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o Summary
o Introduction
o Materials and methods
o Field emergence of seedlings
o Effect of after-ripening on dormancy break and seed germination
o Effect of environmental signals on seed germination
o Results
o Field emergence of seedlings
o Effect of after-ripening on dormancy break and seed germination
o Effect of environmental signals on seed germination
o Discussion
o Acknowledgements
o
o References
o Related Content
o Citing Literature

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Volume 22, Issue 3
June 2008
Pages 470478

Environmental signals for seed germination

reflect habitat adaptations in four temperate
Caryophyllaceae
Authors
F. Vandelook,
 Corresponding authorSearch for more papers by this author

D. Van de Moer,
1. Laboratory of Plant Ecology, K.U. Leuven, Kasteelpark Arenberg 31, Box 2435,
B-3001 Leuven, Belgium

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J. A. Van Assche
1. Laboratory of Plant Ecology, K.U. Leuven, Kasteelpark Arenberg 31, Box 2435,
B-3001 Leuven, Belgium

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First published: 14 February 2008Full publication history

DOI: 10.1111/j.1365-2435.2008.01385.x View/save citation
Cited by (CrossRef): 33 articles Check for updates

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*Corresponding author. E-mail: filip.vandelook@bio.kuleuven.be

Summary
1Requirements for dormancy break and seed germination are specific for all species and
depend chiefly on phylogeny, geographical distribution, habitat preference and life cycle.
Studying germination requirements of closely related species with a similar geographic
distribution allows one to attribute variation in germination requirements to differences in
habitat preference between the species.
2We investigated requirements for dormancy break and the effect of environmental
signals on induction of germination in seeds of four closely related Caryophyllaceae
species growing in a variety of habitats (Moehringia trinervia, Stellaria holostea, S.
nemorum and S. graminea). The species studied depend on disturbances in the vegetation
for seed germination and subsequent seedling establishment.
3Seedlings of all four species emerged both in summer and spring. Stellaria nemorum
and M. trinervia, both growing in temperate forests, emerged mainly in summer under a
 closed forest canopy. Seeds of S. graminea, occurring in grasslands, did germinate in
summer at an open site, but could not germinate under a closed forest canopy. Seedlings
of S. holostea were observed in late summer when buried at an open site or in early
spring when sown in a forest patch.
4Seeds of S. holostea and M. trinervia were completely dormant at dispersal in early
summer, while germination was low in fresh seeds of S. graminea and S. nemorum.
Dormancy was broken, to a certain extent, during all three after-ripening treatments
applied (dry storage, cold and warm stratification).
5The effect of three gap-detection signals (light, fluctuating temperatures, nitrates) on
germination of fresh and dry stored seeds was tested. Seeds of S. holostea only
germinated in response to daily fluctuating temperatures. Although light was the most
important signal affecting germination of S. graminea and M. trinervia, we also observed
a positive effect of fluctuating temperatures and nitrates on germination. The effect of
fluctuating temperatures on germination of S. nemorum was small in both light and dark
incubated seeds. Seed germination in this species generally occurred in response to
addition of light and nitrates.
6This study on dormancy breaking and germination requirements of the four species
enabled us to expose, sometimes subtle, differences in germination requirements. These
contrasting germination patterns were related to differences in the species habitat
preferences.

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Introduction
Timing and location of seed germination are crucial factors in a plant's chances of completing its
life cycle. Germination of seeds in a natural environment is often restricted to locations that meet
specific environmental conditions. These locations are often referred to as safe-sites (Harper
1977) or regeneration niches (Grubb 1977). In many habitats, the establishment of seedlings
depends on the presence of sites that are clear of vegetation, that is, vegetation gaps (Fenner &
Thompson 2005). Environmental conditions in vegetation gaps often differ considerably,
depending on type and size of the gaps, as compared to those of the corresponding intact
vegetation (Bullock 2000). A number of these environmental conditions can act as cues for seed
germination after gap formation or as gap-detection mechanisms (Pons 1989).

