AC TA O E C O L O G I CA 29 (2006) 187–195

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Original article

Ecophysiology of seed germination of wild Dahlia coccinea

(Asteraceae) in a spatially heterogeneous fire-prone habitat

Susana Vivar-Evans, Víctor L. Barradas, María E. Sánchez-Coronado,

Alicia Gamboa de Buen, Alma Orozco-Segovia *
Instituto de Ecología, UNAM, Departamento de Ecología Funcional, Apdo. Postal 70-275, Circuito Exterior S/N, Ciudad Universitaria, 04510
México, D.F., Mexico

A R T I C L E I N F O A B S T R A C T

Article history:
Dahlia coccinea grows on fire-prone xerophilous shrubland, on a lava field located in Mexi-
Received 20 May 2005
co City. Two kinds of experiments were performed to test the role of fire and environmen-
Accepted 3 October 2005
tal heterogeneity on germination. The first experiment tested the effect of environmental
Available online 19 January 2006 conditions (constant and alternating temperatures, cold stratification and light). The sec-
Keywords: ond one tested the effects of fire and high temperatures (dry and moist heat) on germina-
Ash tion. Seeds of Dahlia were indifferent to light. The seeds showed physiological dormancy,
Cold stratification which was lost by after-ripening or by gibberellins. During simulated fires, dry seeds toler-
ated high temperatures of short duration and also withstood prolonged exposure to 60 °C.
Fire
Dry heat treatment reduced the mechanical restriction for embryo growth in dormant
Gibberellic acid
seeds. Ash and prolonged exposure to moist heat inhibited germination. Exogenous gib-
Moist and dry heat
berellins reversed the deleterious effects of prolonged exposure to moist heat. The effect
Shrubland in a lava field
of cold stratification was related to the seeds’ physiological stage and to light conditions;
stratification in the dark reduced germination. Seeds of D. coccinea could tolerate, evade,
or be slightly favored by the effects of low intensity fires occurring in their habitat. Seed
responses to treatments suggest that the spatially heterogeneous lava field could provide
a wide variety of micro-sites where physiological dormancy could be broken and during
fires seeds could maintain their viability and subsequently germinate and/or develop a
seed bank.
© 2006 Elsevier SAS. All rights reserved.

in the 124.5 ha of the reserve (Fire Department, Universidad

1. Introduction
Dahlia coccinea is a wild plant, progenitor of the cultivated or-
namental varieties of this genus (Bye et al., 1999). It is abun-
dant in the ecological reserve of “El Pedregal de San Angel”,
located in the southern part of Mexico City, at 2240 m a.s.l.
(Rzedowski and Rzedowski, 1985). Fires occur periodically in
this area, however, fire frequency increased in 1998 when “El
Niño” caused a serious drought and 202 fires were recorded
*
Corresponding author. Tel.: +52 55 5622 9008; fax: +52 55 5616 1976.
E-mail address: aorozco@miranda.ecologia.unam.mx
(A. Orozco-Segovia).
1146-609X/$ - see front matter © 2006 Elsevier SAS. All rights reserved.
doi:10.1016/j.actao.2005.10.001
Nacional Autónoma de México, CORENA, 1998). It is known
that if climatic change is not reversed, the number of fires
will increase in the future (Gill et al., 2002), in spite of this
fact the effect of fire in the area has not been thoroughly stu-
died (Martínez-Orea, 2001).
D. coccinea was one of the most conspicuous elements
after the fire events of 1998 at the reserve of “El Pedregal de
San Angel” (Martínez-Mateos, 2001). This species could sur-
vive and become successful after a fire event either because
its tubers and/or seeds survive as they are protected by soil,
and/or because germination is enhanced by fire, which is a
common strategy among the species growing in fire-prone
188 ACTA OECOLOGICA 29 (2006) 187–195

