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Article

Interannual Variability in Seed Germination Response to Heat Shock in Cistus ladanifer

by
Belén Luna
Departamento de Ciencias Ambientales, Universidad de Castilla-La Mancha, Av. Carlos III s/n, 45071 Toledo, Spain
Fire 2024, 7(10), 334; https://doi.org/10.3390/fire7100334
Submission received: 16 August 2024 / Revised: 21 September 2024 / Accepted: 23 September 2024 / Published: 25 September 2024
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Abstract

Mediterranean climates, characterised by hot and dry summers, have predictable fire regimes, and many species with physical seed dormancy (PY) thrive after wildfires. While it is well known that PY is released after heat shock in these species, intraspecific variation in seed response to heat is less understood. This research explores, for the first time, the variability in the traits of Cistus ladanifer seeds from the same central Spain population over eight years. It examines seed germination and viability under different heat shocks and the relationships among seed traits and climatic variables. While the response to heat shock remained constant over the years studied, achieving the highest germination percentages after heat shock at 100 °C, seed germination varied between years, and environmental conditions affected seed traits. Seed moisture content was negatively correlated with the maximum summer temperatures, and seed viability was positively related to annual precipitation. Germination at 100 °C was lower in warmer years as more seeds did not break their PY. In conclusion, despite the fact that PY appears to be genetically determined, it also depends on the environmental conditions experienced by the mother plant. This interannual phenotypic variability may help Cistus ladanifer to cope with the increasingly unpredictable conditions imposed by climate change.

1. Introduction

Mediterranean-type ecosystems are characterised by hot and dry summers which lead to frequent fires. These fire-prone areas have limited water, and precipitation variability is common, especially where precipitation is low [1]. The Mediterranean basin is considered as one of the most vulnerable regions for climate change [2]. With climate change, together with higher temperatures, a decrease in precipitation and higher interannual variability are expected [3,4,5]. Fire is a natural ecological factor that forms part of the Mediterranean ecosystems, but in the last few years, fire risk has increased because of climate change. Periods of drought have become more intense and, combined with the increase in temperature, have contributed to the rise in the frequency and intensity of forest fires [6,7].
In these Mediterranean habitats, many plant species have developed regeneration traits which allow them to be maintained or become established after a fire. This is the case of physical seed dormancy (PY) [8,9] which is caused by a water-impermeable hard coat that impedes seed germination until the testa becomes permeable. PY is most commonly found in species occurring in arid and semi-arid regions [10,11], and it has been proposed to have evolved to guarantee the survival of plants in temporally stochastic and harsh environments [8,9]. PY occurs in at least 18 Angiosperm families, among which are Cistaceae. Species of the Cistaceae family dominate large areas of shrubland in the Mediterranean Basin [12], and their occurrence is especially pronounced after fires. All species are obligate seeders, and consequently, their regeneration after fire depends on seed germination.
Fire has been the most studied environmental stimulus in Cistaceae species, and quite a lot of investigations have focussed on the effects of heat shock on the breaking of PY and subsequent seed germination [13,14,15,16,17,18]. Despite variability in seed traits among and within populations being of critical importance for the persistence of a species under variable environmental conditions [19], variation in dormancy temperature thresholds has rarely been studied [20,21,22,23]. Most studies focus on the among-population variation in seed traits along climatic gradients [24]. Natural gradients offer good opportunities for evaluating among-population variability and can provide valuable information about how species may cope with environmental variability [24,25]. However, the relationship between the environment and seed responses is not always consistent along environmental gradients [24]. There is little research based on the interannual study of the effect of the maternal environment on temperature thresholds for dormancy release in physically dormant species [26,27]. Seed traits such as size, dormancy, viability and germination responses to various environmental cues are essential reproductive characteristics that have evolved in response to habitat conditions and significantly contribute to plant fitness [28,29]. The temperature and water availability experienced by the mother plant during seed formation can influence these traits [30] and, consequently, future generations [31].
Physical dormancy is mainly determined by genetic factors, but the maternal environment of the plant during seed development also plays an important role in regulating its development [32]. Seed moisture content is closely related to the onset of seed coat impermeability and determines the degree of hardseededness [33]. Seeds produced under higher maternal temperatures and low water availability produce seeds with higher percentages of PY [34,35,36,37]. Consequently, environmental changes during seed formation can alter thresholds for breaking PY with relevant implications for reproductive success especially in unpredictable environments. Changing climatic conditions will modify the maternal environment likely resulting in changes to seed traits and their functions [24,38]. A warmer, drier climate will also lead to an increased risk of severe fire with consequences for plant population dynamics.
This study will deepen the knowledge of the germination of Cistus ladanifer, a quite common western Mediterranean shrub, considered as a pyrophyte [39] or a generalist and opportunistic coloniser [40]. It occupies strongly disturbed areas associated with early successional stages, and it is capable of colonising highly disturbed soils, like those present in areas affected by fire, abandoned agricultural lands or disturbed woods. The physical dormancy of their seeds allows Cistus to maintain long-lived soil seed banks, where seeds persist while environmental conditions are unfavourable for establishment. Release from dormancy is possible by the scarification of the seed coat, which in fire-prone habitats is often related to the heat generated by fires [13]. Seeds with physical dormancy show specialised structures in the seed coat, such as the chalazal plug in the Cistaceae [8]. In breaking physical dormancy, this plug is pushed slightly into the seed and forms a circular opening (oculus) through which the seeds imbibe water [41,42]. In addition to the unplugging of the seed coat opening, exposure to dry heat also causes cracks in the coat [43,44,45]. Consequently, after a fire, a high abundance of seedlings of Cistaceae is observed [46,47,48,49]. PY allows for seedling establishment under favourable postfire conditions, free of competitors [50].
In this work, the variation in temperature thresholds breaking PY was analysed along eight years in Cistus ladanifer seeds from a single population in the centre of the Iberian Peninsula. In particular, this study focusses on the responses of germination and seed viability to different heat shock treatments in the studied years. In addition, the relationship between seed traits (seed mass, seed moisture content, seed viability, germination after 100 °C heat shock and germination without heat shock) and climatic variables were explored. Interannual variation in seed characteristics is expected, as there must be fine-tuning with the environment to regulate the timing of germination. The specific objectives were as follows: (1) to determine whether the germination and viability of Cistus ladanifer seeds from the same population vary with time, (2) to characterise the response of its germination and viability to heat shock, (3) to ascertain whether the responses to heat shock vary between years and (4) to relate seed trait variations with changes in the maternal environment.