Daily fluctuating temperatures, light and nitrate are the most cited environmental signals
affecting germination of seeds at disturbed sites (Vincent & Roberts 1977; Daws et al. 2002).
Several processes, such as a reduced nutrient uptake and an increased nitrification and
mineralization rate, contribute to an increased soil nitrate content after removal of the vegetation
(Ritter, Starr & Vesterdal 2005). An increased soil nitrate level has been observed after
disturbances ranging from small mole hills in grasslands (Canals & Sebastia 2000) to large clear-
cut forest patches (Likens et al. 1970). Removal of the vegetation cover or leaf litter not only
alters both intensity and quality of the light reaching the soil (Federer & Tanner 1966; Vazquez-
Yanes et al. 1990), but it also results in an increased amplitude of the daily maximum and
minimum temperature, due to the increased amount of radiation reaching the soil surface (Van
Assche & Vanlerberghe 1989). The above-mentioned factors provide a snapshot of the seeds
environment. The efficiency of these factors for inducing germination depends on the dormancy
state of the seed (Bouwmeester & Karssen 1993). Most seeds persisting in the soil for extended
periods of time undergo seasonal changes in their dormancy state. According to Vleeshouwers,
Bouwmeester & Karssen (1995) temperature is the sole environmental factor regulating the
dormancy state of seeds. Dormancy thus provides the seeds with a mechanism to pass favourable
periods for germination, but unfavourable for seedling establishment.

Dormancy breaking and germination requirements are specific for each species and depend on
phylogeny, geographic distribution, habitat and life cycle. Large scale screening studies have
indicated that germination strategies are, to a certain extent, related to the species habitat (Grime
et al. 1981; Baskin & Baskin 1988; Schtz & Rave 1999). Nevertheless, more than one
germination pattern can occur within a given habitat (Angevine & Chabot 1979). Coexistence of
pioneer species in canopy gaps of tropical forests, for example, has been attributed to subtle
differences in germination response to environmental signals (Daws et al. 2002; Pearson et al.
2002). Mirov (1936) and Baskin & Baskin (1988) did not find dormancy breaking and
germination requirements to be phylogenetically constrained, but they did notice some
tendencies within certain plant families. In addition, Nikolaeva (1999) stated that the
physiological properties and dormancy pattern of various seeds are undoubtedly related to plant
position within large taxa. Therefore, if one wants to attribute differing germination
requirements among species to differences in habitat preference, it is necessary to look at closely
related species with similar geographic distribution and life cycle. Relatively few studies have
taken this approach to relate germination strategies to habitat conditions at the species level (e.g.
Daws et al. 2002; Van Assche, Van Nerum & Darius 2002; Pezzani & Montana 2006).

In our study, we focussed on the dormancy breaking and germination requirements of four
closely related Caryophyllaceae species, Moehringia trinervia (Clairv.) L., Stellaria nemorum
subsp. nemorum L., Stellaria holostea L. and Stellaria graminea L. (Fior et al. 2006). All four
species have a similar geographic distribution, occurring throughout Europe and Western Asia.
Stellaria nemorum is somewhat restricted to more continental or alpine regions (Hultn & Fries
1986). The three Stellaria species studied are all perennials that can reproduce both vegetatively
and generatively. Despite the fact that M. trinervia only reproduces through seeds, its life cycle is
less obvious. Some authors consider M. trinervia to be a summer-annual or short lived
polycarpic perennial species, depending on the amount of shade present (Hegi 1975; Grime,
Hodgson & Hunt 1988), while others assume M. trinervia is a winter-annual species (Baskin &
Baskin 1998). The studied species all rely on some sort of disturbance of the vegetation for
germination and subsequent seedling establishment. The most important ecological difference,
although sometimes subtle, between the studied species is found in their habitat preference
(Table 1).

