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Flooding induces secondary dormancy in Setaria parviora seeds
Federico P.O. Mollard, Pedro Insausti and Rodolfo A. Sánchez
Seed Science Research / Volume 17 / Issue 01 / March 2007, pp 55 - 62
DOI: 10.1017/S0960258507659212, Published online: 16 March 2007
Link to this article: http://journals.cambridge.org/abstract_S0960258507659212
How to cite this article:
Federico P.O. Mollard, Pedro Insausti and Rodolfo A. Sánchez (2007). Flooding induces secondary dormancy in Setaria
parviora seeds. Seed Science Research, 17, pp 55-62 doi:10.1017/S0960258507659212
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Seed Science Research (2007) 17, 55 – 62
DOI: 10.1017/S0960258507659212
Flooding induces secondary dormancy in Setaria parviflora
seeds
Federico P.O. Mollard*, Pedro Insausti and Rodolfo A. Sánchez
IFEVA-CONICET, Facultad de Agronomı́a, UBA, Av. San Martı́n 4453, C1417DSE, Buenos Aires, Argentina
Abstract
The effect of flooding on the dormancy level of
Setaria parviflora seeds from a non-flooded upland
and a seasonally (winter– spring) flooded lowland in
the Pampa grasslands of Argentina was investigated. Seeds from both communities were subjected
to reciprocal burial treatments in the two habitats,
and exhumed during and after the flooding season.
Effect of immersion in water at 58C was compared to
incubation of seeds on the surface of watersaturated paper at the same temperature. After
exhumation of the buried seeds or immersion
treatments, germination was assayed at 258C and
at 20/308C in the dark or in combination with light.
Burial in the lowland, which was flooded in winter –
spring, significantly reduced germination, while
burial in the non-flooded upland did not reduce
germination. Similarly, immersion in water at 58C
significantly reduced germination compared to nonimmersed controls. During summer, seeds buried in
the lowland showed increased capacity to germinate, particularly when exposed to fluctuating
temperatures or light. Thus, flooding induced
secondary dormancy in S. parviflora seeds, and it
was broken during the non-flooding season. These
responses of the seeds would prevent germination
until there was no further risk of flooding. Remarkably, in S. parviflora seeds harvested from both
habitats, we observed essentially the same germination requirements after flooding. However, some
slight differences were detected between the seed
populations exhumed from the lowland site, indicating that flooding had larger effects on the seeds
from the upland community. This suggests some
differentiation of these populations evident only after
flooding in the field.
*Correspondence
Fax: þ54 11 4514 8730
Email: fmollard@ifeva.edu.ar
Keywords:
flooding,
fluctuating
temperatures,
germination, grassland, secondary dormancy, seed
dormancy, Setaria parviflora
Introduction
Regulation of seed dormancy by the environment
ensures that germination occurs at a favourable time
for seedling establishment. The annual temperature
cycle is one of the main environmental factors
regulating dormancy of seeds in the soil bank (Baskin
and Baskin, 1980; Bouwmeester and Karssen, 1992,
1993; Batlla and Benech-Arnold, 2005). Nevertheless,
other factors, such as the gaseous environment of the
soil, may influence the dormancy of seeds, particularly in flooded habitats (Baskin and Baskin, 1998;
Baskin et al., 2000). Among the gaseous components of
the soil, oxygen is one of the most important factors
for altering seed dormancy. The effect of hypoxia on
seed dormancy varies among species; some enter
secondary dormancy in the absence of oxygen in the
soil, whereas the dormancy level in others is
attenuated or not changed (Insausti et al., 1995; Baskin
and Baskin, 1998; Crawford, 2003). Once the
dormancy level is sufficiently low, it can be terminated
by different types of environmental signals that
induce germination (Benech-Arnold et al., 2000). In
seeds of many species from natural grasslands,
germination is promoted by fluctuating temperature
or light, signals related to vegetation gaps (Thompson
and Grime, 1983; Insausti et al., 1995). On the other
hand, fluctuating temperature promotes germination
of seeds of many aquatic and wetland habitats, a
response that is associated with decreased water
depth and the consequent exposure of wet soil
(Thompson and Grime, 1983; Pons and Schroder,
1986; Baskin and Baskin, 1998).