2. Materials and Methods

Seeds of Cistus ladanifer L. were collected in the centre of the Iberian Peninsula (39°49′0.3″ N 4°14′14.177″ W) during eight consecutive years, from 2015 to 2023, except for 2017, when seeds could not be harvested because they were aborted. The climate is Mediterranean, with a mean annual temperature of 15 °C and a mean annual precipitation of around 400 mm. Seeds were collected during the summer from at least 50 individuals randomly selected from the same location each year. Then, seeds were carried to the laboratory where they were cleaned and stored in paper bags in laboratory conditions until the start of the experiment in February of 2023. Seeds of C. ladanifer have hard coats that allow them to persist in soil seed banks for long periods [51], and no changes in viability appeared to occur in different periods of storage in the laboratory [21], so no loss of seed viability due to storage was expected in this work.
Five replicates of twenty seeds were weighed using a digital scale to determine the mean seed mass for each year. Then, seeds were dried at 103 °C for 17 h [52] and weighed again in the same way. Seed moisture content was calculated as the percentage of weight attributed to water, which was measured as the change in sample weight after drying, relative to the initial weight. The mean values of dry seed mass and seed moisture content were calculated from the five replicates.
The effects of heat shock on the germination of the seeds collected from the same population in different years were analysed through a factorial experiment. Prior to germination, five heat shock treatments were applied: control, 80 °C, 100 °C and 120 °C for ten minutes and 150 °C for one minute. The timing of exposure to the highest temperature (150 °C) was much lower than the rest of the heat shocks as prolonged exposure to such high temperatures does not result in germination [15]. A total of 4 replicates of 25 seeds each were used per treatment, and each replicate was subjected independently to the heat shock treatments in an air-forced oven. Then, seeds were germinated in Petri dishes (5.5 cm in diameter) over two filter papers moistened with 1.2 mL of distilled water. Seeds were incubated in a temperature- and humidity-controlled chamber (Model G-21, Ibercex), with a 12/12 h daily photoperiod and an alternating temperature regime of 20/15 °C.
The experiment lasted 6 weeks, and dishes were checked three times a week. The criterion of germination was the protrusion of a radicle. At the end of the experiment, ungerminated hard seeds were counted, and the viability of ungerminated seeds was tested by a tetrazolium test. Seeds were cut and incubated in a 1% solution of 2,3,5-triphenyl tetrazolium chloride for 48 h in the dark. Seed viability was estimated as the sum of germinated seeds plus stained seeds after the tetrazolium test. The final germination was assessed in relation to viable seeds and not in relation to the total number of seeds sown. In this way, germination data are not masked by the effect of viability. The germination results refer only to seeds that can germinate, i.e., those that are viable.
Generalised linear models (GLMs) were used to evaluate the effects of heat shock and the year of seed collection on the final germination and viability. GLMs are recommended for the analysis of germination and viability since these data are discrete and binomial [53], and although an analysis of variance (ANOVA) has long been used for the statistical analysis of these data, generalised linear models provide a more consistent theoretical framework. Based on error structure, a binomial error distribution and a logit link function were used for the variables analysed. When factor effects were significant, pairwise comparisons among treatments were performed using Bonferroni correction.
Relationships between seed traits and the maternal environment were analysed through bivariate correlations. Dry seed mass, seed moisture content, seed viability, germination at control and 100 °C treatments were correlated with annual and summer temperature and precipitation. Germination at 100 °C was chosen because this treatment led to the highest germination percentages being the most effective for breaking PY. Germination is highly responsive to environmental stress experienced during seed maturation on the maternal plant, so summer climatic variables were included together with annual variables. The mean annual temperature and precipitation and the mean of the maximum summer temperature and summer precipitation were used to characterise the climatic conditions of each year. These data were obtained from the Integral Irrigation Advisory Service for Farmers (SIAR) of Castilla-La Mancha. All statistical analyses were performed using SPSS Statistics version 28.0 (SPSS, Chicago, IL, USA).