Table 1. Average seed mass, seed length (mean SE) and habitat preference of the species
studied
Length Habitat preference (from Hegi
Mass (mg)
(mm) 1975)
Stellaria graminea L. 038 008 11 01 Dry grasslands, road verges
 Table 1. Average seed mass, seed length (mean SE) and habitat preference of the species
studied
Length Habitat preference (from Hegi
Mass (mg)
(mm) 1975)
Shady sites in deciduous forests,
Stellaria nemorum L. 035 006 12 01
scrubs
Stellaria holostea L. 239 065 26 02 Forest edges, open forests, hedgerows
Moehringia trinervia (L.) Disturbed shady sites in woodlands,
026 001 11 01
Clairv. scrubs

Our study aimed at resolving dormancy breaking and germination requirements of the four
Caryophyllaceae species. In a first experiment, timing of seedling emergence of seeds sown in
natural conditions simulating disturbed sites was recorded. A second series of experiments was
performed in controlled conditions to test whether: (i) seeds of these species have primary
dormancy; (ii) dormancy can be relieved or induced by after-ripening treatments; (iii) nitrates,
light and fluctuating temperatures can induce germination. Since the four species are
phylogenetically and geographically closely related, differences in dormancy breaking and
germination requirements between the studied species were attributed to habitat adaptations or
life cycle of the species.

Materials and methods

Moehringia trinervia (L.) Clairv., Stellaria holostea L. and Stellaria graminea L. with ripe fruits
were collected near Diest, Belgium (5048 N, 53 E) in June and July 2005 and 2007.
Moehringia trinervia and S. holostea were growing on a shady road verge, while S. graminea
was growing in a wet meadow along a river. Stellaria nemorum L. was collected in June 2005
and 2007 in Anseremme, Belgium (5014 N, 454 E) from plants growing in a woodland on a
riverbank. The plant material was spread out at the laboratory for 1 week. During this period ripe
seeds fell out of the dried fruits and were harvested. All experiments were performed within 1
week after harvest.

The seed mass of each species was determined by weighing 100 air dry seeds. To estimate
standard deviation, this sample was visually divided in 10 size classes and total weight of the 10
seeds in each class was calculated. We also measured the maximum length of 20 seeds using a
dissecting microscope with an ocular micrometer.

Field emergence of seedlings

Timing of seedling emergence was studied by sowing 50 seeds outdoors in plastic flower pots
filled with potting soil at a depth of 1 cm and at the soil surface. In each condition three pots
were buried at soil level at either an open place without canopy cover in an experimental garden
near Leuven (Belgium) or in a nearby woodland patch. The tree layer of this woodland patch was
comprised mainly of Quercus rubra L., Aesculus hippocastanum L. and Acer platanoides L. This
experiment was started in early July 2005 and observations were continued for 1 year. Emerged
seedlings were recorded weekly and removed to prevent competition. Afterwards the number of
seedlings emerging in each month was calculated. Pots were covered with a net to prevent
disturbance by birds and a molluscicide was applied. Leaf litter was removed regularly from the
pots to prevent covering. Since we used potting soil in this experiment, nitrate levels might
deviate from those found in natural conditions. Therefore, in May 2006 at the end of the
experiment, two replicate soil samples were taken from the pots buried in the garden and in the
woodland patch. These samples were used for measuring nitrate levels using the 2 m KCl
method (Dahnke & Johnson 1990).

Effect of after-ripening on dormancy break and seed

germination
Germination of seeds collected in 2005 was tested following three different after-ripening
conditions lasting for 16 weeks. These results were compared to a control condition in which
seeds were germinated without storage. During moist storage seeds were placed in Petri dishes
on a filter paper (Schleicher & Schuell No. 2282) moistened with distilled water. Petri dishes
were stored in darkness in a light-tight wooden box at low (5 C) or high (23 C) temperature
conditions. Every week the boxes were opened under a green safe light to keep the filter papers
moist. A third batch of seeds was stored dry at room temperature (c. 20 C). After the respective
pre-treatments, seeds were incubated at constant temperatures of 10 C and 23 C and at daily
alternating temperatures of 15/6 C, 20/10 C and 30/20 C (12 h/12 h). Three replicates of 50
seeds were placed in total darkness or in a 12-h photoperiod, whereby light was provided by
fluorescent tubes (Philips TLD 80) with a photon flux density of 52 mol m2 s1, 400700 nm.
In the case of incubation in light at alternating temperatures, the 12-h photoperiod coincided with
the high temperature part of the temperature cycle. After 2 weeks the number of germinated
seeds was counted and the experiment was terminated. Within each germination condition the
effect of storage condition was tested using one-way anova, followed by the Tukey multiple
comparisons test. Germination percentages were arcsine transformed in order to stabilize
variances.