habitats (Trabaud, 1987). The seeds of species adapted to fire
usually have hard seed coats (Baskin and Baskin, 1998) which
can be broken by high temperatures produced during com-
bustion, facilitating the entry of water and the emergence of
the embryo (Baskin et al., 2000). Additionally, after a fire,
light, temperature and humidity are modified, as well as
other factors such as the release of ethylene from ash or
the smoke/nitrous oxides that promote germination in some
species (Tyler, 1995; Ne’eman et al., 1999; Keeley and Fother-
ingham, 2000; Van Staden et al., 2000; Adkins and Peters,
2001). Elsewhere, fire conditions vary depending on the en-
vironmental characteristics of the region where they occur
(Odion and Davis, 2000; Gill et al., 2002). Thus, it is important
to study the influence of fire on germination in different
plant communities and species.
Studies of D. coccinea are important for maintaining a pool
of genetic variability for the cultivated Dahlia. For this it is
important to understand how sexual reproduction shapes
the genetic variation in natural populations, so the effects
of fire on plant and seed persistence and seedling emergence
and establishment are crucial for this species inhabiting a
fire-prone habitat. Consequently we studied the occurrence
of fire in the natural environment and germination ecophy-
siology of D. coccinea in response to the main environmental
factors that seeds experience in the soil before, during and
after fire.
2. Materials and methods
2.1. Species, seed collections and study area
D. coccinea Cavanilles (Asteraceae) is a perennial herbaceous
wild plant with tuberous roots. It is distributed from North-
ern Mexico to Guatemala and Colombia (Sorensen, 1969).
Though, Dahlia seeds are achenes (indehiscent fruits con-
taining a seed surrounded by the pericarp) we refer to these
here as seeds. Seeds were collected in October 1998 (first co-
hort) and in 2000 (second cohort), in the ecological reserve of
“El Pedregal de San Angel” (19°19’N, 99°11’W, 2240 m a.s.l.)
where D. coccinea is very abundant, growing during the rainy
season and flowering and fruiting from July till October. After
fruiting the shoots die and seeds and tubers remain dor-
mant. The climate in the area is temperate by altitude. The
vegetation in the area is an open xerophilous shrubland
growing on volcanic rock, where soil, moisture and tempera-
ture are heterogeneously distributed (Cano-Santana and
Meave, 1996). Annually, the herbaceous vegetation contri-
butes to the plant biomass 106.6–329.2 g m−2 year−1 (5400 kJ
m−2 year−1). During the dry season, this mass becomes fuel
for the periodical fires occurring in the reserve (Cano-Santa-
na, 1994).
2.2. Germination treatments
2.2.1. General procedures
After collection, seeds were air dried and stored in paper
bags under laboratory conditions at 23–25 °C and 40–50%
RH. There were five replicates of 50 seeds for each treatment,
except otherwise specified. Prior to incubation, the seeds
were washed with 10% sodium hypochlorite; a fungicide
was then applied (Interguzan 30-30, Quintozeno + thiram).
After that, seeds were germinated in plastic Petri dishes on
1% agar. The seeds were incubated in a growth chamber
(125 l; Conviron, Winnipeg, Canada) at 25 °C. Seeds were
counted every 2 days until germination was completed.
Seeds collected in 1998 were used for the majority of the ex-
periments; nevertheless, in order to synchronize the physio-
logical stage of the seeds with natural conditions, some
treatments were carried out with dormant seeds collected
in the year 2000. Table 1 indicates the seed batch used in
each treatment and the events that were simulated with
them.
2.2.2. Storage time and gibberellic acid
To test the presence of physiological dormancy 1-month-old
seeds (collected in 1998) were germinated with 0 or 1000 ppm
of GA3 (Sigma Chemical Co. G-7645, San Louis, MO, USA). To
test the effect of dry storage on physiological dormancy, 1-,
4-, 7- and 18-month-old seeds were germinated on agar.
Seeds collected in 2000 were germinated after 1, 2, 3 and
4 months of dry storage.