Changes in dormancy alter seed sensitivity to the
factors that can promote germination (Benech-Arnold
et al., 2000; Batlla and Benech-Arnold, 2005). Thus, the
different soil conditions experienced by seeds modify
their dormancy level and change their response to
56
F.P.O. Mollard et al.
environmental signals (Probert et al., 1985; Noronha
et al., 1997; Steadman, 2004). In Ambrosia tenuifolia,
immersion in water provokes an increase in sensitivity
to light (Insausti et al., 1995), and the occurrence of
flooding may generate the loss of a light requirement
for germination in seeds of Schoenoplectus purshianus
(Baskin et al., 2000).
The seeds of several species of the genus Setaria L.
have dormancy mechanisms related to the oxygen and
water availability of the soil (Dekker, 2000; Dekker and
Hargrove, 2002). In addition, they have requirements
for low temperatures that alleviate dormancy during
winter, thus permitting the synchronization of
germination with the arrival of spring, and show a
positive germination response to alternating temperatures (Dekker, 2000).
Setaria parviflora (Poir.) Kerguélen is a perennial
grass species, megathermic and with a broad
geographical and ecological distribution, growing in
different ecosystems that are subjected to frequent
disturbances (Dekker, 2000). In the natural grasslands
of the Flooding Pampa (Province of Buenos Aires,
Argentina), it has a considerable cover in communities
situated in landscapes of flat relief, with gentle slopes,
subjected to frequent floods and also in communities
situated in higher topographical positions with betterdrained soils, where flooding does not occur (Burkart
et al., 1990; Insausti et al., 1999). The seeds are
dispersed in summer and form large seed banks
(D’Angela et al., 1988). Germination takes place in late
spring, after the flooding period that occurs during
winter or early spring.
The objective of this study was to evaluate the
effects of winter –spring floods on the dormancy of
S. parviflora seeds from two communities in the
Flooding Pampa grasslands, and how this modulates
their capacity to perceive signals associated with
canopy gaps. Specifically, we addressed the following
questions: (1) Can flooding affect the dormancy level
of S. parviflora seeds? (2) Are there differences in the
dormancy response to floods between upland and
lowland seed populations?
Materials and methods
In March 2003, ripe seeds of S. parviflora were
harvested from two populations situated in two
communities of the Las Chilcas landscape in Flooding
Pampa grasslands, Province of Buenos Aires,
Argentina (Burkart et al., 1990): (1) a non-flooded
community (upland community) of Melica brasiliana,
Diodia dasycephala and Echium plantagineum, associated
with well-drained soils, free from floods and
situated in relatively high areas of the landscape;
and (2) a flooded community (lowland community) of
Piptochaetium montevidense, Ambrosia tenuifolia, Eclipta
bellidioides and Mentha pulegium, situated in a lower
topographic position with respect to the previous
community. Seeds were kept in paper bags in the
laboratory (20 ^ 28C). Germination was evaluated
immediately after harvest and after 3 months of dry
storage, prior to the beginning of experiments.
Seed pre-treatments
Field pre-treatments
A reciprocal burial experiment was performed with S.
parviflora seeds. On 5 June 2003, two groups of 800
seeds per population were placed in fine-mesh
polyester bags (10 £ 8 cm) and buried at a 3-cm
depth in the upland and lowland communities.
During the burial period, soil temperature was
registered hourly with thermistors, and soil volumetric hydric content monitored with ECHO Probes
EC-10 sensors (Decagon Devices, Pullman, USA)
installed in Campbell 21-X dataloggers (Campbell
Scientific, Logan, USA).
One bag per population and site was exhumed in
darkness on 27 November 2003 (spring) after 6 months
of burial and on 23 January 2004 (summer) after 8
months of burial.