Effect of environmental signals on seed germination

The combined action of nitrate, daily fluctuating temperatures and light as signals for
germination were determined by incubating seeds under varying conditions. This experiment was
performed using fresh seeds (collected in 2007) and seeds dry stored for 12 weeks at c. 20 C
prior to germination (collected in 2005). For each species three replicates of 50 seeds were
placed in a Petri dish on a moistened filter paper and incubated under controlled conditions. Petri
dishes were placed in incubators at a constant temperature of 20 C or at daily alternating
temperatures of 20/10 C. To test for effects of nitrate on germination, in each of the above-
mentioned temperature and light conditions, we moistened filter papers with 10 mL of 0, 05 or
10 mm KNO3. These concentrations were based on an experiment performed on Plantago
lanceolata by Pons (1989). In this experiment, < 1 mm KNO3 had a small stimulating effect on
seed germination, while a peak of germination was recorded at 10 mm KNO3. After 2 weeks of
incubation the number of germinated seeds was determined and the experiment was terminated.
The combined effect of light, fluctuating temperatures and nitrate concentration was tested on
fresh and dry stored seeds using a three-way anova. All data were arcsine transformed prior to
analysis.

Results
Stellaria graminea and S. nemorum were very similar in respect to seed size (Table 1).
Moehringia trinervia has slightly smaller seeds that are less variable when compared to seeds of
S. graminea and S. nemorum. Seeds of S. holostea were six to nine times larger, as compared to
the other species examined.

Field emergence of seedlings

Seedlings of all four studied species emerged from July 2005 until April 2006 (Fig. 1).
Emergence occurred mainly during summer and to a lesser extent in the following spring, while
no seedlings were observed in May 2006. Almost all S. graminea seeds sown in the experimental
garden had germinated in the summer of sowing, with a peak in August. Seeds sown in the
woodland patch, however, had germinated to < 30% after 1 year and these seedlings emerged
throughout summer, autumn and spring.

<img class="inline-figure__image" alt="Figure&nbsp;1. "

src="http://onlinelibrary.wiley.com/store/10.1111/j.1365-
2435.2008.01385.x/asset/image_n/FEC_1385_f1.gif?v=1&amp;t=ja14pi4a&amp;s=875c12d113
03b1be265c75c685b180b0fbf52d7d" />

Figure 1.

Open Figure
Download Powerpoint slide

Percentage of emerged seedlings recorded monthly over a 1-year period from seeds sown in
early July 2005. Seeds were sown in an open garden (capital letters) and in a forest patch (small
letters). A,a: Stellaria graminea; B,b: Stellaria nemorum; C,c: Stellaria holostea; D,d:
Moehringia trinervia. Seeds were sown either at the soil surface (white bars) or buried 1 cm deep
(grey bars). Vertical bars denote SE; n = 3.

A different pattern of seedling emergence was observed for S. nemorum and M. trinervia. Many
more seedlings emerged in the woodland patch as compared to the seeds sown in the garden.
Very few seedlings were recorded from seeds sown at the soil surface in the garden. Only 127%
of the S. nemorum and 87% of the M. trinervia seeds had emerged after 1 year. Both in the
garden and in the woodland patch S. nemorum seedlings mainly emerged during summer. In the
woodland patch, a considerable amount of seedlings was also observed in February 2006.
Moehringia trinervia seedlings emerged in summer and spring, although spring germination was
higher for seeds sown in the woodland patch.
There was a clear difference in seasonality of seedling emergence between S. holostea seeds
sown in the open garden and in the woodland patch. Germination of S. holostea in the garden
peaked in August, while for seeds sown in the woodland patch a peak in emergence was
observed in February and March. In the garden up to 80% of the seedlings emerged when seeds
were buried 1 cm deep, while only 181% of the seeds sown at the soil surface had germinated.
At the end of the experiment in May 2006, the nitrate level in the soil was 1576 and
2958 mg/kg, respectively, for the pots buried in the forest and the open garden.

