filled circles) or light/dark (open circles). Each point represents themean of four replications; error bars indicating standard error are shown only
where it was larger than the point size.

characteristic interaction of the effects of light and temperature (Fig. 2A)–for temperature regimes at which the temperature of the dark period was 10  C or lower, and for aconstant temperature of 15  C, GF was almost zero inlight/dark but higher than 90 % in darkness; in other temperature regimes, GF was similar between light/dark anddark treatments. The fact that temperature in the dark period
was important for seed germination of A. squarrosum suggested that some temperature-dependent germination process proceeds only in the dark period for this species. Thiswas supported by the result of an additional experiment,
which indicated that GF was zero at 20  C in continuous
light (data not presented) compared with 94 % in 12 h light/
12-h dark at 20  C (Fig. 2).
Germination experiments in complete darkness (without
daily observation in dim light) showed that GF of bothB. dasyphylla and A. adscensionis in complete darkness
exceeded 90 % and was not significantly different fromthat of seeds observed daily with dim light. However, forA. squarrosum, GF in complete darkness was high (75 667 %; mean 6 s.e.) but significantly lower than that ofseeds observed daily (99 6 10 %). It is possible that thelower GF of A. squarrosum seeds maintained in complete
darkness resulted from water in the dish not being changed
daily, because for seeds of some species, leaching ofgermination-inhibiting chemicals from seeds is necessary
for seed germination (Koller, 1957; Barbour, 1968). To
examine this possibility, an additional experiment was carried out in which A. squarrosum seeds in dishes wereTobe et al. — Initial Growth of Three Chinese Desert Annuals
100

A
75
50
25
0
100

B
GF

75
50
25
0
100

C

75
50
25
0

0

–0·5

–1
–1·5
Water potential (MPa)–2

F I G . 3. Final percentage germination (GF) of seeds (A, A. squarrosum;
B, B. dasyphylla; C, A. adscensionis) when seeds were treated with a
PEG solution of a known water potential at 20  C in dark (filled circles)
or light/dark (open circles). Each point represents the mean of four
replications; error bars indicating standard error are shown only where it
was larger than the point size.

observed daily in dim light, but water in the dishes was
not replaced at all; however, GF in this treatment wasalso high (100 6 00 %), indicating that the lower GF of
A. squarrosum seeds maintained in complete darkness is
not attributable to the water not being changed daily.
The result indicated that, although a proportion of A.
squarrosum seeds may require low-fluence light for theirgermination, seeds of all three species do not substantiallyrequire light for germination.
Effects of PEG and light on seed germination

The effect of CW on GF was significant in all three
species, and the effect of light on GF was significant forA. squarrosum and B. dasyphylla (P = 005; two-way
ANOVA, CW · light). Effects of light on the germination
responses to PEG were most pronounced in A. squarrosum(Fig. 3A). Both the CW at which GF began to decrease
and the CW at which GF approached 0 % varied among
species. The CW at which GF in darkness decreased to 50 %of that at 0 MPa was the lowest (approx. 16 MPa) for
B. dasyphylla, followed by A. adscensionis (approx.
10 MPa), and the highest for A. squarrosum (approx.
08 MPa).
Seedling emergence and survival when seeds were sownon the surface of, or at a depth of 10 mm in, sand andirrigated under different regimes

For A. adscensionis seeds sown on the surface of sand andirrigated at 1-d intervals (Fig. 4A), 41 % of seeds generated