Laboratory pre-treatments
Seeds were incubated in groups of 800 each in plastic
boxes (15 £ 10 £ 6 cm) on cotton covered with absorbent white paper saturated with distilled water. Other
groups of seeds were immersed under 5 cm of distilled
water in similar boxes. All boxes were wrapped in
black polyethylene and were kept in an incubator at
58C for 3 months.
Germination treatments
Fresh seeds, dry-stored seeds and seeds subjected to
pre-treatments were germinated in clear polystyrene
boxes (6 £ 7 £ 1 cm) containing cotton and absorbent
white paper saturated with water. Four replications of
the following treatments, each one with 25 seeds, were
performed: (1) red light pulses for 20 min d21 (R/FR
ratio ¼ 4.09; irradiance ¼ 18.0 mmol m22s 21), provided by two fluorescent tubes (Philips TL 40W/15)
covered with red acetate (lmax ¼ 610 nm) (La Casa del
Acetato, Buenos Aires, Argentina); (2) far red light
pulses for 20 min d21 (R/FR ratio ¼ 0.002;
irradiance ¼ 6.3 mmol m22 s21), provided by a 150 W
Osram incandescent quartz bulb, filtered with 10 cm
of water and Schott RG9 filters (2 mm width;
lmax ¼ 760 nm) (Schott, Mainz, Germany); and (3)
darkness. These treatments were combined with two
others: (1) fluctuating temperatures (20/308C,
9/15 h d21), simulating the average maximum and
Flooding affects Setaria parviflora seed dormancy
Results
Immediately after harvest, none of the seeds from
either population germinated, regardless of test
conditions. After 3 months of dry storage, the seeds
from the upland site germinated . 70% when exposed
to red light; this was significantly more germination
than in darkness. Germination at constant or
fluctuating temperatures did not exhibit significant
differences (Fig. 1a). The seeds from the lowland
community also had considerable germination, but
there were no large differences between the seeds
exposed to the different treatments (Fig. 1b). This was
the condition of the seeds immediately before starting
the experiments described below.
Field reciprocal burial experiments
During the time the seeds were buried, soil in the
lowland site was flooded several times during the
winter and spring, whereas no flooding occurred in
the upland site (Fig. 2). When the first exhumation was
made in late spring (November 2003), the lowland was
(a)
Temp. 0.096
Light 0.0001
Temp. x Light 0.061
Germination (%)
100
75
ab
a
bc
50
abc
bc
c
25
0
(b)
Temp. 0.23
Light 0.33
Temp. x Light 0.011
100
Germination (%)
minimum temperatures occurring in canopy gaps of
the grasslands, with the light treatments provided
during the high temperature phase; and (2) a constant
temperature of 258C.
Seeds were distributed in boxes under very low
intensity green light (Burkart and Sánchez, 1969), and
boxes were covered with black polyethylene. Then they
were exposed to the light treatments for 5 d, followed
by 5 d in the dark. After 10 d, the number of germinated
seeds was counted. In the calculation of average
germination, dead seeds were discounted from the
total number of seeds per box (Herron et al., 2000). The
distinction between live and dead seeds was made in
each repetition based on the hardness of seeds,
determined by holding them with histological tweezers (Steadman, 2004). At the same time, for another
group of seeds subject to the same pre-treatments,
tetrazolium tests were performed [2, 3, 5-triphenyltetrazolium chloride (1%, w/v) for 24 h in the dark at
258C] to determine their viability. The germination
averages were transformed to proportions, and
transformed
again according to an arc sine formula,
p
x (Sokal and Rohlf, 1969). For the study of the effect of
flooding upon the dormancy level of S. parviflora seeds,
the transformed data were analysed using a two-way
analysis of variance. Multiple comparisons were
performed with the Tukey test (P , 0.05). Differences
in behaviour between the upland and lowland seed
populations were tested by studying the triple
interaction, population £ temperature £ light, using a
three-way analysis of variance (Sokal and Rohlf, 1969).