Effect of after-ripening on dormancy break and seed

germination
Germination was generally very low in seeds incubated immediately after harvesting, except for
seeds of S. nemorum (Fig. 2). After-ripening of the seeds occurred during dry storage as well as
during cold or warm stratification. Subsequent germination was stimulated by light in all species,
except for S. holostea were no difference in germination between light and dark incubated seeds
were observed.

<img class="inline-figure__image" alt="Figure&nbsp;2. "

src="http://onlinelibrary.wiley.com/store/10.1111/j.1365-
2435.2008.01385.x/asset/image_n/FEC_1385_f2.gif?v=1&amp;t=ja14pi4b&amp;s=1e3572e936
2a065e2ce6570c5f335f2b422189a2" />

Figure 2.

Open Figure
Download Powerpoint slide

Seed germination percentage of after-ripened seeds incubated at different temperature conditions

in light (capital letters) and darkness (small letters). A,a: Stellaria graminea; B,b: Stellaria
nemorum; C,c: Stellaria holostea; D,d: Moehringia trinervia. Seeds of a control condition were
tested (Fresh), as were seeds after-ripened at warm moist (Warm), warm dry (Dry) and cold
moist (Cold) conditions. Means followed by the same letter within an incubation condition are
not significantly different at the P < 005 level (Tukey multiple comparisons test). n = 3.

All pre-treatments applied had a stimulating effect on germination of S. graminea seeds provided
with light. Dry storage was, however, the most effective treatment for dormancy break in S.
graminea at all test temperatures in both light and darkness. The effect of the warm and cold
stratification was most pronounced in seeds incubated at 10 C, 15/6 C and 20/10 C in light. As
was the case with S. graminea seeds, very few seeds of S. nemorum and M. trinervia germinated
in darkness at any temperature. Subjecting seeds of S. nemorum to a cold stratification led to
significantly more germination at all temperatures in a 12-h photoperiod. Warm moist and dry
storage only had a significant positive effect on S. nemorum seeds incubated at the lowest
(10 C) and highest (30/20 C) temperature condition tested. In contrast to the other species
examined, light was not required for germination of S. holostea. All seeds were primary dormant
and germinated at fluctuating temperatures after dry storage and warm moist stratification.
Fresh seeds of M. trinervia were dormant and did not germinate at any condition tested (Fig. 2).
After cold stratification seeds only germinated when incubated at 20/10 C in the light.
Germination after warm moist and dry storage was also highest at 20/10 C, but after these pre-
treatments seeds also germinated when incubated at 30/20 C, 23 C and 15/6 C.

Effect of environmental signals on seed germination

In almost all conditions tested, higher germination percentages were attained in the 2005 batch
after 12 weeks of dry storage as compared to the fresh seeds collected in 2007. This was true for
all four species studied. Regardless of nitrate concentration, fresh seeds of S. graminea
germinated to c. 14% when incubated at 20/10 C in light (results not shown). At all other
conditions tested, germination of S. graminea seeds was negligible. Much higher germination
percentages were recorded for dry stored seeds (Fig. 3). Light, daily fluctuating temperatures and
addition of nitrates significantly enhanced germination (Table 2). Effects of nitrate concentration
were most pronounced in S. graminea seeds incubated in light. In dry stored seeds of S.
nemorum, on the contrary, nitrate effects are most readily noticed when seeds were incubated in
darkness. Light is, however, the most crucial factor in germination of both fresh and dry stored
seeds of S. nemorum. Fresh seeds incubated in light germinated between 30% and 45%, while
germination was negligible when seeds where incubated in complete darkness for all temperature
and nitrate conditions. The positive effect of daily temperature fluctuations on germination of dry
stored S. nemorum seeds was small, but still significant.

<img class="inline-figure__image" alt="Figure&nbsp;3. "

src="http://onlinelibrary.wiley.com/store/10.1111/j.1365-
2435.2008.01385.x/asset/image_n/FEC_1385_f3.gif?v=1&amp;t=ja14pi4c&amp;s=98a48f94df6
43169538b99e9e2d1331c16eb9d20" />

Figure 3.