3. Results

Heat shock had a significant effect on seed germination and viability (Table 1, Figure 1). Germination was significantly enhanced by all the heat shock treatments. The fraction of permeable soft seeds in the control was around 35% and remained quite constant across the years (Figure 2).
The maximum percentages of germination, around 90%, were reached in the 100 °C treatment (Figure 1). The 150 °C (1 min) treatment was the least effective in breaking PY since germination only reached around 45% (Figure 1). Seed viability was very high, only dropping to almost 80% with the 120 °C treatment (Figure 1).
Germination and seed viability also showed significant differences among the studied years (Table 1). The highest values of germination and viability were reached in 2015, while the lowest germination was in 2022 and the lowest seed viability in 2020 (Table S1). The interaction between both factors, heat shock and year, was not significant for germination (Table 1). This means that the response of germination to heat shock maintained constant across the studied years. On the contrary, the interaction between heat shock and year was significant for viability (Table 1); that is, the viability response to heat shock changed across years (Figure 2). Seed viability remained unaltered among heat shock treatments for 4 years (2015, 2020, 2021 and 2023), and it was significantly decreased at 120 °C for the rest of the years (Figure 2).
While seed mass was not correlated with climatic conditions, seed moisture content was negatively correlated with the mean of the maximum summer temperatures (Table 2, Figure 3). Seed viability was positively correlated with annual precipitation (Figure 3). Germination in the control treatment was not related to climatic conditions, but germination at 100 °C was negatively correlated with temperature variables (Table 2, Figure 3).