Table 1 – Summary of treatments, environmental conditions and physiological stages of the seeds when the treatments
were applied

Year of seed Season Treatments Seed Seed age

collection physiological (months)
stage
1998 Dry with random Autumn Seed dissemination Dormant seeds 0–3
rains Seeds sown in the field
Winter and spring Wet and dry stratification (5 °C) Partial dormancy 4–7
Moist heat , GA3
Fire simulations
Rainy Summer Field germination 9–10
Autumn

2000 Rainy Autumn Ash and stratification effect Dormant seeds ≥1

Dry, with random Spring Dry heat
rains
 ACTA OECOLOGICA
2.2.3. Cold stratification
To overcome physiological dormancy, we simulated the win-
ter–spring soil conditions for the natural habitat—flat exten-
sions, cavities (pockets, indentations and others) or cre-
vasses in a rough substrate—and exposed seeds to the light
and temperature conditions experienced before fires. Dry
seeds and seeds imbibed on agar remained at 5 °C for 28 days
in light and dark conditions inside a refrigerator (RC-600-N,
American Refrigeration Products, Mexico) illuminated with
four fluorescent lamps (40 W). Time exposure to cold tem-
perature was based on the total time at ≤ 5 °C in the reserve
recorded with a data logger along the period 1998–1999 using
a temperature–humidity probe (HMP35C, Campbell Scientific,
Inc., Logan, UT, USA). After pretreatment, all seeds were in-
cubated at 25 °C. Since soil disturbance in the area is very
infrequent, seeds are commonly stratified in the same light
environment where they will germinate in the rainy season.
Therefore seeds were stratified and germinated in the same
light regime. Controls consisted of untreated seeds germi-
nated under conditions of light and darkness.
2.2.4. Moist heat
To simulate the high fire-induced temperatures experienced
within rock cavities and crevasses were soil is moist all year
long, seeds were placed in each of three volumes: 10, 50 and
100 ml; V1, V2 and V3, respectively; of boiling water (96 °C at
2240 m a.s.l.) which took varying lengths of time to return to
room temperature, therefore providing different periods of
time of heat exposure to the seeds. When the seeds and the
thermocouple were placed in water, the temperature fell to
89 °C. Temperature course was measured until the water
cooled down to room temperature (24 °C). Temperature was
recorded with a thermocouple (T copper–constantan, Cole
Parmer, Vernon Hills, IL, USA) connected to a data logger
(21X, Campbell Scientific, Inc., UT, USA). Control seeds were
not immersed in hot water. In order to test the interaction
between seed physiological stage and moist heat, after treat-
ments, seeds were sown in agar with 0 or 1500 ppm of GA3.
2.2.5. Simulated fires
Soil and litter were collected to simulate the natural condi-
tions at the reserve. To determine the quantity of litter on
the soil surface of the area, the 10 representative microhabi-
tats in the Pedregal were sampled. Litter was dried in an
oven at 60 °C for 24 h. The soil was sieved and dried at
80 °C for 48 h. Fires were carried out in six aluminum con-
tainers 18 × 6.5 × 7.5 cm in height (117 cm2 and 877.5 cm3,
surface and volume, respectively). Each container was filled
with 242 g of volcanic rock, 92 g (S1) or 223 g (S2) of dry soil,
Table 2 – Quantity of litter commonly found on the soil in the reserve of “El Pedregal de San Angel” before the fires and its
equivalent in ash after fires (N = 10). In the three last columns are indicated the three levels of litter (L) and the ash used in
the fire or ash treatments described in methods; and its equivalent per area unit
(g m−2) Field conditions
Mean (± S.D.) Range
Litter 1546.16 ± 1611.56 395.21–5041.44
Ash 265.93 ± 277.18 44.91–867.13
29 (2006) 187–195 189
and 10 g (L1), 32 g (L2), or 58 g (L3) of dry litter. Rocks, soil and
litter were uniformly distributed in the containers. The litter
quantities were similar to those found in the field (Table 2).
Three hundred seeds were distributed between the litter and
the soil layer. The litter was ignited during the dry season
(T ≈ 26 °C, RH = 30%, wind speed = 1.5–3.0 m s−1) with a lit
match placed at one end of the container. Temperature dur-
ing the fires was recorded with six thermocouples (type E
chromel–constantan, Cole Parmer, Vernon Hills, IL, USA) lo-
cated at seed level and connected to a data logger (21X,
Campbell Scientific, Inc., Logan, UT, USA). Temperatures
were monitored until the containers reached room tempera-
ture. After the fire, the seeds were removed and three repli-
cations of 50 seeds per fire treatment were sown on agar.
Seeds that were not exposed to fire were the control.
2.2.6. Germination in the field
In order to test the germination capacity in the field during
the rainy season, 50 seeds were sown in each one of 12 cloth
pots filled with soil sterilized for 20 min in a microwave
oven. Cloth pots (8 cm in diameter × 5 cm in height) were
covered with a nylon mesh to restrict the entry of any other
seeds. Each pot was set inside a wire cage (25 cm
length × 25 cm width × 10 cm height, 0.2 cm2 opening) to pro-
tect seeds from predators. The pots were randomly placed in
the field in December 1998 in 12 sites (one pot per site) differ-
ing in light conditions and rock exposure, which represented
the environments where D. coccinea grows (shaded by rocks
or trees and in open places). Germination in the pots was re-