Open Figure
Download Powerpoint slide

Mean seed germination percentages of seeds incubated for 2 weeks at different temperature, light
and nitrate conditions after 12 weeks of dry storage. A, Stellaria graminea; B, Stellaria
nemorum; C, Stellaria holostea; D, Moehringia trinervia. Seeds were incubated in light (open
symbols) or darkness (full symbols), at 20 C (squares) or 20/10 C (triangles). Vertical bars
denote SE. n = 3.

Table 2. Results of a three-way anova applied to seed germination percentages of seeds

incubated at different light, nitrate and temperature conditions for 2 weeks after 12 weeks of dry
storage
Stellaria Stellaria Stellaria Moehringia
holostea graminea nemorum trinervia
1. NS, not significant, *P < 005, **P < 001, ***P < 0001.
 Table 2. Results of a three-way anova applied to seed germination percentages of seeds
incubated at different light, nitrate and temperature conditions for 2 weeks after 12 weeks of dry
storage
Stellaria Stellaria Stellaria Moehringia
holostea graminea nemorum trinervia
Nitrate (N) ** *** *** ***
Temperature (T) *** *** ** ***
Light (T) NS *** *** ***
NT * * NS ***
NL NS *** * ***
TL NS *** NS *
NTL * * NS ***

None of the fresh seeds of S. holostea had germinated after 2 weeks of incubation in any of the
test conditions. After a 12 week dry storage period, between 10% and 20% of S. holostea seeds
germinated during 2 weeks of incubation at 20/10 C (Fig. 3). No germination was recorded in
seeds incubated at constant 20 C. After 12 weeks of dry storage, light did not seem to affect
germination of S. holostea seeds, while a small stimulating effect of nitrates was recorded. When
fresh seeds of M. trinervia were incubated in a combined regime of light, daily fluctuating
temperature and 10 mm KNO3, a germination percentage of c. 10% was recorded after 2 weeks.
In all other regimes tested, no or very few seeds germinated. A very different pattern was
observed for dry stored seeds of M. trinervia. A low nitrate concentration enhanced germination
of seeds incubated in light at daily fluctuating temperatures, while higher nitrate concentrations
also stimulated germination of seeds incubated at constant temperature in the light and at daily
fluctuating temperatures in darkness.

Discussion
In general, small seeded species are more likely to have a light requirement for germination, than
species with larger seeds (Milberg, Andersson & Thompson 2000). Jankowska-Blaszczuk &
Daws (2007) considered a seed mass of 15 mg as a threshold, that separates between temperate
forest herbs requiring light for germinating and those that do not. When this threshold is applied
to the species we studied, S. holostea, with relatively large seeds, can be distinguished from the
three remaining species. A light requirement for germination is regarded as an important
determinant for predicting seed persistence in the soil, as are seed size and shape (Thompson,
Band & Hodgson 1993). Stellaria nemorum, S. graminea and M. trinervia all have fairly small
round seeds that are regularly retrieved in soil seed bank studies (Staaf, Jonsson & Olsen 1987;
Jankowska-Blaszczuk & Grubb 1997; Edwards & Crawley 1999). Despite the fact that these
three species are able to form a persistent seed bank, many seedlings were observed during our
experiment on seedling emergence (Fig. 1). This can be attributed to the fact that the conditions
in which the seeds were sown resembled natural disturbance conditions. During the course of the
experiment no vegetation was present in the pots and leaf litter was removed regularly. Due to
the use of commercial potting soil, nitrate levels in the plastic pots were expected to be high
throughout the experiment. This was confirmed by the nitrate levels we measured at the end of
the experiment. These were fairly high and resembled those of disturbed sites in forests and
grasslands (Canals & Sebastia 2000; Ritter & Vesterdal 2006). Since the same substrate was
used to fill the pots buried in the garden and the forest, nitrate levels at the start of the experiment
had to be equal at both sites. After 1 year, however, the pots in the garden contained almost twice
as much nitrate as the pots in the forest. An increased uptake of nitrates by small tree roots, that
had invaded the pots in the forest patch during the experiment, might offer one possible
explanation for this discrepancy.