4. Discussion

The germination of Cistus ladanifer was triggered by heat shock, as expected and in agreement with previous results [13,15,16,18]. The maximum germination was near 90% and was reached after a heat shock of 100 °C. On the contrary, germination in the treatment of 150 °C for 1 min was expected to be much higher than the approximately 45% found, showing that this treatment was not very effective in breaking PY in contrast to that found by Valbuena et al. [15]. Seed viability was very high, around 90%, and was only affected by the treatment at 120 °C, which reduced it by 10%. In other work, seeds of C. ladanifer also tolerated heat shocks of moderate severity, but contrary to this work, 150 °C caused the death of all seeds [54]. The ability of seeds to survive heat shock may be associated with physical and physiological seed traits [55]. Seed survival in high temperatures associated with fire is usually associated with hardseededness [56,57], and it is related to seed moisture content [58,59]. Tangney et al. [58] found that drier seeds tolerate heat shock better than those with a high moisture content, but their drier studied seeds had much higher percentages of seed moisture content (15–50%) than our seeds (around 5%). The very low moisture content of C. ladanifer seeds may explain the low viability loss found with heat shock.
Germination varied significantly among years, but the response to heat shock was similar. This means that although the mean germination varied between the highest in 2015 (75%) to the lowest in 2022 (54%), the temperature thresholds breaking PY were quite constant all the years, with the highest levels of PY break at 100 °C and the lowest at 150 °C. No correlation between seed germination in control conditions and climatic variables was found, which may be because the proportion of nondormant permeable soft seeds is genetically fixed, ensuring the same proportion of seeds is available for immediate germination. This stable fraction of permeable seeds could be constant and exclusive of each population and not determined by the mother environment [60,61]. Germination in the control without heat shock was around 35%, which can be considered a relatively high percentage in Cistus, but germination percentages even above 50% have also been registered [13,20,62], finding a high variability between populations and within populations (between 4 and 77%) [20,63]. For other species with PY, especially legumes, a high PY variability within the same site has been described over the years because maternal environmental factors such as drought influence the proportion of seeds that enter dormancy [37,64]. On the other hand, germination at 100 °C was negatively correlated with temperature; that is, higher temperatures led to high levels of seed dormancy. These results imply that C. ladanifer shows a constant, fixed proportion of soft nondormant seeds, while environmental conditions, in this case, temperature, only affect the degree of hardness of the already-hard seeds.
By having seeds with various degrees of dormancy, plants can spread their offspring over time and bet-hedge against unpredictably variable environments [65]. Plastic responses to external stimuli provide seeds with a strong bet-hedging capacity and the potential to cope with high levels of environmental heterogeneity and, in the case of PY, to a variety of fire conditions. Variation in temperature thresholds allows seeds to break PY under the heterogeneity of temperatures produced during fires and guarantee the persistence of a population because it ensures the germination of a portion of seeds from the seed bank after a particular fire, while other portions remain in the seed bank, available to germinate after later fires, thus spreading the risk of extinction [66].
Seed moisture content was very low, between 2.9% and 7.4%, which agree quite well with the results found for different mother plants of this species (6.2–7.9%) [32]. Seed moisture content was negatively correlated with the mean of the maximum summer temperature, probably because of the higher levels of desiccation associated with the low relative humidity in the seed maturation environment, which affect the drying capacity of seeds [32]. Although both germination at 100 °C and seed moisture content were correlated with the mean of the maximum temperature in summer, no correlation between germination at 100 °C and seed moisture content was found, maybe because of the very low levels of seed moisture content. Pérez-García [21] also found no significant relationship in any case between germination and the seed moisture content in C. ladanifer.
Seed traits can be altered by environmental conditions during seed formation and maturation, which could affect the population dynamics since what happens later is dependent on what has happened before [31]. In areas where water is a limiting factor for plant development [67], as in the Mediterranean environments, water stress can affect important seed traits like seed size and viability. Seed mass is an important functional trait since it is usually correlated with improved seedling establishment and survival [68]. Consequently, seed maturation conditions could have important consequences for the next generation of seedlings [31]. However, the seed mass of C. ladanifer was not related to climatic conditions, which matches with the results found in a drought experiment with this species, where the seed mass from drought-exposed mother plants was similar to that of the control plants [61]. Likewise, no differences in seed mass were found for other Cistaceae species such as Helianthemum syriacum [69]. Contrary to seed mass, seed viability was positively correlated with annual precipitation and, although only marginally, was also negatively related to the annual mean temperature. That is, as expected for these habitats where vegetative activity is limited by water deficit and high temperatures, particularly dry and hot years will reduce the seed viability of C. ladanifer. However, these results differ from those of the earlier drought experiment, which found high viability values (over 90%) regardless of the mother’s drought treatment [61].
Changing climatic conditions will alter the maternal environment, likely resulting in changes to seed traits and their functions [38]. With climate change, both higher temperatures and reduced precipitation are already a fact [70,71], including their additional impacts on fire activity increasing its incidence and severity [7]. Thus, significant consequences for plant population dynamics and species persistence are expected, especially for those species sensitive to fire. Based on the results found in this work, a lower seed viability of C. ladanifer is expected in years with reduced precipitation. However, seed viability was not reduced below 70% in any case, even in the driest year with 200 mm of precipitation. Additionally, we do not know whether a serious problem may arise if the reduction in precipitation to 200 mm becomes the norm rather than the exception. Higher temperatures, especially during seed development, may lead to seeds with even lower moisture contents, which may affect hard seeds but not the genetically fixed proportion of soft seeds. This could be related to the consistent negative relationship between germination after a 100 °C heat shock and temperature (mean annual and maximum summer temperatures). This means that in hotter years, a fraction of seeds would have hard seeds with deeper levels of dormancy and would need more intense heat shocks to break their PY [32]. This higher level of dormancy could be an advantage in responding to more intense fires, as long as they are not too intense to cause seed mortality. C. ladanifer relies entirely on its tiny, hard seeds for regeneration, which seems very successful as its high germination ability and responsiveness to heat shock allow it to thrive in unfriendly environments. The germination of C. ladanifer is unlikely to be threatened by climate change, as its seed traits are already adapted to harsh and unpredictable habitats. However, the impact on seedling survival and plant establishment remains uncertain.