corded periodically. Soil temperatures were considered an in-
dicator of the differences between micro-environmental con-
ditions, thus temperature was recorded in each of the 12
sites with micro-data loggers (model H01-001-01, HOBO, On-
set Computer Corporation, Pocasset, MA, USA).
2.2.7. Ash and cold stratification
To break physiological dormancy and simultaneously to eval-
uate the effect of ash on germination, seeds collected in year
2000 were sown on agar in the following conditions: 1) cov-
ered with ash, 2) covered with ash during cold stratification
and 3) cold stratified seeds, later covered with ash, 4) only
cold stratified seeds, or 5) without any other treatment (con-
trol). Ash was added at 2.3 g to the germination substrate.
Ash was obtained from burning litter from the reserve. Un-
treated control seeds and only-stratified seeds were covered
with wet filter paper to simulate the humid conditions cre-
ated by the cinder. Control seeds were sown when the cold-
stratification treatments were over and all seeds were placed
in incubators.
Laboratory condition
Treatment Material used per Equivalent in g m–2
treatment (g)
L1 10 854.7
L2 32 2735.04
L3 58 4957.26
Ash 2.3 457.57
190 ACTA OECOLOGICA
Water potential and pH were measured in both a sample
of the ash mixed with distilled water (1:2, w/v, ash to water;
Ne’eman et al., 1999) as well as in a sample of the ash mixed
with 1% agar (2.3:40, w/v), using a Dew point microvoltmeter
HR-33T-R in a C52 thermocouple psychrometer chamber
(Wescor, Inc., Logan, UT, USA), and a pH meter (Hanna In-
struments, HI9219, Ann Arbor, MI, USA).
2.2.8. Dry heat
To know the effect on germination of the high temperatures
occurring during the dry season in the Pedregal, seeds col-
lected in year 2000 were left for 180 h in an oven at 60 °C.
Exposure time was calculated as the time ≥ 60 °C recorded
in the reserve with the data logger. After treatment, seeds
were sown on agar and germinated.
2.3. Data analysis
All germination data were arcsine transformed. Statistical
tests were applied depending on homogeneity of variances
(Bartlett’s test). When variances were homogeneous, data
were compared by one- or two-way ANOVA tests and multi-
ple comparisons were done with Tukey’s test; alternatively
Student’s t-test was used. When variances were not homoge-
neous, Kruskal–Wallis or Mann–Whitney’s tests were used
(Statgraphics, ver. 5.0, Statistical Graphics Co., Rockville, MD,
USA). Cumulative germination was fitted to exponential sig-
moid curves (y = a/[1+b(–cx)]). All fittings were made with a
computer program (Table Curve 2D, ver 5, 2000AISN Software,
Inc., Chicago, IL, USA).
3. Results
3.1. Seeds collected in year 1998
3.1.1. Storage time and gibberellic acid
Storage time had a positive effect on germination (Fig. 1;
H = 9.11, P = 0.02). Germination was significantly lower in 1-
Fig. 1 – Mean cumulative germination (± S.D.) at 25 °C of D. coccinea seeds. Seeds collected in 1998 (a) were germinated after
different storage times; one (○), 4 (▽), 7 (□) and 18 months (Δ). One-month-old seeds were also germinated with GA3
1000 ppm (b). Seeds collected in 2000 (c) were germinated after 1 (○), 2 (●), 3 (■) and 4 months (▼) of storage. Small letters
indicate significant differences among storage treatments; capital letters indicate significant differences between
gibberellins treatments.
29 (2006) 187–195
month-old seeds, and was not synchronous. A 4-month
after-ripening sufficed to reach full germination; neverthe-
less, 4- and 7-month-old seeds required more than 42 days
for full germination (Fig. 1a), whereas, maximum germina-
tion of 18-month-old seeds occurred in only 6 days. Gibberel-
lins significantly increased germination in 1-month-old
seeds (Fig. 1a, b; t = 1.92, P = 0.04). Immediately after collec-
tion, the two cohorts from 1998 and 2000 did not differ in
germination capacity. Germination success increased with
storage for the 1998 cohort, while decreasing for the 2000 co-
hort (Fig. 1a, c). In contrast, the cohort from 2000 showed an
inverse relation between storage time and germination capa-
city (y = 57.67 + [–0.57x3], R2 = 0.96), which was reduced signif-
icantly at 4 months (Fig. 1c, H = 8.91, P = 0.03), whereas the
cohort collected in 1998 at the same age reached maximum
germination capacity (Fig. 1a). In similar way to 1-month-old
seeds of this batch, seeds collected in 2000 had an asynchro-
nous germination.
3.1.2. Cold stratification
Exposure to 5 °C did not affect the germination capacity at
25 °C (Fig. 2) (H = 2.93, P = 0.71). But stratification of seeds im-
bibed in darkness resulted in a lower germination and a wide
heterogeneity in seed response (Fig. 2). In addition, depend-
ing on light conditions, stratification affected germination
velocity. When dry or imbibed seeds were both exposed to
cold and germinated in the dark, germination was very slow;
time to reach 80% germination increased.
3.1.3. Moist heat
Seeds immersed in V3 did not germinate. Seeds immersed in
V2 germinated slower than control seeds and the germina-
tion capacity was reduced significantly (Table 3, Fig. 3). Gib-
berellins had no significant main effect on germination but
the interaction between gibberellin treatment and moist heat
was significant, with gibberellin treatment increasing the
germination capacity of seeds in the V2 treatment. Germina-
tion was not affected by the other treatments.
 ACTA OECOLOGICA 29 (2006) 187–195 191