Seeds of species that are able to form a persistent seed bank are often dormant at the moment of
dispersal, that is, primary dormant. Primary dormancy prevents seeds from germinating
immediately after dispersal and increases the seeds chances to become buried and incorporated
in the soil seed bank (Thompson & Grime 1979). Fresh seeds of M. trinervia and S. holostea do
not germinate at all in any of the conditions tested and they require an after-ripening period to
break primary dormancy. Grime et al. (1981) obtained similar results from experiments on fresh
and dry stored seeds of M. trinervia. Fresh seeds of S. nemorum and S. graminea, on the other
hand, already germinated to low percentages, but even in these two species an after-ripening
period increased the percentage of germinated seeds. Since dry storage can overcome primary
dormancy, seeds of all four studied species have non-deep physiological dormancy, according to
the classification system proposed by Baskin & Baskin (1998).

In general, primary dormancy in seeds with non-deep physiological dormancy is broken by either
cold or warm stratification (Probert 2000). In the species we studied, both warm and cold
stratification alleviated dormancy to a certain extent, while no induction of dormancy was
observed after any stratification treatment (Fig. 2). In Spergula arvensis (Caryophyllaceae)
dormancy could also be broken by either a warm or cold stratification (Karssen, Derkx & Post
1988). Moehringia trinervia is one of the few annual species occurring in Western European
forests (Grime et al. 1988). Since both warm and cold stratification can break dormancy in this
species, no clear-cut conclusion can be drawn on the life cycle. Moreover, in our experiment on
seedling emergence, seedlings were observed in both summer and spring. Further experiments on
seedling survival should clarify whether M. trinervia can exhibit both a winter- and summer-
annual life cycle as is found in Stellaria media (L.) Vill. (van der Vegte 1978).

Cold and warm stratification treatments were not always able to break dormancy of S. holostea
seeds, probably due to an incubation period that was too short. The pattern of seedling
emergence in the field, however, suggests that both cold and warm stratification affect the seeds
dormancy status. Seeds sown in the open garden emerged in late summer after a period at high
temperatures, while seeds buried in the forest patch germinated generally after a cold period in
late winter and early spring. Thus it seems that seeds of S. holostea are able to germinate in late
summer or in early spring depending on the seeds environment and especially the degree of
vegetation cover. A facultative autumn or spring emergence pattern has previously been
observed in the North American Schoenolirion croceum (Liliaceae), a species generally growing
in more open habitats (Walck & Hidayati 2004). A delay of germination until spring was caused
by a light requirement in buried seeds of S. croceum. Seeds of S. holostea, however, are
indifferent to light and a delay in germination until spring is probably caused by the small daily
temperature amplitude in the forest patch. From an ecological point of view this strategy can be
understood as follows. Stellaria holostea grows in a variety of habitat types ranging from closed
forests to forest edges and hedges (Grime et al. 1988). When seeds are experiencing shady
conditions from the surrounding vegetation, germination is delayed until spring. In a temperate
climate, spring is often the most suitable season for germination, since seedlings can avoid low
winter temperatures and grow in conditions of reduced competition before the canopy closes
(Gross 1980). When no vegetation is present and seedlings can overcome cold winter conditions
it might be more profitable to germinate in summer or autumn and not to delay germination until
spring (Arthur, Gale & Lawrence 1973). This way seedlings will have more time to grow in
suitable environmental conditions and thereby increase their survival rate (Verdu & Traveset
2005).

Although S. graminea is considered a species colonizing grassland gaps, recruitment from the
seed bank into gaps appears to be limited (Edwards & Crawley 1999). This means that
colonisation of gaps occurs mainly through recently dispersed seeds or by vegetative expansion.
Dry storage was the most effective pre-treatment for breaking dormancy in seeds of S. graminea.
After-ripening during dry storage has been shown to be an important mechanism regulating
dormancy in winter annuals, preventing germination in dry summer months (Van Assche &
Vandelook 2006). A stimulating effect of dry storage was also found in a large number of
temperate grassland species surveyed by Grime et al. (1981). Almost all seedlings of S.
graminea buried in the garden emerged in the summer they were sown. Many more seedlings of
S. graminea emerged in the garden as compared to seeds buried in the forest patch, which can be
explained by differences in light composition at both sites. Light falling through a closed forest
canopy becomes far red enriched, due to absorption of red wavelengths by tree leafs (Federer &
Tanner 1966). The small number of seedlings in the forest is likely caused by the inhibiting
effect of FR enriched light on germination of S. graminea seeds. Light, daily fluctuating
temperatures and nitrate are the most important factors regulating seed germination of grassland
species in vegetation gaps (Williams 1983; Von Boberfeld et al. 2002). Seed germination of S.
graminea was stimulated by all three of these signals after a dry storage period that broke
primary dormancy (Fig. 2). A stimulating effect of nitrate, however, only occurred in seeds
incubated in the light, offering an additional explanation for the lack of germination under the
forest canopy, even in the presence of increased soil nitrate levels.