653

normal established seedlings (although root bases were
exposed by 2–3 mm above the sand). In addition, 19 %were found to have germinated on the sand, but the emerging radicles and plumules desiccated, and the seedlings did
not develop into normal seedlings. When A. adscensionis
seeds that did not develop into established seedlings weretransferred to Petri dishes, only 4 % of them subsequently
germinated. For B. dasyphylla seeds sown on the surface ofthe sand and irrigated at 1-d intervals, only 1 % of seeds
became established; and 19 % of seeds were found to havegerminated, but their radicles elongated laterally and eventually desiccated. When B. dasyphylla seeds were transferred to Petri dishes, most seeds germinated, but only
13 % of seeds developed normal radicles, and the rest
developed abnormal radicles, which were missing tips andelongated upward. Only normally germinated seeds of
B. dasyphylla were counted in the germination percentage
shown in Fig. 4A. For A. squarrosum, no seeds germinatedon the surface of the sand, but after transfer to Petri dishes,
94 % of the seeds germinated normally. When seeds
were sown on the surface of the sand and irrigated at 2-dintervals (Fig. 4B), no seeds of any species germinated on
the sand surface, and after transfer to Petri dishes, highpercentages of seeds germinated normally.
When seeds were sown at a depth of 10 mm, both irrigation at 1-d (Fig. 4C) and 2-d (Fig. 4D) intervals resulted inhigh percentages of seedling emergence 4–6 d after
the beginning of irrigation in all three species, while irrigation at 4-d or 6-d intervals (Fig. 4E and F) resulted inpronounced seedling emergence only in A. adscensionis.
For B. dasyphylla, the percentage of emerging seedlings
was higher and seedling emergence was more rapid after
irrigation at 1-d intervals than at 2-d intervals, while for
A. adscensionis, the percentage of seedling emergence waslower after irrigation at 1-d intervals. When irrigated at both
1-d and 2-d intervals, all the emerging seedlings of all three
species survived until the end of the experiment (Fig. 4C
and D). However, during irrigation at 4-d or 6-d intervals,
some or most of the emerging seedlings died before the endof the initial 14-d treatment.
When pots irrigated at 6-d intervals for 14 d were
subsequently irrigated at 1-d intervals (Fig. 4F), 83 %(A. squarrosum), 61 % (B. dasyphylla) or 6 % (A. adscensionis) of seedlings newly emerged. All the newly emerging
seedlings and many of the A. adscensionis seedlings surviving at the end of the initial 14-d irrigation survived until
the end of the experiment. At the end of the later favourable
irrigation, percentages of surviving seedlings were considerably lower in A. adscensionis (12 %) than in B. dasyphylla(61 %) and A. squarrosum (72 %).

Seedling emergence and survival when seeds wereburied at different depths in sand and irrigatedunder different regimes

Moisture content in sand at different depths in long pots
irrigated under different regimes is shown in Fig. 5. For
single initial-day irrigation treatments ([8+0], [16+0] and[24+0]), an increase in the initial day irrigation resulted inTobe et al. — Initial Growth of Three Chinese Desert Annuals

654
100

A

B

Sand surface

75

Sand surface

50
25
0
100
Percentage

C

D

75
50
10 mm depth

25

10 mm depth

0
100

E

F

10 mm depth

75
50
25

10 mm depth

0
0

2

4

6

8

10 12 14 16 18 20 22 24 0
Day

2

4

6

8

10 12 14 16 18 20 22 24
Day

Moisture content (%)

Moisture content (%)

F I G . 4. Percentage of emerging and surviving seedlings when seeds were sown on the surface (A and B) or at the 10-mm depth (C–F) of sand (open symbols).
The pots were irrigated initially with water of 16 mmP (A and C) or 8 mmP (B, D, E and F), and subsequently with 3 mmP at 1-d (A and C), 2-d (B and D),
4-d (E), or 6-d (F) intervals for 14 d. When seeds were sown on the sand surface, seeds were transferred to Petri dishes on day 14 and observed for another10 d (the germination percentage is shown by filled symbols). When seeds were sown at the 10-mm depth and irrigated at 6-d intervals, seeds were irrigatedwith 8 mmP on day 14 and subsequently with 3 mmP at 1-d intervals for 10 d (F). Circles, A. squarrosum; squares, B. dasyphylla; triangles, A. adscensionis.
Each point represents the mean of six replications; error bars indicating standard error are shown only where it was larger than the point size.

12
[8+0]

[16+0]

8
40
12[24+0]
8
4[16+3]
0

0–10 10–20 20–30 30–40 40–50 50–60 60–90
Sand depth range (mm)0–10 10–20 20–30 30–40 40–50 50–60 60–90
Sand depth range (mm)F I G . 5. Moisture content in sand at different depth ranges in pots when the pots were irrigated initially with water equivalent to 8 mm, 16 mm or 24 mm ofrainfall and subsequently not irrigated at all ([8+0], [16+0] and [24+0], respectively), or irrigated initially with water equivalent to 16 mm of rainfall andsubsequently with water equivalent to 3 mm of rainfall at 1-d intervals ([16+3]). Moisture content in sand was measured 3 d (filled circles), 5 d (filled squares),10 d (open circles), 15 d (open squares) or 25 d (open triangles) after the beginning of irrigation. Moisture contents 15 d and 25 d after irrigation for [8+0] andmoisture content 3 d after the beginning of irrigation for [16+3] were not measured. Each point represents the mean of four replications; error bars indicating
standard error are shown only where it was larger than the point size.