Fig. 2 – Mean germination (± S.D.) percentage at 25 °C of D. coccinea seeds collected in 1998; control (a) and cold stratified
were germinated in light (○) or in darkness (●). Seeds were exposed to the stratification (5 °C for 28 days) in a dry (b) or
imbibed state (c); the seeds were exposed to the same light conditions during this treatment and during germination.
Small letters indicate significant differences among treatments.

Table 3 – Results of two-way ANOVA carried out to test significant inverse linear relation (y = –0.88x + 117.27, R2
the effect of moist heat treatment and gibberellins on the = 0.93, P < 0.05) between the germination percentages and
germination response of D. coccinea seeds (collected in the mean temperature produced by the fires (mean tempera-
1998). Degrees of freedom (df), F values and significance ture from the beginning of fire until temperature reached
level (P) are given room temperature again). However, this trend was caused
Parameter Source of variation df F P only by S2L2 and S2L3 (Table 4). In these two treatments ger-
Germination Moist heat treatment 3,39 153.68 0.0001 mination was significantly lower than in the others, and fire
(%) GA3 1,39 1.78 0.19 had the longest residence time at high temperature.
Moist heat treatment * 3,39 3.78 0.02
GA3
3.1.5. Field germination
Mean temperature in the field was 17.6 ± 3.9 °C, varying
3.1.4. Simulated fires among the 12 sites from 14.5 to 26.8 °C. Rains began in the
Temperatures experienced by seeds varied across litter and middle of June (Fig. 4a) and germination began 1 week later
soil treatments, with higher temperatures with more soil (Fig. 6c). Germination finished in July (Fig. 4b). 72.5 ± 17.4% of
and more litter (Table 4). Less germination was observed for seeds germinated and the regression analysis did not show a
seeds that had experienced temperatures higher than 100 °C relation between germination and the mean, minimal or
for a long time (Table 4, F6, 20 = 23.54, P = 0.0001). There was a maximal temperature of the microsites (P > 0.05).