57
75
a
ab
50
ab
ab
b
b
25
0
FT + R
FT + FR FT + Dark CT + R
CT + FR CT + Dark
Figure 1. Germination (%) under different temperature and
light treatments for Setaria parviflora seeds before the start of
pre-treatments. Seeds were harvested from the upland (a) or
the lowland (b), and dry-stored for 3 months at 208C. FT,
fluctuating temperatures (20–308C); CT, continuous temperature (258C); R, light with a high R/FR ratio; FR, light with
a low R/FR ratio; Dark, darkness. Values are means ^ SE. The
significance of the two-way ANOVA (dfError ¼ 18) appears
inside each panel. Different letters indicate significant
differences (P , 0.05). Differences in germination behaviour
were detected between populations with a three-way
ANOVA (population £ temperature £ light: P ¼ 0.0036).
The viability of seeds was 92% in (a) and 96% in (b).
flooded, but when the second exhumation was made
in mid-summer (January 2003), both sites were under
a drought (Fig. 2).
The differences in soil environment had a large
influence on the dormancy of seeds of both communities, but affected them in a similar way. After
exhumation following 6 months of burial, the seeds
buried in the upland site (Fig. 3a, c) germinated to
higher percentages than those buried in the lowland
site (Fig. 3b, d). Whereas seeds buried in the upland
germinated to higher percentages than before burial
(Fig. 3a, c), those buried in the lowland germinated
to lower percentages than before burial, and
only showed significant germination at fluctuating
temperatures (Fig. 3b, d). There were no significant
differences between the seeds from the upland and
F.P.O. Mollard et al.
58
lowland communities in their behaviour after being
buried in the upland soil (population £ temperature £
light: P ¼ 0.289). On the other hand, seeds from the
upland community buried in the lowland were more
affected by burial than seeds harvested in the lowland
(population £ temperature £ light: P ¼ 0.023).
Germination of the seeds exhumed during the
summer drought, after 8 months of burial, was higher
than in the previous exhumation date, particularly
under the most stimulating conditions: light plus
fluctuating temperatures (Fig. 4). Moreover, the lowest
values of germination were observed at constant
temperature in the absence of red light, especially in
seeds buried in the lowland community (Fig. 4b, d).
There were no differences in germination between
seed populations buried in the upland and exhumed
in summer (population £ temperature £ light;
P ¼ 0.680). However, at the same exhumation time,
the seeds from the lowland community were less
dormant than those from the upland community
Soil volumetric hydric content (%)
45
40
35
30
25
20
15
10
5
0
19/07/03 02/09/03 17/10/03 01/12/03 15/01/04
Figure 2. Soil volumetric hydric content of the upland
(discontinuous line) and lowland (continuous line) communities during the field reciprocal burial experiments. The
horizontal line above the x-axis shows flooding periods in
the lowland community. Arrows show the exhumation dates
of seeds.
Temp. < 0.0001
Light 0.025
Temp. x Light 0.74
(a)
100
a
Germination (%)
a
Temp. 0.0001
Light 0.033
Temp. x Light 0.38
(b)
a
75
b
50
b
a
b
25
ab
ab
b
b
0
Temp. < 0.0001
Light 0.012
Temp. x Light 0.065
(c)
100
Germination (%)
ab
a
b
Temp. < 0.0001
Light 0.0004
Temp.x Light 0.0004
(d)
ab
ab
75
bc
a
50
a
c
25
b
c
0
FT + R
FT + FR FT + Dark CT + R
CT + FR CT + Dark
FT + R
FT + FR FT + Dark
CT + R
c
c
CT + FR CT + Dark
Figure 3. Germination (%) under different temperature and light treatments of Setaria parviflora seeds from a reciprocal burial
experiment between seeds harvested in an upland community (a, b), or harvested in a lowland community (c, d). Seeds were
buried in the upland community (a, c) or in the lowland community (b, d). Seeds remained buried in the field for 6 months and
were exhumed in spring during flooding in the lowland. FT, fluctuating temperatures (20– 308C); CT, continuous temperature
(258C); R, light with high R/FR; FR, light with low R/FR; Dark, darkness. Values are means ^ SE. The significance of the twoway ANOVA (dfError ¼ 18) appears inside the panels. Different letters indicate significant differences (P , 0.05). Viability of
seeds was 84% in (a), 92% in (b), 80% in (c) and 84% in (d).