higher moisture contents in all sand layers and moisteningof sand in deeper sand layers. When the sand appeared to bedry, the sand had a minimum moisture content of approx.
06 %, which was regarded to be the moisture content of thesand when water is in equilibrium between the air and thesand. Moisture in deeper sand layers persisted for longer
periods, while moisture in shallower sand layers was lostquickly. For example, 8-mmP irrigation caused sand

655

Tobe et al. — Initial Growth of Three Chinese Desert Annuals

T A B L E 1. Final percentage of emerging seedlings when seeds sown at different depths in sand in pots were treated with [16+3]
irrigation for 20 d, or [16+0] or [8+0] irrigation for 16 d (refer to the caption of Fig. 5 for each treatment)
Agriophyllum squarrosum

Bassia dasyphylla

Aristida adscensionis

Depth (mm)[16+3][16+0][8+0][16+3][16+0][8+0][16+3][16+0]

[8+0]

5
10
20
30
40

–
(84a)
76a
52a,b
30b,c

10c,d
41b
12c,d
7c,d
–

0d
0d
9c,d
0d
–

–
(85a)
16b
0b
0b

55a
64a
19b
2b
–

7b
19b
2b
1b
–

–
(69a,b)
19d,e
4e
2e

56a,b,c
76a
67a,b
27c,d
–

14d,e
69a,b
40b,c,d2e–

For each species, the values with the same letter are not significantly different from each other (P = 005; Tukey’s test).
Dashes denote that no experiment was carried out under these conditions.
Data from Fig. 4 are indicated in parenthesis.
Data are the means of five replications.

moistening to a depth of 30 mm and most of the moisture in
the sand was lost within 5 d, while 24-mmP irrigation moistened all the sand layers in the pot and moisture persisted indeeper sand layers on 25 d after irrigation (moisture content
at 60–90 mm, 26 %).
On the other hand, the [16+3] treatment maintained sufficiently moist conditions without large variations either
temporally or vertically in the moisture content of thesand (Fig. 5). Moisture content 25 d after the beginningof irrigation was in the range 65–75 % in different sandlayers. This result indicated that repeated 3-mmP irrigation
after 16-mmP irrigation was effective in keeping the sandmoist for relatively long periods, while a single 4-mmP
irrigation moistened only a 0–10 mm sand layer for <3 d(data not shown).
To investigate seedling emergence and survival when all
sand layers are maintained sufficiently moist, pots weretreated with [16+3] irrigation (Table 1). In this treatment,
percentage seedling emergence of B. dasyphylla andA. adscensionis was considerably lower at a seed burial
depth of 20 mm than at 10 mm, and was almost zero atseed burial depths of 30 and 40 mm. For seeds of A. squarrosum, however, percentage seedling emergence decreased
less markedly with increasing seed burial depth, althoughseedling emergence was considerably slower and tended tocontinuously increase until the end of the experiment when
the seed burial depth was 20 mm or more. For all three
species, all the emerging seedlings survived until the end of
the experiment.
To determine the amount of precipitation that results inseedling emergence and survival, pots were treated with
[8+0] or [16+0] irrigation (Table 1). In both treatments,
percentage seedling emergence tended to be higher at aseed burial depth of 10 mm than at 5 mm (Table 1). At
seed burial depths of 10 mm or more, percentage seedlingemergence of all three species decreased with increasing
seed burial depth, except that in the [8+0] treatment,
seedling of A. squarrosum emerged only from seeds buried
at a depth of 20 mm.
In the [16+0] treatment, percentage seedling emergence
was lower for A. squarrosum and B. dasyphylla than for
A. adscensionis at seed burial depths of 20 and 30 mm. For
A. adscensionis, seedlings generally tended to emerge morein the [16+0] treatment than in the [16+3] treatment, indicating that higher sand moisture content did not always
favour seedling emergence of this species. On the other
hand, for A. squarrosum, percentage seedling emergence
was lower in the [16+0] treatment than in the [16+3]
treatment. No marked difference in percentage seedlingemergence was evident for B. dasyphylla between the[16+3] and the [16+0] treatments. Less than 30 % of
emerging seedlings of B. dasyphylla and A. adscensionis
died before the end of the experiment. For A. squarrosum,
90 % and 61 % of seedlings emerging from seeds buried at
respective depths of 5 and 10 mm died before the end of theexperiment, while at seed burial depths of 20 and 30 mm,
seedling emergence of this species was considerably slower,
and all the emerging seedlings survived until the end of theexperiment.
Percentage seedling emergence was lower in the [8+0]treatment than in the [16+0] treatment for all three species(Table 1). Seedling emergence in the [8+0] treatment was
the most favourable for A. adscensionis and the least
favourable for A. squarrosum. In the [8+0] treatment, seedlings of B. dasyphylla and A. adscensionis began to emerge
after 2–6 d from irrigation but all the seedlings died after 4–
6 d from emergence. For A. squarrosum, seedlings emerged
6–12 d after the irrigation from 9 % of seeds sown at a depthof 20 mm, and some of them survived until the end of theexperiment.
To investigate the fate of deeply buried seeds from whichseedlings did not emerge at the sand surface, seed germination and seedling growth were examined when seeds were
irrigated ([16+3], [16+0], [24+0]; Table 2) in sand at a depthof 50 mm and subsequently transferred to Petri dishes.
Percentage seedling emergence from sand was 1–7 % for
A. squarrosum and 0 % for the other two species. Whenseeds were dug out from the sand, the percentage of seeds
that had germinated, but from which seedlings did not
emerge at the surface of the sand, were 0–5 % for
A. squarrosum and 2–10 % for B. dasyphylla (Table 2);
all the radicles or seedlings emerging from A. squarrosum
seeds in sand were white and healthy, but all the radicles
emerging from B. dasyphylla seeds in sand were short (5–17 mm) and brownish. For A. adscensionis, many (40–49 %)seeds seemed to have germinated in the sand, but all the656