Fig. 3 – Mean germination (± S.D.) percentage at 25 °C of D. coccinea seeds collected in 1998. Seeds were germinated without
(open symbols) and with GA3 1500 ppm (solid symbols) after exposure to one of three different volumes of boiling water. In
V1 (square) water reached room temperature in 11 min, and water mean temperature was 24 °C, in V2 (triangle) these
values were 28 min and 32 °C, and in V3 (inverted triangle), 63 min and 40 °C; respectively. Control seeds did not
experience the exposure to boiling water (circles). Small letters indicate significant differences among treatments.
192 ACTA OECOLOGICA 29 (2006) 187–195

Table 4 – Germination percentages (± S.D.), at 25 °C, of D. coccinea seeds collected in 1998, after exposure to simulated fires
in containers with 242 g of volcanic rock and different quantities of soil and litter. Ti = initial temperature (23.7 ± 0.16).
Small letters indicate significant differences among treatments

Treatment Fire temperature Residence (min) Time to reach Ti Germination

Soil (g) Litter (g) Mean (°C) Maximum (°C) > 100 °C (min) (%)
92 10 (S1L1) 27.6 ± 5.7 45 0 38 94 ± 3.6 c
32 (S1L2) 36.2 ± 21.6 156 3 90 91.3 ± 7.2 c
58 (S1L3) 31.6 ± 8.2 57 0 56 88.7 ± 4.5 c
223 10 (S2L1) 32.4 ± 14.6 112 1 38 92 ± 6.5 c
32 (S2L2) 78.5 ± 34.3 124 36 162 52 ± 4.7 b
58 (S2L3) 109 ± 70.1 230 52 178 15.3 ± 8.5 a
Control 88.7 ± 8.3 c

Table 5 – Germination percentages (± S.D.), at 25 °C, of

D. coccinea seeds collected in 2000 after exposure to ash
(2.3 g), and/or cold stratification (5 °C for 28 days). Small
letters indicate significant differences among treatments

Pretreatment Germination Germination (%)

condition
Stratified Covered with wet fil- 42.4 ± 26.9 ab
ter paper
Stratified and Covered with ash 0
covered with ash
Stratified Covered with ash 9.2 ± 18.4 a
None Covered with ash 6.4 ± 12.8 a
None (control) Covered with wet fil- 57.6 ± 6.4 b
ter paper