5. Conclusions

Plants living in Mediterranean environments have to cope with high summer temperatures, limited water and unpredictable variation in precipitation together with recurrent fires, and they have consequently developed traits which allow them to survive the harshness of these habitats, such as PY [8]. PY is a seed trait that undoubtedly confers fitness advantages in fire-prone environments [72], and it has been hypothesised that plants with PY will thrive in the more variable and warmer climate predicted for the future [9]. This is the case of C. ladanifer, which maintains or increases its levels of viability and germination after different heat shocks even under the pressure of extreme environmental conditions affecting the timing of seed formation and maturation. Although PY is genetically determined, it is also influenced by the environmental conditions experienced by the mother plant. Seed dormancy, as one of the earliest traits expressed in the life cycle of plants, can be a critical determinant of colonisation and establishment success. The different degrees of dormancy involve the need of different requirements for breaking dormancy and regulate the timing of germination, providing a form of bet-hedging, which allows seeds to spread the risk of extinction. The annual phenotypic variability in seed traits may help Cistus ladanifer adapt to the increasingly unpredictable conditions caused by climate change.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/fire7100334/s1, Table S1: Final germination and seed viability percentages for each year. Table S2: Environmental variables for each year.

Funding

This research was funded by University of Castilla-La Mancha.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

We thank Manuel Hernández Fernández for their valuable comments and Sergio Corral and María Gómez for their assistance in the laboratory.

Conflicts of Interest

The author declares no conflicts of interest.

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Figure 1. Seed germination and viability (means and standard errors) in different heat shock treatments. Different letters show significant differences (p < 0.05) between heat shock treatments based on pairwise comparisons with Bonferroni correction after GLM analysis.
Figure 1. Seed germination and viability (means and standard errors) in different heat shock treatments. Different letters show significant differences (p < 0.05) between heat shock treatments based on pairwise comparisons with Bonferroni correction after GLM analysis.
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Figure 2. Seed germination and viability (means and standard errors) for different heat shock treatments and years (from 2014 to 2023).
Figure 2. Seed germination and viability (means and standard errors) for different heat shock treatments and years (from 2014 to 2023).
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Figure 3. Correlations between seed traits (seed moisture content, seed viability and germination at 100 °C) and climatic variables (precipitation in mm, temperature in °C) during eight years.
Figure 3. Correlations between seed traits (seed moisture content, seed viability and germination at 100 °C) and climatic variables (precipitation in mm, temperature in °C) during eight years.
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Table 1. Results from GLM for main effects of year and heat shock treatments and their interactions on final germination and seed viability.
Table 1. Results from GLM for main effects of year and heat shock treatments and their interactions on final germination and seed viability.
YearHeat ShockYear x Heat Shock
ꭓ2pꭓ2pꭓ2p
Germination23.759<0.001290.772<0.00130.0470.361
Seed viability93.957<0.00140.284<0.00151.9020.004
Table 2. Correlation coefficients between seed traits (seed mass, SMC: seed moisture content, viability, Germ C: germination in control treatment, Germ 100: germination in 100 °C treatment) and climatic variables (Tmean: mean annual temperature, Annual P: annual precipitation; Tmax: mean of the maximum summer temperature; Summer P: summer precipitation). Significant correlations are shown in bold (p < 0.05) and marginally significant correlations in cursive (0.05 < p < 0.01).
Table 2. Correlation coefficients between seed traits (seed mass, SMC: seed moisture content, viability, Germ C: germination in control treatment, Germ 100: germination in 100 °C treatment) and climatic variables (Tmean: mean annual temperature, Annual P: annual precipitation; Tmax: mean of the maximum summer temperature; Summer P: summer precipitation). Significant correlations are shown in bold (p < 0.05) and marginally significant correlations in cursive (0.05 < p < 0.01).
AnualSummer
TmeanpTmaxp
Seed mass−0.4590.614−0.2970.166
SMC−0.5430.601−0.7970.552
Viability−0.6740.768−0.2500.237
Germ C0.401−0.441−0.1800.092
Germ 100−0.9520.473−0.7470.558
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Luna, B. Interannual Variability in Seed Germination Response to Heat Shock in Cistus ladanifer. Fire 2024, 7, 334. https://doi.org/10.3390/fire7100334

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Luna B. Interannual Variability in Seed Germination Response to Heat Shock in Cistus ladanifer. Fire. 2024; 7(10):334. https://doi.org/10.3390/fire7100334

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Luna, Belén. 2024. "Interannual Variability in Seed Germination Response to Heat Shock in Cistus ladanifer" Fire 7, no. 10: 334. https://doi.org/10.3390/fire7100334

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Luna, B. (2024). Interannual Variability in Seed Germination Response to Heat Shock in Cistus ladanifer. Fire, 7(10), 334. https://doi.org/10.3390/fire7100334

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