Tobe et al. — Initial Growth of Three Chinese Desert Annuals

T A B L E 2. Fates of seeds sown at a depth of 50 mm and treated with [16+3] irrigation for 35 d, or [16+0] or [24+0] irrigation for
20 d (refer to the caption of Fig. 5 for each treatment)
Species

Emerged from sand[16+3] (35 d after beginning of irrigation)
A. squarrosum
7 (4.6)
B. dasyphylla
0 (0)A. adscensionis
0 (0)[16+0] (20 d after irrigation)
A. squarrosum
1 (1.2)B. dasyphylla
0 (0)A. adscensionis
0 (0)[24+0] (20 d after irrigation)
A. squarrosum
1 (1.3)B. dasyphylla
0 (0)Germinated in sandbut not emerged

Newly germinatedin Petri dishes

Total
germination

1 (1.3)
11 (2.3)>40 (5.8)

59 (8.9)62 (9.8)0 (0)68 (9.2)
73 (9.5)>40 (5.8)0 (0)9 (3.5)>49 (4.4)

91 (2.5)
82 (3.7)0 (0)92 (1.2)
91 (5.0)>49 (4.4)

5 (3.2)2 (1.5)84 (4.1)
85 (4.6)

91 (3.1)
88 (4.0)

After irrigation in pots, ungerminated seeds in sand were transferred to filter paper in Petri dishes and irrigated with water, and seeds in the Petri dishes were
examined for germination for another 10 d.
Data are the means of five replications with standard errors in parenthesis.