3.2.2. Dry heat

Fig. 4 – (a) Daily precipitation during June and (b) July of
1999. (c) Mean cumulative germination (± S.D.) of D. coccinea
(seed batch collected in 1998) occurred in the field, during
the rainy season of 1999. (d) Precipitation and mean (– –),
minimum (—), and maximum (·····) temperature in the
Pedregal de San Ángel in a 20-year period (Sánchez-Huerta,
1990). The arrow indicates the beginning of germination in
the field.
3.2. Seeds collected in the year 2000
3.2.1. Ash and stratification
The germination capacity of non-stratified and stratified
seeds was drastically reduced when ash was added to the
substrate during the germination period (Table 5, H = 11.3,
P < 0.01). Exposure to ash during cold-stratification prevented
total germination. Stratification itself reduced the germina-
tion capacity and increased heterogeneity in seed response.
Water potential of ash paste was –1.1 MPa while that of the
mixture of ash and agar was of –0.9 MPa, the pH was 10.45
and 9.66, respectively.
Dry heat increased germination capacity from 21.6 ± 14.2% to
47.6 ± 35%, but the Mann–Whitney’s tests did not indicate
significant differences due to the heterogeneity in seed re-
sponse (U = 17, P = 0.4). Time to reach full germination was
reduced from 40 to 25 days. Regardless of the treatment
used, maximal germination was low in relation to seeds col-
lected during 1998.
4. Discussion
D. coccinea seeds had physiological attributes that may be im-
portant in understanding its population biology in a hetero-
geneous environment subject to frequent fires. Fire was not
required for germination, although heat increased the germi-
nation capacity of dormant seeds. Conversely, cold stratifica-
tion in the dark may favor the formation of a seed bank.
D. coccinea seeds were indifferent to light and showed pri-
mary dormancy, expressed as low and slow germination that
took more than 2 months to complete. For seeds collected in
1998, after-ripening sufficed to overcome dormancy and in-
creased gradually germination rate and synchrony but this
was not observed for seeds collected in 2000. In D. rudis Sor
(Acosta-Bautista, 1999) and in other Asteraceae species, phy-
siological dormancy is also gradually eliminated by after-ri-
pening (Corbineau et al., 1990; Seiler, 1998). In the field, phy-
siological dormancy prevented germination during the rains
occurring in the cold-dry season. Seeds gradually lost dor-
mancy over the winter–spring and then they were ready to
germinate rapidly with the onset of summer rains.
 ACTA OECOLOGICA
In contrast, the cohort from 2000 lost germination capa-
city with time, due to secondary dormancy that was over-
come in a fraction of the seed population by dry heat. In this
cohort, stratification reduced germination and increased the
spread in germination, which could indicate a deleterious ef-
fect. However, in the other cohort (1998) germination syn-
chrony and rate increased slightly when imbibed seeds were
cold-stratified in light. Although, seeds are indifferent to
light, during stratification light conditions became relevant
for subsequent germination. In the dark, stratification re-
duced germination capacity or reduced germination rate
and increased germination variability. In some Asteraceae,
cold stratification does not affect primary dormancy or re-
duce germination (Corbineau et al., 1990), but in Dahlia the
effect of cold stratification was related to the physiological
stage of the seed batch, to seed hydration and to light condi-
tions during stratification, as in other plants (Borghetti et al.,
1989; Derkx and Karssen, 1993).
Seeds exposed simultaneously to cold and light probably
will have a high germination in the rainy season; whereas a
fraction of seeds that remains in darkness may have a higher
probability to form a permanent seed bank. Moreover, seeds
from different seed batches may contribute differentially to
the seed bank due to variation in the intensity of dormancy
among cohorts. The seed bank of D. coccinea tends to be tran-
sient, due to rapid and concerted germination occurring at
the beginning of the rainy season; as in Pistacia lentiscus
(García-Fayos and Verdú, 1988). Thus, any mechanism that
favors the permanence of D. coccinea in the seed bank and
seed burial may be relevant for the population maintenance
in a fire-prone habitat.
In D. coccinea the pericarp could be an obstacle for radicle
protrusion, but when the embryo was mature and vigorous
(after 7–18 months) seeds germinated fast and synchro-
nously. With physiological dormancy gibberellins also favor
breaking of the seed covering by embryos (Baskin and Baskin,
1998). After exposure to 60 °C for 80 h germination increased,
but temporal spread in germination suggests heterogeneity
in the seed covers or the in intensity of dormancy in the seed
population. In the Pedregal the longest exposure to heat oc-
curs during the dry season. At noon, temperature runs up to
60 °C on the rocks or up to 59 °C under 5 cm of soil (Olvera-
Carrillo, 2001). These temperatures can increase germination