In a seed burial experiment performed by Staaf (1992) in a Swedish beech forest, most S.
nemorum subsp. glochidosperma seeds germinated during summer. In our experiment, seedlings
of S. nemorum also mainly emerged during summer. In contrast to S. graminea, however, most
seedlings of S. nemorum were found in the forest patch. This pattern is in accordance with the
habitat preferences of these species. Jankowska-Blaszczuk & Grubb (1997) and Piroznikow
(1998) drew attention to the importance of small scale disturbances in the herb and litter layer for
seedling recruitment in temperate forests. Moehringia trinervia and S. nemorum belong to a
group of species that are able to survive under a closed forest canopy, but show an enhanced
growth in gaps resulting from uprooted trees or disturbances by wild animals (Staaf et al. 1987;
Jankowska-Blaszczuk & Grubb 1997). Although the effect of light on germination of these
species is not always consistent, both species are able to germinate in low and FR-enriched light
conditions under a closed forest canopy (Grime & Jarvis 1975; Jankowska-Blaszczuk & Grubb
1997, Jankowska-Blaszczuk & Daws 2007).
The role of gap-detection mechanisms in regulating germination has been studied primarily in
weeds and grassland species (Vincent & Roberts 1977; Williams 1983) and occasionally in
forest herbs (Hintikka 1987). Our results show that daily fluctuating temperatures and nitrates
also significantly affect seed germination of S. nemorum and M. trinervia. In S. nemorum
fluctuating temperatures seem to be of minor importance in stimulating germination. We did,
however, find a major positive response to fluctuating temperatures for M. trinervia, perhaps
indicating subtle differences in regeneration niche between S. nemorum and M. trinervia. In
combination with high nitrate concentrations, fluctuating temperatures even triggered
germination of M. trinervia seeds in complete darkness. Nitrates could be a useful indicator for
small scale disturbances in forests, since a rise in the soil nitrate level can even be observed in
single tree-fall gaps (Denslow, Ellison & Sanford 1998; Ritter et al. 2005). Considering the fact
that M. trinervia and S. nemorum can germinate in the presence of FR-light, a positive response
to elevated nitrate levels might provide a good indication that these species can germinate in
response to small scale disturbances under a closed forest canopy.

A combined study of seedling emergence in field conditions and factors regulating dormancy
break and germination in controlled conditions allowed us to, at least partially, expose
environmental factors controlling timing of seed germination of the four Caryophyllaceae in the
field. Apparent inter-specific differences in timing and location of seedling emergence were
observed. These differences are mainly attributable to distinct habitat preferences of these
species, since phylogenetic and geographical differences are small. A number of studies had
already attempted to test for differences in germination requirements of related species. In these
studies, very often only a limited number of dormancy breaking and germination inducing
treatments were applied (e.g. Thompson 1970; Schtz & Rave 1999). Our approach of subjecting
the seeds to an array of dormancy breaking treatments and testing the effect of multiple gap
related signals on germination, contributed to the exposure of subtle differences in germination
requirements between these closely related species.

Acknowledgements
We would like to thank Olivier Honnay for providing useful comments on the manuscript.

Ancillary
Article Information

DOI

10.1111/j.1365-2435.2008.01385.x

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Keywords

disturbance;
dormancy;
fluctuating temperature;
nitrate;
Stellaria

Publication History

Issue online: 14 February 2008

Version of record online: 14 February 2008
Received 14 November 2007; accepted 10 January 2008Handling Editor: Ken Thompson

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