radicles and plumules (total length 1–12 mm) emerging inthe sand were brownish, and some were detached fromseeds or decomposed. When seeds dug out from the sandwere transferred to Petri dishes, high percentages ofA. squarrosum and B. dasyphylla seeds germinated newly
2–3 d (A. squarrosum) or 1–2 d (B. dasyphylla) after transfer. For both species, the germination velocity was similar tothat when seeds that had not been pre-irrigated in sand were
irrigated in Petri dishes under the same conditions. The
percentage of seed germination in Petri dishes was lower
after the [16+3] treatment than after any of the other treatments. For seeds that had germinated in sand, the emerging
radicles of A. squarrosum continued to elongate in Petridishes, whereas those of B. dasyphylla did not elongate
in Petri dishes. For A. adscensionis, no seeds germinated
newly in Petri dishes and no emerging radicles or plumules
continued to elongate in Petri dishes.
In an additional experiment, seeds of these species that
had not been pre-irrigated in sand were irrigated on filter
paper in Petri dishes at 12 h 15  C/12 h 25  C in the dark. For
all three species, high percentages of seeds germinated andproduced normal seedlings in Petri dishes, the lengths of theseedlings (mean 6 s.e.) being 58 6 75 mm (A. squarrosum;
7 d after irrigation; n = 20), 74 6 52 mm (B. dasyphylla; 4 dafter irrigation; n = 21) and 69 6 35 mm (A. adscensionis;
5 d after irrigation; n = 19). This result indicated that the
inhibition of seedling elongation of B. dasyphylla andA. adscensionis in deep sand was caused by one or morefactors in the deep sand environment.

DISCUSSION
Seeds of all three tested species germinated at most temperatures common between spring and autumn in Shapotou
and many other desert regions in China, indicating thattemperature is not a critical factor limiting seed germinationof these species in the field. Moreover, seed dormancy was
not found in any of the three species. Additionally, seedlongevity of A. squarrosum and B. dasyphylla at room

temperature was rather short. These results suggest that
seeds of the three species tested germinate readily andtend not to remain ungerminated for long periods.
In some reports on seed bank dynamics of desert plants,
persistence in seed banks has been reported to be importantfor species adaptation to environments with unpredictable
precipitation (Philippi, 1993a, b). On the other hand, others
reported rapid depletion of seed banks for species distributed in deserts of North America and Australia (Mott, 1972;
Kemp, 1989; Kigel, 1995). It seems that characteristics ofseed banks (temporary vs. persistent) in desert environments
depend on the reliability and abundance of precipitationin the growing season of plants (Freas and Kemp, 1983;
Baskin et al., 1993).
The fact that three annuals tested in this study showedrather temporary characteristics in germination responses
may partly be attributable to monoseasonality of plant
growth in deserts of China, where a dry and cold winteris disadvantageous for seed germination and plant growth.
This is in contrast to the conditions in many other desert
regions in the world, where dependence of seed germinationon temperature (Went, 1948; Mott, 1972; Ackerman, 1979)or seed dormancy (Mott, 1972; Baskin et al., 1993) determines seasonal emergence of different species. In addition,higher predictability of precipitation in deserts in China may
be related to the germination characteristics of these
species. That is, in Shapotou and many other deserts in
China, a greater amount of precipitation is expected annually in the summer; many seeds will germinate in late spring
to early summer and the emerging seedlings are provided
with sufficient water, resulting in the survival of a large
proportion of seedlings.
Photoinhibition of seed germination was found to be very
noticeable in A. squarrosum, but was very modest in theother two species. Photoinhibition of seed germination has
been reported in a wide range of species including those
distributed in deserts (Koller, 1957; Koller et al., 1963;
Barbour, 1968) and shore dunes (Thanos et al., 1991,
1994), and is reported to inhibit the germination of seeds
located on the surface where emerging seedlings would be