of species adapted to fire (Bradstock and Auld, 1995; Pugnaire
and Lozano, 1997; Hanley and Fenner, 1998). Additionally,
every day or during fires, the seeds staying in the moist soil
of rock crevasses and cavities are exposed to brief periods of
moist heat, which may not affect the germination of
D. coccinea. However, relatively long exposure to moist heat
(63 min) during severe fires could prevent germination. Con-
trasting effects of moist and dry heat on germination have
been previously reported (Cushwa et al., 1967; Baskin et al.,
1998).
Moist heat could have damaged the seeds and/or induced
secondary dormancy (Baskin and Baskin, 1998; Corbineau et
al., 2002). In these seeds gibberellins could have broken sec-
ondary dormancy and/or compensated the effect of moist
heat of intermediate duration (28 min). Gibberellins bind to
a receptor in the cell membrane as a first step of the signal
transduction pathway involved in the stimulation of starch
29 (2006) 187–195 193
degradation (Lovegrove et al., 1998; Jones et al., 1998). Thus
a loss in membrane integrity, as a result of heat shock could
reduce the interaction among the elements involved in this
pathway. Therefore, it is possible that in heat-treated seeds
exogenous gibberellins increased the efficiency of the first
step of this process. On the other hand, it has been reported
that smoke stimulates germination in a similar way as gib-
berellins (Keeley and Fotheringham, 1998; Van Staden et al.,
2000), thus, during fires, smoke could also play an important
role in repairing cells damaged by high temperatures. This
interesting trait requires further study (J.E. Keeley, personal
communication).
The effect of fire on germination of D. coccinea was not de-
leterious in all cases; germination was only reduced in the
two containers where fires reached temperatures over
100 °C and residence time was long. Conversely, these tem-
peratures at shorter duration were not inhibitory. Similar re-
sults have been reported in other studies (Keeley et al., 1985,
Tarrega et al., 1992; Nuñez and Calvo, 2000). During natural
fires temperature is not uniform in space and time; it de-
pends on the type, amount and distribution of litter, soil
depth and wind. Consequently, “fire regime” has a relevant
role in the ecological outcome (Gill et al., 2002); in the Pedre-
gal, the environmental heterogeneity is determining for fire
regime, simultaneously may provide potential refuges for
seeds determining differential survival of seeds (Tyler, 1995;
Pugnaire and Lozano, 1997; Odion and Davis, 2000). Thus,
surviving seeds of Dahlia could survive and take advantage
of the openings for seedling establishment created by the fire
(Auld and Bradstock, 1996).
In this study ashes including small pieces of charred
wood inhibited germination in contrast to previously re-
ported favorable effects (Keeley, 1987). Probably the quantity
of ash added to the germination substrate made that its ba-
sic pH and/or the low water potential drastically inhibit ger-
mination of D. coccinea (Ne’eman et al., 1999; González-Raba-
nal and Casal, 1995). In the Pedregal ash remains
accumulated in most of the cavities where the litter was
burned or is accumulated in them by the action of wind;
however, it may be washed or diluted by water during preci-
pitations, favoring germination when the rainy season is
well established.
5. Conclusions
D. coccinea is a species adapted to a seasonal temperate cli-
mate mediated by altitude and to a spatially heterogeneous
habitat; both determine the “fire regime” and extreme daily
temperature fluctuations. This changing habitat, in space
and time, could favor the expression and maintaining of the
seed physiological diversity and the genetic variability in this
species (Spicer and Gaston, 1999). In D. coccinea dormancy
prevented germination during the random winter–spring
rains. During this period seeds overcome physiological dor-
mancy and low temperatures may accelerate or inhibit ger-
mination increasing opportunities for seed bank formation,
depending on light conditions and/or the seed physiological
stage during stratification. On the other hand, seeds can tol-
erate, evade or be slightly favored by the effect of fires that
194 ACTA OECOLOGICA
occur in the area and by high temperatures occurring in the
reserve. This species could display a seeder and/or a sprout-
ing strategy to respond to the fire effects (Whelan et al., 2002;
Gill et al., 2002; Fernández-Santos et al., 2004). Lack of infor-
mation on Dahlia tubers gives stance to their future study,
which could also be relevant for conservation of wild popula-
tions of Dahlia.
Acknowledgments
The authors thank Lourdes González-Zertuche for their
technical assistance and Dr. Pilar Huante-Pérez and Dr. Fran-
cisca Acevedo for their conscientious review. Specially, we
thank the Editor Jacqui Shykoff and two anonymous re-
viewers. This research was funded by Mexico’s National
Council for Science and Technology (CONACYT); Research
Grant Ref. G0011N.
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