Flooding affects Setaria parviflora seed dormancy
(a)
a
Germination (%)
100
Temp. < 0.0001
Light < 0.0001
Temp. x Light 0.0082
a
b
75
59
(b)
Temp. < 0.0001
Light < 0.0001
Temp. x Light 0.15
b
a
a
50
c
c
b
25
b
c
cd
0
(c)
Germination (%)
100
a
Temp. < 0.0001
Light < 0.0001
Temp. x Light 0.0018
a
bc
(d)
d
Temp. < 0.0001
Light 0.0001
Temp. x Light 0.069
a
b
a
75
a
cd
a
d
50
b
25
b
0
FT + R
FT + FR FT + Dark CT + R
CT + FR CT + Dark
FT + R
FT + FR FT + Dark CT + R
CT + FR CT + Dark
Figure 4. Germination (%) under different temperature and light treatments of Setaria parviflora seeds from a reciprocal burial
experiment between seeds harvested in an upland community (a, b), or harvested in a lowland community (c, d). Seeds were
buried in the upland community (a, c) or in the lowland community (b, d). Seeds remained buried in the field for 8 months and
were exhumed in summer. FT, fluctuating temperatures (20– 308C); CT, continuous temperature (258C); R, light with high R/FR;
FR, light with low R/FR; Dark, darkness. Values are means ^ SE. The significance of the two-way ANOVA (dfError ¼ 18) appears
inside each panel. Different letters indicate significant differences (P , 0.05). Viability of seeds was 88% in (a), 72% in (b), 76% in
(c) and 80% in (d).
when both were buried in the lowland (population £
temperature £ light; P ¼ 0.018).
The effect of immersion in water under controlled
conditions
The soil conditions in the burial experiment suggested
that immersion in water was the predominant factor
modulating the secondary dormancy of S. parviflora
seeds. To test this possibility, the effect of immersion in
water was assayed with seeds from both communities
under controlled conditions.
After exposure to an immersion pre-treatment, the
seeds of both populations of S. parviflora showed a
reduced capacity to germinate at constant temperature (Fig. 5b, d). The decrease of the germination
percentage at constant temperature was nearly 45% in
the seeds from the upland community (Fig. 5b) and
42% in those from the lowland (Fig. 5d), compared
with germination at fluctuating temperatures. This
temperature effect on the control seeds incubated on
water-saturated white paper was much less noticeable; the seeds from the upland community germinated, on average, 20% less at continuous
temperatures than at fluctuating temperatures
(Fig. 5a), while in the lowland community seeds, this
difference was only 10% (Fig. 5c). Seed populations
did not differ after immersion in water (Fig. 5b, d)
(population £ temperature £ light, P ¼ 0.354). The
seeds harvested in the upland were less dormant
than seeds from the lowland after incubation on
water-saturated filter paper (Fig. 5a, c). However,
there were no differences between seed populations in
the response to germination treatments (population £
temperature £ light; P ¼ 0.486).
Discussion
Non-dormant seeds may enter secondary dormancy
in response to environmental conditions that are not
F.P.O. Mollard et al.