Tobe et al. — Initial Growth of Three Chinese Desert Annuals
likely to die of desiccation. Nevertheless, it is unknown
whether photoinhibition substantially affects seed germination of these species in the field, because as will be discussed
later, inhibition of the germination of seeds located on thesurface in the field may result mostly from limitations ofseed water uptake.
Water potentials that reduced seed germination of thethree species (10 MPa to 20 MPa) were not greatly
different from those that reduced seed germination ofother species distributed in deserts (e.g. Mott, 1974) ormore mesic habitats (e.g. Evans and Etherington, 1990).
Among the three species, A. squarrosum had reduced germination at the highest water potential and took the longest
time to germinate after irrigation, and required the mostfavourable irrigation for seedling emergence from sand.
This may be related to the fact that the habitat ofA. squarrosum is mobile sand dunes in which the waterconditions in sand are more favourable than in semi-stableor stable sand dunes (Mo et al., 1997) where the other two
species grow. On the other hand, while B. dasyphylla seeds
germinated more rapidly and at lower water potentials thanA. adscensionis seeds, seedling emergence from sand withlimited irrigation was favoured more for A. adscensionis
than for B. dasyphylla. Sand does not tend to strongly retain
water by matric forces (Bowers, 1982), and seeds in sandtend to be exposed to either favourable or unfavourable
water conditions for seed water uptake. In such environments, seed germinability at lower water potentials may notfavour seed germination. One possibility for favourable
seedling emergence of A. adscensionis is that water
absorbed by appendages of A. adscensionis seeds persisted
longer and water was supplied to the seeds even after thesand had dried. The longer imbibition time of A. adscensionis seeds may therefore be compensated for by retentionof water by seed appendages.
Although the initial 8-mmP irrigation and the subsequent
3-mmP irrigation at 2-d intervals allowed highpercentages of seedlings to emerge and survive in all
three species, a single 8-mmP irrigation, which moistenedsand near the surface only for several days, allowed smaller
percentages of seedlings to emerge and was not sufficient toallow emerging seedlings to survive for long in any species.
On the other hand, a single 16-mmP irrigation, whichcaused moistening of sand to deeper sand layers andpersistence of moisture for longer periods, resulted infavourable seedling emergence and seedling survival.
These results indicate that both the amount and frequency
of precipitation are important for seedling emergenceand survival.
When these results were compared with precipitation in
Shapotou, it was found that emergence or survival of seedlings of the three species tested from early to middle springis inhibited due to low and infrequent precipitation, and thatprecipitation from late spring to early autumn results in seedgermination, seedling emergence and seedling survival ofthese species. These results indicate that precipitation is themost important determinant regulating seasonal emergenceof seedlings of these species in the field.
The amount and frequency of irrigation required to cause
seedling emergence differed among species. This is in657

agreement with the report of field studies in a desert in
Israel by Loria and Noy-Meir (1979/1980). For the species(A. adscensionis) in which the seeds germinated underunfavourable moisture conditions, emerging seedlings
were more liable to be killed by desiccation and theseeds to be lost from the seed bank, thus indicating thatseed germination under unfavourable moisture conditions is
not always advantageous for adaptation to the environment.
This indicates that precipitation patterns determine which
species are advantageously established. In these experiments, seed density in pots may be higher than that in
the field, and competition among seedlings for moisturehastened the death of seedlings that were subjected tounfavourable irrigation regimes. However, general featuresof the responses of seedlings to moisture conditions in thefield are not expected to differ substantially.
Reduced seedling emergence from seeds sown on thesand surface or buried at 5 mm may be due to deficiency
of moisture at shallower sand layers (Batanouny andZiegler, 1971; Maun and Lapierre, 1986). When seeds
were sown on the sand surface, seed germination of
A. squarrosum was almost completely suppressed even in
irrigation at 1-d intervals. This can be attributable to therequirement of the higher water potential and longer
imbibition time of this species’ seeds for germination,and photoinhibition of seed germination. For the othertwo species, however, irrigation at 1-d intervals caused
germination of considerable percentages of seeds sownon the surface of sand, but germinated seeds did not
become established seedlings, except for some of theA. adscensionis seeds. In this irrigation treatment, highpercentages of seeds of these two species germinated but
many radicles died, because low percentages of seeds
germinated normally after transfer to Petri dishes. The
radicle death of these two species would have been caused
primarily by water deficiency, and some radicles would
have died before they became visibly detectable. For
B. dasyphylla, very short and nearly invisible radicle tips
seemed to have emerged from some seeds but were
desiccated and lost, and after transfer of the seeds toPetri dishes, radicles without tips seemed to have emerged
from the seeds. Another reason for the failure of the establishment of B. dasyphylla seedlings emerging from seeds
sown on the surface of sand seemed to be that the emerging
radicles could not penetrate into the sand; the same type ofseeds has been reported in other species (Maun and Riach,
1981; Maun and Lapierre, 1986). These results indicate thatfor most of B. dasyphylla seeds and some of A. adscensionis
seeds, seed germination at the surface of sand tends to resultin loss of seeds from seed banks. On the other hand, whenirrigation was limited to 2-d intervals, the germination ofseeds sown on the surface of sand was almost completely
suppressed and most seeds remained viable. In these
species’ habitat, the sand surface frequently may not bemoistened sufficiently as in the conditions of the 1-d interval
irrigation treatment in this study. In the field, many ofthese species’ seeds located on the surface of sand are
expected to remain ungerminated and viable. In addition,
photoinhibition may inhibit seed germination on the surface
of sand more strongly in the field, where light658

Tobe et al. — Initial Growth of Three Chinese Desert Annuals

intensity is much stronger than that in our experimental
conditions.
Seedling emergence was suppressed when seeds wereburied at 20 mm or deeper for all three species. For
A. squarrosum and B. dasyphylla, many seeds buried deeply
did not germinate. The results for A. squarrosum in thisstudy are essentially in agreement with those reported by
Wang et al. (1998), who examined seed germination of thisspecies when the seeds were buried at different depths insand and irrigated sufficiently. While seeds of some species
were reported to have become dormant when they weredeeply buried (Maun and Lapierre, 1986; Zhang andMaun, 1990), this would not be the case for A. squarrosumor B. dasyphylla because their seeds germinated soon after
being transferred to Petri dishes. On the other hand, forA. adscensionis, many seeds that were deeply buried seemed
to have germinated, but the emerging seedlings seemed tohave been prevented from elongating for some reason.
A similar response was found in B. dasyphylla seedlings
generated from seeds that were deeply buried, while theseedlings of A. squarrosum seemed to elongate favourably
in deep sand. Unfavourable growth of seedlings in deepsand has also been reported for other species (Pemadasa
and Lovell, 1975; Chen and Maun, 1999).
Two hypotheses can be given to explain the suppressionof seed germination of A. squarrosum and B. dasyphylla
and inhibition of seedling elongation in A. adscensionis andB. dasyphylla in deep sand. One hypothesis is that
deficiency of oxygen in deep sand caused these
responses–as water content in sand increases, air content
in sand decreases, and the resulting oxygen deficiency may
inhibit seed germination and/or seedling elongation. Indeed,a reduction in oxygen availability causes deleterious effects
on seed germination and seedling growth in many species(Gill and Miller, 1956; VanderZee and Kennedy, 1981;
Crawford, 1992). Based on this hypothesis, more favourable
seedling emergence of A. adscensionis with [16+0] treatment than with [16+3] treatment may have resulted from thelower air content in sand with a higher moisture content.
However, based on this hypothesis, it is difficult to explain
the result of an additional experiment (data not presented)
that A. squarrosum seeds buried at a depth of 5 mm insubmerged sand were maintained ungerminated but viable,
while 90 % of A. squarrosum seeds germinated when they
were sown on the surface of submerged sand. Anotherhypothesis is that higher mechanical resistance of deeper
sand impeded seed germination and/or seedling elongation.
Mechanical restraint by soil can impede shoot or root
growth of seedlings (Gill and Miller, 1956; Barley andGreacen, 1967), or cause adverse effects on seed germination (Collis-George and Williams, 1968; Hadas, 1977).
When sand contains water, sand particles coagulate andsand hardens (Hornbaker et al., 1997); hardened sandmay suppress seed germination and/or inhibit seedlingelongation. At deeper sand layers where the water content
is higher, the sand becomes more hardened and the weightof sand in upper layers increases the hardening of the sand,and seedlings need to elongate a greater distance in thehardened sand before they reach the surface. Based on
this hypothesis, more favourable seedling emergence ofA. adscensionis in sand of lower moisture content can beinterpreted to have resulted from the lower hardness of sandwith lower moisture content. Germination suppression of A.
squarrosum seeds at shallower depths in submerged sandmay be attributable to stronger hardening of sand withhigher water content. Unfortunately, no clear-cut conclusion can be drawn from the present study on how seedgermination was suppressed or seedling elongation was
inhibited in deep sand.
The present study indicated that temperature or dormancy
is not crucial in determining the seed germination of thethree species tested, and suggested that seedling emergencein the field of the three species tested is regulated primarily
by precipitation. Many of the A. squarrosum and B. dasyphylla seeds that were located deeply or shallowly in sandand the A. adscensionis seeds that were located shallowly insand would remain ungerminated but viable even after aheavy rainfall, and these seeds may germinate in futureyears if they are moved to a depth appropriate for germination. Thus, the vertical distribution of seeds in sand is
expected to determine the proportion of seeds that germinate after precipitation and act to maintain seed banks overmany years.

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