60
Temp. 0.0002
Light 0.0040
Temp. x Light 0.14
(a)
Germination (%)
100
Temp. < 0.0001
Light 0.0039
Temp. x Light 0.033
(b)
a
75
ab
bc
a
abc
a
c
50
a
c
b
25
c
c
0
Temp. 0.03
Light 0.14
Temp. x Light 0.07
(c)
Germination (%)
100
Temp. < 0.0001
Light 0.46
Temp. x Light 0.87
(d)
75
a
50
a
a
a
ab
ab
ab
ab
b
25
b
b
0
FT + R
FT + FR FT + Dark CT + R
CT + FR CT + Dark
FT + R
FT + FR FT + Dark
CT + R
b
CT + FR CT + Dark
Figure 5. Germination (%) under different temperature and light treatments of Setaria parviflora seeds, previously incubated on
saturated white paper (a, c) or immersed in water (b, d) for 90 d at 58C. Seeds were harvested in the upland (a, b) or in the
lowland (c, d). FT, fluctuating temperatures (20– 308C); CT, continuous temperature (258C); R, light with high R/FR; FR, light
with low R/FR; Dark, darkness. Values are means ^ SE. The significance of the two-way ANOVA (dfError ¼ 18) appears
inside each panel. Different letters indicate significant differences (P , 0.05). The viability of the seeds was 92% in (a, c, d) and
88% in (b).
favourable for seedling establishment (Bouwmeester
and Karssen, 1992; Hilhorst, 1998). Floods, among
other environmental unfavourable conditions, have a
major role in many habitats because of their
consequences for seedling survival (Crawford, 2003).
Our results show that a significant proportion of
Setaria parviflora seeds enter secondary dormancy in
the soil during flooding, in contrast to seeds in nearby
non-flooded areas that continue to lose primary
dormancy.
As a signal that promotes germination of seeds,
fluctuating temperature is part of a mechanism
allowing the seeds to perceive particular environmental conditions (Thompson et al., 1977; Benech-Arnold
et al., 1988). In seeds of many wetland species,
temperature fluctuations can promote germination
(Thompson and Grime, 1983). Sensitivity to fluctuating temperatures is a mechanism that would allow
seeds to detect a decrease in water depth, i.e.
temperature fluctuations increase as water depth
decreases (Thompson and Grime, 1983; Pons and
Schroder, 1986; Ekstam and Forseby, 1999). In
addition, alternating temperature permits the detection of vegetation gaps, as do other mechanisms, such
as the R/FR ratio of light acting through phytochrome
(Casal and Sánchez, 1998). In Flooding Pampa
grasslands, seeds of Ambrosia tenuifolia germinate
after perceiving light with high R/FR reaching the soil
in vegetation gaps created by plant death during
previous waterlogged conditions (Insausti et al., 1995).
Our data show that, in the studied populations of
S. parviflora, entrance into secondary dormancy
during immersion was expressed by a decrease in
the germination capacity and by an increase in the
dependence on fluctuating temperatures for germination. Moreover, this fluctuating temperature requirement was accompanied by a light requirement to
reach maximum germination. Induction of secondary
dormancy in flooded S. parviflora seeds will prevent
not only germination when the area is flooded (Pons
and Schroder, 1986; Ekstam and Forseby, 1999), but
will also delay seedling emergence until well after
flooding ceases. So, seeds exhumed from flooded soils
do not germinate immediately, even when incubated
Flooding affects Setaria parviflora seed dormancy
in the laboratory under fluctuating temperatures and
light. Secondary dormancy is lost slowly after the end
of the flooding season, and is still detected 2 months
after the end of flooding (Fig. 4). Thus, germination
cannot occur until well after the risk of flooding
subsides.
Within a species, habitat is a prevailing factor in the
natural selection of the regulatory mechanisms of
germination (Meyer et al., 1997; Donohue et al., 2005).
Remarkably, in S. parviflora seeds harvested from the
non-flooded upland, we observed essentially the same
requirements after flooding as in seeds harvested in
the lowland. The lack of a substantial difference
between the two populations may be due to the
proximity of the flooded and non-flooded areas.
Nevertheless, some relatively small differences were
detected in the degree of secondary dormancy
induced in each population by flooding. These
dissimilarities were perceived only in the field
experiment and not after immersion in water in the
laboratory. A proper assessment of the relevance of
these differences requires additional exploration.
Acknowledgements
We specially thank Gustavo Striker for assistance and
comments about manuscript. This study was supported by a grant of ANPCyT Foncyt PICT 08-09934.
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Received 2 August 2006
accepted after revision 21 November 2006
q 2007 Cambridge University Press